Introduction to Fungi, Third Edition

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Introductionto Fungi 

This new edition of the universally acclaimed and 

widely used textbook on fungal biology has been 

completely rewritten, drawing directly on the 

authors’ research and teaching experience. The 

text takes account of the rapid and exciting 

progress that has been made in the taxonomy, cell 

and molecular biology, biochemistry, pathology 

and ecology of the fungi. Features of taxonomic 

significance are integrated with natural functions, 

including their relevance to human affairs. Special 

emphasis is placed on the biology and control of 

human and plant pathogens, providing a vital 

link between fundamental and applied mycology. 

The book is richly illustrated throughout with 

specially prepared drawings and photographs, 

based on living material. Illustrated life cycles are 

provided, and technical terms are clearly explained. 

Extensive reference is made to recent literature and 

developments, and the emphasis throughout is on 

whole-organism biology from an integrated, multidisciplinary 

perspective. 

John Webster is Professor Emeritus of the School of 

Biosciences at the University of Exeter, UK. 

Roland W.S. Weber was a Lecturer in the Department 

of Biotechnology at the University of Kaiserslautern, 

Germany, and is currently at the Fruit Experiment 

station (OVB) in Jork, Germany.

Introduction to Fungi 

JohnWebster 

University of Exeter 

and 

Roland Weber 

University of Kaiserslautern 

Third Edition

CAMBRIDGE UNIVERSITY PRESS 

Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo 

Cambridge University Press 

The Edinburgh Building, Cambridge CB2 8RU, UK 

Published in the United States of America by Cambridge University Press, New York 

www.cambridge.org 

Information on this title: www.cambridge.org/9780521807395 

© J. Webster and R. W. S. Weber 2007 

This publication is in copyright. Subject to statutory exception and to the provision of 

relevant collective licensing agreements, no reproduction of any part may take place 

without the written permission of Cambridge University Press. 

First published in print format 

2007 

ISBN-13 978-0-511-27783-2 eBook (EBL) 

ISBN-10 0-511-27783-0 eBook (EBL) 

ISBN-13 978-0-521-80739-5 hardback 

ISBN-10 0-521-80739-5 hardback 

ISBN-13 978-0-521-01483-0 paperback 

ISBN-10 0-521-01483-2 paperback 

Cambridge University Press has no responsibility for the persistence or accuracy of urls 

for external or third-party internet websites referred to in this publication, and does not 

guarantee that any content on such websites is, or will remain, accurate or appropriate.

To Philip M. Booth

Contents 

Preface to the first edition 

Preface to the second edition 

Preface to the third edition 

Acknowledgements 

page xiii 

xv 

xvii 

xix 

Chapter 1 Introduction 1 

1.1 What are fungi? 1 

1.2 Physiology of the growing hypha 3 

1.3 Hyphal aggregates 14 

1.4 Spores of fungi 22 

1.5 Taxonomy of fungi 32 

Chapter 2 Protozoa: Myxomycota (slime moulds) 40 

2.1 Introduction 40 

2.2 Acrasiomycetes: acrasid cellular slime moulds 40 

2.3 Dictyosteliomycetes: dictyostelid slime moulds 41 

2.4 Protosteliomycetes: protostelid plasmodial 

slime moulds 45 

2.5 Myxomycetes: true (plasmodial) slime moulds 47 

Chapter 3 Protozoa: Plasmodiophoromycota 54 


3.2 Plasmodiophorales 54 

3.3 Control of diseases caused by Plasmodiophorales 62 

3.4 Haptoglossa (Haptoglossales) 64 

Chapter 4 Straminipila: minor fungal phyla 67 


4.2 The straminipilous flagellum 68 

4.3 Hyphochytriomycota 70 

4.4 Labyrinthulomycota 71 

Chapter 5 Straminipila: Oomycota 75 


5.2 Saprolegniales 79 

5.3 Pythiales 95 

5.4 Peronosporales 115 

5.5 Sclerosporaceae 125

viii 

CONTENTS 

Chapter 6 Chytridiomycota 127 


6.2 Chytridiales 134 

6.3 Spizellomycetales 145 

6.4 Neocallimastigales (rumen fungi) 150 

6.5 Blastocladiales 153 

6.6 Monoblepharidales 162 

Chapter 7 Zygomycota 165 


7.2 Zygomycetes: Mucorales 165 

7.3 Examples of Mucorales 180 

7.4 Zoopagales 200 

7.5 Entomophthorales 202 

7.6 Glomales 217 

7.7 Trichomycetes 222 

Chapter 8 Ascomycota (ascomycetes) 226 


8.2 Vegetative structures 226 

8.3 Life cycles of ascomycetes 228 

8.4 Conidia of ascomycetes 230 

8.5 Conidium production in ascomycetes 231 

8.6 Development of asci 236 

8.7 Types of fruit body 245 

8.8 Fossil ascomycetes 246 

8.9 Scientific and economic significance 

of ascomycetes 246 

8.10 Classification 247 

Chapter 9 Archiascomycetes 250 


9.2 Taphrinales 251 

9.3 Schizosaccharomycetales 253 

9.4 Pneumocystis 259 

Chapter 10 Hemiascomycetes 261 


10.2 Saccharomyces (Saccharomycetaceae) 263 

10.3 Candida (anamorphic Saccharomycetales) 276 

10.4 Pichia (Saccharomycetaceae) 281 

10.5 Galactomyces (Dipodascaceae) 281 

10.6 Saccharomycopsis (Saccharomycopsidaceae) 282 

10.7 Eremothecium (Eremotheciaceae) 284

CONTENTS 

ix 

Chapter 11 Plectomycetes 285 


11.2 Ascosphaerales 286 

11.3 Onygenales 289 

11.4 Eurotiales 297 

Chapter 12 Hymenoascomycetes: Pyrenomycetes 315 


12.2 Sordariales 315 

12.3 Xylariales 332 

12.4 Hypocreales 337 

12.5 Clavicipitales 348 

12.6 Ophiostomatales 364 

12.7 Microascales 368 

12.8 Diaporthales 373 

12.9 Magnaporthaceae 377 

12.10 Glomerellaceae 386 

Chapter 13 Hymenoascomycetes: Erysiphales 390 


13.2 Phylogenetic aspects 392 

13.3 Blumeria graminis 393 

13.4 Erysiphe 401 

13.5 Podosphaera and Sphaerotheca 404 

13.6 Sawadaea 405 

13.7 Phyllactinia and Leveillula 405 

13.8 Control of powdery mildew diseases 408 

Chapter 14 

Hymenoascomycetes: Pezizales 

(operculate discomycetes) 414 


14.2 Pyronema (Pyronemataceae) 415 

14.3 Aleuria (Pyronemataceae) 417 

14.4 Peziza (Pezizaceae) 419 

14.5 Ascobolus (Ascobolaceae) 419 

14.6 Helvella (Helvellaceae) 423 

14.7 Tuber (Tuberaceae) 423 

14.8 Morchella (Morchellaceae) 427 

Chapter 15 

Hymenoascomycetes: Helotiales 

(inoperculate discomycetes) 429 


15.2 Sclerotiniaceae 429 

15.3 Dermateaceae 439

x 

CONTENTS 

15.4 Rhytismataceae 440 

15.5 Other representatives of the Helotiales 442 

Chapter 16 

Lichenized fungi (chiefly 

Hymenoascomycetes: Lecanorales) 446 


16.2 General aspects of lichen biology 447 

16.3 Lecanorales 455 

Chapter 17 Loculoascomycetes 459 


17.2 Pleosporales 460 

17.3 Dothideales 480 

Chapter 18 Basidiomycota 487 


18.2 Basidium morphology 487 

18.3 Development of basidia 488 

18.4 Basidiospore development 490 

18.5 The mechanism of basidiospore discharge 493 

18.6 Numbers of basidiospores 495 

18.7 Basidiospore germination and hyphal growth 496 

18.8 Asexual reproduction 501 

18.9 Mating systems in basidiomycetes 506 

18.10 Fungal individualism: vegetative incompatibility 

between dikaryons 510 

18.11 Relationships 511 

18.12 Classification 512 

Chapter 19 Homobasidiomycetes 514 


19.2 Structure and morphogenesis of basidiocarps 517 

19.3 Importance of homobasidiomycetes 525 

19.4 Euagarics clade 532 

19.5 Boletoid clade 555 

19.6 Polyporoid clade 560 

19.7 Russuloid clade 566 

19.8 Thelephoroid clade 572 

19.9 Hymenochaetoid clade 573 

19.10 Cantharelloid clade 574 

19.11 Gomphoid phalloid clade 575 

Chapter 20 Homobasidiomycetes: gasteromycetes 577 


20.2 Evolution and phylogeny of gasteromycetes 578

CONTENTS 

xi 

20.3 Gasteromycetes in the euagarics clade 581 

20.4 Gasteromycetes in the boletoid clade 585 

20.5 Gasteromycetes in the gomphoid phalloid clade 588 

Chapter 21 Heterobasidiomycetes 593 


21.2 Ceratobasidiales 594 

21.3 Dacrymycetales 598 

21.4 Auriculariales 601 

21.5 Tremellales 604 

Chapter 22 Urediniomycetes: Uredinales (rust fungi) 609 

22.1 Urediniomycetes 609 

22.2 Uredinales: the rust fungi 609 

22.3 Puccinia graminis, the cause of black stem rust 620 

22.4 Other cereal rusts 627 

22.5 Puccinia and Uromyces 629 

22.6 Other members of the Pucciniaceae 631 

22.7 Melampsoraceae 634 

Chapter 23 

Ustilaginomycetes: smut fungi and 

their allies 636 

23.1 Ustilaginomycetes 636 

23.2 The ‘true’ smut fungi (Ustilaginomycetes) 636 

23.3 Microbotryales (Urediniomycetes) 652 

23.4 Exobasidiales (Ustilaginomycetes) 655 

Chapter 24 Basidiomycete yeasts 658 


24.2 Heterobasidiomycete yeasts 660 

24.3 Urediniomycete yeasts 666 

24.4 Ustilaginomycete yeasts 670 

Chapter 25 

Anamorphic fungi (nematophagous and 

aquatic forms) 673 

25.1 Nematophagous fungi 673 

25.2 Aquatic hyphomycetes (Ingoldian fungi) 685 

25.3 Aero-aquatic fungi 696 

References 702 

Index 817 

Colour plate section appears between pages 412 and 413

Preface to the first edition 

There are several available good textbooks of 

mycology, and some justification is needed for 

publishing another. I have long been convinced 

that the best way to teach mycology, and indeed 

all biology, is to make use, wherever possible, of 

living material. Fortunately with fungi, provided 

one chooses the right time of the year, a wealth 

of material is readily available. Also by use 

of cultures and by infecting material of plant 

pathogens in the glasshouse or by maintaining 

pathological plots in the garden, it is possible to 

produce material at almost any time. I have 

therefore tried to write an introduction to fungi 

which are easily available in the living state, and 

have tried to give some indication of where they 

can be obtained. In this way I hope to encourage 

students to go into the field and look for fungi 

themselves. The best way to begin is to go with 

an expert, or to attend a Fungus Foray such 

as those organized in the spring and autumn 

by mycological and biological societies. I owe 

much of my own mycological education to such 

friendly gatherings. A second aim has been to 

produce original illustrations of the kind that a 

student could make for himself from simple 

preparations of living material, and to illustrate 

things which he can verify for himself. For this 

reason I have chosen not to use electron micrographs, 

but to make drawings based on them. 

The problem of what to include has been 

decided on the criterion of ready availability. 

Where an uncommon fungus has been included 

this is because it has been used to establish some 

important fact or principle. A criticism which I 

must accept is that no attempt has been made to 

deal with Fungi Imperfecti as a group. This is not 

because they are not common or important but 

that to have included them would have made the 

book much longer. To mitigate this shortcoming 

I have described the conidial states of some 

Ascomycotina rather fully, to include reference 

to some of the form-genera which have been 

linked with them. A more difficult problem has 

been to know which system of classification to 

adopt. I have finally chosen the ‘General Purpose 

Classification’ proposed by Ainsworth, which is 

adequate for the purpose of providing a framework 

of reference. I recognize that some might 

wish to classify fungi differently, but see no great 

merit in burdening the student with the arguments 

in favour of this or that system. 

Because the evidence for the evolutionary 

origins of fungi is so meagre I have made only 

scant reference to the speculations which have 

been made on this topic. There are so many 

observations which can be verified, and for this 

reason I have preferred to leave aside those 

which never will. 

The literature on fungi is enormous, and 

expanding rapidly. Many undergraduates do not 

have much time to check original publications. 

However, since the book is intended as an 

introduction I have tried to give references to 

some of the more recent literature, and at the 

same time to quote the origins of some of the 

statements made. 

Exeter, 27 April 1970 

J.W.

Preface to the second edition 

In revising the first edition, which was first 

published about ten years ago, I have taken the 

opportunity to give a more complete account 

of the Myxomycota, and to give a more general 

introduction to the Eumycota. An account 

has also been given of some conidial fungi, 

as exemplified by aquatic Fungi Imperfecti, 

nematophagous fungi and seed-borne fungi. 

The taxonomic framework has been based on 

Volumes IVA and IVB of Ainsworth, Sparrow 

and Sussman’s The Fungi: An Advanced Treatise 

(Academic Press, 1973). 

Exeter, January 1979 

J.W.

Preface to the third edition 

Major advances, especially in DNA-based technology, 

have catalysed a sheer explosion of mycological 

knowledge since the second edition of 

Introduction to Fungi was published some 

25 years ago. As judged by numbers of publications, 

the field of molecular phylogeny, i.e. the 

computer-aided comparison of homologous DNA 

or protein sequences, must be at the epicentre of 

these developments. As a result, information is 

now available to facilitate the establishment of 

taxonomic relationships between organisms or 

groups of organisms on a firmer basis than that 

previously assumed from morphological resemblance. 

This has in turn led to revised systems of 

classification and provided evidence on which to 

base opinions on the possible evolutionary origin 

of fungal groups. We have attempted to reflect 

some of these advances in this edition. In general 

we have followed the outline system of classification 

set out in The Mycota Volume VII (Springer- 

Verlag) and the Dictionary of the Fungi (ninth 

edition, CABI Publishing). However, the main 

emphasis of our book remains that of presenting 

the fungi in a sensible biological context which 

can be understood by students, and therefore 

some fungi have been treated along with 

taxonomically separate groups if these share 

fundamental biological principles. Examples 

include Microbotryum, which is treated together 

with smut fungi rather than the rusts to which 

it belongs taxonomically, or Haptoglossa, which 

we discuss alongside Plasmodiophora rather than 

with the Oomycota. 

Molecular phylogeny has been instrumental 

in clarifying the relationships of anamorphic 

fungi (fungi imperfecti), presenting an opportunity 

to integrate their treatment with sexually 

reproducing relatives. There are only a few 

groups such as nematophagous fungi and the 

aquatic and aero-aquatic hyphomycetes which 

we continue to treat as ecological entities rather 

than scattered among ascomycetes and basidiomycetes. 

Similarly, the gasteromycetes, clearly 

an unnatural assemblage, are described together 

because of their unifying biological features. 

However, in all these cases taxonomic affinities 

are indicated where known. We have also 

included several groups now placed well outside 

the Fungi, such as the Oomycota (Straminipila) 

and Myxomycota and Plasmodiophoromycota 

(Protozoa). This is because of their biological 

and economic importance and because they have 

been and continue to be studied by mycologists. 

There have been major advances in other 

areas of research, notably the molecular cell 

biology of the two yeasts Saccharomyces and 

Schizosaccharomyces, ‘model organisms’ which 

have a bearing far beyond mycology. Further, 

much exciting progress is being made in elucidating 

the molecular aspects of the infection 

biology of human and plant pathogens, and in 

developing fungi for biotechnology. These trends 

are represented in the current edition. 

Nevertheless, the fundamental concept of 

Introduction to Fungi remains that of the previous 

two editions: to place an organism in its 

taxonomic context while discussing as many 

relevant aspects of its biology as possible in a 

holistic manner. Many of the illustrations are 

based on original line drawings because we 

believe that these can readily portray an understanding 

of structure and that drawing as a 

record of interpretation is a good discipline. 

However, we have also extended the use of 

photographs, and we now provide illustrated 

life cycles because these are more easily understood. 

As before, our choice of illustrated species 

has been influenced by the ready availability of 

material, enabling students and their teachers 

to examine living fungi, which is a cornerstone 

of good teaching. At their first introduction most 

technical terms have been printed in bold, their 

meanings explained and their derivations given. 

The page numbers where these definitions are 

given have been highlighted in the index. 

The discipline of mycology has evolved and 

diversified so enormously in recent decades that 

it is now a daunting task for individual authors 

to give a balanced, integrated account of the 

fungi. Of course, there will be omissions or

xviii 

PREFACE TO THE THIRD EDITION 

misrepresentations in a work of this scale, and 

we offer our apologies to those who feel that 

their work or that of others has not been 

adequately covered. At the same time, it has 

been a fascinating experience for us to write this 

book, and we have thoroughly enjoyed the 

immense diversity of approaches and ideas 

which make mycology such a vibrant discipline 

at present. We hope to have conveyed some of its 

fascination to the reader in the text and by 

referring to as many original publications as 

possible. 

Exeter and Kaiserslautern, 1 March 2006 

J.W. and R.W.S.W.

Acknowledgements 

We are indebted to many people who have 

helped us in our extensive revisions to Introduction 

to Fungi. This edition is dedicated to Mr Philip M. 

Booth in profound gratitude for his financial 

support and his encouragement over many years. 

We have acknowledged in the figure legends 

the many friends and colleagues who have 

responded so enthusiastically to our call for 

help by providing us with illustrations, sometimes 

previously unpublished, and we thank 

numerous publishing houses for permission to 

include published figures. We thank Caroline 

Huxtable and Rob Ford (Exeter University 

Library) and Jennifer Mergel and Petra Tremmel 

(Kaiserslautern University Library) for help 

beyond the call of duty in obtaining interlibrary 

loans. Dr Wolf-Rüdiger Arendholz and 

Dr Roger T.A. Cook have read the entire manuscript 

or parts of it, and their feedback and 

corrections have been most valuable to us. We are 

immensely grateful to Professors Heidrun and 

Timm Anke (Kaiserslautern) for their support of 

this project, their encouragement and for providing 

such a stimulating environment for research 

and teaching of fungal biology. 

By far the heaviest toll has been paid by our 

families and friends who have had only cursory 

sightings of us during the past six years. We owe 

a debt of gratitude to them for their patient 

forbearance and unwavering support.

1 

Introduction 

1.1 What are fungi? 

About 80 000 to 120 000 species of fungi have been 

described to date, although the total number of 

species is estimated at around 1.5 million 

(Hawksworth, 2001; Kirk et al., 2001). This would 

render fungi one of the least-explored biodiversity 

resources of our planet. It is notoriously difficult 

to delimit fungi as a group against other eukaryotes, 

and debates over the inclusion or exclusion 

of certain groups have been going on for well over 

a century. In recent years, the main arguments 

have been between taxonomists striving towards 

a phylogenetic definition based especially on the 

similarity of relevant DNA sequences, and others 

who take a biological approach to the subject and 

regard fungi as organisms sharing all or many key 

ecological or physiological characteristics the 

‘union of fungi’ (Barr, 1992). Being interested 

mainly in the way fungi function in nature and in 

the laboratory, we take the latter approach and 

include several groups in this book which are now 

known to have arisen independently of the monophyletic 

‘true fungi’ (Eumycota) and have been 

placed outside them in recent classification 

schemes (see Fig. 1.25). The most important 

of these ‘pseudofungi’ are the Oomycota 

(see Chapter 5). Based on their lifestyle, fungi 

may be circumscribed by the following set of 

characteristics (modified from Ainsworth, 1973): 

1. Nutrition. Heterotrophic (lacking photosynthesis), 

feeding by absorption rather than 

ingestion. 

2. Vegetative state. On or in the substratum, 

typically as a non-motile mycelium of 

hyphae showing internal protoplasmic 

streaming. Motile reproductive states may 

occur. 

3. Cell wall. Typically present, usually based on 

glucans and chitin, rarely on glucans and 

cellulose (Oomycota). 

4. Nuclear status. Eukaryotic, uni- or multinucleate, 

the thallus being homo- or heterokaryotic, 

haploid, dikaryotic or diploid, the 

latter usually of short duration (but exceptions 

are known from several taxonomic 

groups). 

5. Life cycle. Simple or, more usually, complex. 

6. Reproduction. The following reproductive 

events may occur: sexual (i.e. nuclear 

fusion and meiosis) and/or parasexual 

(i.e. involving nuclear fusion followed by 

gradual de-diploidization) and/or asexual 

(i.e. purely mitotic nuclear division). 

7. Propagules. These are typically microscopically 

small spores produced in high numbers. 

Motile spores are confined to certain 

groups. 

8. Sporocarps. Microscopic or macroscopic and 

showing characteristic shapes but only 

limited tissue differentiation. 

9. Habitat. Ubiquitous in terrestrial and freshwater 

habitats, less so in the marine 

environment. 

10. Ecology. Important ecological roles as saprotrophs, 

mutualistic symbionts, parasites, or 

hyperparasites. 

11. Distribution. Cosmopolitan.

2 INTRODUCTION 

With photosynthetic pigments being absent, 

fungi have a heterotrophic mode of nutrition. 

In contrast to animals which typically feed by 

ingestion, fungi obtain their nutrients by extracellular 

digestion due to the activity of secreted 

enzymes, followed by absorption of the solubilized 

breakdown products. The combination of 

extracellular digestion and absorption can be 

seen as the ultimate determinant of the fungal 

lifestyle. In the course of evolution, fungi have 

conquered an astonishingly wide range of habitats, 

fulfilling important roles in diverse ecosystems 

(Dix & Webster, 1995). The conquest of new, 

often patchy resources is greatly facilitated by 

the production of numerous small spores rather 

than a few large propagules, whereas the 

colonization of a food source, once reached, is 

achieved most efficiently by growth as a system 

of branching tubes, the hyphae (Figs. 1.1a,b), 

which together make up the mycelium. 

Hyphae are generally quite uniform in different 

taxonomic groups of fungi. One of the few 

features of distinction that they do offer is the 

presence or absence of cross-walls or septa. The 

Oomycota and Zygomycota generally have aseptate 

hyphae in which the nuclei lie in a common 

mass of cytoplasm (Fig. 1.1a). Such a condition is 

described as coenocytic (Gr. koinos ¼ shared, in 

common; kytos ¼ a hollow vessel, here meaning 

cell). In contrast, Asco- and Basidiomycota and 

their associated asexual states generally have 

septate hyphae (Fig. 1.1b) in which each segment 

contains one, two or more nuclei. If the nuclei 

are genetically identical, as in a mycelium 

derived from a single uninucleate spore, the 

mycelium is said to be homokaryotic, but where 

Fig1.1 Various growth forms of fungi. (a) Aseptate hypha of Mucor mucedo (Zygomycota).The hypha branches to form a mycelium. 

(b) Septate branched hypha of Trichoderma viride (Ascomycota). Septa are indicated by arrows. (c) Yeast cells of Schizosaccharomyces 

pombe (Ascomycota) dividing by binary fission. (d) Yeast cells of Dioszegia takashimae (Basidiomycota) dividing by budding. 

(e) Pseudohypha of Candida parapsilosis (Ascomycota), which is regarded as an intermediate stage between yeast cells and true 

hyphae. (f) Thallus of Rhizophlyctisrosea (Chytridiomycota) from which a system of branching rhizoids extends into the substrate. 

(g) Plasmodia of Plasmodiophora brassicae (Plasmodiophoromycota) inside cabbage root cells. Scale bar ¼ 20 mm(a,b,f,g)or 

10 mm(c e).

PHYSIOLOGYOF THE GROWING HYPHA 

3 

a cell or mycelium contains nuclei of different 

genotype, e.g. as a result of fusion (anastomosis) 

of genetically different hyphae, it is said to be 

heterokaryotic. A special condition is found in 

the mycelium of many Basidiomycota in which 

each cell contains two genetically distinct nuclei. 

This condition is dikaryotic, to distinguish it 

from mycelia which are monokaryotic. It should 

be noted that septa, where present, are usually 

perforated and allow for the exchange of 

cytoplasm or organelles. 

Not all fungi grow as hyphae. Some grow 

as discrete yeast cells which divide by fission 

(Fig. 1.1c) or, more frequently, budding (Fig. 1.1d). 

Yeasts are common, especially in situations 

where efficient penetration of the substratum 

is not required, e.g. on plant surfaces or in the 

digestive tracts of animals (Carlile, 1995). A few 

species, including certain pathogens of humans 

and animals, are dimorphic, i.e. capable of 

switching between hyphal and yeast-like growth 

forms (Gow, 1995). Intermediate stages between 

yeast cells and true hyphae also occur and are 

termed pseudohyphae (Fig. 1.1e). Some lower 

fungi grow as a thallus, i.e. a walled structure in 

which the protoplasm is concentrated in one or 

more centres from which root-like branches 

(rhizoids) ramify (Fig. 1.1f). Certain obligately 

plant-pathogenic fungi and fungus-like organisms 

grow as a naked plasmodium (Fig. 1.1g), 

a uni- or multinucleate mass of protoplasm 

not surrounded by a cell wall of its own, or as 

a pseudoplasmodium of amoeboid cells which 

retain their individual plasma membranes. 

However, by far the most important device 

which accounts for the typical biological features 

of fungi is the hypha (Bartnicki-Garcia, 1996), 

which therefore seems an appropriate starting 

point for an exploration of these organisms. 

1.2 Physiology of the 

growing hypha 

1.2.1 Polarity of the hypha 

By placing microscopic markers such as small 

glass beads beside a growing hypha, Reinhardt 

(1892) was able to show that cell wall extension, 

measured as an increase in the distance between 

two adjacent markers, occurred only at the 

extreme apex. Four years earlier, H. M. Ward 

(1888), in an equally simple experiment, had 

collected liquid droplets from the apex of hyphae 

of Botrytis cinerea and found that these ‘fermentdrops’ 

were capable of degrading plant cell walls. 

Thus, the two fundamental properties of the vegetative 

fungal hypha the polarity of both growth 

and secretion of degradative enzymes have 

been known for over a century. Numerous studies 

have subsequently confirmed that ‘the key to the 

fungal hypha lies in the apex’ (Robertson, 1965), 

although the detailed mechanisms determining 

hyphal polarity are still obscure. 

Ultrastructural studies have shown that many 

organelles within the growing hyphal tip are 

distributed in steep gradients, as would be 

expected of a cell growing in a polarized 

mode (Girbardt, 1969; Howard, 1981). This 

is visible even with the light microscope by 

careful observation of an unstained hypha using 

phase-contrast optics (Reynaga-Peña et al., 1997), 

and more so with the aid of simple staining 

techniques (Figs. 1.2a d). The cytoplasm of 

the extreme apex is occupied almost exclusively 

by secretory vesicles and microvesicles 

(Figs. 1.2a, 1.3). In the higher fungi (Asco- and 

Basidiomycota), the former are arranged as a 

spherical shell around the latter, and the 

entire formation is called the Spitzenkörper or 

‘apical body’ (Fig. 1.4c; Bartnicki-Garcia, 1996). 

The Spitzenkörper may be seen in growing 

hyphae even with the light microscope. Hyphae 

of the Oomycota and some lower Eumycota 

(notably the Zygomycota) do not contain a 

recognizable Spitzenkörper, and the vesicles are 

instead distributed more loosely in the apical 

dome (Fig. 1.4a,b). Hyphal growth can be simulated 

by means of computer models based on the 

assumption that the emission of secretory vesicles 

is coordinated by a ‘vesicle supply centre’, 

regarded as the mathematical equivalent of the 

Spitzenkörper in higher fungi. By modifying 

certain parameters, it is even possible 

to generate the somewhat more pointed apex 

often found in hyphae of Oomycota and 

Zygomycota (Figs. 1.4a,b; Diéguez-Uribeondo 

et al., 2004).


Fig1.3 Transmission electron microscopy of a hyphal tip of 

Fusarium acuminatum preserved by the freeze-substitution 

method to reveal ultrastructural details.The vesicles of the 

Spitzenko«rper as well as mitochondria (dark elongated 

organelles), a Golgi-like element (G) and microtubules 

(arrows) are visible. Microtubules are closely associated with 

mitochondria. Reproduced from Howard and Aist (1980), by 

copyright permission of The Rockefeller University Press. 

Fig1.2 The organization of vegetative hyphae as seen by light microscopy. (a) Growing hypha of Galactomyces candidus showing the 

transition from dense apical to vacuolate basal cytoplasm.Tubular vacuolar continuities are also visible. (b e) Histochemistry in 

Botrytiscinerea. (b) Tetrazolium staining for mitochondrial succinate dehydrogenase.The mitochondria appear as dark filamentous 

structures in subapical and maturing regions. (c) Staining of the same hypha for nuclei with the fluorescent DNA-binding dye DAPI. 

The apical cell contains numerous nuclei. (d) Staining of acid phosphatase activity using the Gomori lead-salt method with a fixed 

hypha. Enzyme activity is localized both in the secretory vesicles forming the Spitzenko«rper, and in vacuoles. (e) Uptake of Neutral 

Red into vacuoles in a mature hyphal segment. All images to same scale.


5 

Fig1.4 Schematic drawings of the arrangement of vesicles 

in growing hyphal tips. Secretory vesicles are visible in all 

hyphal tips, but the smaller microvesicles (chitosomes) are 

prominent only in Asco- and Basidiomycota and contribute 

to the Spitzenko«rper morphology of the vesicle cluster. 

(a) Oomycota. (b) Zygomycota. (c) Ascomycota and 

Basidiomycota. 

A little behind the apical dome, a region of 

intense biosynthetic activity and energy generation 

is indicated by parallel sheets of endoplasmic 

reticulum and an abundance of 

mitochondria (Figs. 1.2b, 1.3). The first nuclei 

usually appear just behind the biosynthetic zone 

(Fig. 1.2c), followed ultimately by a system of 

ever-enlarging vacuoles (Fig. 1.2d). These may fill 

almost the entire volume of mature hyphal 

regions, making them appear empty when 

viewed with the light microscope. 

1.2.2 Architecture of the fungal cell wall 

Although the chemical composition of cell walls 

can vary considerably between and within 

different groups of fungi (Table 1.1), the basic 

design seems to be universal. It consists of 

a structural scaffold of fibres which are crosslinked, 

and a matrix of gel-like or crystalline 

material (Hunsley & Burnett, 1970; Ruiz-Herrera, 

1992; Sentandreu et al., 1994). The degree of 

cross-linking will determine the plasticity (extensibility) 

of the wall, whereas the pore size 

(permeability) is a property of the wall matrix. 

The scaffold forms the inner layer of the wall and 

the matrix is found predominantly in the outer 

layer (de Nobel et al., 2001). 

In the Ascomycota and Basidiomycota, the 

fibres are chitin microfibrils, i.e. bundles of 

linear b-(1,4)-linked N-acetylglucosamine chains 

(Fig. 1.5), which are synthesized at the plasma 

membrane and extruded into the growing 

(‘nascent’) cell wall around the apical dome. 

The cell wall becomes rigid only after the 

microfibrils have been fixed in place by crosslinking. 

These cross-links consist of highly 

branched glucans (glucose polymers), especially 

those in which the glucose moieties are linked by 

b-(1,3)- and b-(1,6)-bonds (Suarit et al., 1988; 

Wessels et al., 1990; Sietsma & Wessels, 1994). 

Such b-glucans are typically insoluble in alkaline 

solutions (1 M KOH). In contrast, the alkalisoluble 

glucan fraction contains mainly a-(1,3)- 

and/or a-(1,4)-linked branched or unbranched 

chains (Wessels et al., 1972; Bobbitt & Nordin, 

1982) and does not perform a structural role 

but instead contributes significantly to the 

cell wall matrix (Sietsma & Wessels, 1994). 

Proteins represent the third important chemical 

Table 1.1. The chemical composition of cell walls of selected groups of fungi (dry weight of total cell wall 

fraction, in per cent). Data adapted from Ruiz-Herrera (1992) and Griffin (1994). 

Group Example Chitin Cellulose Glucans Protein Lipid 

Oomycota Phytophthora 0 25 65 4 2 

Chytridiomycota Allomyces 58 0 16 10 ? 

Zygomycota Mucor 9 0 44 6 8 

Ascomycota Saccharomyces 1 0 60 13 8 

Fusarium 39 0 29 7 6 

Basidiomycota Schizophyllum 5 0 81 2 ? 

Coprinus 33 0 50 10 ? 

Mainly chitosan.


Fig1.5 Structural formulae of the principal fibrous 

components of fungal cell walls. 

constituent of fungal cell walls. In addition to 

enzymes involved in cell wall synthesis or lysis, 

or in extracellular digestion, there are also 

structural proteins. Many cell wall proteins are 

modified by glycosylation, i.e. the attachment of 

oligosaccharide chains to the polypeptide. The 

degree of glycosylation can be very high, especially 

in the yeast Saccharomyces cerevisiae, where 

up to 90% of the molecular weight of an 

extracellular protein may be contributed by its 

glycosylation chains (van Rinsum et al., 1991). 

Since mannose is the main component, such 

proteins are often called mannoproteins or 

mannans. In S. cerevisiae, the pore size of the 

cell wall is determined not by matrix glucans but 

by mannoproteins located close to the external 

wall surface (Zlotnik et al., 1984). Proteins 

exposed at the cell wall surface can also 

determine surface properties such as adhesion 

and recognition (Cormack et al., 1999). Structural 

proteins often contain a glycosylphosphatidylinositol 

anchor by which they are attached to the 

lumen of the rough endoplasmic reticulum (ER) 

and later to the external plasma membrane 

surface, or a modified anchor which covalently 

binds them to the b-(1,6)-glucan fraction of the 

cell wall (Kollár et al., 1997; de Nobel et al., 2001). 

In the Zygomycota, the chitin fibres are 

modified after their synthesis by partial or 

complete deacetylation to produce poly-b-(1,4)- 

glucosamine, which is called chitosan (Fig. 1.5) 

(Calvo-Mendez & Ruiz-Herrera, 1987). Chitosan 

fibres are cross-linked by polysaccharides containing 

glucuronic acid and various neutral 

sugars (Datema et al., 1977). The cell wall 

matrix comprises glucans and proteins, as it 

does in members of the other fungal groups. 

One traditional feature to distinguish the 

Oomycota from the ‘true fungi’ (Eumycota) has 

been the absence of chitin from their cell walls 

(Wessels & Sietsma, 1981), even though chitin is 

now known to be produced by certain species of 

Oomycota under certain conditions (Gay et al., 

1993). By and large, however, in Oomycota, the 

structural role of chitin is filled by cellulose, an 

aggregate of linear b-(1,4)-glucan chains (Fig. 1.5). 

As in many other fungi, the fibres thus produced 

are cross-linked by an alkali-insoluble glucan 

containing b-(1,3)- and b-(1,6)-linkages. In addition 

to proteins, the main matrix component 

appears to be an alkali-soluble b-(1,3)-glucan 

(Wessels & Sietsma, 1981). 

1.2.3 Synthesis of the cell wall 

The synthesis of chitin is mediated by specialized 

organelles termed chitosomes (Bartnicki- 

Garcia et al., 1979; Sentandreu et al., 1994) in 

which inactive chitin synthases are delivered to 

the apical plasma membrane and become activated 

upon contact with the lipid bilayer 

(Montgomery & Gooday, 1985). Microvesicles, 

visible especially in the core region of the 

Spitzenkörper, are likely to be the ultrastructural 

manifestation of chitosomes (Fig. 1.6). In 

contrast, structural proteins and enzymes travel 

together in the larger secretory vesicles and 

are discharged into the environment when 

the vesicles fuse with the plasma membrane


7 

Fig1.6 The Spitzenko«rper of Botrytis cinerea which is 

differentiated into an electron-dense core consisting of 

microvesicles (chitosomes) and an outer region made up of 

larger secretory vesicles, some of which are located close 

to the plasma membrane. Reprinted from Weber and Pitt 

(2001), with permission from Elsevier. 

(Fig. 1.6). Whereas most proteins are fully 

functional by the time they traverse the plasma 

membrane (see p. 10), the glucans are secreted by 

secretory vesicles as partly formed precursors 

(Wessels, 1993a) and undergo further polymerization 

in the nascent cell wall, or they are 

synthesized entirely at the plasma membrane 

(Sentandreu et al., 1994; de Nobel et al., 2001). 

Cross-linking of glucans with other components 

of the cell wall takes place after extrusion into 

the cell wall (Kollár et al., 1997; de Nobel et al., 

2001). 

Wessels et al. (1990) have provided experimental 

evidence to support a model for 

cell wall synthesis in Schizophyllum commune 

(Basidiomycota). The individual linear b-(1,4)-Nacetylglucosamine 

chains extruded from the 

plasma membrane are capable of undergoing 

self-assembly into chitin microfibrils, but this is 

subject to a certain delay during which crosslinking 

with glucans must occur. The glucans, 

in turn, become alkali-insoluble only after they 

have become covalently linked to chitin. Once 

the structural scaffold is in place, the wall matrix 

can be assembled. Wessels (1997) suggested that 

hyphal growth occurs as the result of a continuously 

replenished supply of soft wall material at 

the apex, but there is good evidence that the 

softness of the apical cell wall is also influenced 

by the activity of wall-lytic enzymes such as 

chitinases or glucanases (Fontaine et al., 1997; 

Horsch et al., 1997). Further, when certain 

Oomycota grow under conditions of hyperosmotic 

stress, their cell wall is measurably softer 

due to the secretion of an endo-b-(1,4)-glucanase, 

thus permitting continued growth when the 

turgor pressure is reduced or even absent 

(Money, 1994; Money & Hill, 1997). Since, in 

higher Eumycota, both cell wall material and 

synthetic as well as lytic enzymes are secreted 

together by the vesicles of the Spitzenkörper, 

the appearance, position and movement of 

this structure should influence the direction 

and speed of apical growth directly. This has 

indeed been shown to be the case (López-Franco 

et al., 1995; Bartnicki-Garcia, 1996; Riquelme 

et al., 1998). 

Of course, cell wall-lytic enzymes are also 

necessary for the formation of hyphal branches, 

which usually arise by a localized weakening of 

the mature, fully polymerized cell wall. An 

endo-b-(1,4)-glucanase has also been shown to be 

involved in softening the mature regions of 

hyphae in the growing stipes of Coprinus fruit 

bodies, thus permitting intercalary hyphal 

extension (Kamada, 1994). Indeed, the expansion


of mushroom-type fruit bodies in general seems 

to be based mainly on non-apical extension 

of existing hyphae (see p. 22), which is a 

rare exception to the rule of apical growth in 

fungi. 

The properties of the cell wall depend in 

many ways on the environment in which the 

hypha grows. Thus, when Schizophyllum commune 

is grown in liquid submerged culture, a significant 

part of the b-glucan fraction may diffuse 

into the liquid medium before it is captured by 

the cell wall, giving rise to mucilage (Sietsma 

et al., 1977). In addition to causing problems 

when growing fungi in liquid culture for experimental 

purposes, mucilage may cause economic 

losses when released by Botrytis cinerea in grapes 

to be used for wine production (Dubourdieu 

et al., 1978a). On the other hand, secreted 

polysaccharides, especially of Basidiomycota, 

may have interesting medicinal properties and 

are being promoted as anti-tumour medication 

both in conventional and in alternative medicine 

(Wasser, 2002). 

Another difference between submerged and 

aerial hyphae is caused by the hydrophobins, 

which are structural cell wall proteins with 

specialized functions in physiology, morphogenesis 

and pathology (Wessels, 2000). Some hydrophobins 

are constitutively secreted by the hyphal 

apex. In submerged culture, they diffuse into the 

medium as monomers, whereas they polymerize 

by hydrophobic interactions on the surface 

of hyphae exposed to air, thereby effectively 

impregnating them and rendering them 

hydrophobic (Wessels, 1997, 2000). When freezefractured 

hydrophobic surfaces of hyphae or 

spores are viewed with the transmission electron 

microscope, polymerized hydrophobins may be 

visible as patches of rodlets running in parallel 

to each other. Other hydrophobins are produced 

only at particular developmental stages and are 

involved in inducing morphogenetic changes of 

the hypha, leading, for example, to the formation 

of spores or infection structures, or aggregation 

of hyphae into fruit bodies (Stringer et al., 

1991; Wessels, 1997). 

Some fungi are wall-less during the assimilative 

stage of their life cycle. This is true especially 

of certain plant pathogens such as the 

Plasmodiophoromycota (Chapter 3), insect pathogens 

(Entomophthorales; p. 202) and some 

members of the Chytridiomycota (Chapter 6). 

Since their protoplasts are in direct contact 

with the host cytoplasm, they are buffered 

against osmotic fluctuations. The motile spores 

(zoospores) of certain groups of fungi swim freely 

in water, and bursting due to osmotic inward 

movement of water is prevented by the constant 

activity of water-expulsion vacuoles. 

1.2.4 The cytoskeleton 

In contrast to the hyphae of certain Oomycota, 

which seem to grow even in the absence of 

measurable turgor pressure (Money & Hill, 1997), 

the hyphae of most fungi extend only when a 

threshold turgor pressure is exceeded. This can 

be generated even at a reduced external water 

potential by the accumulation of compatible 

solutes such as glycerol, mannitol or trehalose 

inside the hypha (Jennings, 1995). The correlation 

between turgor pressure and hyphal growth 

might be interpreted such that the former drives 

the latter, but this crude mechanism would lead 

to uncontrolled tip extension or even tip bursting. 

Further, when hyphal tips are made to burst 

by experimental manipulation, they often do 

so not at the extreme apex, but a little further 

behind (Sietsma & Wessels, 1994). It seems, 

therefore, that the soft wall at the apex is protected 

internally, and there is now good evidence 

that this is mediated by the cytoskeleton. 

Both main elements of the cytoskeleton, 

i.e. microtobules (Figs. 1.7a,b) and actin filaments 

(Fig. 1.7c), are abundant in filamentous fungi and 

yeasts (Heath, 1994, 1995a). Intermediate filaments, 

which fulfil skeletal roles in animal cells, 

are probably of lesser significance in fungi. 

Microtubules are typically orientated longitudinally 

relative to the hypha (Fig. 1.7a) and are 

involved in long-distance transport of organelles 

such as secretory vesicles (Fig. 1.7b; Seiler et al., 

1997) or nuclei (Steinberg, 1998), and in the 

positioning of mitochondria, nuclei or vacuoles 

(Howard & Aist, 1977; Steinberg et al., 1998). They 

therefore maintain the polarized distribution of 

many organelles in the hyphal tip.


9 

Fig1.7 The cytoskeleton in fungi. (a) Microtubules in Rhizoctonia solani (Basidiomycota) stained with an a-tubulin antibody. 

(b) Secretory vesicles (arrowheads) associated with a microtubule in Botrytis cinerea (Ascomycota). (c) The actin system of 

Saprolegnia ferax (Oomycota) stained with phalloidin rhodamine. Note the dense actin cap in growing hyphal tips. (a) reproduced 

from Bourett et al. (1998), with permission from Elsevier; original print kindly provided by R. J.Howard. (b) reproduced fromWeber 

and Pitt (2001), with permission from Elsevier. (c) reproduced from I.B. Heath (1987), by copyright permission of Wissenschaftliche 

Verlagsgesellschaft mbH, Stuttgart; original print kindly provided by I.B. Heath. 

Actin filaments are found in the centre of the 

Spitzenkörper, as discrete subapical patches, and 

as a cap lining the inside of the extreme hyphal 

apex (Heath, 1995a; Czymmek et al., 1996; 

Srinivasan et al., 1996). The apical actin cap is 

particularly pronounced in Oomycota such as 

Saprolegnia (Fig. 1.7c), and it now seems that the 

soft wall at the hyphal apex is actually being 

assembled on an internal scaffold consisting of 

actin and other structural proteins, such as 

spectrin (Heath, 1995b; Degousée et al., 2000). 

The rate of hyphal extension might be 

controlled, and bursting prevented, by the 

actin/spectrin cap being anchored to the rigid, 

subapical wall via rivet-like integrin attachments 

which traverse the membrane and might bind to 

wall matrix proteins (Fig. 1.8; Kaminskyj & 

Heath, 1996; Heath, 2001). Indeed, in Saprolegnia 

the cytoskeleton is probably responsible for 

pushing the hyphal tip forward, at least in the 

absence of turgor (Money, 1997), although it 

probably has a restraining function under 

normal physiological conditions. Heath (1995b) 

has proposed an ingenious if speculative model 

to explain how the actin cap might regulate the 

rate of hyphal tip extension in the Oomycota. 

Stretch-activated channels selective for Ca 2þ ions 

are known to be concentrated in the apical 

plasma membrane of Saprolegnia (Garrill et al., 

1993), and the fact that Ca 2þ ions cause contractions 

of actin filaments is also well known. 

A stretched plasma membrane will admit Ca 2þ 

ions into the apical cytoplasm where they cause 

localized contractions of the actin cap, thereby 

reducing the rate of apical growth which leads to 

closure of the stretch-activated Ca 2þ channels. 

Sequestration of Ca 2þ by various subapical 

organelles such as the ER or vacuoles lowers 

the concentration of free cytoplasmic Ca 2þ , 

leading to a relaxation of the actin cap and of 

its restrictive effect on hyphal growth. 

In the Eumycota, there is only indirect 

evidence for a similar role of actin, integrin 

and other structural proteins in protecting the 

apex and restraining its extension (Degousée 

et al., 2000; Heath, 2001), and the details of


Fig1.8 Diagrammatic representation of the internal scaffold 

model of tip growth in fungi proposed by Heath (1995b). 

Secretory vesicles and chitosomes are transported along 

microtubules from their subapical sites of synthesis to the 

growing apex.The Spitzenko«rper forms around a cluster of 

actin filaments. An actin scaffold inside the extreme apex is 

linked to rivet-like integrin molecules which are anchored in 

the rigid subapical cell wall.The apex is further stabilized by 

spectrin molecules lining the cytoplasmic surface of the 

plasma membrane. Redrawn and modified from Weber and 

Pitt (2001). 

regulation are likely to be different. Whereas a 

tip-high Ca 2þ gradient is present and is required 

for growth, stretch-activated Ca 2þ channels 

are not, and the apical Ca 2þ seems to be 

of endogenous origin. Silverman-Gavrila and 

Lew (2001, 2002) have proposed that the signal 

molecule inositol-(1,4,5)-trisphosphate (IP 3 ), 

released by the action of a stretch-activated 

phospholipase C in the apical plasma membrane, 

acts on Ca 2þ -rich secretory vesicles in the 

Spitzenkörper region. These would release Ca 2þ 

from their lumen, leading to a contraction of the 

apical scaffold. As in the Oomycota, sequestration 

of Ca 2þ occurs subapically by the ER from 

which secretory vesicles are formed. These therefore 

act as Ca 2þ shuttles in the Eumycota 

(Torralba et al., 2001). Although hyphal tip 

growth appears to be a straightforward affair, 

none of the conflicting models accounts for 

all aspects of it. A good essay in hyphal tip 

diplomacy has been written by Bartnicki-Garcia 

(2002). 

Numerous inhibitor studies have hinted at 

a role of the cytoskeleton in the transport of 

vesicles to the apex. Depolymerization of 

microtubules results in a disappearance of the 

Spitzenkörper, termination or at least severe 

reduction of apical growth and enzyme secretion, 

and an even redistribution of secretory 

vesicles and other organelles throughout the 

hypha (Howard & Aist, 1977; Rupeš et al., 1995; 

Horio & Oakley, 2005). In contrast, actin depolymerization 

leads to uncontrolled tip extension 

to form giant spheres (Srinivasan et al., 1996). 

Long-distance transport of secretory vesicles 

therefore seems to be brought about by microtubules, 

whereas the fine-tuning of vesicle fusion 

with the plasma membrane is controlled by actin 

(Fig. 1.8; Torralba et al., 1998). The integrity of the 

Spitzenkörper is maintained by an interplay 

between actin and tubulin. Not surprisingly, 

the yeast S. cerevisiae, which has a very short 

vesicle transport distance between the mother 

cell and the extending bud, reacts more sensitively 

to disruptions of the actin component 

than the microtubule component of its cytoskeleton; 

continued growth in the absence of 

the latter can be explained by Brownian motion 

of secretory vesicles (Govindan et al., 1995; 

Steinberg, 1998). 

1.2.5 Secretion and membrane traffic 

One of the most important ecological roles of 

fungi, that of decomposing dead plant matter, 

requires the secretion of large quantities of 

hydrolytic and oxidative enzymes into the 

environment. In liquid culture under optimized 

experimental conditions, certain fungi


11 

are capable of secreting more than 20 g of a 

single enzyme or enzyme group per litre culture 

broth within a few days’ growth (Sprey, 1988; 

Peberdy, 1994). Clearly, this aspect of fungal 

physiology holds considerable potential for 

biotechnological or pharmaceutical applications. 

However, for reasons not yet entirely understood, 

fungi often fail to secrete the heterologous 

proteins of introduced genes of commercial 

interest to the same high level as their own 

proteins (Gwynne, 1992). There are still 

great deficits in our understanding of the 

fundamental mechanisms of the secretory 

route in filamentous fungi, although much is 

known in the yeast S. cerevisiae. An overview is 

given in Fig. 1.10. 

As in other eukaryotes, the secretory route in 

fungi begins in the ER. Ribosomes loaded with 

a suitable messenger RNA dock onto the 

ER membrane and translate the polypeptide 

product which enters the ER lumen during 

its synthesis unless specific internal signal 

sequences cause it to be retained in the ER 

membrane. As soon as the protein is in contact 

with the ER lumen, oligosaccharide chains may 

be added onto selected amino acids. These 

glycosylation chains are subject to successive 

modification steps as the protein traverses the 

secretory route, whereby the chains in S. cerevisiae 

become considerably larger than those in most 

filamentous fungi (Maras et al., 1997; Gemmill & 

Trimble, 1999). Paradoxically, even though filamentous 

fungi possess such powerful secretory 

systems, morphologically recognizable Golgi 

stacks have not generally been observed except 

for the Oomycota, Plasmodiophoromycota and 

related groups (Grove et al., 1968; Beakes & 

Glockling, 1998). In all other fungi, the Golgi 

apparatus seems to be much reduced to single 

cisternae (Howard, 1981; see Fig. 1.3), with 

images of fully fledged Golgi stacks only 

published occasionally (see e.g. Fig. 10.1). In 

S. cerevisiae and probably also in filamentous 

fungi, the transport of proteins from the ER 

to the Golgi system occurs via vesicular 

carriers (Schekman, 1992), although continuous 

membrane flow is also possible (see p. 272). 

Membrane lipids seem to be recycled to the ER 

by a different mechanism relying on tubular 

continuities (Rupeš et al., 1995; Akashi et al., 

1997). 

In the Golgi system, proteins are subjected to 

stepwise further modifications (Graham & Emr, 

1991), and proteins destined for the vacuolar 

system are separated from those bound for 

secretion (Seeger & Payne, 1992). Both destinations 

are probably reached by vesicular carriers, 

the secretory vesicles moving along microtubules 

to reach the growing hyphal apex (Fig. 1.7b), 

which is the site for secretion of extracellular 

enzymes as well as new cell wall material 

(Peberdy, 1994). Collinge and Trinci (1974) 

estimated that 38 000 secretory vesicles per 

minute fuse with the plasma membrane of 

a single growing hypha of Neurospora crassa. 

Microvesicles (chitosomes) probably arise from a 

discrete population of Golgi cisternae (Howard, 

1981). 

There is mounting evidence that fungi, like 

most eukaryotes, are capable of performing 

endocytosis by the inward budding of the 

plasma membrane at subapical locations. 

Endocytosis may be necessary to retrieve 

membrane material in excess of that which is 

required for extension at the growing apex, i.e. 

endocytosis and exocytosis may be coupled 

(Steinberg & Fuchs, 2004). The prime destination 

of endocytosed membrane material or vital 

stains is the vacuole (Vida & Emr, 1995; Fischer- 

Parton et al., 2000; Weber, 2002). In fungi, large 

vacuoles (Figs. 1.2e, 1.9) represent the main 

element of the lytic system and are the sink 

not only for endocytosed material but also 

for autophagocytosis, i.e. the sequestration 

and degradation of organelles or cytoplasm. 

Autophagocytosis is especially prominent under 

starvation conditions (Takeshige et al., 1992). 

Careful ultrastructural studies have revealed 

that adjacent vacuoles may be linked by thin 

membranous tubes, thereby providing a potential 

means of transport (Rees et al., 1994). These 

tubes can extend even through the septal 

pores and show peristaltic movement, possibly 

explaining why especially mycorrhizal fungi are 

capable of rapid translocation of solutes over 

long hyphal distances (Fig. 1.9; Cole et al., 1998; 

Ashford et al., 2001).


Fig1.9 Tubular continuities linking adjacent vacuoles of Pisolithus tinctorius. (a) Light micrograph of the vacuolar system of Pisolithus 

tinctorius stained with a fluorescent dye. (b) TEM image of a freeze-substituted hypha. Reproduced from Ashford et al.(2001),with 

kind permission of Springer Science and Business Media.Original images kindly provided by A.E. Ashford. 

1.2.6 Nutrient uptake 

One of the hallmarks of fungi is their ability to 

take up organic or inorganic solutes from 

extremely dilute solutions in the environment, 

accumulating them 1000-fold or more against 

their concentration gradient (Griffin, 1994). The 

main barrier to the movement of water-soluble 

substances into the cell is the lipid bilayer of 

the plasma membrane. Uptake is mediated by 

proteinaceous pores in the plasma membrane 

which are always selective for particular solutes. 

The pores are termed channels (system I) if they 

facilitate the diffusion of a solute following its 

concentration gradient whilst they are called 

porters (system II) if they use metabolic energy 

to accumulate the solute across the plasma 

membrane against its gradient (Harold, 1994). 

Fungi often possess one channel and one porter 

for a given solute. The high-affinity porter system 

is repressed at high external solute concentrations 

such as those found in most laboratory 

media (Scarborough, 1970; Sanders, 1988). 

In nature, however, the concentration of 

nutrients is often so low that the porter systems 

are active. Porters do not directly convert 

metabolic energy (ATP) into the uptake of 

solutes; rather, ATP is hydrolysed by ATPases 

which pump protons (H þ ) to the outside of 

the plasma membrane, thus establishing a 

transmembrane pH gradient (acid outside). It 

has been estimated that one-third of the total 

cellular ATP is used for the establishment of 

the transmembrane H þ gradient (Gradmann 

et al., 1978). The inward movement of H þ following 

its electrochemical gradient is harnessed 

by the porters for solute uptake by means of 

solute porter H þ complexes (Slayman & 

Slayman, 1974; Slayman, 1987; Garrill, 1995). 

Different types of porter exist, depending on 

the charge of the desired solute. Uniport and 

symport carriers couple the inward movement 

of H þ with the uptake of uncharged or negatively 

charged solutes, respectively, whereas antiports 

harness the outward diffusion of cations such as 

K þ for the uptake of other positively charged 

solutes. Charge imbalances can be rectified by 

the selective opening of K þ channels. Porters 

have been described for NH þ 4 ,NO 3 , amino acids, 

hexoses, orthophosphate and other solutes 

(Garrill, 1995; Jennings, 1995). 

The ATPases fuelling active uptake mechanisms 

are located in subapical or mature regions 

of the plasma membrane, whereas the porter 

systems are typically situated in the apical 

membrane (Harold, 1994), closest to the site 

where the solutes may be released by the activity 

of extracellular enzymes. Thus, mature hyphal 

segments make a substantial direct contribution


13 

(Fig. 1.11), which was at one time thought to be 

a causal factor of hyphal tip polarity but is now 

regarded as a consequence of it (Harold, 1994). 

Proton pumps fuelled by ATP are prominent 

also in the vacuolar membrane, the tonoplast 

(Fig. 1.11), and their activity acidifies the vacuolar 

lumen (Klionsky et al., 1990). The principle of 

proton-coupled solute transport is utilized by 

the vacuole to fulfil its role as a system for the 

storage of nutrients, for example phosphate 

(Cramer & Davis, 1984) or amino acids such as 

arginine (Keenan & Weiss, 1997), or for the 

removal of toxic compounds from the cytoplasm, 

e.g. Ca 2þ or heavy metal ions (Cornelius & 

Nakashima, 1987). 

Fig1.10 Schematic summary of the pathways of membrane 

flow in a growing hypha. Secretory proteins (), vacuolar 

luminal proteins (), membrane-bound proteins ( ), 

endocytosed (g) and autophagocytosed (m) material is 

indicated, as are vacuolar degradation products (). Redrawn 

and modified from Weber (2002). 

to the growth of the hypha at its tip. The spatial 

separation of H þ expulsion and re-entry generates 

an external electric field carried by protons 

1.2.7 Hyphal branching 

Assimilative hyphae of most fungi grow monopodially 

by a main axis (leading hypha) capable 

of potentially unlimited apical growth. Branches 

arise at some distance behind the apex, suggesting 

some form of apical dominance, i.e. the 

presence of a growing apex inhibits the development 

of lateral branches close to it. Dichotomous 

branching is rare, but does occur in Allomyces 

(see Fig. 6.20d) and Galactomyces geotrichum. 

In septate fungi, branches are often located 

immediately behind a septum. Branches usually 

arise singly in vegetative hyphae, although 

whorls of branches (i.e. branches arising near a 

common point) occur in reproductive structures. 

Branching may thus be under genetic or external 

control (Burnett, 1976). An even spacing between 

vegetative hyphae results from a combination of 

chemotropic growth towards a source of diffusible 

nutrients, and growth away from staling 

products secreted by other hyphae which have 

colonized a substratum. The circular appearance 

of fungal colonies in Petri dish cultures 

arises because certain lateral branches grow out 

and fill the space between the leading radial 

branches, keeping pace with their rate of growth. 

This invasive growth is the most efficient way to 

spread throughout a substratum. In nature, 

it may be obvious even to the naked eye, 

for example, in the shape of fairy rings (see 

Figs. 19.18a,b).


Fig1.11 Ion fluxes in a growing hypha.The 

proton (H þ ) gradient across the plasma 

membrane is generated by subapical 

ATP-driven expulsion of protons. It is used 

for the active uptake of nutrients by porters. 

Channels also exist for most of the nutrients 

but are not shown here, except for the K þ 

channel which operates to compensate for 

charge imbalances. Dotted arrows 

indicate movement of a solute against its 

concentration gradient; solid arrows 

indicate movement from concentrated to 

dilute.For details, see Garrill (1995). 

1.3 Hyphal aggregates 

Whereas plants and animals form genuine 

tissues by their ability to perform cell divisions 

in all directions, fungi are limited by their 

growth as one-dimensional hyphae. None the 

less, fungi are capable of producing complex 

and characteristic multicellular structures which 

resemble the tissues of other eukaryotes. This 

must be controlled by the positioning, growth 

rate and growth direction of individual hyphal 

branches (Moore, 1994). Further, instead of 

spacing themselves apart as during invasive 

growth, hyphae must be made to aggregate. 

Very little is known about the signalling events

HYPHAL AGGREGATES 

15 

leading to the synchronized growth of groups 

of hyphae. However, it may be speculated that 

the diffusion of signalling molecules takes place 

between adjacent hyphae, i.e. that a given hypha 

is able to influence the gene expression of adjacent 

hyphae by secreting chemical messengers. 

This may be facilitated by an extrahyphal glucan 

matrix within which aggregating hyphae are 

typically embedded (Moore, 1994). Such matrices 

have been found in rhizomorphs (Rayner et al., 

1985), sclerotia (Fig. 1.16c; Willetts & Bullock, 

1992) and fruit bodies (Williams et al., 1985). 

The composition of proteins on the surface of 

hyphal walls may also play an important role in 

recognition and adhesion phenomena (de Nobel 

et al., 2001). 

1.3.1 Mycelial strands 

The formation of aggregates of parallel, relatively 

undifferentiated hyphae is quite common 

in the Basidiomycota and in some Ascomycota. 

For instance, mycelial strands form the familiar 

‘spawn’ of the cultivated mushroom Agaricus 

bisporus. Strands arise most readily from a 

well-developed mycelium extending from an 

exhausted food base into nutrient-poor surroundings 

(Fig. 1.12a). When a strand encounters 

a source of nutrients exceeding its internal 

supply, coherence is lost and a spreading 

assimilative mycelium regrows (Moore, 1994). 

Alternatively, mycelial strands may be employed 

by fungi which produce their fructifications 

some distance away from the food base, as in 

the stinkhorn, Phallus impudicus. Here the mycelial 

strand is more tightly aggregated and is 

referred to as a mycelial cord. The tip of the 

mycelial cord, which arises from a buried tree 

stump, differentiates into an egg-like basidiocarp 

initially upon reaching the soil surface 

(Fig. 1.12b). 

The development of A. bisporus strands has 

been described by Mathew (1961). Robust leading 

hyphae extend from the food base and branch at 

fairly wide intervals to form finer laterals, most 

of which grow away from the parent hypha. 

A few branch hyphae, however, form at an acute 

angle to the parent hypha and tend to grow 

parallel to it. Hyphae of many fungi occasionally 

Fig1.12 Mycelial strands. (a) Strands of Podosordaria tulasnei (Ascomycota) extending from a previously colonized rabbit pellet 

(arrow) over sand. Note the dissolution of the strand upon reaching a new nutrient source, in this case fresh sterile rabbit pellets. 

(b) Excavated mycelial cords of the stinkhorn Phallus impudicus, which can be traced back from the egg-like basidiocarp primordium 

to the base of an old tree stump (below the bottom of the picture, not shown).


grow alongside each other or another physical 

obstacle which they chance to encounter. A later 

and specific stage in strand development is 

characterized by the formation of numerous 

fine, aseptate ‘tendril hyphae’ as branches from 

the older regions of the main hyphae. The tendril 

hyphae, which may extend forwards or backwards, 

become appressed to the main hypha and 

branch frequently to form even finer tendrils 

which grow round the main hyphae and 

ensheath them. Major strands are consolidated 

by anastomoses between their hyphae, and they 

increase in thickness by the assimilation of 

minor strands. A similar development has been 

noted in the strands of Serpula lacrymans, the dryrot 

fungus (Fig. 1.13), which are capable of 

extending for several metres across brickwork 

and other surfaces from a food base in decaying 

wood (Jennings & Watkinson, 1982; Nuss et al., 

1991). 

By recovering the nutrients from obsolete 

strands and forming new strands, colonies can 

move about and explore their vicinity in the 

search for new food bases (Cooke & Rayner, 1984; 

Boddy, 1993). Mycelial strands are capable of 

translocating nutrients and water in both directions 

(Boddy, 1993; Jennings, 1995). This property 

is important not only for decomposer fungi, but 

also for species forming mycorrhizal symbioses 

with the roots of plants, many of which produce 

hyphal strands (Read, 1991). 

Fig1.13 The tip of a hyphal strand of Serpula lacrymans 

(Basidiomycota). Note the formation of lateral branches 

which grow parallel to the direction of the main hyphae.The 

buckle-shaped structures at the septa are clamp connections. 

1.3.2 Rhizomorphs 

In contrast to mycelial strands or cords which 

consist of relatively undifferentiated aggregations 

of hyphae and are produced by a great 

variety of fungi, rhizomorphs are found in 

only relatively few species and contain highly 

differentiated tissues. Well-known examples of 

rhizomorph-forming fungi are provided by 

Armillaria spp. (Figs. 1.14 and 18.13b), which are 

serious parasites of trees and shrubs. In 

Armillaria, a central core of larger, thin-walled, 

elongated cells embedded in mucilage is 

surrounded by a rind of small, thicker-walled 

cells which are darkly pigmented due to melanin 

deposition in their walls. These root-like aggregations 

are a means for Armillaria to spread 

underground from one tree root system to 

another. In nature, two kinds are found a 

dark, cylindrical type and a paler, flatter type. 

The latter is particularly common beneath the 

bark of infected trees (see p. 546). Rhizomorphs 

on dead trees measure up to 4 mm in diameter. It 

has been estimated that a rhizomorph only 

1 mm in diameter must contain over 1000 

hyphae aggregated together. The development 

of rhizomorphs in agar culture has been 

described by Garrett (1953, 1970) and Snider 

(1959). Initiation of rhizomorphs can first be


17 

Fig1.14 Rhizomorph structure of Armillaria 

mellea (Basidiomycota). (a) Longitudinal 

section. (b) Transverse section, diagrammatic. 

(c) L.S. diagrammatic. (d) T.S. showing details of 

cells in the rind (r), cortex (c) and medulla (m). 

(e)L.S.showingdetailsofcells. 

observed after about 7 days’ mycelial growth on 

the agar surface as a compact mass of darkly 

pigmented hypertrophied cells. These pigmented 

structures have been termed microsclerotia. 

From white, non-pigmented points on their 

surface, the rhizomorphs develop. The growth 

of rhizomorphs can be several times faster than 

that of unorganized hyphae (Rishbeth, 1968). 

The most striking feature of the development of 

rhizomorphs is their compact growing point at 

the apex, which consists of small isodiametric 

cells protected by an apical cap of intertwined 

hyphae immersed in mucilage which they 

produce. Because of its striking similarity with 

a growing plant root, the rhizomorph tip was 

initially interpreted as a meristematic zone 

(Motta, 1967), but its hyphal nature can be 

demonstrated by careful ultrastructural observations 

(Powell & Rayner, 1983; Rayner et al., 1985). 

Behind the apex there is a zone of elongation. 

The centre of the rhizomorph may be hollow or 

solid. Surrounding the central lumen or making 

up the central medulla is a zone of enlarged 

hyphae 4 5 times wider than the vegetative 

hyphae (Fig. 1.14e). Possibly these vessel hyphae 

serve in translocation (Cairney, 1992; Jennings, 

1995). Towards the periphery of the rhizomorph, 

the cells become smaller, darker, and thicker 

walled. Extending outwards between the outer 

cells of the rhizomorph, there may be a growth 

of vegetative hyphae somewhat resembling the 

root-hair zone in a higher plant. Rhizomorphs 

may develop on monokaryotic mycelia derived 

from single basidiospores, or on dikaryotic


Fig1.15 Rhizomorphs of Podosordariatulasnei (Ascomycota). (a) Subterraneanrhizomorphsby which the fungus spreads through the 

soil. (b) T.S. showing the dark rind (1 2 cells thick) and a cortex consisting of thick-walled hyaline cells. 

mycelia following fusion of compatible monokaryotic 

hyphae. Dikaryotic rhizomorphs of 

Armillaria do not possess clamp connections 

(Hintikka, 1973). 

Rhizomorphs are also produced by other 

Basidiomycota and a few Ascomycota (Fig. 1.15; 

Webster & Weber, 2000). They are mainly formed 

in soil. An interesting exception is presented by 

tropical Marasmius spp., which form a network 

of aerial rhizomorphs capable of intercepting 

falling leaves before they reach the ground 

(Hedger et al., 1993). Because these rhizomorphs 

have a rudimentary fruit body cap at their 

extending apex (Hedger et al., 1993), they have 

been interpreted as indefinitely extending fruit 

body stipes (Moore, 1994). Mycelial strands and 

rhizomorphs represent extremes in a range of 

hyphal aggregations, and several intergrading 

forms can be recognized (Rayner et al., 1985). 

1.3.3 Sclerotia 

Sclerotia are pseudoparenchymatous aggregations 

of hyphae embedded in an extracellular 

glucan matrix. A hard melanized rind may be 

present or absent. Sclerotia serve a survival 

function and contain intrahyphal storage 

reserves such as polyphosphate, glycogen, 

protein, and lipid (Willetts & Bullock, 1992). 

The glucan matrix, too, may be utilized as a 

carbohydrate source during sclerotium germination 

(Backhouse & Willetts, 1985). Sclerotia may 

also have a reproductive role and are the only 

known means of reproduction in certain species. 

They are produced by a relatively small number 

of Asco- and Basidiomycota, especially plantpathogenic 

species such as Rhizoctonia spp. 

(p. 595), Sclerotinia spp. (p. 429) and Claviceps 

purpurea (p. 349). The form of sclerotia is very 

variable (Butler, 1966). The subterranean sclerotium 

of the Australian Polyporus mylittae (see Figs. 

18.13c,d) can reach the size of a football and is 

known as native bread or blackfellow’s bread. At 

the other extreme, they may be of microscopic 

dimensions consisting of a few cells only. Several 

kinds of development in sclerotia have been 

distinguished (Townsend & Willetts, 1954; 

Willetts, 1972). 

The loose type 

This is exemplified by Rhizoctonia spp., which 

are sclerotial forms of fungi belonging to the 

Basidiomycota. Sclerotia of the loose type are 

readily seen as the thin brownish-black 

scurfy scales so common on the surface of


19 

Fig1.16 Development of sclerotia. (a) The loose type, as seen in Rhizoctonia (Moniliopsis) solani.(b)HyphaofBotrytiscinerea showing 

dichotomous branching on a glass coverslip to initiate the terminal type of sclerotium. (c) Later stage of sclerotium formation 

in B. cinerea.The hyphae have become melanized and are growing away from the glass surface.They are embedded in a glucan 

matrix (arrows). (d) Mature sclerotia of B. cinerea on a stem of Conium. Some sclerotia are germinating to produce tufts of 

conidiophores. (e) Sclerotia of Claviceps purpurea from an ear of rye (Secale cereale). Rye grains are shown for size comparison. 

(a) and (b) to same scale. 

potato tubers. In pure culture, sclerotial initials 

arise by branching and septation of hyphae 

(Fig. 1.16a). These cells become filled with dense 

contents and numerous vacuoles, and darken to 

reddish-brown. The mature sclerotium does not 

show well-defined zones or ‘tissues’. It is made 

up of a central part which is pseudoparenchymatous, 

although its hyphal nature can be seen. 

Towards the outside, the hyphae are more 

loosely arranged; a rind of thick-walled hyphae 

is absent (Willetts, 1969). 

The terminal type 

This form is characterized by a well-defined 

pattern of branching. It is produced, for example, 

by Botrytis cinerea, the cause of grey mould 

diseases on a wide range of plants, and by the 

saprotrophic Pyronema domesticum (see p. 415). 

Sclerotia of B. cinerea are found on overwintering 

stems of herbaceous plants, especially 

umbellifers such as Angelica, Anthriscus, Conium 

and Heracleum. They can also be induced to form 

in culture, especially on agar media with a high


carbon/nitrogen ratio. When growing on host 

tissue, the sclerotia of Botrytis may include host 

cells, a feature shared also by sclerotia of 

Sclerotinia spp. to which Botrytis is related (see 

p. 429). Sclerotia arise by repeated dichotomous 

branching of hyphae, accompanied by cross-wall 

formation (Fig. 1.16b). The hyphae then aggregate, 

melanize and produce mucilage, giving the 

appearance of a solid tissue (Fig. 1.16c). A mature 

sclerotium may be about 10 mm long and 

3 5 mm wide, and is usually flattened, measuring 

1 3 mm in thickness. It is often orientated 

parallel to the long axis of the host plant 

(Fig. 1.16d). It is differentiated into a rind 

composed of several layers of rounded, dark 

cells, a narrow cortex of thin-walled pseudoparenchymatous 

cells with dense contents, and a 

medulla made up of loosely arranged filaments. 

Nutrient reserves are stored in the cortical and 

medullary regions (Willetts & Bullock, 1992). 

The strand type 

Sclerotinia gladioli, the causal agent of dry rot of 

corms of Gladiolus, Crocus and other plants, 

forms sclerotia of this type. Sclerotial initials 

commence with the formation of numerous 

side branches which arise from one or more 

main hyphae. Where several hyphae are 

involved, they lie parallel. They are thicker than 

normal vegetative hyphae, and become divided 

by septa into chains of short cells. These cells 

may give rise to short branches, some of which 

lie parallel to the parent hypha, whilst others 

grow out at right angles and branch again before 

coalescing. The hyphae at the margin continue 

to branch, and the whole structure darkens. 

The mature sclerotium is about 0.1 0.3 mm in 

diameter, and is differentiated into a rind of 

small, thick-walled cells and a medulla of large, 

thin-walled hyphae. More complex sclerotia are 

found in Sclerotium rolfsii, the sclerotial state of 

Pellicularia rolfsii (Basidiomycota). Here the 

mature sclerotium is differentiated into four 

zones: a fairly thick skin or cuticle, a rind made 

up of 2 4 layers of tangentially flattened cells, a 

cortex of thin-walled cells with densely staining 

contents, and a medulla of loose filamentous 

hyphae with dense contents. Chet et al. (1969) 

have shown that the skin or cuticle is made up of 

the remnants of cell walls attached to the 

outside of the empty, melanized, thick-walled 

rind cells. All the cells of the strand-type 

sclerotium have thicker walls than those of 

vegetative hyphae. Cells of the outer cortex 

contain large storage bodies which consist of 

protein (Kohn & Grenville, 1989) and leave little 

room for cytoplasm or other organelles. The 

inner cortex is also densely packed with storage 

granules. 

Other types 

There is a great diversity of other types of 

sclerotia (Butler, 1966). The sclerotia of Claviceps 

purpurea, the ‘ergots’ of grasses and cereals 

(Fig. 1.16e; see also p. 349), develop from a preexisting 

mass of mycelium which fills and 

replaces the cereal ovary, starting from the base 

and extending towards the apex. The outer layers 

form a violet, dark grey or black rind enclosing 

colourless, thick-walled cells. These contain 

abundant storage lipids which constitute 45% 

of the dry weight of a C. purpurea sclerotium 

(Kybal, 1964). Cordyceps militaris, an insect parasite, 

forms a dense mass of mycelium in the 

buried insect’s body (p. 360). This mass of 

mycelium, from which fructifications develop, 

is enclosed by the exoskeleton of the host, not by 

a fungal rind. Many wood-rotting fungi enclose 

colonized woody tissue with a black zone-line of 

dark, thick-walled cells, and the whole structure 

may be regarded as a kind of sclerotium. 

The giant sclerotium of Polyporus mylittae is 

marbled in structure, comprising white strata 

and translucent tissue. It has an outer, smooth, 

thin black rind. Three distinct types of hyphae 

make up the tissues: thin-walled, thick-walled 

and ‘layered’ hyphae. Thin- and thick-walled 

hyphae are abundant in the white strata but 

sparse in the translucent tissue, whereas the 

layered hyphae occur only in the translucent 

tissue. Detached sclerotia are capable of forming 

basidiocarps without wetting. It is believed that 

the translucent tissue functions as an extracellular 

nutrient and water store (Macfarlane et al., 

1978). The structure of the sclerotium appears to 

be related to its ability to fruit in dry conditions, 

such as occur in Western Australia.


21 

Germination of sclerotia 

Sclerotia can survive for long periods, sometimes 

for several years (Coley-Smith & Cooke, 1971; 

Willetts, 1971). Germination may take place in 

three ways by the development of mycelium, 

asexual spores (conidia) or sexual fruit bodies 

(ascocarps or basidiocarps). Mycelial germination 

occurs in Sclerotium cepivorum, the cause 

of white-rot of onion, and is stimulated by 

volatile exudates from onion roots (see p. 434). 

Conidial development occurs in Botrytis cinerea 

and can be demonstrated by placing overwintered 

sclerotia in moist warm conditions 

(Fig. 1.16d; Weber & Webster, 2003). The development 

of ascocarps (i.e. carpogenic germination) 

is seen in Sclerotinia, where stalked cups 

or apothecia, bearing asci, arise from sclerotia 

under suitable conditions (Fig. 15.2), and in 

Claviceps purpurea, where the overwintered sclerotia 

give rise to a perithecial stroma (Fig. 12.26c). 

Depending on environmental conditions, the 

sclerotia of some species may respond by 

germinating in different ways. 

1.3.4 The mantle of ectomycorrhiza 

The root tips of many coniferous and deciduous 

trees with ectomycorrhizal associations, 

especially those growing in relatively infertile 

soils, are covered by a mantle. This is a 

continuous sheet of fungal hyphae, several 

layers thick (see Fig. 19.10). The mycelium 

extends outwards into the litter layer of the 

soil, and inwards as single hyphae growing 

intercellularly, i.e. between the outer cortical 

cells of the root, to form the so-called Hartig 

net. Hyphae growing outwards from the 

mantle effectively replace the root hairs as a 

system for the absorption of minerals from the 

soil, and there is good evidence that, in most 

normal forest soils of low to moderate fertility, 

the performance and nutrient status 

of mycorrhizal trees is superior to that of 

uninfected trees (Smith & Read, 1997). 

Most fungi causing ectomycorrhizal infections 

are Basidiomycota, especially members of the 

Homobasidiomycetes (pp. 526 and 581). Within 

the soil or in pure culture, mycelial 

strands may form, but the mycelium is not 

aggregated into the tissue-like structure of the 

mantle. 

1.3.5 Fruit bodies of Ascomycota and 

imperfect fungi 

In the higher fungi, hyphae may aggregate in a 

highly regulated fashion to form fruiting structures 

which are an important and often speciesspecific 

feature of identification. In the 

Ascomycota, the fruit bodies produce sexual 

spores (i.e. as the result of nuclear fusion and 

meiosis) which are termed ascospores and are 

contained in globose or cylindrical cells called 

asci (Lat. ascus ¼ a sac, tube). In most cases, 

the asci can discharge their ascospores explosively. 

Asci, although occasionally naked, are 

usually enclosed in an aggregation of hyphae 

termed an ascocarp or ascoma. Ascocarps are 

very variable in form, and several types have 

been distinguished (see Fig. 8.16). Their features 

and development will be described more fully 

later. Forms in which the asci are totally 

enclosed, and in which the ascocarp has no 

special opening, are termed cleistothecia. In 

contrast, gymnothecia consist of a loose mesh 

of hyphae. Both are found in the Plectomycetes 

(Chapter 11). A modified cleistothecium is characteristic 

of the Erysiphales (Chapter 13). Cup 

fungi (Discomycetes, Chapters 14 and 15) possess 

saucer-shaped ascocarps termed apothecia, with 

a mass of non-fertile hyphae supporting a layer 

of asci lining the upper side of the fruit body. The 

non-fertile elements of the apothecium often 

show considerable differentiation of structure. 

The asci in apothecia are free to discharge their 

ascospores at the same time. In other 

Ascomycota, the asci are contained within 

ascocarps with a very narrow opening or ostiole, 

through which each ascus must discharge its 

spores separately. Ascocarps of this type are 

termed perithecia or pseudothecia. Perithecia 

are found in the Pyrenomycetes (Chapter 12) 

whilst pseudothecia occur in the 

Loculoascomycetes (Chapter 17). These two 

types of ascocarp develop in different ways. In 

many of the Pyrenomycetes, the perithecia are 

borne on or embedded in a mass of fungal tissue 

termed the perithecial stroma, and these are


well shown by the Xylariales (p. 332), and by 

Cordyceps (p. 360) and Claviceps (p. 349). In some 

cases, in addition to the perithecial stroma, a 

fungus may develop a stromatic tissue on or 

within which asexual spores (conidia) develop. 

Nectria cinnabarina (p. 341), the coral spot fungus 

so common on freshly dead deciduous twigs, is 

such an example. It initially forms pink conidial 

stromata which later, under suitable conditions 

of humidity, become converted into perithecial 

stromata. 

Among the imperfect (asexual) fungi, mycelial 

aggregations bearing conidia are seen in 

various genera. In some, there are tufts 

of parallel conidiophores termed coremia 

or synnemata, exemplified by Penicillium 

claviforme (see Fig. 11.19). In some imperfect 

fungi formerly called Coelomycetes, the conidia 

develop in flask-shaped cavities termed pycnidia 

(see Figs. 17.3 17.5). Various other 

kinds of mycelial fruiting aggregates are also 

known. 

1.3.6 Fruit bodies of Basidiomycota 

The fruit bodies of mushrooms, toadstools, 

bracket fungi, etc., are all examples of basidiocarps 

or basidiomata which bear the sexually 

produced spores (basidiospores) on basidia. 

Basidiocarps are almost invariably constructed 

from dikaryotic hyphae, but how vegetative 

hyphae aggregate to form a mushroom fruit 

body is still a mystery (Moore, 1994). Wessels 

(1997) has suggested that hydrophobins coating 

the surface of hyphae may confer adhesive 

properties, leading to their aggregation to form 

a fruit body initial as the first step in morphogenesis. 

Once an initial has been formed, its 

glucan matrix may provide an environment for 

the exchange of signalling molecules between 

hyphae. Moore (1994) speculated that morphogenesis 

might ultimately be determined by 

induction hyphae exerting a control over 

surrounding hyphae, leading to the development 

of morphogenetic units. This morphogenetic 

commitment must happen at a very early stage. 

For instance, in the ink-cap (Coprinus cinereus) an 

initial measuring only 1% of the final fruit body 

size is already differentiated into stipe and cap 

(Moore et al., 1979). Therefore, when a mushroom 

fruit body expands, this is due mainly to the 

enlargement of existing hyphae, whereas new 

apical growth is restricted mainly to branches 

filling up the space generated during expansion 

(Moore, 1994). Hyphae making up the mature 

basidiocarp may show considerable differentiation 

in structure and function. This is perhaps 

most highly developed in polypore-type basidiocarps, 

where a number of morphologically 

distinct hyphal types have been recognized 

(p. 517). 

1.4 Spores of fungi 

The reproduction by means of small spores is 

a cornerstone in the ecology of fungi. Although 

a single spore may have a negligible chance of 

reaching a suitable substrate, spores may be 

produced in such quantities that even discrete 

substrates can be exploited by the species as a 

whole. Only a few fungi make do without spores, 

surviving solely by means of mycelium and 

sclerotia. Spores may be organs of sexual or 

asexual reproduction, and they are involved in 

dispersal and survival. Gregory (1966) distinguished 

between xenospores (Gr. xenos ¼ 

a foreigner) for spores which are dispersed from 

their place of origin and memnospores 

(Gr. mémnon ¼ steadfast, to persist), which stay 

where they were formed. Some spores are 

violently discharged from the organs which 

bear them, energy for dispersal being provided 

by the spore itself or the structure producing 

it (Ingold, 1971). However, many spores are 

dispersed passively by the action of gravity, air 

or water currents, rain splash, or by animals, 

especially insects. Dispersal may also occur by 

human traffic. Spores may be present in the 

outdoor air at such high concentrations (e.g. 

100 Cladosporium spores l 1 ) that they can cause 

allergic respiratory diseases when inhaled (Lacey, 

1996). In freshwater, the asexually produced 

spores (conidia) of aquatic hyphomycetes, which 

colonize autumn-shed tree leaves, may reach 

concentrations of 10 000 20 000 spores l 1 (see 

p. 685). Long-range dispersal of air-borne spores

SPORES OF FUNGI 

23 

over thousands of kilometres is known to occur 

in nature. For instance, the urediniospores of 

the coffee rust fungus, Hemileia vastatrix, are 

thought to have travelled from Africa to South 

America by wind at high altitudes, and the 

urediniospores of black stem rust of wheat 

(Puccinia graminis) undergo an annual migration 

from states bordering the Gulf of Mexico to 

the prairies of North America and Canada 

(Fig. 22.11). These spores are protected from 

the deleterious effects of UV irradiation in 

the upper atmosphere by pigments in the 

spore wall. 

Some spores are not dispersed but survive 

in situ, e.g. the oospores of many soil-inhabiting 

Oomycota (Chapter 5), the zygospores of 

Zygomycota (Chapter 7) and the chlamydospores 

of Glomales (see p. 217) and other fungi. Fungal 

spores may remain dormant for many years, 

especially under dry and cold conditions 

(Sussman & Halvorson, 1966; Sussman, 1968). 

An extreme example of spore survival is shown 

by the recovery of viable spores of several fungi 

from glacial ice cores, including those of 

Cladosporium cladosporioides from ice samples 

4500 years old (Ma et al., 2000). 

The morphology and structure of fungal 

spores show great variability, from unicellular 

to multicellular, branched or unbranched or 

sometimes spirally coiled, thin- or thick-walled 

with hyaline or pigmented walls, dry or sticky, 

smooth or ornamented by mucilaginous extensions, 

spines, folds or reticulations. A number of 

general descriptive terms have been applied to 

characterize spores in relation to the number of 

cells and septa which they contain. Single-celled 

spores are termed amerospores (Gr. a ¼ not, 

meros ¼ a part; i.e. not divided), two-celled spores 

are didymospores (Gr. didymos ¼ double), spores 

with more than one transverse septum are 

phragmospores (Gr. phragmos ¼ a hedge, barricade), 

and spores with transverse and longitudinal 

septa are dictyospores (Gr. dictyon ¼ 

a net). These terms may be qualified by prefixes 

indicating spore pigmentation such as hyalo- for 

colourless (hyaline) spores and phaeo- for spores 

with dark-coloured (melanized) walls. 

Special terms have also been used to refer to 

spore shape. Scolecospores (Gr. skolex ¼ a worm) 

are worm-shaped, helicospores (Gr. helix ¼ 

twisted or wound) are spores with a two- or 

three-dimensional spiral shape, whilst staurospores 

(Gr. stauros ¼ a cross) have arms radiating 

from a central point or axis. Spore septation, 

colour and shape, along with other criteria such 

as the arrangement of structures which bear the 

spores, have been used in classification and 

identification, especially in conidial fungi 

which do not show sexual reproduction. These 

criteria rarely lead to natural systems of classification, 

but to ‘form genera’ or ‘anamorph 

genera’ made up of species unified by having 

similar spore forms. 

Some of the more common spore types 

are described below. There are numerous 

other, less-common kinds of spore found in 

fungi, and they are described later, in relation 

to the particular fungal groups in which they 

occur. 

1.4.1 Zoospores 

These are spores which are self-propelled by 

means of flagella. Propulsion is often coupled 

with chemotactic movement, zoospores having 

the ability to sense chemicals diffusing from 

suitable substrata and to move towards them, or 

gametes detecting and following extremely low 

concentrations of hormones. In some cases 

oxygen or light are also stimuli for tactic movement. 

The fungal groups which possess flagella 

are mostly aquatic or, if terrestrial, rely on water 

for dispersal or infection. Their zoospores are of 

four kinds (see Fig. 1.17): 

1. Posteriorly flagellate zoospores with 

flagella of the whiplash type are characteristic 

of the Chytridiomycota (Chapter 6). Each 

whiplash flagellum has 11 microtubules 

arranged in the 9 þ 2 pattern typical of 

eukaryotes. The microtubules are enclosed in 

a smooth, membranous axoneme sheath continuous 

with the plasma membrane. In most 

members of the Chytridiomycota there is a 

single posterior flagellum (Fig. 1.17a), but in 

the rumen-inhabiting Neocallimastigales there 

may be up to 16 flagella (Fig. 1.17b). Such spores 

are driven forward by sinusoidal rhythmic 

beating of the flagellum. This type of zoospore


Fig1.17 Zoospore types found in fungi, diagrammatic and not to scale.The arrow indicates the direction of movement of the 

zoospore. (a) Posteriorly uniflagellate (opisthokont) zoospore with a flagellum of the whiplash type found in many Chytridiomycota. 

(b) Posteriorly multiflagellate zoospore with numerous (up to16) whiplash flagella which occur in certain anaerobic rumen-inhabiting 

Chytridiomycota (Neocallimastigales). (c) Zoospore with unequal (anisokont) whiplash flagella characteristic of the Myxomycota 

and the Plasmodiophoromycota. (d) Anteriorly uniflagellate zoospore with a flagellum of the tinsel type, the axoneme being clothed 

with rows of mastigonemes, typical of the Hyphochytriomycota. (e,f) Biflagellate zoospores with heterokont flagella, one of the 

whiplash and the other of the tinsel type, which are found in different groups of the Oomycota. For more details turn to the 

different fungal groups. 

flagellation is termed opisthokont (Gr. opisthen ¼ 

behind, at the back; kontos ¼ a pole). Detailed 

descriptions of the fine structure of chytridiomycete 

zoospores are given on p. 129. 

2. Biflagellate zoospores with two whiplash 

flagella of unequal length are called anisokont 

(Fig. 1.17c) and are found in some Myxomycota 

and the Plasmodiophoromycota, both now 

classified among the Protozoa (see Chapters 2 

and 3). 

3. Anteriorly uniflagellate zoospores with 

a flagellum of the tinsel type are characteristic 

of the Hyphochytriomycota (Chapter 4). The 

axoneme sheath of the tinsel or straminipilous 

flagellum (Lat. stramen ¼ straw; pilus ¼ hair) is 

adorned by two rows of fine hairs (Fig. 1.17d). 

These are called tripartite tubular hairs or 

mastigonemes (Gr. mastigion ¼ a small whip; 

nema ¼ a thread). Rhythmic sinusoidal beating of 

the tinsel type flagellum pulls the zoospore 

along, in contrast to the pushing action of 

whiplash flagellum. Details of the fine structure 

of this type of zoospore are given in Fig. 4.5. 

4. Biflagellate zoospores with anteriorly or 

laterally attached flagella, one of which is of 

the whiplash type and the other of the tinsel 

type (Figs. 1.17e,f), are characteristic of the 

Oomycota (Chapter 5). Zoospores with the two 

different kinds of flagellum are heterokont. 

Where the two types of flagellum are attached 

anteriorly, as in the first-released zoospores of 

Saprolegnia, their propulsive actions tend to 

work against each other and the zoospore is 

a very poor swimmer (Fig. 1.17e). However, 

the secondary zoospore (termed the principal 

zoospore) in Saprolegnia and in many other 

Oomycota has laterally attached flagella, with 

the tinsel-type (pulling action) flagellum pointing 

forwards and the whiplash-type (pushing 

action) flagellum directed backwards and possibly 

acting as a rudder, jointly providing much 

more effective propulsion (Fig. 1.17f). 

1.4.2 Sporangiospores 

In the Zygomycota, and especially in the 

Mucorales (see p. 180), the asexual spores are 

contained in globose sporangia (Fig. 1.18) or 

cylindrical merosporangia. Because they are 

non-motile, the spores are sometimes termed 

aplanospores (Gr. a ¼ not, planos ¼ roaming).


25 

Fig1.18 Sporangia in Mortierella (Umbelopsis) 

vinacea. (a) Maturing sporangium in which 

the cytoplasm is being cleaved into 

numerous sporangiospores. (b) Release of 

sporangiospores by breakdown of the 

sporangial wall. Unusually, in M. vinacea the 

sporangiospores are angular in shape. 

The spores may be uni- or multinucleate and are 

unicellular. They generally have thin, smooth 

walls and are almost always globose or ellipsoid 

in shape. They are formed by cleavage of the 

sporangial cytoplasm. They vary in colour from 

hyaline (colourless) to yellow, due to carotenoid 

pigments in the cytoplasm. When mature, they 

may be surrounded by mucilage, in which case 

they are usually dispersed by rain splash or 

insects, or they may be dry and dispersed by wind 

currents. In some genera, e.g. Pilobolus, entire 

sporangia become detached. The number of 

sporangiospores per sporangium may vary from 

several thousand to only one. The detachment 

and dispersal of intact sporangia containing a 

few sporangiospores or a single one is indicative 

of the way in which conidia may have evolved 

from one-spored sporangia. 

1.4.3 Ascospores 

Ascospores are the characteristic spores of the 

largest group of fungi, the Ascomycota or 

ascomycetes. They are meiospores and are 

formed in the developing ascus as a result of 

nuclear fusion immediately followed by meiosis. 

The four haploid daughter nuclei then divide 

mitotically to give eight haploid nuclei around 

which the ascospores are cut out. Details of 

ascospore development are described in Fig. 8.11. 

In most ascomycetes, the eight ascospores are 

contained within a cylindrical ascus, from which 

they are squirted out together with the ascus 

sap when the tip of the turgid ascus breaks down 

and the elastic ascus walls contract. The distance 

of discharge may be 1 cm or more. In some cases, 

for example, the Plectomycetes (Chapter 11) 

and in ascomycetes with subterranean fruit 

bodies, such as the false truffles (Elaphomyces 

spp.; Fig. 11.21) and truffles (Tuber spp. and their 

allies; p. 423), ascospore release is non-violent 

and their asci are not cylindrical but globose. 

Ascospores vary greatly in size, shape and colour. 

In size, the range is from about 4 5 1 mm in 

small-spored forms such as the minute cup 

fungus Dasyscyphus, to 130 45 mm in the lichen 

Pertusaria pertusa. The shape of ascospores varies 

from globose to oval, elliptical, lemon-shaped, 

sausage-shaped, cylindrical, or needle-shaped. 

Ascospores are often asymmetric in form with 

a wider, blunter, anterior part and a narrower, 

more tapering posterior. This shape increases 

their acceleration as they are squeezed out 

through the opening of the ascus. Ascospores 

may be uninucleate or multinucleate, unicellular 

or multicellular, divided up by transverse or 

by transverse and longitudinal septa. In some


genera, e.g. Hypocrea (Fig. 12.15) or Cordyceps 

(Fig. 12.33), the multicellular ascospores may 

break up into part-spores within the ascus prior 

to discharge. The ascospore wall may be thin or 

thick, hyaline or coloured, smooth or rough, 

sometimes cast into reticulate folds or ornamented 

by ridges, and it may have a mucilaginous 

outer layer which is sometimes extended to form 

simple or branched appendages, especially in 

marine ascomycetes where they aid buoyancy 

and attachment. In many cases, ascospores are 

resting structures which survive adverse conditions. 

They may have extensive food reserves in 

the form of lipids and sugars such as trehalose. 

Because the formation of ascospores involves 

meiosis, they are important not only as a means 

of dispersal and survival but also in genetic 

recombination. 

It is obvious that there is no such thing as 

a typical ascospore. Neurospora tetrasperma will 

serve as an example of an ascospore whose 

structure has been extensively studied (Lowry & 

Sussman, 1958, 1968). This fungus is somewhat 

unusual in that it has four-spored asci and the 

ascospores are binucleate. The spores are black, 

thick-walled and shaped rather like a rugby 

football, but with flattened ends. The name 

Neurospora refers to the ribbed spores, because 

the dark outer wall is made up of longitudinal 

raised ribs, separated by interrupted grooves. The 

structure of a spore in section is shown in 

Fig. 1.19. Within the cytoplasm of the spore 

are the two nuclei, fragments of endoplasmic 

reticulum (not illustrated), swollen mitochondria 

and vacuoles, bounded by single unit membranes. 

The wall surrounding the protoplast is 

composed of several layers. The innermost layer 

is the endospore, outside of which is the 

epispore. The ribbed layer is termed the perispore. 

Between the ribs are lighter intercostal 

veins containing a material which is chemically 

distinct from the ribs. This material is continuous 

over the whole surface of the spore, giving 

it a relatively smooth surface. The spore germinates 

by the extrusion of germ tubes from a preexisting 

germ pore, a thin area in the epispore at 

either end of the spore. In many ascomycetes a 

trigger is required for germination, e.g. heat 

shock in Neurospora or a chemical stimulus, for 

example in ascomycetes which grow and fruit on 

the dung of herbivorous mammals and whose 

spores are subjected to digestive treatment. 

1.4.4 Basidiospores 

Basidiospores are the sexual spores which 

characterize a large group of fungi, the 

Basidiomycota or basidiomycetes. In comparison 

with the morphological diversity of ascospores, 

basidiospores are more uniform. They also show 

a smaller size range, from about 3 to 20 mm, 

which is possibly related to their unique method 

of discharge. They are normally found in 

groups of four attached by tapering sterigmata 

to the cell which bears them, the basidium. At 

the time of their discharge all basidiospores 

Fig1.19 Neurospora tetrasperma.T.S. 

ascospore. Simplified diagram based on 

an electron micrograph by Lowry in 

Sussman and Halvorson (1966).


27 

are unicellular, but they may become septate 

after release in some members of the 

Heterobasidiomycetes (Chapter 21). In shape, 

basidiospores are asymmetric and vary from 

sub-globose, sausage-shaped, fusoid, to almondshaped 

(i.e. flattened), and the wall may be 

smooth or ornamented with spines, ridges or 

folds. The colour of basidiospores is important 

for identification. They may be colourless, 

white, cream, yellowish, brown, pink, purple 

or black. The spore colour may be due to pigments 

in the spore cytoplasm or in the spore 

wall. The appearance of pigments in the wall 

occurs relatively late in spore development. 

This explains the change of colour of the gill 

of a domestic mushroom (Agaricus) from pink, 

due to cytoplasmic spore pigments, to dark 

purplish-brown when mature, due to wall 

pigments. 

The generalized structure of a basidiospore is 

illustrated in Fig. 1.20. Most basidiospores have 

a flatter adaxial face and a more curved abaxial 

face. The point of attachment of the spore to the 

sterigma is the hilum, which persists as a scar 

at the base of a discharged spore. Close to the 

hilum is a small projection, the hilar appendix. 

This is involved in the unique mechanism of 

basidiospore discharge, in which a drop of liquid 

perched on the hilar appendix coalesces with 

a second blob of liquid on the spore surface, 

Fig1.20 Generalized view of a median vertical section 

through a basidiospore as seen by transmission electron 

microscopy.For clarity, structures such as endoplasmic 

reticulum and ribosomes are not illustrated. Diagram 

based on Agrocybe acericola, after Ruch and Nurtjahja 

(1996).


creating a momentum which leads to acceleration 

of the spore (Money, 1998; see p. 493). The 

spore is projected for a short distance (usually 

less than 2 mm) from the basidium. Violently 

projected spores are termed ballistospores (Lat. 

ballista ¼ a military engine for throwing large 

stones), but whilst most basidiospores are ballistospores, 

some are not. For example, in the 

Gasteromycetes (Chapter 20), which include puffballs, 

stinkhorns and their allies, violent spore 

projection has been lost in the course of 

evolution from ancestors which possessed it. 

Likewise, the basidiospores of smut fungi 

(Ustilaginales, Chapter 23) are not violently 

discharged. The term statismospore (Lat. statio 

¼ standing still) is sometimes used for a spore 

which is not forcibly discharged. 

The cytoplasm of basidiospores usually 

contains a single haploid nucleus resulting 

from meiotic division in the basidium; sometimes 

a post-meiotic division gives rise to two 

genetically identical nuclei. The structure of the 

wall is complex. In Agrocybe acericola there are 

two layers, a thicker, dark-pigmented, electrondense 

outer layer or epispore, and a thinner, 

electron-transparent inner layer, the endospore 

(Ruch & Nurtjahja, 1996; see Fig. 1.20). The 

cultivated mushroom, Agaricus bisporus, has a 

three-layered wall making up some 35% of the 

dry weight of the spore (Rast & Hollenstein, 

1977), whereas the wall of the Coprinus cinereus 

basidiospore comprises six distinct layers 

(McLaughlin, 1977). A histochemical feature of 

the walls of some basidiospores is that they 

are amyloid, i.e. they include starch-like 

material which stains bluish-purple with iodinecontaining 

stains such as Melzer’s reagent. This 

reaction is used as a taxonomic character. 

The amyloid reaction is due to the presence of 

unbranched, short-chain amylose molecules. It 

has been suggested that this ‘fungal starch’ may 

aid dormancy by creating a permeability barrier 

to oxygen in dry spores. When the amyloid 

material is dissolved as water becomes available, 

dormancy is lost and spore germination can 

proceed (Dodd & McCracken, 1972). In some 

basidiospores, e.g. those of Coprinus cinereus and 

Agrocybe acericola, the basidiospore has a distinct 

germ pore at the end opposite to the hilum 

(see Fig. 1.20). In other basidiomycetes, e.g. 

Oudemansiella mucida, Schizophyllum commune and 

Flammulina velutipes, the basidiospores have no 

specialized pore. 

The reserve contents of the spore may vary. 

In some species, lipid is the major storage 

product, and there is an apparent lack of 

insoluble polysaccharides such as glycogen 

(Ruch & Motta, 1987). In other spores, glycogen 

predominates. Where lipid is present, germination 

may be fuelled by its breakdown and 

utilization, but where it is absent spores are 

dependent on external nutrient supplies before 

germination and further development is possible. 

In addition to the usual organelle complement, 

microbodies are also prominent in 

basidiospores. These are single membranebound 

organelles often associated with mitochondria 

and lipid globules; they may function 

as glyoxisomes containing enzymes involved 

in the oxidation of lipids (Ruch & Nurtjahja, 

1996). 

1.4.5 Zygospores 

Zygospores are sexually produced resting structures 

formed as a result of plasmogamy between 

gametangia which are usually equal in size 

(Fig. 1.21a). Nuclear fusion may occur early, or 

may be delayed until shortly before meiosis and 

zygospore germination. Zygospores are typical 

of Zygomycota (Chapter 7). They are often large, 

thick-walled, warty structures with abundant 

lipid reserves and are unsuitable for longdistance 

dispersal, usually remaining in the 

position in which they were formed and awaiting 

suitable conditions for further development. 

The gametangia which fuse to form the zygospore 

may be uninucleate or multinucleate, 

and correspondingly the zygospore may have 

one, two or many nuclei within it. Zygospore 

germination may be by a germ tube or by the 

formation of a germ sporangium. 

1.4.6 Oospores 

An oospore is a sexually produced spore which 

develops from unequal gametangial copulation 

or markedly unequal (oogamous) gametic fusion 

(Fig. 1.21b). It is the characteristic sexually


29 

Fig1.21 Sexual resting structures. (a) Zygospore of Rhizopus sexualis.The zygote has been produced by fusion of two gametangia 

and has laid down a thick wall with warty ornamentations. (b) Oospore of Phytophthora erythroseptica.The oogonium (o) has grown 

through the antheridium (a), and the oosphere has picked up a fertilization nucleus in the process. a kindly provided by H.-M. Ho; 

reprinted from Ho and Chen (1998) with permission of Botanical Bulletin of Academia Sinica. 

produced spore of the Oomycota (Chapter 5), 

although oospores are also found in the 

Monoblepharidales (Chytridiomycota; Fig. 6.25). 

In the Oomycota, oospore development begins 

with the formation of one or more oospheres 

within the larger gametangium, the oogonium. 

After fertilization, i.e. the receipt of an antheridial 

nucleus by the oosphere, this lays down a 

thick wall and becomes the oospore. The number 

of oospores per oogonium may vary, and this is 

an important taxonomic criterion. Meiotic 

nuclear divisions precede oosphere and antheridial 

maturation in the Oomycota and nuclear 

fusion follows fertilization, so that the oospore is 

diploid. The oospore develops a thick outer wall 

and lays down food reserves, usually in the form 

of lipids. In the Peronosporales the outer wall of 

the oospore is surrounded by periplasm, the 

residual cytoplasm left in the oogonium after 

the oospheres have been cleaved out. Oospores 

are sedentary (memnospores) and are important 

in survival rather than dispersal. They 

often require a period of maturation before 

germination can occur and may remain dormant 

for long periods. 

1.4.7 Chlamydospores 

In most groups of fungi, terminal or intercalary 

segments of the mycelium may become packed 

with lipid reserves and develop thick walls 

within the original hyphal wall (Fig. 1.22). 

The new walls may be colourless or pigmented, 

and are often hydrophobic. Structures of 

this type have been termed chlamydospores 

(Gr. chlamydos ¼ a thick cloak). They are formed 

asexually. Generally there is no mechanism for 

detachment and dispersal of chlamydospores, 

but they may become separated from each other 

by the collapse of the hyphae producing them. 

They are therefore typical memnospores, forming 

important organs of asexual survival, especially 

in soil fungi. Chlamydospores may develop 

within the sporangiophores of some species 

of the Mucorales, e.g. in Mucor racemosus (see 

Fig 7.14). The Glomales, which are fungal 

partners in symbiotic mycorrhizal associations 

with many vascular plants, reproduce primarily 

by large, thick-walled chlamydospores. These 

develop singly or in clusters (sporocarps) on 

coarse hyphae attached to their host plants. 

They are sedentary in soil but may be dispersed


Fig1.22 Chlamydospores formed by soil-borne fungi. (a) Intercalary hyphal chlamydospores in Mucor plumbeus (Zygomycota). 

(b) Terminal chlamydospore in Pythium undulatum (Oomycota). Both images to same scale. 

by wind or by burrowing rodents which eat the 

spores. Chlamydospores may also develop within 

the multicellular macroconidia of Fusarium spp. 

and may survive when other, thin-walled cells 

making up the spore are degraded by soil microorganisms. 

Similar structures are found in old 

hyphae of the aquatic fungus Saprolegnia (see 

Fig. 5.6g), either singly or in chains. In this genus, 

the chlamydospores may break free from the 

mycelium and be dispersed in water currents. 

Chlamydospores which are dispersed in this way 

are termed gemmae (Lat. gemma ¼ a jewel). 

The term chlamydospore is also sometimes 

used to describe the thick-walled dikaryotic spore 

characteristic of smut fungi (Ustilaginales; 

Chapter 23) but the term teliospore is preferable 

in this context. Hughes (1985) has discussed the 

use of the term chlamydospore. 

1.4.8 Conidia (conidiospores) 

Conidiospores, commonly known as conidia, are 

asexual reproductive structures. The word is 

derived from the Greek konidion, a diminutive 

of konis, meaning dust (Sutton, 1986). Conidia 

are found in many different groups of 

fungi, but especially within Ascomycota and 

Basidiomycota. The term conidium has, unfortunately, 

been used in a number of different ways, 

so that it no longer has any precise meaning. 

It has been defined by Kirk et al. (2001) as 

‘a specialized non-motile (cf. zoospore) asexual 

spore, usually caducous (i.e. detached), not 

developed by cytoplasmic cleavage (cf. 

sporangiospore) or free cell formation (cf. ascospore); 

in certain Oomycota produced through the 

incomplete development of zoosporangia which 

fall off and germinate to produce a germination 

tube’. In many fungi conidia represent a means 

of rapid spread and colonization from an initial 

focus of infection. 

In general, conidia are dispersed passively, but 

in a few cases discharge is violent. For instance, in 

Nigrospora the conidia are discharged by a squirt 

mechanism (Webster, 1952), and in Epicoccum 

(Fig. 17.8) discharge is brought about by the 

rounding-off of a two-ply septum separating the 

conidium from its conidiogenous cell (Webster, 

1966; Meredith, 1966). In the Helminthosporium 

conidial state of Trichometasphaeria turcica, drying 

and shrinkage of the conidiophore is associated 

with the sudden development of a gas phase, 

causing a jolt sufficient to project the conidium 

(Meredith, 1965; Leach, 1976). 

There is great variation in conidial ontogeny. 

This topic will be dealt with more fully 

later when considering the conidial states of 

Ascomycota, and at this stage it is sufficient to 

distinguish between the major types of conidial 

development, which may be either thallic or 

blastic. Cells which produce conidia are conidiogenous 

cells. The term thallic is used to describe 

development where there is no enlargement of 

the conidium initial (Fig. 1.23a), i.e. the conidium 

arises by conversion of a pre-existing segment of 

the fungal thallus. An example of this kind is 

Galactomyces candidus, in which the conidia are


31 

Fig1.23 Diagrams to illustrate different kinds of conidial development. (a) Thallic development.There is no enlargement of the 

conidium initial. (b) Holoblastic development. All the wall layers of the conidiogenous cell balloon out to form a conidium initial 

recognizably larger than the conidiogenous cell. (c) Enteroblastic tretic development: only the inner wall layers of the conidiogenous 

cell are involved in conidium formation.The inner wall layers balloon out through a narrow channel in the outer wall. (d) Phialidic 

development: the conidiogenous cell is a phialide.The wall of the phialide is not continuous with the wall surrounding the conidium. 

The conidial wall arises de novo from newly synthesized material in the neck of the phialide. Diagrams based on Ellis (1971a). 

formed by dissolution of septa along a hypha 

(Fig. 10.10). In most conidia, development is 

blastic, i.e. there is enlargement of the conidium 

initial before it is delimited by a septum. 

Two main kinds of blastic development have 

been distinguished: 

1. Holoblastic, in which both the inner and 

outer wall layers of the conidiogenous cell contribute 

to conidium formation (Fig. 1.23b). An 

example of this kind of development is shown 

by the conidia of Sclerotinia fructigena (Fig. 15.3). 

2. Enteroblastic, in which only the inner wall 

layers of the conidiogenous cell are involved in 

conidium formation. Where the inner wall layer 

balloons out through a narrow pore or channel 

in the outer wall layer, development is described 

as tretic (Fig. 1.23c). Examples of enteroblastic 

tretic development are found in Helminthosporium 

velutinum (Fig. 17.12) and Pleospora herbarum 

(Fig. 17.9d). Another important method of enteroblastic 

development is termed phialidic 

development. Here the conidiogenous cell is 

a specialized cell termed the phialide. During 

the expansion of the first-formed conidium, the 

tip of the phialide is ruptured. Further conidia 

develop by the extension of cytoplasm enclosed 

by a new wall layer which is laid down in the 

neck of the phialide and is distinct from the 

phialide wall. The protoplast of the conidium is 

pinched off by the formation of an inwardly 

growing flange which closes to form a septum 

(Fig. 1.23d). New conidia develop beneath the 

earlier ones, so that a chain may develop with 

the oldest conidium at its apex and the youngest 

at its base. Details of phialidic development are 

discussed more fully in relation to Aspergillus and 

Penicillium (p. 299), which reproduce by means of 

chains of dry phialoconidia dispersed by wind. 

Sticky phialospores which accumulate in slimy 

droplets at the tips of the phialides are common 

in many genera; they are usually dispersed by 

insects, rain splash or other agencies.


As mentioned on p. 24, the term conidium is 

sometimes used for structures which are probably 

homologous to sporangia. A series can be 

erected in the Peronosporales in which there 

are forms with deciduous sporangia which 

release zoospores when in contact with water 

(e.g. Phytophthora), and other forms which germinate 

directly, i.e. by the formation of a germ tube 

(e.g. Peronospora). A similar series can be erected 

in the Mucorales where in some forms the 

number of sporangiospores per sporangium is 

reduced to several or even one (see Figs. 7.24, 

7.26, 7.30). One-spored sporangia may be distinguished 

from conidia by being surrounded by 

two walls, i.e. that of the sporangium and that 

of the spore itself. 

There are numerous other kinds of spore 

found in fungi, and they are described later in 

this book in relation to the particular groups in 

which they occur. 

1.4.9 Anamorphs and teleomorphs 

Fungi may exist in a range of forms or morphs, 

i.e. they may be pleomorphic. The morph which 

includes the sexually produced spore form, 

e.g. the ascocarp of an ascomycete or the 

basidiocarp of a basidiomycete, is termed the 

teleomorph (Gr. teleios, teleos ¼ perfect, entire; 

morphe ¼ shape, form) (Hennebert & Weresub, 

1977). Many fungi also have a morph bearing 

asexually produced spores, e.g. conidiomata. 

These asexual morphs are termed anamorphs 

(Gr. ana ¼ throughout, again, similar to). In the 

older literature, the term perfect state was used 

for the teleomorph and imperfect state for 

the anamorph. This is the origin of the name 

of the artificial group Fungi Imperfecti or 

Deuteromycetes, which included fungi believed 

to reproduce only by asexual means. The term 

mitosporic fungi is sometimes used alternatively 

for such fungi. The complete range of morphs 

belonging to any one fungus is termed the 

holomorph (Gr. holos ¼ whole, entire) (see 

Sugiyama, 1987; Reynolds & Taylor, 1993; 

Seifert & Samuels, 2000). Some fungi have more 

than one anamorph as in the microconidia and 

macroconidia of some Neurospora, Fusarium and 

Botrytis species. These distinctive states are 

synanamorphs and may play different roles in 

the biology of the fungus. The morph may have a 

purely sexual role as a fertilizing agent, e.g. in 

the case of spermatia of many ascomycetes and 

rust fungi. Such states have been termed 

andromorphs (Gr. andros ¼ a man, male) 

(Parbery, 1996a). 

The existence of different states in the life 

cycle of a fungus has nomenclatural consequences, 

because they had often been described 

separately and given different names before the 

genetic connection between them was established. 

Further, even after the proof of an 

anamorph teleomorph relationship, usually 

achieved by pure-culture studies, the 

anamorphic name may still be in wide use, 

especially where it is the more common state 

encountered in nature or culture. For example, 

most fungal geneticists refer to Aspergillus 

nidulans (the name of the conidial state) instead 

of Emericella nidulans (the name for the ascosporic 

state; p. 308). Similarly, most plant pathologists 

use Botrytis cinerea, the name for the conidial 

state of the fungus causing the common grey 

mould disease of many plants, in preference to 

the rarely encountered Sclerotinia (Botryotinia) 

fuckeliana, the name given to the apothecial 

(ascus-bearing) state (see p. 434). 

1.5 Taxonomy of fungi 

Taxonomy is the science of classification, i.e. the 

‘assigning of objects to defined categories’ (Kirk 

et al., 2001). Classification has three main functions: 

it provides a framework of recognizable 

features by which an organism under examination 

can be identified; it is an attempt to group 

together organisms that are related to each 

other; and it assists in the retrieval of information 

about the identified organism in the form of 

a list or catalogue. 

All taxonomic concepts are man-made and 

therefore to a certain extent arbitrary. This is 

especially true of classical approaches relying 

on macroscopic or microscopic observations 

because it is a matter of opinion whether the 

difference in a particular character say, a spore

TAXONOMY OF FUNGI 

33 

or the way in which it is formed is significant 

to distinguish two fungi and, if so, at which 

taxonomic level. The great fungal taxonomist 

R. W. G. Dennis (1960) described taxonomy as ‘the 

art of classifying organisms: not a science but an 

art, for its triumphs result not from experiment 

but from disciplined imagination guided by 

intuition’. 

Recently, great efforts have been made at 

introducing a seemingly more objective set of 

criteria based directly on comparisons of selected 

DNA sequences encoding genes with a conserved 

biological function, instead of or in addition to 

phenotypic characters. The results of such 

comparisons are usually displayed as phylogenetic 

trees (see Fig. 1.26), which imply a common 

ancestry to all organisms situated above a given 

branch. Such a grouping is ideally ‘monophyletic’. 

However, as we shall see later, quite 

different phylogenies may result if different 

genes are chosen for comparison. Further, a 

decision on the degree of sequence divergence 

required for a taxonomic distinction is based 

mainly on numerical parameters generated by 

elaborate computerized statistical treatments, 

occasionally at the expense of sound judgement. 

An excessive emphasis on such purely descriptive 

studies in the recent literature has led an 

eminent mycologist to characterize phylogenetic 

trees as ‘the most noxious of all weeds’. Despite 

their limitations, these methods have led to a 

revolution in the taxonomy of fungi. At present, 

a new, more ‘natural’ classification is beginning 

to take shape, in which DNA sequence data are 

integrated with microscopic, ultrastructural and 

biochemical characters. However, many groups 

of fungi are still poorly defined, and many more 

trees will grow and fall before a comprehensive 

taxonomic framework can be expected to be in 

place. One of the core problems in fungal 

taxonomy is the seemingly seamless transition 

between the features of two taxa, and the 

question as to where to apply the cut-off point. 

To quote Dennis (1960) again, ‘a taxonomic 

species cannot exist independently of the 

human race; for its constituent individuals can 

neither taxonomise themselves into a species, 

nor be taxonomised into a species by science in 

the abstract; they can only be grouped into 

species by individual taxonomisers’. 

1.5.1 Traditional taxonomic methods 

Early philosophers classified matter into three 

Kingdoms: Animal, Vegetable, and Mineral. 

Fungi were placed in the Vegetable Kingdom 

because of certain similarities to plants such as 

their lack of mobility, absorptive nutrition, and 

reproduction by spores. Indeed, it was at one 

time thought that fungi had evolved from algae 

by loss of photosynthetic pigmentation. This was 

indicated by the use of such taxonomic groups 

as Phycomycetes, literally meaning ‘algal fungi’. 

This grouping, approximately synonymous with 

the loose term ‘lower fungi’, is no longer used 

because it includes taxa not now thought to 

be related to each other (chiefly Oomycota, 

Chytridiomycota, Zygomycota). Early systems of 

classification were based on morphological 

(macroscopic) similarity, but the invention of 

the light microscope revealed that structures 

such as fruit bodies which looked alike could be 

anatomically distinct and reproduce in fundamentally 

different ways, leading them to be 

classified apart. 

Until the 1980s, the taxonomy of fungi was 

based mainly on light microscopic examination 

of typical morphological features, giving rise to 

classification schemes which are now known to 

be unnatural. Several examples of unnatural 

groups may be found by comparing the present 

edition with the previous edition of this textbook 

(Webster, 1980). Examples of traditional taxonomic 

features include the presence or absence 

of septa in hyphae, fine details of the type, 

formation and release mechanisms of spores (e.g. 

Kendrick, 1971), or aspects of the biology and 

ecology of fungi. Useful ultrastructural details, 

provided by transmission electron microscopy, 

concern the appearance of mitochondria, properties 

of the septal pore, details of the cell wall 

during spore formation or germination, or the 

arrangement of secretory vesicles in the apex of 

growing hyphae (Fig. 1.4). Biochemical methods 

have also made valuable contributions, especially 

in characterizing higher taxonomic levels. 

Examples include the chemical composition of


the cell wall (Table 1.1), alternative pathways 

of lysine biosynthesis (see p. 67), the occurrence 

of pigments (Gill & Steglich, 1987) and the types 

and amounts of sugars or polyols (Pfyffer et al., 

1986; Rast & Pfyffer, 1989). 

Microscopic features are still important today 

for recognizing fungi and making an initial 

identification which can then, if necessary, be 

backed up by molecular methods. Indeed, the 

comparison of DNA sequences obtained from 

fungi is meaningful only if these fungi have 

previously been characterized and named by 

conventional methods. It is therefore just as 

necessary today as it ever was to teach mycology 

students the art of examining and identifying 

fungi. 

1.5.2 Molecular methods of 

fungal taxonomy 

A detailed description of modern taxonomic 

methods is beyond the scope of this book, and 

the reader is referred to several in-depth reviews 

of the topic (e.g. Kohn, 1992; Clutterbuck, 1995). 

A particularly readable introduction to this 

subject has been written by Berbee and Taylor 

(1999). Only the most important molecular 

methods are outlined here. They are based 

either directly on the DNA sequences or on the 

properties of their protein products, especially 

enzymes. 

Proteins extracted from the cultures of fungi 

can be separated by their differential migration 

in the electric field of an electrophoresis gel. The 

speed of migration is based on the charge and 

size of each molecule, resulting in a characteristic 

banding pattern. Numerous bands will be 

obtained if the electrophoresis gel is stained with 

a general protein dye such as Coomassie Blue. 

More selective information can be obtained by 

isozyme analysis, in which the gel is incubated 

in a solution containing a particular substrate 

which is converted into a coloured insoluble 

product by the appropriate enzyme, or in which 

an insoluble substrate such as starch is digested. 

In this way, the number and electrophoretic 

migration patterns of isoenzymes can be 

compared between different fungal isolates. 

Protein analysis is useful mainly for 

distinguishing different strains of the same 

species or members of the same genus (Brasier, 

1991a). 

Gel electrophoresis can also be used for the 

separation of DNA fragments generated by 

various methods. One such method is called 

RFLP (restriction fragment length polymorphisms) 

and involves the digestion of a total 

DNA extract or a previously amplified target 

sequence with one or more restriction endonucleases, 

i.e. enzymes which cut DNA only at 

a particular target site defined by a specific 

oligonucleotide sequence. Fragments from this 

digest can be blotted from the gel onto 

a membrane; fragments belonging to a known 

gene can be visualized by hybridizing with 

a fluorescent or radioactively labelled DNA 

probe of the same gene. In this way, a banding 

pattern is obtained and can be compared with 

that of other fungal isolates prepared under 

identical experimental conditions. 

A similar method, RAPD (random amplified 

polymorphic DNA), produces DNA bands not by 

digestion, but by the amplification of DNA 

sequences. For this purpose, a DNA extract is 

incubated with a DNA polymerase, deoxynucleoside 

triphosphates and one or more short 

oligonucleotides which act as primers for the 

polymerase by binding to complementary DNA 

sequences which should be scattered throughout 

the genome. Amplification is achieved by means 

of the PCR (polymerase chain reaction), in which 

the mixture is subjected to repeated cycles of 

different temperatures suitable for annealing of 

DNA and primer, polymerization, and dissociation 

of double-stranded DNA. The largest possible 

size of the amplification product depends on the 

polymerization time; bands visible on a gel will 

be produced only if two primer binding sites 

happen to be in close proximity to each other, so 

that the intervening stretch of DNA sequence can 

be amplified from both ends within the chosen 

polymerization time. The number and size of 

RAPD bands on electrophoresis gels can be 

compared between different fungi, provided 

that all samples have been produced under 

identical conditions. 

Isozyme, RFLP and RAPD analyses all generate 

data which are useful mainly for comparing


35 

closely related isolates. Since the results strongly 

depend on the experimental conditions 

employed, there are no universal databases for 

these types of analysis. Further, they are unsuitable 

for comparisons of distantly related or 

unrelated organisms. A breakthrough in the 

taxonomy of fungi as well as other organisms 

was achieved when primers were developed 

which guided the PCR amplification of specific 

stretches of DNA universally present and fulfilling 

a homologous function in all life forms. Once 

amplified, the sequence of bases can be determined 

easily. Such methods were first applied to 

bacterial systematics with spectacular results 

(Woese, 1987). In eukaryotes, the most widely 

used target sequences are those encoding the 18S 

or 28S ribosomal RNA (rRNA) molecules, which 

fulfil a structural role in the small or large 

ribosomal subunits (respectively), or the noncoding 

DNA stretches (ITS, internal transcribed 

spacers), which physically separate these genes 

from each other and from the 5.8S rRNA 

sequence in the nuclear genome (Fig. 1.24; 

White et al., 1990). The structural role which 

rRNA molecules play in the assembly of ribosomes 

requires them to take up a particular 

configuration which is stable because of intramolecular 

base-pairing. Since certain regions of 

each rRNA molecule hybridize with complementary 

regions within the same molecule or with 

other rRNA molecules, mutations in the DNA 

encoding these regions are rare because they 

would impair hybridization and thus the functioning 

of the rRNA molecule unless accompanied 

by a mutation at the complementary 

binding site. The non-pairing loop regions of 

the rRNA gene and the ITS sequences are not 

subjected to such a strong selective pressure and 

thus tend to show a higher rate of mutation. 

Nucleotide sequences therefore permit the 

comparison of closely related species or even 

strains of the same species (ITS sequences), as 

well as that of distantly related taxa or even 

members of different kingdoms (18S or 28S 

rRNA). Further, because extensive databases are 

now available, the sequence analysis of a single 

fungus can provide meaningful taxonomic information 

when compared with existing sequences. 

In addition to ribosomal DNA sequences, genes 

encoding cytochrome oxidase (COX), tubulins or 

other proteins with conserved functions are now 

used extensively for phylogenetic purposes. 

Once comparative data have been obtained 

either by banding patterns or gene sequencing, 

they need to be evaluated. This is usually done by 

converting the data into a matrix, e.g. by scoring 

the absence or presence of a particular band. 

With comparisons of aligned DNA sequences, 

only informative positions are selected for the 

matrix, i.e. where variations in the nucleotides 

between different fungi under investigation are 

observed. When the matrix has been completed, 

it can be subjected to statistical treatments, 

and phylogenetic trees are drawn by a range of 

algorithms. In some, the degree of relatedness 

of taxa is indicated by the length of the branch 

separating them (see Figs. 1.25, 1.26). Such 

information is thought to be of evolutionary 

significance; the greater the number of differences 

between two organisms, the earlier the 

separation of their evolutionary lines should 

have occurred. 

1.5.3 How old are fungi? 

Several lines of evidence indicate that fungi are a 

very ancient group of organisms. Berbee and 

Taylor (2001) have attempted to add a timescale 

to phylogenetic trees by applying the concept of 

a ‘molecular clock’, i.e. the assumption that the 

rate of mutations leading to phylogenetic diversity 

is constant over time and in various groups 

of organisms. By calibrating their molecular 

clock against fossil evidence, Berbee and Taylor 

(2001) estimated that fungi may have separated 

from animals some 900 million years ago, 

i.e. long before the evolution of terrestrial 

organisms. This estimate is consistent with the 

discovery of fossilized anastomozing hypha-like 

structures in sediments about 1 billion years 

old (Butterfield, 2005). Fungi recognizable as 

Chytridiomycota, Zygomycota and Ascomycota 

have been discovered among fossils of early 

terrestrial plants from the Lower Devonian 

Rhynie chert, formed some 400 million years 

ago (Taylor et al., 1992, 1999, 2005). It is apparent 

that these early terrestrial plants already entertained 

mycorrhizal symbiotic associations


Fig1.24 The spatial arrangement of a nuclear rRNA gene repeat unit. Each haploid fungal genome contains about 50 250 copies 

of this repeat, depending on the species (Vilgalys & Gonzalez,1990).The three structural rRNA genes encoded by one repeat unit, 

i.e.18S, 5.8S and 28S, are separated by internal and external transcribed spacers (ITS and ETS, respectively). Adjacent copies of 

the repeat unit are separated by a short non-transcribed spacer (NTS).The whole unit is transcribed into a 45S precursor RNA in 

one piece, followed by excision of the three structural RNA molecules from the spacers which are not used.The 5S rRNA gene 

is encoded at a separate locus.The18S rRNA molecule is part of the small ribosomal subunit, whereas the other three contribute 

to the large subunit. 

Fig1.25 The phylogenetic relationships of Fungi and fungus-like organisms studied by mycologists (printed in bold), with other 

groups of Eukaryota.The analysis is based on comparisons of18SrDNA sequences.Modified andredrawn from Brunset al.(1991)and 

Berbee and Taylor (1999).


37 

Fig1.26 Phylogenetic relationships within the Eumycota, based on18S rDNA comparisons.This tree illustrates the analytical 

power of molecular phylogenetic analyses; all four phyla of Eumycota are resolved. However, it also highlights problems in that 

Basidiobolus groups with the Chytridiomycota, although sharing essential biological features with the Zygomycota, and that 

conversely Blastocladiella groups with the Zygomycota instead of the Chytridiomycota. Modified and redrawn from Berbee and 

Taylor (2001), with kind permission of Springer Science and Business media. 

with glomalean members of the Zygomycota 

(see p. 218). 

1.5.4 The taxonomic system adopted 

in this book 

The discipline of fungal taxonomy is evolving at 

an unprecedented speed at present due mainly 

to the contributions of molecular phylogeny. 

Numerous taxonomic systems exist, but this is 

not the place to discuss their relative merits 

(see Whittaker, 1969; Margulis et al., 1990; 

Alexopoulos et al., 1996; Cavalier-Smith, 2001; 

Kirk et al., 2001). In this book we have tried to 

follow the classification proposed in The Mycota 

Volumes VIIA and VIIB (McLaughlin et al., 2001), 

but even in these volumes the authors of 

different chapters have used their own favoured 

systems of classification rather than adopting 

an imposed one. In cases of doubt, we have 

attempted to let clarity prevail over pedantry. 

Fungi in the widest sense, as organisms 

traditionally studied by mycologists, currently 

fall into three kingdoms of Eukaryota, i.e. the 

Eumycota which contain only fungi, and the 

Protozoa and Chromista (¼ Straminipila), both 

of which contain mainly organisms not studied 

by mycologists and were formerly lumped 

together under the name Protoctista (Beakes, 

1998; Kirk et al., 2001). The Protozoa are 

notoriously difficult to resolve by phylogenetic 

means, and the only firm statement which can 

be made at present is that they are a diverse 

and ancient group somewhere between the 

higher Eukaryota (‘crown eukaryotes’) and the


Table1.2. The classification scheme adopted in 

this book, showing mainly those groups treated in 

some detail. 

KINGDOM PROTOZOA 

Myxomycota (Chapter 2) 

Acrasiomycetes 

Dictyosteliomycetes 

Protosteliomycetes 

Myxomycetes 

Plasmodiophoromycota (Chapter 3) 

Plasmodiophorales 

Haptoglossales (Oomycota?) 

KINGDOM STRAMINIPILA 

Hyphochytriomycota (Chapter 4) 

Labyrinthulomycota (Chapter 4) 

Labyrinthulomycetes 

Thraustochytriomycetes 

Oomycota (Chapter 5) 

Saprolegniales 

Pythiales 

Peronosporales 

KINGDOM FUNGI (EUMYCOTA) 

Chytridiomycota (Chapter 6) 

Chytridiomycetes 

Zygomycota (Chapter 7) 

Zygomycetes 

Trichomycetes 

Ascomycota (Chapter 8) 

Archiascomycetes (Chapter 9) 

Hemiascomycetes (Chapter10) 

Plectomycetes (Chapter11) 

Hymenoascomycetes 

Pyrenomycetes (Chapter12) 

Erysiphales (Chapter13) 

Pezizales (Chapter14) 

Helotiales (Chapter15) 

Lecanorales/lichens (Chapter16) 

Loculoascomycetes (Chapter17) 

Basidiomycota (Chapter18) 

Homobasidiomycetes (Chapter19) 

Homobasidiomycetes: gasteromycetes 

(Chapter 20) 

Heterobasidiomycetes (Chapter 21) 

Urediniomycetes (Chapter 22) 

Ustilaginomycetes (Chapter 23) 

prokaryotes (Kumar & Rzhetsky, 1996). An overview 

of eukaryotic organisms, in which those 

groups treated in this book are highlighted, 

is given in Fig. 1.25. Among the Protozoa, the 

Plasmodiophoromycota are given extensive 

treatment because of their role as pathogens 

of plants (Chapter 3), whereas the various 

forms of slime moulds are considered only 

briefly (Chapter 2). Similarly brief overviews 

will be given of most groups of Straminipila 

studied by mycologists (Chapter 4), except for 

the Oomycota which, despite their separate 

evolutionary origin, represent a major area of 

mycology (Chapter 5). All remaining chapters 

deal with members of the Eumycota (¼ Kingdom 

Fungi). The scheme is summarized in Table 1.2 

and illustrated in Fig. 1.26. An overview of the 

nomenclature used for describing taxa within 

the Eumycota is given in Table 1.3. 

In the past, fungi which solely or mainly 

reproduce asexually (Fungi Imperfecti, 

Deuteromycota, mitosporic fungi, anamorphic 

fungi) were considered separately from their 

sexually reproducing relatives the teleomorphs, 

and separate anamorph and teleomorph 

genera were erected. However, information 

from pure-culture studies and molecular phylogenetic 

approaches has linked many anamorphs 

with their teleomorphs. For instance, the conidial 

(imperfect) state of the common brownrot 

fungus of apples and other fruits is called 

Monilia fructigena, whereas the sexual (perfect) 

Table 1.3. Example of the hierarchy of taxonomic 

terms. The wheat stem rust fungus, Puccinia 

graminis, is used as an example. 

Kingdom Fungi 

Subkingdom Eumycota 

Phylum Basidiomycota 

Class Urediniomycetes 

Order Uredinales 

Family Pucciniaceae 

Genus Puccinia 

Species Puccinia graminis 

Race Puccinia graminis 

f. sp. tritici


39 

state is apothecial, being called Sclerotinia 

(Monilinia) fructigena. As far as is possible, we 

shall consider anamorphic states of fungi in 

the context of their known sexual state. Thus, 

an account of the brown-rot of fruits, although 

encountered predominantly as the conidial 

state, will be given in the chapter dealing 

with apothecial fungi (Helotiales, Chapter 15). 

Where practical, we have given the teleomorph 

name priority over the anamorph. As a longterm 

future goal, Seifert and Samuels (2000) 

and Seifert and Gams (2001) have outlined 

a unified taxonomy which might ultimately 

lead to the abolition of the names of anamorphic 

genera. 

However, with certain ecological groups 

such as the Ingoldian aquatic fungi (Section 

25.2) and nematophagous fungi (Section 25.1), 

which have diverse relationships, we have 

deliberately chosen to consider them in their 

ecological context rather than along with their 

varied taxonomic relatives.

2 

Protozoa: Myxomycota (slime moulds) 

2.1 Introduction 

When the first slime moulds were described 

by Johann H. F. Link in 1833, they were given 

the term myxomycetes (Gr. myxa ¼ slime). Link 

used the suffix -mycetes because of the superficial 

similarity of the fructifications of slime moulds 

with the fruit bodies of certain fungi, notably 

Gasteromycetes (see Chapter 20). Although it 

has been appreciated for some time that they 

lack any true relationship with the Eumycota 

(de Bary, 1887; Whittaker, 1969), slime moulds 

have none the less been studied mainly by 

mycologists rather than protozoologists, probably 

because they occur in the same habitats 

as fungi and are routinely encountered during 

fungus forays. Since slime moulds are only 

rarely covered by zoology courses even today, 

they are briefly described in this chapter, 

referring to more specialized literature as 

appropriate. 

Slime moulds differ substantially from 

the Eumycota not only in phylogenetic terms, 

but also regarding their physiology and ecology. 

Their vegetative state is that of individual 

amoebae in the cellular slime moulds, or of 

a multinuclear (coenocytic) plasmodium in the 

plasmodial slime moulds. Motile stages bearing 

usually two anterior whiplash-type flagella may 

be present in the plasmodial slime moulds 

(Sections 2.4, 2.5) and in the Plasmodiophoromycota 

(Chapter 3). Amoebae or plasmodia feed 

by the ingestion (phagocytosis) of bacteria, 

yeast cells or other amoebae. This is followed by 

intracellular digestion in vacuoles. The mode of 

nutrition in slime moulds is therefore fundamentally 

different from extracellular degradation 

and absorption as shown by Eumycota. 

Numerous phylogenetic analyses of DNA 

sequences encoding rRNA molecules and various 

structural proteins or enzymes have been carried 

out, but the results obtained are difficult to 

interpret because the comparison of different 

genes have led to rather variable phylogenetic 

schemes. Of the four groups treated in this chapter, 

it seems that the Dictyosteliomycetes, 

Protosteliomycetes and Myxomycetes are related 

to each other whereas the Acrasiomycetes have 

a different evolutionary origin (Baldauf, 1999; 

Baldauf et al., 2000). The general evolutionary 

background is, however, still rather diffuse in 

these lower eukaryotes. 

2.2 Acrasiomycetes: acrasid cellular 

slime moulds 

The Acrasiomycetes, or Acrasea as they are called 

in zoological classification schemes, are a small 

group currently comprising 12 species in six 

genera (Kirk et al., 2001). Although appearing 

somewhat removed from the bulk of the slime 

moulds, they still clearly belong to the Protozoa 

(Roger et al., 1996). The trophic stage consists 

of amoebae which are morphologically distinct 

from those of the dictyostelid cellular slime 

moulds (Section 2.3) in having a cylindrical, 

rather than flattened, body bearing a single

DICTYOSTELIOMYCETES: DICTYOSTELID SLIME MOULDS 

41 

Fig 2.1 Amoebae of cellular slime moulds.The arrows indicate the direction of movement at the time when the photomicrographs 

were taken. (a) Limax-type amoeba of Acrasisrosea, an acrasid cellular slime mould.Note the absence of granular contents from the 

lobose pseudopodium at the tip of the amoeba. (b) Amoeba of Protostelium mycophaga with filose pseudopodia. Reproduced from 

Zuppinger and Roos (1997), with permission from Elsevier; original prints kindly supplied by C. Zuppinger. 

large-lobed (lobose) anterior pseudopodium. The 

granular cellular contents trail behind the pseudopodium, 

which appears clear. The posterior 

end is knob-shaped and is called the uroid 

(Fig. 2.1a). Such amoebae are of the limax type 

because their movement resembles that of slugs 

of the genus Limax. Good accounts of the acrasids 

have been given by Olive (1975) and Blanton 

(1990). 

Acrasid slime moulds are common on decaying 

plant matter, in soil, on dung and on rotting 

mushrooms, but they are rarely recorded 

because of their small size, which necessitates 

observations with a dissecting microscope. The 

most readily recognized species is Acrasis rosea, 

which has orange- or pink-coloured amoebae 

due to the presence of carotenoid pigments, 

including torulene (Fuller & Rakatansky, 1966). 

Acrasis rosea can be observed if dead twigs, 

leaves or fruits are incubated on weak nutrient 

agar for a few days. Spore-bearing structures 

called sorocarps (Gr. sorus ¼ heap, karpos ¼ fruit) 

will develop, and spores can be transferred to 

fresh agar with yeast cells as a food source 

(Blanton, 1990). The uninucleate amoebae feed 

on yeast cells, bacteria or fungal spores and can 

encyst under unfavourable conditions, especially 

drought, to form microcysts. Each microcycst 

germinates again to release a single amoeba. 

Eventually amoebae aggregate to form a pseudoplasmodium, 

in which the individual amoebae 

retain their identity but are surrounded by a 

common sheath. The chemical signal for aggregation 

is unknown but it is not cyclic AMP (cAMP) 

as in the dictyostelid slime moulds (see below). 

The pseudoplasmodium develops into a 

branched sorocarp in which the amoebae align 

themselves in single rows and then round off, 

each forming a walled spore. Each spore germinates 

to release a single amoeba. The cells 

making up the stalk of the sorocarp also encyst 

and are capable of germination (Olive, 1975). 

Sexual reproduction in the acrasid slime 

moulds is unknown. 

2.3 Dictyosteliomycetes: 

dictyostelid slime moulds 

The Dictyosteliomycetes (zool.: Dictyostelia) are 

a group of cellular slime moulds comprising

42 PROTOZOA: MYXOMYCOTA (SLIME MOULDS) 

46 species in four genera (Kirk et al., 2001). 

The best-known example is Dictyostelium which 

has been so named because the stalk of its multicellular 

sorocarp appears as a network, made up 

from cellulose walls secreted by the amoebae 

from which it is formed. Dictyostelium spp. are 

common in soil, on decaying plant material 

and on dung, and can be demonstrated by smearing 

non-nutrient agar with cells of a suitable 

bacterial food such as Escherichia coli or Klebsiella 

aerogenes, and adding a small crumb of moistened 

soil to the centre of the bacterial smear. 

Amoebae will creep out of the soil and consume 

the bacteria. At the end of the feeding 

phase, sorocarps develop and isolations can be 

made (Cavender, 1990). An axenic defined 

medium has been developed for D. discoideum 

and has greatly facilitated experimentation 

with this organism (Franke & Kessin, 1977). 

Good general accounts of the dictyostelids are 

those by K. B. Raper (1984), Cavender (1990) and 

Alexopoulos et al. (1996). The history of research 

on Dictyostelium has been recounted by Bonner 

(1999). Work on D. discoideum has contributed 

significantly to our understanding of the key 

features of eukaryotic cell biology, especially 

signalling events, phagocytosis, and the evolution 

of multicellularity in animals. Consequently, 

there is a vast literature on this organism. 

An excellent introduction to the impact of 

research on D. discoideum on general eukaryotic 

biology is the book by Kessin (2001), and challenging 

questions have been summarized by Ratner 

and Kessin (2000). Bonner (2001) has also 

provided a stimulating read. 

The life cycle of D. discoideum is shown in 

Fig. 2.2. Amoebae of dictyostelids are morphologically 

different from those of acrasids in that 

they have filose (acutely pointed) rather than 

lobose pseudopodia (see Fig. 2.1b). Each spore 

from a sorocarp germinates to give rise to one 

uninucleate haploid amoeba which feeds by 

phagocytosis of bacteria. Amoebae reproduce 

asexually by division to form two haploid daughter 

amoebae. As with acrasid slime moulds, 

the amoebae of dictyostelids can form microcysts 

under unfavourable environmental conditions. 

Encystment may be triggered by the production 

of ammonia, which thus functions as a 

signal molecule (Cotter et al., 1992). Sexual reproduction 

occurs by means of macrocysts and is 

initiated when two compatible amoebae meet 

and fuse. Both homothallic and heterothallic 

species and strains of Dicytostelium are known. 

In D. discoideum, fusion is inhibited by light and 

by the presence of cAMP, but is stimulated by 

ethylene (Amagai, 1992). The fusion cell is greatly 

enlarged relative to the two progenitor amoebae. 

This giant cell attracts unfused amoebae which 

aggregate and secrete a sheath (primary wall) 

around themselves and the zygote. Inside the 

primary wall, the giant cell undergoes karyogamy, 

and the resulting zygote feeds cannibalistically 

on the other amoebae by phagocytosis 

and eventually produces a secondary wall. 

Cellulose seems to be the main structural wall 

polymer. Meiosis is followed by mitotic divisions 

and cytoplasmic cleavage, and the macrocyst 

germinates to release numerous haploid uninucleate 

amoebae (Nickerson & Raper, 1973; 

Szabo et al., 1982). 

The most striking feature of D. discoideum 

is the aggregation of thousands of amoebae to 

form a pseudoplasmodium with radiating arms 

(Figs. 2.3a,b). This is a vegetative process not 

involving meiosis or mitosis. Aggregation is 

initiated when the bacterial food supply is 

exhausted, and follows the gradient of a hormone 

which causes directional (chemotactic) 

movement of starving amoebae (Konijn et al., 

1967; Swanson & Taylor, 1982). In the case of 

D. discoideum, the hormone is cAMP (Konijn 

et al., 1967), but other molecules are implicated 

in this role in different dictyostelids. Upon exposure 

to a cAMP gradient, amoebae of D. discoideum 

change their shape from isodiametric to elongated, 

with the migrating tip pointing towards 

the highest cAMP concentration. Migration 

occurs in waves which correspond to the production 

of cAMP by starving amoebae, its detection 

and further synthesis by neighbouring amoebae, 

and its degradation by cAMP phosphodiesterase 

(Nagano, 2000; Weijer, 2004). In this way, waves 

of cAMP diffuse outwards, and waves of amoebae 

migrate inwards. During aggregation, amoebae 

migrate to the centre or one of the arms of the 

pseudoplasmodium. This is a highly co-ordinated 

effort in which hundreds of thousands of

DICTYOSTELIOMYCETES: DICTYOSTELID SLIME MOULDS 

43 

Fig 2.2 Life cycle of Dictyostelium discoideum.The central feature is the haploid amoeba which is free-living in the soil. It divides 

mitotically to produce two daughter amoebae or, under unfavourable conditions, may form a microcyst. If two amoebae of 

compatible mating type meet, a diploid macrocyst may be formed which can remain dormant for some time and eventually 

germinates by meiosis and then mitosis to release numerous haploid amoebae.Under certain circumstances, starvation may lead to 

aggregation of amoebae to form a slug and a sorocarp in which individual amoebae become converted into spores.These are purely 

asexual, and meiosis is not involved in their formation or germination.Open and closed circles represent haploid nuclei of opposite 

mating type; diploid nuclei are larger and half-filled. Key events in the life cycle are plasmogamy (P), karyogamy (K) and meiosis (M). 

amoebae from an area of 1 cm 2 of soil can be 

involved. Aggregating amoebae adhere to each 

other and secrete a common slime sheath 

(Figs. 2.3c,d). Eventually they pile up to form a 

compact bullet-shaped slug which flops over 

onto the substratum. In D. discoideum and some 

other species, the slug undergoes a period of 

migration towards the light (Figs. 2.3e g). The 

individuality of amoebae is retained within the 

slug. As the slug moves along, it leaves behind a 

slime trail. Within the slug, the amoebae are 

divided into two functionally different populations, 

i.e. an anterior group of large, highly 

vacuolated cells (pre-stalk cells) and a posterior 

group of smaller ones, the pre-spore cells 

(Fig. 2.4). It is the pre-stalk group of cells which 

co-ordinates slug migration by secreting cAMP. 

Various environmental stimuli can direct movement. 

For instance, the anterior end of the slug 

follows an oxygen gradient but is repelled by 

ammonia. Temperature as well as light can also 

act as triggers of directed movement. The end of 

the migration phase is marked by the roundingoff 

and erection of the pseudoplasmodium to 

form a flat-based, somewhat conical structure, 

which undergoes further development by differentiating 

into a multicellular stalk composed of 

the large anterior cells, and the sorus which rises 

up on the outside of the stalk (Figs. 2.3h j, 2.4). 

This final stage of development is called culmination. 

About 80% of the amoebae become 

converted into spores, with the remainder 

being sacrificed for the formation of the fruit 

body structure.


Fig 2.3 Dictyostelium discoideum development. (a) Aggregation of amoebae. (b) Aggregation, enlarged. (c) Amoebae feeding 

on bacteria; note their isodiametric shape. (d) Aggregating amoebae; note their elongated shape. (e) Late aggregation stage. 

(f,g) Migration stage. (h) Culmination; the spore mass is rising around the stalk. (i) Spore mass almost at the apex of the stalk. 

(j) Mature sorocarps. 

The ability of free-living individual amoebae 

of Dictyostelium to aggregate into the multicellular 

slug has led to dictyostelid slime moulds 

being called social amoebae (Kessin, 2001). This 

phenomenon gives rise to interesting and fundamental 

questions. To give an example, since 

amoebae in the anterior end of the slug become 

stalk cells and are thus excluded from perpetuation 

as spores, cells skiving off to the rear of the 

slug and thereby avoiding self-sacrifice would 

have a selective advantage. ‘Cheater strains’ are 

indeed known from nature and the laboratory;

PROTOSTELIOMYCETES: PROTOSTELID PLASMODIAL SLIME MOULDS 

45 

Fig 2.4 Dictyostelium discoideum. Development of sorocarp (after Bonner,1944). (a) (c) Aggregation. (d) (h) Migration. 

(i) (n) Culmination. C 1 

End of aggregation. H 1 

End of migration. I 1 

Beginning of culmination and stalk formation. J 1 

Flattened stage 

of culmination. I 1 

A later stage of culmination. 

some of them cheat only to a degree or only 

if altruistic non-cheater strains are present, 

whereas others are entirely unable to make a 

fruit body in the absence of wild-type amoebae 

prepared to form the pre-stalk cells (Dao et al., 

2000; Strassmann et al., 2000). The cheater 

phenomenon has raised thought-provoking questions 

about the evolution and control of cheating 

in social systems (Hudson et al., 2002). 

Another interesting aspect involves the mode 

of nutrition of Dictyostelium by the phagocytosis 

of bacterial cells. Several bacteria pathogenic to 

humans and other animals, e.g. Pseudomonas 

aeruginosa and Legionella pneumophila, also kill 

Dictyostelium upon ingestion (Solomon et al., 

2000; Pukatzki et al., 2002). The observation 

that interactions between Dictyostelium amoebae 

and phagocytosed bacterial pathogens are similar 

to those involving human phagocytes may 

stimulate further research on this fascinating 

slime mould (Steinert & Heuner, 2005). 

2.4 Protosteliomycetes: protostelid 

plasmodial slime moulds 

This class of organisms (zool.: Protostelea) comprises 

14 genera and 35 species (Kirk et al., 2001).


Useful treatments of the group have been 

written by Olive (1967, 1975) and Spiegel (1990). 

Protostelids are ubiquitous on decaying plant 

parts in soil and humus, as well as on dung 

or in freshwater. They occur in all climatic 

zones from the tundra to tropical rainforests. 

Protostelids produce amoebae with filose pseudopodia 

(Fig. 2.1b), feeding phagocytotically on 

bacteria, yeast cells or spores of fungi. Some 

species also produce small plasmodia, thereby 

providing structural affinities to both the cellular 

and plasmodial slime moulds. Sporulation 

occurs by the conversion of a feeding amoeba 

or plasmodium into a round prespore cell 

which then rises at the tip of a delicate acellular 

stalk, ultimately forming one or several spores 

in a single sporangium. It is possible to isolate 

protostelids by transferring a spore from its 

stalk onto a weak nutrient agar plate with 

appropriate food organisms. 

Protostelium is a typical member of the group 

(Fig. 2.5). The sporocarp consists of a long, slender 

stalk about 75 mm long, bearing a single spherical 

spore about 4 10 mm in diameter. The spore 

is deciduous and readily detached. Upon germination, 

a single uninucleate amoeba with thin 

pseudopodia emerges. The amoeboid stage 

feeds voraciously on yeast cells and may also 

feed cannibalistically on amoebae of the same 

species. Development of the sporocarp probably 

follows the generalized pattern described by 

Olive (1967) and summarized in Fig. 2.6. When 

feeding stops, the amoeba rounds off and 

heaps its protoplasm in the centre to form the 

‘hat-shaped’ stage (Fig. 2.6b). A membranous, 

pliable, impermeable sheath develops over the 

surface of the cell. When the protoplast contracts 

into the central hump, the sheath collapses 

at the margins, forming the disc-like base to 

the stalk of the sporocarp. This may be the 

structural equivalent of the hypothallus of the 

Myxomycetes (see p. 48). Within the protoplast, 

a granular basal core, the steliogen, differentiates 

and begins to mould a hollow tube 

(Figs. 2.6d,e). As the tube extends at its tip, 

the protoplast migrates upwards, always seated 

on top of the growing tip. The entire structure 

remains covered by the sheath. Tube extension 

is an actin myosin-driven process (Spiegel 

et al., 1979). Ultimately, the steliogen is left 

behind at the tip of the stalk to form an apophysis 

(Fig. 2.5a), and the protoplast secretes a cell 

wall and becomes the spore. 

Variations of this pattern occur within 

the protostelids. For instance, some species 

produce spores which are discharged forcibly 

(e.g. Spiegel, 1984). In Ceratiomyxa fruticulosa, 

a species which may or may not belong to 

the Protosteliomycetes (Spiegel, 1990; Kirk et al., 

2001; Clark et al., 2004), numerous spores are 

formed externally on a sporocarp (Figs. 2.7a,b) 

and are the product of meiosis. They germinate 

to release a single quadrinucleate protoplast 

(Figs. 2.7c e) which divides repeatedly to 

produce a clump of four and later eight haploid 

cells, the octette stage (Figs. 2.7f,g). Each of these 

cells releases a motile cell (a swarmer) which 

has one or two whiplash-type flagella (Fig. 2.7h). 

Fig 2.5 Protostelium sp. (a) Two sporocarps, one 

immature, the other with a detached spore. Note the 

apophysis beneath the spore. (b) Empty spore case after 

germination. (c) Amoeboid phase.

MYXOMYCETES: TRUE (PLASMODIAL) SLIME MOULDS 

47 

Fig 2.6 Sporogenesis in a 

protostelid (after Olive,1967). 

(a) Early pre-spore stage. 

(b) Hat-shaped stage. 

(c) Appearance of the steliogen. 

(d) Beginning of stalk formation. 

(e) Later stage in stalk development, 

with steliogen extending into 

upper part of stalk tube. (f) Mature 

sporocarp showing terminal spore, 

with subtending apophysis, outer 

sheath, and inner stalk tube. 

The swarmers eventually fuse to form a diploid 

zygote which initiates the plasmodial stage 

(Figs. 2.7i,j), from which the sporocarp develops 

(Spiegel, 1990). Ceratiomyxa fruticulosa thus 

shows features of both the Protosteliomycetes 

in producing its spores externally, and the 

Myxomycetes (see below) in having a flagellated 

stage in its life cycle. Its precise phylogenetic 

position remains to be established. This species 

is probably homothallic (Clark et al., 2004). 

Its whitish semitransparent sporocarps are 

rather common on the surface of rotting wood 

(Plate 1a). 

2.5 Myxomycetes: true (plasmodial) 

slime moulds 

Fig 2.7 Ceratiomyxa fruticulosa. (a) Fruiting sporocarp bearing 

stalked spores. (b) Portion of the surface of the sporocarp 

showing spores and their attachment. (c) Spore. (d) Naked 

protoplast emerging from the spore at germination. (e) Naked 

protoplast before cleavage. (f) Cleavage of protoplast to form 

a tetrad of protoplasts. (g) Octette stage: a clump of eight 

protoplasts. (h) Uniflagellate and biflagellate swarmer released 

from the octette protoplasts. (i) Copulation of swarmers by 

their posterior ends. (j) Young plasmodium: c, contractile 

vacuole; s, ingested spore within food vacuole. (c i) to same 

scale. 

The Myxomycetes (zool.: Myxogastrea) are by 

far the largest group of slime moulds, comprising 

some 800 species in 62 genera which 

are currently divided into five orders (Kirk 

et al., 2001). General accounts have been given 

by Frederick (1990), Stephenson and Stempen 

(1994) and Alexopoulos et al. (1996). A monograph 

of British species has been compiled by Ing 

(1999). These are the familiar slime moulds 

so common on moist, decaying wood and 

other organic substrata. They are also abundant 

in soil and may fulfil ecological functions 

which are as yet poorly understood (Madelin, 

1984). 

The vegetative phase is a free-living plasmodium, 

i.e. a multinucleate wall-less mass of 

protoplasm. This may or may not be covered


by a slime sheath. Plasmodia vary in size and can 

be loosely grouped into three categories. 

(1) Protoplasmodia are inconspicuous microscopic 

structures usually giving rise only to a 

single sporangium. They resemble the simple 

plasmodia of protostelids. 

(2) Aphanoplasmodia (Gr. aphanes ¼ invisible) 

are thin open networks of plasmodial strands. 

The aphanoplasmodium is transparent, with 

individual strands only 5 10 mm wide and the 

entire plasmodium about 100 200 mm in diameter. 

Most aphanoplasmodia are only seen 

with the aid of a dissection microscope. 

(3) Phaneroplasmodia (Gr. phaneros ¼ visible) 

are large sheets or networks with conspicuous 

veins (Fig. 2.8a) within which the protoplasm 

shows rhythmic and reversible streaming, each 

pulse lasting about 60 90 s. This striking phenomenon 

is readily observed with a dissection 

microscope and is probably due to interactions 

of Ca 2þ ions with cytoskeletal elements lining 

the veins (see Section 2.5.3). 

2.5.1 Life cycle of myxomycetes 

The life cycle of Physarum polycephalum, a typical 

myxomycete, is summarized in Fig. 2.9. The plasmodium 

is diploid and feeds by phagocytosis of 

bacteria, yeasts or fungal mycelia or spores. 

It gives rise to a sporophore under appropriate 

conditions. The haploid spores are dispersed 

Fig 2.8 Phaneroplasmodia of Physarum polycephalum. 

(a) Margin of extending plasmodium.The protoplasm 

is particularly dense at the advancing edge.Further 

behind, protoplasm is concentrated in large veins 

which show rhythmic pulsation. (b) Fusion between 

compatible plasmodia. Note the complete fusion of 

veins. (c) Lethal reaction following fusion between 

incompatible plasmodia. (a) from Carlile (1971), 

(b) and (c) from Carlile and Dee (1967), by permission 

of Academic Press (a) and Macmillan Journals (b,c). 

Original prints kindly supplied by M. J.Carlile.


49 

Fig 2.9 Life cycle of the myxomycete Physarum polycephalum. Spores released from the sporangium are haploid and can germinate 

by releasing either a single myxamoeba or a swarmer cell.These two cell types are interconvertible.The myxamoeba can divide 

mitotically. In P. polycephalum, plasmogamy (P) usually takes place between swarmers which must belong to different mating types. 

Karyogamy (K) follows, and the diploid zygote establishes a phaneroplasmodium.When nutrients become limiting, a sporophore is 

formed and differentiates sporangia in which meiosis (M) occurs.Unfavourable conditions can be overcome at the haploid stage 

when the myxamoeba forms a microcyst, or at the diploid stage when the plasmodium forms sclerotia.Open and closed circles 

represent haploid nuclei of opposite mating type; diploid nuclei are larger and half-filled. 

by wind or insects and, depending on environmental 

conditions such as moisture, germinate 

by releasing either amoebae or zoospores 

(swarmers) with usually two anterior whiplash 

flagella, of which one is shorter than the other 

and is thus often invisible (Fig. 2.10). The amoebae 

are called myxamoebae, in order to distinguish 

them from the amoebae of cellular 

slime moulds which have a different function 

in the life cycle. Myxamoebae are capable of 

asexual reproduction by division. Swarmers 

cannot divide, but can readily and reversibly 

convert into myxamoebae. Under adverse conditions, 

myxamoebae secrete a wall to form 

microcysts. Both swarmers and myxamoebae 

form filose pseudopodia with which they engulf 

their prey. Sexual reproduction is initiated when 

two haploid myxamoebae or swarmers of compatible 

mating type fuse to form a zygote from 

which the diploid plasmodium develops. The 

plasmodium can survive adverse conditions by 

turning into a resistant sclerotium in which 

numerous walled compartments (spherules), 

each containing several nuclei, are formed. 

Upon resumption of growth, the protoplasts 

emerge from their spherules and fuse to re-establish 

the plasmodium. When sexual reproduction 

ensues, the entire content of a plasmodium is 

converted into one or more sporangia in which 

meiosis takes place. Beneath the developing sporangia, 

the plasmodium deposits a specialized 

layer, the hypothallus, which is very variable in


Fig 2.10 Spore germination and swarmers in Physarum and Reticularia.a.Physarum polycephalum:1,sporesgerminating torelease 

myxamoebae; 2, uniflagellate and biflagellate swarmers, note the pseudopodia at the front end of one swarmer; 3, myxamoeba; 

4, fusion between two myxamoebae. b. Reticularia lycoperdon:1, spore showing cracked wall; 2, swarmers, one with pseudopodia; 

3, encystment stage; 4, fusion between two swarmers. 

form (disc-like, membranous, horny or spongy). 

In P. polycephalum, sexual reproduction is triggered 

by environmental factors such as 

starvation and light, and by chemical factors, 

e.g. Ca 2þ and malate (Renzel et al., 2000). 

Depending on species, the sporophores may 

take a range of shapes. Intermediates between 

these different types of sporophore are possible. 

The most common form is the sporangium, 

a vessel enclosed by a wall (peridium) within 

which the spores are contained (Plates 1e,f,h). 

Protoplasmodia produce only one sporangium 

each, but numerous sporangia may arise from 

phaneroplasmodia. Sporangia may be stalked 

or sessile. A second common sporophore is the 

aethalium (Gr. aethes ¼ irregular, curious, 

unusual) in which the entire plasmodium 

becomes converted into a hemispherical or 

cushion-shaped structure (Plates 1b d,g). This 

can comprise several sporangia, but these have 

usually lost their structural identity and are 

surrounded by one common peridium. In a 

pseudoaethalium, several sporangia are grouped 

together but are still recognized as structurally 

distinct. In the plasmodiocarp, the protoplasm 

accumulates in the main veins of the plasmodium, 

and spores are produced there. 

Frederick (1990) has described methods for 

the isolation and cultivation of myxomycetes. 

Some species, such as Physarum polycephalum, 

can be grown in axenic culture and have 

become valuable systems for experimentation. 

Other species need to be fed with bacteria or 

sterile oat flakes. Plasmodia can be maintained 

for prolonged periods in a vegetative state, and 

sclerotia can be stored dry for months. Spores


51 

have been revived after more than 50 years’ 

storage in a herbarium (Elliott, 1949). 

2.5.2 Orders of myxomycetes 

Myxomycetes are currently grouped into five 

orders, all of which are frequently found either 

in nature or upon incubating suitable plant 

material on moist filter paper. 

The Echinosteliales (e.g. Echinostelium, 

Clastoderma) contain the smallest known 

myxomycetes. They form protoplasmodia, with 

each protoplasmodium giving rise to only one 

sporangium. The Echinosteliales resemble the 

protostelids from which they are probably 

derived (Frederick, 1990; Spiegel, 1991; see 

Fig. 2.5). 

The Liceales (e.g. Lycogala, Dictydium, Cribraria, 

Reticularia) are common on the bark of dead 

trees. Some of the smaller species produce protoplasmodia, 

but most have phaneroplasmodia. 

Various types of sporophores are formed; the 

aethalia of Lycogala epidendron (Plate 1b) and 

Reticularia (= Enteridum) lycoperdon (Plates 1c,d) 

are particularly common. 

The Trichiales (e.g. Arcyria, Trichia, Hemitrichia) 

are ubiquitous on fallen logs. The plasmodia are 

intermediate between aphanoplasmodia and 

phaneroplasmodia. Fructifications in Trichia floriforme 

are well-defined sporangia which contain 

an internal meshwork of threads, collectively 

called the capillitium. The peridium breaks 

open at maturity, and the spores are released 

over time by the twisting of the capillitial 

threads which thus act as elaters (Fig. 2.11). 

Arcyria denudata produces reddish sporangia 

on rotting wood (Plate 1e). Another member, 

Hemitrichia serpula, produces plasmodiocarps. 

The Physarales (e.g. Physarum, Fuligo) produce 

the largest plasmodia. Physarum polycephalum has 

been used extensively in fundamental research 

on cell biology, for example on the nature 

of protoplasmic streaming, or the synchrony of 

nuclear division in a large plasmodium comprising 

thousands of nuclei (see below). The plasmodia 

are typical phaneroplasmodia, each of 

which produces numerous sporangia at maturity 

(Plate 1f). Fuligo septica forms particularly large 

sporophores (aethalia) which are bright yellow 

and are frequently seen on decaying wood 

(Plate 1g). 

The Stemonitales include such genera as 

Comatricha and Stemonitis. Stemonitis spp. produce 

clusters of stalked sporangia from aphanoplasmodia 

which are visible on rotting wood 

(Plate 1h). 

2.5.3 Physarum polycephalum as an 

experimental tool 

This species has been used to investigate several 

aspects of cell biology. The conspicuous cytoplasmic 

shuttle streaming in the veins of its large 

phaneroplasmodia is a fascinating phenomenon 

and has been examined extensively. The pulse is 

caused by actin myosin interactions controlled 

by Ca 2þ (Smith, 1994). It is brought about not 

by the direct binding of organelles to actin 

cables, but by the constriction and relaxation 

of an actin myosin skeleton lining the veins. 

Several proteins interacting with actin and 

myosin are directly or indirectly regulated by 

Ca 2þ , but the most important effect of Ca 2þ 

is on one of the myosin light chains. This is a 

regulatory subunit which directly binds Ca 2þ . 

In contrast to most animal actin myosin 

systems which are stimulated by Ca 2þ , that of 

Physarum is inhibited, i.e. contraction occurs 

at low Ca 2þ concentrations, and relaxation at 

higher concentrations. Ca 2þ -inhibited actin 

myosin interaction also occur in plant cells 

where they are visible as cytoplasmic streaming. 

Nakamura and Kohama (1999) have written a 

thorough review of the actin myosin system 

in Physarum. 

Mitotic division of all nuclei throughout 

the plasmodium of P. polycaphalum occurs in a 

synchronized manner, and Physarum was one 

of the pioneer organisms in which the existence 

of the cell cycle was demonstrated. Synchrony of 

mitosis is regulated by a protein kinase which 

catalyses the phosphorylation of H1 histones, 

leading to the condensation of chromosomes at 

the onset of mitosis (Bradbury et al., 1974; Inglis 

et al., 1976). This protein kinase is now known to 

be homologous to the cdc2 product in the fission 

yeast Schizosaccharomyces pombe (see Fig. 9.5; 

Langan et al., 1989).


Fig 2.11 Trichia floriforme. (a) Undehisced 

sporangia. Note that the sporangial stalks are 

continuous with the hypothallus. (b) Dehisced 

sporangia releasing spores by twisting of 

elaters. (c) Elaters and spores. 

A further interesting feature of P. polycephalum 

is the behaviour of the plasmodium 

and the manner in which its actions are coordinated. 

Little work has been carried out 

beyond descriptions of striking phenomena. 

One is the ability of P. polycephalum plasmodia 

to find the shortest way to a food source through 

an artificially constructed maze (Nakagaki, 2001). 

Another is the pattern of veins which is established 

when different regions of a plasmodium 

are presented with food sources; the configuration 

of the plasmodium has been called a ‘smart 

network’ because it presents the shortest 

possible total length of veins to provide good 

interconnections while making allowances for 

blockage of individual veins (Nakagaki et al., 

2004). 

When separate plasmodia of P. polycephalum 

or other species meet, two reactions are possible, 

i.e. a compatible reaction in which the plasmodia 

fuse and their veins coalesce (Fig. 2.8b) or an 

incompatible reaction in which the plasmodia 

fail to fuse and move away from each other, or 

fusion is attempted but stalls and is followed by 

death of the fusion regions of both plasmodia 

(Fig. 2.8c). This is called the lethal reaction.


53 

Genetic studies have shown that fusion occurs 

between plasmodia of genetically closely related 

strains (Carlile & Dee, 1967). The type of incompatibility 

brought about by the interaction of 

genetically distinct plasmodia is an example 

of a widespread phenomenon called vegetative 

incompatibility which is found not only in 

slime moulds, but also in the Eumycota, vertebrates 

and other organisms. In humans, a similar 

phenomenon accounts for blood grouping or 

the failure of tissue transplantations. It is interesting 

to consider the paradox that fusion 

between genetically dissimilar myxamoebae is 

encouraged during sexual reproduction by the 

existence of different mating types, whereas 

it is discouraged during vegetative fusion of 

plasmodia.

3 

Protozoa: Plasmodiophoromycota 


The Plasmodiophoromycota are a group of 

obligate (i.e. biotrophic) parasites. The bestknown 

examples attack higher plants, causing 

economically significant diseases such as clubroot 

of brassicas (Plasmodiophora brassicae), 

powdery scab of potato (Spongospora subterranea; 

formerly S. subterranea f. sp. subterranea) and 

crook-root disease of watercress (S. nasturtii; formerly 

S. subterranea f. sp. nasturtii). In addition to 

damaging crops directly, some species (S. subterranea, 

Polymyxa betae, P. graminis) also act as 

vectors for important plant viruses (Adams, 1991; 

Campbell, 1996). Other species infect roots 

and shoots of non-cultivated plants, especially 

aquatic plants. Algae, diatoms and Oomycota are 

also attacked. If the nine species of Haptoglossa, 

which parasitize nematodes and rotifers, are 

included in the Plasmodiophoromycota, the 

phylum currently comprises 12 genera and 51 

species (Dick, 2001a). Genera are separated 

from each other largely by the arrangement of 

resting spores in the host cell (Waterhouse, 

1973). This feature has also been used for 

naming most genera; for instance, in Polymyxa, 

numerous resting spores are contained within 

each sorus, whereas in Spongospora the resting 

spores are grouped loosely in a sponge-like 

sorus (Fig. 3.6). Accounts of the Plasmodiophoromycota 

have been given by Sparrow (1960), 

Karling (1968), Dylewski (1990) and Braselton 

(1995, 2001). 

3.1.1 Taxonomic considerations 

Plasmodiophoromycota have traditionally been 

studied by mycologists and plant pathologists. 

Many general features of their biology and 

epidemiology are similar to those of certain 

members of the Chytridiomycota such as 

Olpidium (see p. 145). However, it is now clear 

from DNA sequence analysis and other criteria 

that Plasmodiophora is related neither to the 

Oomycota and other Straminipila (Chapters 4 

and 5) nor to the true fungi (Eumycota). Instead, 

it is distantly related to the Myxomycota 

discussed in Chapter 2 but belongs to a different 

grouping within the Protozoa (Barr, 1992; 

Castlebury & Domier, 1998; Ward & Adams, 

1998; Archibald & Keeling, 2004). 

Some believe that Haptoglossa is related to the 

Oomycota rather than Protozoa, although no 

molecular data seem to be available as yet to 

support this claim. Since Haptoglossa strikingly 

resembles Plasmodiophora in its infection biology, 

we shall include it in this chapter. With the 

possible exception of Haptoglossa, the phylum 

Plasmodiophoromycota is monophyletic and contains 

a single class (Plasmodiophoromycetes). We 

consider two orders in this chapter, Plasmodiophorales 

and Haptoglossales. 

3.2 Plasmodiophorales 

The zoospore of the Plasmodiophorales is biflagellate. 

The flagella are inserted laterally and are

PLASMODIOPHORALES 

55 

of unequal length, the anterior one being 

shorter. Both flagella are of the whiplash type 

(Fig. 1.17c). Zoospores of this type are said to be 

anisokont. Transmission electron microscopy 

(TEM) studies have shown that the tips of the 

flagella are tapered rather than blunt (Clay & 

Walsh, 1997). Like the zoospore, the main 

vegetative unit the amoeba, which enlarges 

to become a plasmodium is wall-less. It is 

present freely within host plant cells, its 

membrane being in direct contact with the 

host cytoplasm. The plasmodia possess amoeboid 

features because they can produce pseudopodia 

and engulf parts of the host cytoplasm by 

phagocytosis (Claxton et al., 1996; Clay & Walsh, 

1997). This has been interpreted as a primitive 

trait perhaps betraying a free-living amoeboid 

ancestor with a phagocytotic mode of nutrition 

(Buczacki, 1983). Some Plasmodiophorales can 

now be grown away from their host on artificial 

media for prolonged periods if bacteria are 

present. These are phagocytosed by amoeboid 

growth forms (Arnold et al., 1996). In their hosts, 

amoeboid plasmodia can digest their way 

through plant cell walls, moving to adjacent 

uninfected cells and thus spreading the infection 

within an infected root (Mithen & Magrath, 1992; 

Claxton et al., 1996). 

The walled stages of Plasmodiophorales are 

confined to the zoospore cysts on the plant 

surface, and the zoosporangia and resting sporangia 

inside host plant cells. The wall of resting 

spores is particularly thick and has been shown 

to contain chitin (Moxham & Buczacki, 1983). 

3.2.1 Life cycle of Plasmodiophorales 

Certain details of the life cycle of the 

Plasmodiophorales are still doubtful (Fig. 3.1). 

However, the known stages show very little 

variation between different species, indicating 

that the life cycle is conserved throughout the 

order. A resting spore germinates by releasing 

a single haploid zoospore (primary zoospore) 

which encysts on a suitable surface by secreting a 

cell wall. After a while, an amoeba is injected 

from the cyst into a host cell such as a root hair 

where it enlarges to form a plasmodium, accompanied 

by mitotic nuclear divisions. Nuclear 

divisions at this stage are cruciform; the nucleolus 

is prominently visible throughout the mitotic 

process, elongating in two directions to take 

up a cross-like shape when viewed in certain 

sections by transmission electron microscopy. 

This feature is unique to the Plasmodiophorales 

(Braselton, 2001). After a while, nuclei divide 

mitotically in a non-cruciform manner, and the 

contents of the plasmodium differentiate into 

zoospores. This type of plasmodium is termed 

the primary plasmodium or sporangial plasmodium 

because it produces zoospores. The zoospores 

are called secondary zoospores because 

they arise from a sporangium, not from a resting 

spore. Once released, secondary zoospores may 

re-infect the host to give rise to further primary 

plasmodia and zoosporangia. Eventually, however, 

a different type of plasmodium, the secondary 

plasmodium or sporogenic plasmodium, is 

formed which undergoes meiotic nuclear divisions 

and produces resting spores (Garber & Aist, 

1979; Braselton, 1995). It is not known where 

plasmogamy and karyogamy occur in the life 

cycle of the Plasmodiophorales. 

All developmental stages of P. brassicae can be 

produced readily in the laboratory. Clubbed 

roots should be collected from a field or garden 

and kept frozen at 20°C. Seedlings of brassicas, 

susceptible Chinese cabbage cultivars or 

Arabidopsis thaliana should be grown in a soil 

with a high peat content which must be kept 

well watered. Infections can be established 

by adding slices of infected root material 

or a resting spore suspension to the soil. 

Zoosporangia will be formed within a few days, 

and root galls should be visible within 3 7 weeks 

(Castlebury & Glawe, 1993). Potato or tomato 

plants can be infected with Spongospora subterranea 

using similar protocols. Cabbage callus 

cultures are occasionally used as a simplified 

experimental system for life cycle studies of 

P. brassicae (Tommerup & Ingram, 1971). 

3.2.2 Plasmodiophora brassicae 

Plasmodiophora brassicae is the causal organism of 

club root or finger-and-toe disease of brassicas 

(Fig. 3.2) and was first described by Woronin 

(1878). The disease is common in gardens where

56 PROTOZOA: PLASMODIOPHOROMYCOTA 

Fig 3.1 Probable life cycle of Plasmodiophora brassicae. A haploid resting spore forms a haploid primary zoospore giving rise to a 

multinucleate haploid primary plasmodium upon infection of a root hair. Secondary zoospores are also haploid, and the way in 

which they meet to form a secondary heterokaryotic plasmodium is not known for sure.Open and closed circles represent haploid 

nuclei of opposite mating type; the position of the diploidphase in the life cycle is unclear.Key events in the life cycle are plasmogamy 

(P), karyogamy (K) and meiosis (M). AfterTommerup and Ingram (1971), Buczacki (1983) and Dylewski (1990). 

brassicas are frequently grown, especially if the 

soil is acidic and poorly drained. A wide range of 

brassicaceous hosts is attacked, and root-hair 

infection of some non-brassicaceous hosts can 

also occur (Ludwig-Müller et al., 1999). The 

disease is widely distributed throughout the 

world. 

Club root symptoms 

Infected crucifers usually have greatly swollen 

roots. Both tap roots and lateral roots may be 

affected. Occasionally, infection results in the 

formation of adventitious root buds which give 

rise to swollen stunted shoots. Above ground, 

however, infected plants may be difficult to 

distinguish from healthy ones. The first symptom 

is wilting of the leaves in warm weather, 

although such wilted leaves often recover at 

night. Later the rate of growth of infected plants 

is retarded so that they appear yellow and 

stunted. Plants infected at the seedling stage 

may be killed, but if infection is delayed the 

effect is much less severe and well-developed 

heads of cabbage, cauliflower, etc., can form on 

plants with quite extensive root hypertrophy 

(swelling of cells) and hyperplasia (enhanced


57 

Fig 3.2 Club root of cabbage caused by 

Plasmodiophora brassicae. 

division of cells). Microscopically, even infected 

root hairs are expanded at their tips to form 

club-shaped swellings which are sometimes 

lobed and branched (Fig. 3.3). Rausch et al. 

(1981) followed the growth of infected and 

uninfected seedlings of Chinese cabbage, a 

particularly susceptible host. Within the first 30 

days, the growth rates of infected and control 

plants were almost identical, and clubs developed 

in proportion to shoot growth. Wilting of 

infected plants was observed beyond 30 days 

when the clubs developed at the expense of 

shoots. Plants growing in suboptimal conditions, 

e.g. in the shade, produced disproportionately 

smaller clubs. Generally, the root/shoot ratio is 

appreciably higher in infected plants, suggesting 

a diversion of photosynthetic product to the 

clubbed roots. The P. brassicae infection therefore 

acts as a new carbon sink. 

The process of infection 

Swollen roots contain a large number of small 

spherical resting spores, and when these roots 

decay the spores are released into the soil. 

Electron micrographs show that the resting 

spores have spiny walls (Yukawa & Tanaka, 

1979). The resting spore germinates to produce 

a single zoospore with two flagella of unequal 

length, both of the whiplash type and with the 

usual 9 þ 2 arrangement of microtubules (Aist & 

Williams, 1971). Germination of resting spores is 

stimulated by substances specific to Brassicaceae, 

possibly allyl isothiocyanates, which diffuse from 

the cabbage roots into the soil (Macfarlane, 

1970). 

The primary zoospore (i.e. the first motile 

stage released from the resting spore) swims by 

means of its flagella, the long flagellum trailing 

and the short one pointing forward. The process 

of root hair infection has been followed in a 

classical study by Aist and Williams (1971). Since 

the first such study, on penetration by Polymyxa 

betae, was written in German (Keskin & Fuchs, 

1969), the German terminology is still in use 

today. Primary zoospores of P. brassicae are 

released some 26 30 h after placing a suspension 

of resting spores close to seedling roots of 

cabbage. The zoospores may collide several times 

with a root hair before becoming attached, and 

appear to be attached at a point opposite to the 

origin of the flagella. 

The flagella coil around the zoospore body, 

which becomes flattened against the host wall, 

and pseudopodium-like extensions of the zoospore 

develop, being continuously extended and 

withdrawn. The flagella are then withdrawn, and 

the zoospore encysts, attached to the root hair 

(Fig. 3.4). The zoospore cyst contains lipid bodies 

and a vacuole which enlarges during cyst 

maturation, which takes a few hours. The most 

conspicuous ultrastructural feature of mature 

cysts is a long Rohr (tube), with its outer end 

pointing towards the root hair wall. This end 

of the tube is occluded by a plug. Within the tube


Fig 3.3 Plasmodiophora brassicae.(a)T.S. 

through young infected cabbage root showing 

secondary (sporogenic) plasmodia in the 

cortex. Note the hypertrophy of some of the 

host cells containing plasmodia, and the 

presence of young plasmodia in cells 

immediately outside the xylem. (b) T.S. cabbage 

root at a later stage of infection, showing the 

formation of resting spores. (c) Primary 

(zoosporangial) plasmodium in cabbage root 

hair 4 days after planting in a heavily 

contaminated soil. (d) Young primary 

zoosporangia in root hair. Note the 

club-shaped swelling of the infected root hair. 

(e) Mature and discharged primary 

zoosporangia. a and b to same scale; (c e) to 

same scale. 

Fig 3.4 Plasmodiophora brassicae. (a) Resting 

spores, one full, one empty (showing a pore in 

the wall). (b) Zoospore. (c) Attachment of 

zoospore to root hair. (d) Zoospore cyst with 

adhesorium following withdrawal of flagellar 

axonemes. (e) Entry of amoeba into root hair. 

Based on Aist and Williams (1971).


59 

Fig 3.5 Plasmodiophora brassicae. Diagrammatic summary of penetration process (after Aist & Williams,1971).The diagram shows 

a zoospore cyst attached to the wall of a root hair. (a) Cyst vacuole not yet enlarged. (b) About 3 h later, the cyst vacuole enlarges 

and a small adhesorium appears. (c) About1min later, the stylet punctures the host cell wall. (d) Penetration has occurred and the 

host protoplast has deposited a papilla at the penetration site. 

is a bullet-shaped Stachel (stylet), the outer part 

of which is made up of parallel fibrils. Behind the 

blunt posterior end of the stylet, the tube 

narrows to form a Schlauch (sac). 

Penetration of the root hair wall occurs about 

3 h after encystment, as after this time the first 

empty vacuolated cysts are observed. The penetration 

process takes place rapidly, and an 

interpretation of it is shown in Fig. 3.5. Firm 

attachment of the tube to the root hair is 

brought about by the adhesorium, which may 

develop by partial evagination (i.e. turning inside 

out) of the tube (Fig. 3.5b). During evagination, 

an adhesive substance which has a fibrillar 

appearance in TEM micrographs is released 

onto the adhesorial surface from its storage site 

inside the tube. The enlargement of the vacuole 

is presumably the driving force which brings 

about complete evagination of the tube within 

1 min, followed by thrusting the stylet through 

the host wall. The pathogen is injected into the 

host cell as a small, spherical, wall-less amoeba 

which becomes caught up by cytoplasmic streaming. 

After penetration (Fig. 3.5d), a papilla of 

callose is deposited around the penetration 

point beneath the adhesorium, possibly as a 

wound-healing response. Similar penetration 

mechanisms have been described for other 

Plasmodiophorales, including Spongospora subterranea 

(Merz, 1997), S. nasturtii (Claxton et al., 1996) 

and Polymyxa betae (Keskin & Fuchs, 1969). Details 

of the infection process by P. betae have been 

filmed (see Webster, 2006a). A yet more elaborate 

process of infection is found in Haptoglossa, 

which parasitizes nematodes and rotifers 

(see p. 65). 

Development of zoosporangia 

Within the infected root hair, the amoeba may 

divide into several uninucleate amoebae. Later 

the nuclei within each amoeba show cruciform 

divisions, giving rise to small multinucleate


primary plasmodia. Each plasmodium divides up 

to form a group (sorus) of roughly spherical 

thin-walled zoosporangia lying packed together 

in the host cell (Fig. 3.3). Separate protoplasts 

might coalesce at this stage. Each zoosporangium 

finally contains 4 8 uninucleate zoospores. 

These are morphologically identical to 

primary zoospores. Some mature zoosporangia 

become attached to the host cell wall and an exit 

pore develops at this point through which the 

zoospores escape. The zoospores of other sporangia 

are released into those with an exit pore. 

Occasionally, zoospores escape into the lumen of 

the host cell. Liberated zoospores can re-infect 

plant roots, thereby completing an asexual cycle 

(Fig. 3.1). 

Sexual reproduction 

In P. brassicae, resting sporangia are not formed 

in root hairs after the first cycle of infection, but 

are located mainly in older infections in strongly 

hypertrophied regions of the root cortex. There is 

evidence that resting sporangia are involved in 

sexual reproduction (Fig. 3.1) because meiotic 

nuclear divisions with synaptonemal complexes 

have been observed in maturing resting sporangia 

(Garber & Aist, 1979). Further, each resting 

spore normally contains one haploid nucleus 

(Narisawa et al., 1996). Thirdly, infection experiments 

have established that resting sporangia 

are formed only if two genetically dissimilar 

nuclei are present (Narisawa & Hashiba, 1998) 

which could be contributed either by two 

uninucleate zoospores or by a binucleate 

zoospore. 

The positions of the preceding stages of 

sexual reproduction plasmogamy and karyogamy 

in the life cycle of P. brassicae are still a 

matter of doubt. One possibility is that secondary 

zoospores fuse to form a dikaryon, followed by 

karyogamy. Quadriflagellate binucleate swarmers 

have indeed been observed and can result 

from the fusion of zoospores (Tommerup & 

Ingram, 1971). However, it is not yet clear 

whether these quadriflagellate spores can infect 

plant cells from the outside. Quadriflagellate 

binucleate zoospores may also arise from incomplete 

cleavage of cytoplasm during zoospore 

formation. 

Plasmodia of P. brassicae have been shown to 

break through plant cell walls, thereby spreading 

an infection from root hairs into deeper tissues 

of the root cortex (Mithen & Magrath, 1992). 

A conceivable alternative would be their migration 

through plasmodesmata. It is possible that 

two primary plasmodia or uninucleate amoebae 

arising from separate root hair infections fuse 

upon encountering each other deep inside the 

host plant. Such a fusion would produce a 

secondary plasmodium, and could be followed 

by karyogamy and meiosis, which would lead to 

the development of resting spores (Fig. 3.1). 

Hypertrophy of infected host cells 

As the plasmodia within a host cell 

enlarge, the host nucleus remains active and 

undergoes repeated divisions. Hypertrophy and 

an increased ploidy of the host nuclei result, at 

least in callus culture experiments, because the 

mechanism for host cell division is apparently 

blocked (Tommerup & Ingram, 1971). 

Unsurprisingly, the grossly hypertrophied 

clubs contain enhanced levels of plant growth 

hormones. The concentration of auxins (especially 

indole-3-acetic acid, IAA) in clubbed roots 

was measured to be about 1.7 times as high as in 

uninfected roots (Ludwig-Müller et al., 1993), and 

that of cytokinins was 2 3 times elevated 

(Dekhuijzen, 1980). Isolated secondary plasmodia 

of P. brassicae have been demonstrated to synthesize 

the cytokinin zeatin (Müller & Hilgenberg, 

1986), and the amount of zeatin produced would 

be sufficient to establish a new carbon sink. The 

situation is more complicated with respect to 

auxins which are not synthesized by plasmodia. 

Instead, the pathogen interferes with the host’s 

auxin metabolism, which is complex (Normanly, 

1997). The tissues of healthy crucifers contain 

relatively large amounts of indole glucosinolates 

such as glucobrassicin (¼ indole-3-methylglucosinolate) 

which is converted by the enzyme 

myrosinase to 3-indoleacetonitrile (IAN), a 

direct IAA precursor. Conversion of IAN to IAA 

is catalysed by nitrilase. Increased concentrations 

of indole glucosinolates, IAN and IAA have 

been measured in clubbed roots (Ludwig-Müller, 

1999), and the expression of nitrilase and 

myrosinase was also enhanced. Further, nitrilase


61 

protein was detectable by immunohistochemical 

methods only in cells containing sporulating 

plasmodia. The activities of the above enzymes 

might be regulated by the signalling molecule, 

jasmonic acid (Grsic et al., 1999). However, these 

metabolic changes were confined to a narrow 

window of time, and other sources of IAA, such 

as its release from IAA alanine conjugates by 

the activity of amidohydrolase, are likely to 

contribute (Ludwig-Müller et al., 1996). The 

host pathogen interactions leading to enhanced 

auxin levels in clubbed roots are therefore very 

intricate. 

At first, only cortical cells of the young root 

are infected, but later small plasmodia can be 

found in the medullary ray cells and in the 

vascular cambium. Subsequently, tissues derived 

from the cambium are infected as they are 

formed. In large swollen roots, extensive wedgeshaped 

masses of hypertrophied medullary ray 

tissue may cause the xylem tissue to split. At this 

stage, the root tissue shows a distinctly mottled 

appearance. When the growth of the plasmodia 

is complete, they are transformed into masses of 

haploid resting spores. Only during the late 

stages of resting spore development do the host 

nuclei begin to degenerate. Eventually, the 

resting spores are released into the soil as the 

root tissues decay. 

3.2.3 Spongospora 

The life cycle of S. subterranea, the cause of 

powdery scab of potato, is similar to that of 

P. brassicae (Harrison et al., 1997; Hutchison & 

Kawchuk, 1998). Diseased tubers show powdery 

pustules at their surface, containing masses of 

resting spores clumped into hollow balls. The 

resting spores release anisokont zoospores which 

can infect the root hairs of potato or tomato 

plants. In the root hairs, plasmodia form which 

develop into zoosporangia. Zoospores from such 

zoosporangia are capable of infection, resulting 

in a further crop of zoosporangia. Zoospores 

released from the zoosporangia have also been 

observed to fuse in pairs or occasionally in 

groups of three to form quadri- or hexaflagellate 

swarmers, but whether these represent true 

sexual fusion stages is uncertain. Spongospora 

nasturtii causes a disease of watercress in which 

the most obvious symptom is a coiling or bending 

of the roots. Zoosporangia and resting spore 

balls are found in infected root cells (Fig. 3.6), 

and plasmodia can migrate through the root 

tissue by breaking through host cell walls 

(Claxton et al., 1996; Clay & Walsh, 1997). The 

encounter of two plasmodia might initiate 

sexual reproduction and thus complete the life 

cycle without any need for the parasite to leave 

the host (Heim, 1960). 

Fig 3.6 Spongospora nasturtii. Spore balls from watercress 

roots with crook root disease.


In addition to being the causal agent of powdery 

scab of potatoes, S. subterranea is also important 

as the vector of potato mop-top virus disease, 

which can reduce the yield of tubers by over 20% 

in some varieties (Campbell, 1996; Harrison et al., 

1997). The virus is transmitted by the zoospores 

and can also persist for several years in spore balls 

in the soil. It seems to be located inside the resting 

spores (Merz, 1997). Zoospores of S. subterranea 

can cause zoosporangial infections in the root 

hairs of a wide range of host plants outside 

the family Solanaceae, and can transmit viruses 

to them. Thus S. subterranea and numerous wild 

plants can provide a reservoir of infection for 

the potato mop-top virus even if potatoes have 

not been grown in a field for many years. Other 

members of the Plasmodiophorales also act as 

vectors for plant viruses, notably Polymyxa betae 

which transmits the beet necrotic yellow vein 

virus, and P. graminis which transmits several 

mosaic viruses on most major cereal crops. 

3.3 Control of diseases caused by 

Plasmodiophorales 

3.3.1 Club root 

The control of club root disease is difficult. 

Because resting spores retain their viability in 

the soil for up to 20 years, short-term crop 

rotation will not eradicate the disease. The fact 

that Plasmodiophora brassicae can infect brassicaceous 

weeds such as shepherd’s purse (Capsella 

bursa-pastoris) or thalecress (Arabidopsis thaliana) 

suggests that the disease can be carried over on 

such hosts and that weed control is important. 

Moreover, it is known that root hair infection 

can also occur on many ubiquitous nonbrassicaceous 

hosts such as Papaver and Rumex, 

or the grasses Agrostis, Dactylis, Holcus and Lolium. 

All infections of non-brassicaceous hosts are 

probably reduced to the zoosporangial cycle, 

and no root clubs are formed. Whether such 

infections play any part in maintaining the 

disease in the prolonged absence of a brassicaceous 

host is not known. 

General measures aimed at mitigating the 

incidence of clubroot traditionally include 

improved drainage and the application of lime, 

which retards the primary infection of root hairs. 

Since the effect of liming does not persist, it is 

possible that it may simply delay the germination 

of resting spores and thus prolong their 

existence in the soil (Macfarlane, 1952). More 

recently, boron added at 10 20 mg kg 1 soil in 

conjunction with a high soil pH has been shown 

to suppress primary as well as secondary infections 

(M. A. Webster & Dixon, 1991). Early infection 

of seedlings can result in particularly severe 

symptoms, so it is important to raise seedlings in 

non-infected or steam-sterilized soil. The young 

plants can then be transplanted to infested 

soil. Since it is known that some resting spores 

survive animal digestion, manure from animals 

fed with diseased material should not be used 

for growing brassicas. 

Infection can be retarded by the application 

of mercury-containing compounds or benomyl, 

but these are now banned in many countries. At 

present, no economically and ecologically acceptable 

fungicide appears to be available, although 

research efforts continue (Mitani et al., 2003). 

Some attempts have been made to establish biological 

control methods for P. brassicae (Narisawa 

et al., 1998; Tilston et al., 2002), but it is doubtful 

whether such methods will gain full commercial 

viability in the near future. 

In recent years, increasing emphasis has been 

placed on breeding club root resistant cultivars 

of crop plants. The weed Arabidopsis thaliana, 

which develops the full set of club root symptoms, 

has been used as a host for such studies 

because it is accessible by molecular biological 

methods. Natural resistance in Arabidopsis is 

based on a single gene and involves the hypersensitive 

response, in which infected plant 

cells die before the pathogen has had a chance 

to multiply. The resistance of susceptible cultivars 

can be enhanced by transformation with 

various resistance genes, e.g. a gene from 

mistletoe (Viscum album) encoding viscotoxin, 

a thionin-type cystein-rich polypeptide with 

antimicrobial activity (Holtorf et al., 1998). 

Further, mutant lines with reduced levels of 

IAA precursors show reduced club development 

(Ludwig-Müller, 1999).

CONTROL OF DISEASES CAUSED BY PLASMODIOPHORALES 

63 

In contrast to Arabidopsis, natural resistance 

in cabbage is multigenic, with no obvious 

hypersensitive response (Ludwig-Müller, 1999). 

Breeding for resistance is difficult (Bradshaw 

et al., 1997) and may not provide long-lasting 

success due to the development of new virulent 

races of P. brassicae on the resistant cultivars after 

a few years in the field. By 1975, 34 different 

physiological races of P. brassicae from Europe 

had already been differentiated based on infection 

experiments with Brassica cultivars varying 

in their degree of resistance (Buczacki et al., 

1975). Further, P. brassicae can still infect root 

hairs and reproduce by zoosporangia even in 

resistant cultivars. 

3.3.2 Powdery scab and crook root 

Powdery scab of potatoes is normally of relatively 

slight economic importance and amelioration of 

the disease can be brought about by good drainage. 

Potato mop-top virus infections can be more 

serious, however. Transgenic plants containing 

the viral coat protein gene have been shown to be 

completely resistant against infections by the 

virus (Reavy et al., 1995), and it may be possible to 

produce transgenic crop plants in future. 

Crook root of watercress can be controlled by 

application of zinc to the water supply. The zinc 

can be applied by dripping zinc sulphate into 

the irrigation water for watercress beds to give 

a final concentration of about 0.5 ppm, or by the 

Fig 3.7 Haptoglossa heteromorpha parasitizing nematodes. (a) Single young thallus in a dead nematode. (b) Single maturing 

sporangium with developing dome-shaped exit papillae. (c) Nematode body containing several plasmodia and sporangia. 

One sporangium has released large aplanospores, and an adjacent one small ones. (d) Small aplanospores, one germinating to 

form a gun cell. (e) Large aplanospores, one germinating to form a gun cell. (a c) to same scale; d,e to same scale. Redrawn from 

Glockling and Beakes (2000a).


addition of finely powdered glass containing 

zinc oxide (zinc frit) to the beds. The slow 

release of zinc from the frits maintains a sufficiently 

high concentration to inhibit infection 

(Tomlinson, 1958). 

3.4 Haptoglossa 

(Haptoglossales) 

3.4.1 General biological features of 

Haptoglossa 

If a slurry of soil or herbivore dung is spread on a 

weak medium such as tap water agar or cornmeal 

agar, the nematodes or rotifers contained within 

these samples may become parasitized and killed 

by fungi producing thalli within the cadavers. 

Although superficially resembling the plasmodia 

of Plasmodiophora, this term cannot be applied to 

Haptoglossa because its thalli are surrounded by a 

wall at all stages of development. One or several 

thalli may fill almost the entire body cavity of 

a nematode and become converted into sporangia 

upon maturity (Fig. 3.7). Sporangia of some 

species of Haptoglossa release zoospores which 

are anisokont, with both flagella of the whiplash 

type. Zoospore release occurs through one or 

several exit papillae (Barron, 1977). Zoospores of 

Haptoglossa are weak swimmers and encyst within 

a few minutes in the vicinity of the host cadaver 

from which they were released. Other species 

of Haptoglossa do not release zoospores but 

produce non-motile spores (aplanospores) resembling 

cysts of the zoospore-forming species. 

Aplanospore release occurs by explosive rupture 

of the exit tube, followed by several further, 

progressively weaker bursts of discharge 

(Glockling & Beakes, 2000a). A few hours after 

their formation or release, cysts or aplanospores 

germinate to produce an elongated or glossoid 

(¼ tongue-shaped) cell, which is also often called 

a gun cell or an infection cell. This explosively 

injects a small amount of walled protoplasm 

(sporidium) containing a nucleus and a few 

organelles into a host passing by (see below). The 

sporidium enlarges to form a new thallus and, 

upon host death, a new sporangium. The mechanism 

of gun cell discharge is rather similar to 

that found in cysts of Plasmodiophora or Polymyxa. 

This, together with the occurrence of anisokont 

zoospores, has been taken as an indication that 

Haptoglossa should be included in the Plasmodiophoromycota 

(Beakes & Glockling, 1998; Dick, 

2001a), whereas formerly the genus was thought 

to be related to the Oomycota. 

The aplanosporic species of Haptoglossa produce 

spores of two distinctly different sizes, 

Fig 3.8 Haptoglossa sp. (a) Tip of a developing gun cell. 

The muzzle is still sealed by its plug (Pl). Bore (Bo) and 

needle chamber (NC) are visible. (b) Transmission 

electron micrograph of a mature gun cell.The basal part 

of the gun cell is entirely occupied by the enlarging 

posterior vacuole (Vac).Original prints kindly supplied by 

S.L.Glockling.

HAPTOGLOSSA (HAPTOGLOSSALES) 

65 

although any one sporangium produces propagules 

only of either size (Glockling & Beakes, 

2000a; Fig. 3.7). In contrast to the Plasmodiophorales, 

sexual reproduction or resting stages 

have not yet been described for any species 

of Haptoglossa, and it is difficult at present to 

explain the occurrence of spores of different 

sizes. What appears clear is that each thallus is 

the result of a discrete infection event. 

3.4.2 The gun cell of Haptoglossa 

Germination of the spherical zoospore cyst or 

aplanospore of Haptoglossa occurs by means of 

a short germ tube which enlarges to form the 

elongated gun cell (Robb & Lee, 1986a). This 

remains attached to the cyst until maturity and 

is perched on top of it in many species. The 

mature gun cell (Figs. 3.8, 3.9a) shows strong 

ultrastructural similarities to the infection 

apparatus of Plasmodiophora (see Fig. 3.5) and is 

the object of considerable mycological curiosity. 

A tube leads into the pointed tip of the gun cell 

but its opening (muzzle) is separated from the 

exterior by a thin wall (plug) for most of its 

development (Fig. 3.8a). The formation of this 

internal tube from the tip of the gun cell 

backwards has been likened to inverted internal 

tip growth and is mediated by a scaffold of actin 

fibres against the turgor pressure of the gun cell 

(Beakes & Glockling, 1998). The inner (noncytoplasmic) 

surface of the anterior part of 

the tube (bore) is lined with fibrillar material. 

A second wall separates the bore from a swollen 

section of the tube, the needle chamber. This 

contains a projectile (needle) resembling the 

bullet of Plasmodiophora, but terminating in a 

much finer tip, possibly reflecting the different 

properties of the host surface which it has to 

puncture. The needle is held in place by a 

complex set of cones and cylinders (Fig. 3.8a) 

which are thought to exercise a restraining 

function, fixing the needle against the high 

turgor pressure of the gun cell. The cones and 

cylinders may contain actin filaments. The shaft 

of the needle is much wider than its tip. The 

posterior (innermost) part of the tube (tail) coils 

around itself and the nucleus, almost touching 

the side of the needle chamber. The tail is walled, 

Fig 3.9 Schematic drawings of the nematode penetration 

mechanism in Haptoglossa.(a)Guncellreadyfordischarge.The 

tube has already protruded to form a beak (Bk), the exterior of 

which is lined by a glue originating from the inside surface of 

the bore.This aids in the attachment of the gun cell to a passing 

nematode.The needle (Ne) is held in position by actin 

filaments inside the needle chamber (NC), which is separated 

from the outside by a wall. Behind the needle chamber is the 

coiled tail (T) which contains wallmaterialin its lumen (dotted 

area). In fact, the tail is multi-layered, but this has not been 

illustrated here.The tail coils round the nucleus (Nuc) and a 

Golgi stack (G), and mitochondria (Mit) are also located in the 

vicinity.The posterior of the gun cell is filled by one large 

vacuole (Vac). (b) Tip of a fired gun cell showing the everted 

tail which has penetrated the nematode cuticle and has 

formed a sporidium inside the nematode body (above the 

cuticle).The wall material formerly located inside the tail has 

formed the sporidium wall.The detached needle is also visible 

inside the nematode body.For a more detailed description of 

the eversion process, see Glockling and Beakes (2000b).


and additional electron-dense cell wall precursor 

material is deposited within the lumen of the 

tail. Synthesis of the tube is mediated by one 

large Golgi stack which is always closely associated 

with the nucleus and faces the inwardgrowing 

tube tip, emitting vesicles towards it. As 

the tube extends and coils round the nucleus, 

the nucleus and Golgi stack turn like a dial by 

360° (Beakes & Glockling, 1998, 2000). The turgor 

pressure of the gun cell is probably generated by 

a large posterior vacuole (Fig. 3.8b), similar to 

that found in cysts of Plasmodiophora. The 

osmotically active solutes required for turgor 

generation may originate from the degradation 

of lipid droplets within the enlarging vacuole. 

Shortly before discharge, the increasing 

turgor pressure of the posterior vacuole is 

thought to push the tip of the gun cell forward; 

the wall sealing the muzzle is lost, and the bore 

shortens and extends a beak-like projection 

(Fig. 3.9a). The cell wall material from the 

interior of the bore now forms the external 

beak wall, and the needle is ready for injection. 

The nature of the discharge trigger probably 

varies between different species of Haptoglossa 

and may be chemical or mechanical. The beak 

wall is thought to act as an adhesive and 

immediately glues the gun cell to the cuticle of 

a passing nematode or rotifer. Firm attachment 

is necessary to provide resistance against the 

recoil of the needle attempting to penetrate 

the tough cuticle of the host, as it is for the 

penetrating bullet in adhesoria of Plasmodiophora. 

Beakes and Glockling (1998) speculated 

that stretch-activated membrane channels 

(see p. 8) might be involved in triggering the 

launch of the needle. Following attachment, 

Ca 2þ ions entering the needle chamber would 

cause the actin-rich cones and cylinders near the 

needle tip to contract and rupture. Once the 

constraints exercised by the cones and cylinders 

are broken, the high turgor pressure of the gun 

cell will immediately fire the needle, followed by 

explosive eversion of the entire tube which forms 

a syringe, conducting the nucleus, Golgi apparatus 

and mitochondria of the gun cell through 

the nematode cuticle (Fig. 3.9b). The infective 

propagule is called a sporidium because it is 

surrounded by a wall, the material for which is 

probably contributed by precursor material at 

the end of the tail section (Robb & Lee, 1986b; 

Glockling & Beakes, 2000b).

4 

Straminipila: minor fungal phyla 


The kingdom Chromista was erected by Cavalier- 

Smith (1981, 1986) to accommodate eukaryotic 

organisms which are distinguishable from the 

Protozoa by a combination of characters. Some 

of these are concerned with details of photosynthesis, 

such as the enclosure of chloroplasts 

in sheets of endoplasmic reticulum, and the 

absence of chlorophyll b, the latter feature 

being used for the naming of the kingdom. 

Other defining characters apply also to the nonphotosynthetic 

members of the Chromista (Kirk 

et al., 2001). These are as follows: 

1. The structural cell wall polymer is cellulose, 

in contrast to walls of Eumycota which 

contain chitin. 

2. The inner mitochondrial membrane is 

folded into tubular cristae (Fig. 4.1a) which are 

also found in plants. In contrast, mitochondrial 

cristae are generally lamellate in the kingdoms 

Eumycota (Fig. 4.1b) and Animalia. 

3. Golgi stacks (dictyosomes) are present; 

these are also found in the Protozoa (see p. 64). 

In contrast, in the Eumycota the Golgi apparatus 

is usually reduced to single cisternae (see 

Figs. 1.3, 1.10). 

4. Flagella are usually present during particular 

stages of the life cycle; they always include 

one straminipilous flagellum (Lat. stramen ¼ 

straw, pilus ¼ hair). Dick (2001a) considered 

this feature to be of such high phylogenetic 

significance that he has renamed the kingdom 

Chromista as Straminipila. The straminipilous 

flagellum is discussed in detail in the following 

section. 

5. The amino acid lysine is synthesized via 

the a,e-diaminopimelic acid (DAP) pathway. 

Diaminopimelic acid originates from aspartic 

semialdehyde and pyruvic acid and is present 

in terrestrial plants, green algae, Chromista 

and prokaryotes. The alternative route, the 

a-aminoadipic acid (AAA) pathway, draws on 

a-ketoglutaric acid and acetyl-CoA and is found 

almost exclusively in members of the Eumycota. 

Yet other organisms, including animals and 

Protozoa, are auxotrophic for lysine (Griffin, 

1994). Lysine biosynthesis has been used as a 

chemotaxonomic marker for some time (Vogel, 

1964; LéJohn, 1972). 

The kingdom Chromista/Straminipila currently 

includes the diatoms, golden and 

brown algae, chrysophytes and cryptomonads, 

as well as three phyla of straminipilous organisms 

traditionally studied by mycologists, 

i.e. the Oomycota, Hyphochytriomycota and 

Labyrinthulomycota. The first two groups are 

also called straminipilous fungi because of the 

similarity of their mode of life to the fungal 

lifestyle (Dick, 2001a). The Oomycota are by far 

the more important of these, and are considered 

in detail in Chapter 5. The Hyphochytriomycota 

and Labyrinthulomycota are treated briefly in 

the present chapter. The Straminipila as circumscribed 

above are a diverse but natural

68 STRAMINIPILA: MINOR FUNGAL PHYLA 

Fig 4.1 Mitochondrial ultrastructure observed by 

transmission electron microscopy. (a) Mitochondrion of 

Phytophthora erythroseptica (Oomycota).The inner 

mitochondrial membrane is folded into a complex tubular 

network. (b) Mitochondrion of Sordaria fimicola (Ascomycota) 

with the inner membrane appearing lamellate. Mitochondrial 

ribosomes (arrows) are also visible. Reprinted from Weber 

et al. (1998), with permission from Elsevier. 

(monophyletic) grouping which has been 

confirmed by comparisons of the small-subunit 

(18S) ribosomal DNA sequences (e.g. Hausner 

et al., 2000; Fig. 4.2). 

4.2 The straminipilous 

flagellum 

The eukaryotic flagellum is a highly conserved 

structure. It is formed within the cytoplasm by a 

kinetosome, i.e. a microtubule-organizing centre 

resembling the centriole which co-ordinates the 

formation of the microtubular spindle during 

nuclear division. Like the centriole, the kinetosome 

contains an outer ring of nine triplets 

of microtubules surrounding two central microtubules 

(see Figs. 6.2 and 6.19). The flagellum 

extends outwards from the centriole as nine 

doublets of microtubules surrounding the two 

single central microtubules. This is the 9 þ 2 

arrangement. Where the eukaryotic flagellum 

protrudes beyond the cell surface, it is 

ensheathed by the plasma membrane. Within 

the flagellum, there are no obvious cytoplasmic 

features other than the microtubules which 

together are called the axoneme. Flagella 

which are entirely smooth or bear a coat of 

fine fibrillar surface material visible only by 

high-resolution electron microscopy (Fig. 4.3a; 

Andersen et al., 1991) are commonly called 

whiplash flagella. Dick (2001a) has pointed out 

that whiplash flagella in a strict sense are 

pointed at their tip due to the fact that the two 

inner microtubules are longer than the nine 

outer doublets (Fig. 4.3a). 

A second type of flagellum is decorated with 

hair-like structures 1 2 mm long (Fig. 4.3b). This 

is the tinsel or straminipilous flagellum (Dick, 

1997). The hairs are called tripartite tubular 

hairs (TTHs) because they are divided into three 

parts. They were formerly called mastigonemes, 

thereby naming the fungi which produced them 

Mastigomycotina, but both terms are no longer 

used. Each TTH is attached to the flagellum by a 

conical base pointed towards the axoneme. 

The main part of the TTH is a long tubular 

shaft thought to consist of two fibres of different 

thickness coiled around each other (Domnas 

et al., 1986). At the tip of the TTH, the two 

fibres separate from each other to form loose 

ends (Figs. 4.3b, 4.4). In the TTHs of some 

straminipilous organisms, only one loose end is 

visible (Fig. 4.7b). TTHs are assembled in antiparallel 

arrays in Golgi-derived vesicles of the 

maturing zoospore, and are released by fusion of 

the vesicles with the plasma membrane (Fig. 4.5; 

Heath et al., 1970; Cooney et al., 1985). When a 

spore encysts, the flagellum may be withdrawn, 

shed or coiled around the spore. If it is withdrawn, 

the TTHs are sloughed off and left behind 

as a tuft on the surface of the cyst (Dick, 1990a). 

TTHs are arranged in two rows along the 

axoneme. The cones of each row are adjacent to 

an outer microtubule doublet, and because there 

are nine such doublets, the two rows of TTHs 

are at an angle of about 160° rather than 180° 

to each other (Fig. 4.4a). In zoospores of

THE STRAMINIPILOUS FLAGELLUM 

69 

Fig 4.2 Unrooted phylogenetic tree of the Straminipila and members of other kingdoms, based on analyses of18S rDNA 

sequences.Redrawn and modified from Hausner et al. (2000), by copyright permission of the National Research Council of Canada. 

Fig 4.3 Ultrastructure of flagella in Straminipila. (a) Whiplash flagellum of Pythium monospermum (Oomycota).The tip is narrower 

than the main body of the flagellum because the two central microtubules are longer than the nine outer doublets. Arrows indicate 

the coating of the flagellum with very fine hairs. (b) Tinsel flagellum of Achlya colorata (Oomycota) with numerousTTHs. EachTTH 

ends in two fibres, one longer and thicker than the other (arrows).Original images kindly provided by M.W. Dick and I.C. Hallett.


Fig 4.4 Organization of the straminipilous flagellum. 

(a) Postulated attachment of TTHs to the microtubule 

doublets1and 5 of the axoneme as seen in transverse section 

(after Dick, 2001a). (b) Longitudinal arrangement of TTHs 

along the axoneme of a straminipilous flagellum.Only one row 

of TTHs is drawn.TheTTHs are thought to be arranged in an 

alternating fashion as regards the orientation of long and 

short fibres in adjacent TTHs. b redrawn from Dick (1990a). 

ß 1990 Jones and Bartlett Publishers, Sudbury, MA. 

www.jbpub.com. 

straminipilous fungi, the straminipilous flagellum 

always seems to point towards the direction 

of movement, and Dick (1990a, 2001a) has 

advanced a theory to explain how movement 

can be generated from a sinusoidal wave starting 

at the flagellar base, likening the straminipilous 

flagellum to ‘a rowing eight with fixed oars and 

a flexible keel’ (Fig. 4.4b; Dick, 2001a). An anterior 

straminipilous flagellum therefore pulls the 

spore through the water, whereas a backwardly 

directed whiplash flagellum pushes the spore. 

The construction of the straminipilous flagellum 

is so elaborate that it is most unlikely to 

have arisen more than once during evolution 

(Dick, 2001a). The presence of a straminipilous 

flagellum, whether or not accompanied by 

another, smooth flagellum, therefore indicates 

membership in the Straminipila. 

4.3 Hyphochytriomycota 

This group, formerly called Hyphochytridiomycetes 

probably due to the perpetuation of 

Fig 4.5 Schematic drawing of a L.S. of a zoospore of the 

hyphochytrid Hyphochytrium catenoides.The elongated shape 

of the zoospore and of the nucleus (N) is maintained by a 

system of ‘rootlets’consisting of parallel bundles of 

microtobules (thick lines).The straminipilous flagellum arises 

from a kinetosome (Kin). A second, non-functional 

kinetosome (NFK) is interpreted as the base of a whiplash 

flagellum lost in the course of evolution from a heterokont 

ancestor. Mitochondria (Mit),TTH-containing vesicles (TV), 

a Golgi stack (G), ER, ribosomes (Rib), a large basal lipid 

droplet (LD) and microbodies (MB) are also visible. Some 

organelles of unknown function, e.g. electron-opaque bodies 

and osmiophilic bodies, have been omitted from the 

original for improved clarity. Redrawn and modified from 

Cooney et al. (1985). 

a typographical error (see Dick, 1983), is a very 

small phylum currently comprising 23 species in 

6 genera (Kirk et al., 2001). The Hyphochytriomycota 

(colloquially called hyphochytrids) are

LABYRINTHULOMYCOTA 

71 

phylogenetically closely related to the Oomycota 

(van der Auwera et al., 1995; Hausner et al., 2000; 

see Fig. 4.2). Treatments of the group have been 

given by Karling (1977), Fuller (1990, 2001) and 

Dick (2001a). The diagnostic feature is the 

zoospore with its single anterior straminipilous 

flagellum (Fig. 4.5). This kind of zoospore is not 

found in any other known life form. The 

zoospore of hyphochytrids contains one prominent 

Golgi stack, one nucleus, and lipid droplets 

and microbodies (Barr & Allan, 1985; Cooney 

et al., 1985). The latter are not arranged in a 

microbody lipid complex like they are in 

chytrids (cf. Fig. 6.3). The TTHs are localized 

within Golgi-derived vesicles. The flagellum 

arises from a kinetosome, with microtubules 

rooting deeply within the spore and probably 

maintaining its shape. A second (dormant) 

kinetosome lies adjacent but at an angle, at the 

same position as that which gives rise to the 

backward-directed smooth flagellum in zoospores 

of Oomycota. This whiplash flagellum is 

missing in Hyphochytriomycota, and Barr and 

Allan (1985) have speculated that it could have 

been lost during evolution of the latter from the 

former. Like the Oomycota, hyphochytrids 

synthesize lysine by the a,e-diaminopimelic acid 

(DAP) pathway (Vogel, 1964). 

Hyphochytrids occur in the soil and in 

aquatic environments (both freshwater and 

marine) as saprotrophs or parasites of algae, 

oospores of Oomycota or azygospores of 

Glomales. Hyphochytrium peniliae was reported 

once as the cause of a devastating epidemic of 

marine crayfish (Artemchuk & Zelezinkaya, 

1969), but no further cases have been observed 

since. Some species can be isolated into pure 

culture relatively easily (Fuller, 1990). 

Zoospores encyst by withdrawing their flagellum 

and secreting a wall, leaving the TTHs 

dispersed on the surface of the cyst wall 

(Beakes, 1987). The cyst germinates by enlargement 

or by putting out rhizoids. Because of the 

similarity of their vegetative thalli with those of 

Chytridiomycota (see Chapter 6), hyphochytrids 

have been studied primarily by comparison with 

chytrids, and the same terminology has been 

used (see Fig. 6.1). Depending on the species, 

cysts germinate to develop in three different 

ways, which have been used to subdivide 

the Hyphochytriomycota into families: 

(1) Holocarpic thalli are produced by simple 

enlargement of the cyst. The entire content of 

the sac-like thallus ultimately becomes converted 

into zoospores (Anisolpidiae, e.g. Anisolpidium 

which parasitizes marine algae; Canter, 1950). 

(2) In eucarpic monocentric thalli, the cyst 

produces a bunch of rhizoids at one end, which 

anchor the enlarging thallus to the substratum 

and/or absorb nutrients (Rhizidiomycetidae, e.g. 

Rhizidiomyces; Wynn & Epton, 1979). (3) In 

eucarpic polycentric thalli, a broad hypha-like 

germ tube emerges, branches and produces 

several zoosporangia (Hyphochytriaceae, e.g. 

Hyphochytrium; Ayers & Lumsden, 1977). The 

asexual life cycle is completed when a fresh 

crop of zoospores is released. Sexual reproduction 

has not yet been reliably described for the 

hyphochytrids. 

4.4 Labyrinthulomycota 

Whereas the Hyphochytriomycota described in 

the previous section have a strong resemblance 

to true fungi (especially Chytridiomycota), 

the Labyrinthulomycota do not, and the 

only justification for mentioning them here is 

the fact that they have traditionally been 

studied by mycologists. They have been the 

subject of numerous taxonomic rearrangements, 

and are known under many different names such 

as Labyrinthomorpha, Labyrinthista and 

Labyrinthulea. Some 48 species are currently 

recognized (Kirk et al., 2001). DNA sequence 

comparisons have placed them within the 

Straminipila (Fig. 4.2; Hausner et al., 2000; 

Leander & Porter, 2001), and they are characterized 

by having heterokont flagellation, i.e. 

possessing a straminipilous and a whiplash 

flagellum with a pointed tip (Fig. 4.7). In addition, 

they have mitochondria with tubular cristae. 

Recent treatments of this group can be found in 

Moss (1986), Porter (1990) and Dick (2001a). 

Labyrinthulomycota occur in freshwater and 

marine environments where they are attached to 

solid substrata by means of networks of slime


within which individual vegetative cells are 

contained. For this reason, they are sometimes 

referred to as ‘slime nets’ (Porter, 1990). The 

vegetative cells possess a wall which, uniquely, 

is produced from Golgi-derived scales of a 

polymer of l-galactose (Dick, 2001a). These 

scales are located between the plasma membrane 

and the inner membrane of the slime net. The 

slime net is delimited by an inner and an outer 

membrane and is produced by specialized organelles 

termed sagenogens or bothrosomes; the 

net membranes are continuous with the plasma 

membrane at the sagenogen (Perkins, 1972). 

Labyrinthulomycota feed by absorption (osmotrophy) 

of nutrients. The nets contain degradative 

enzymes which can lyse plant material or 

microbial cells. Two orders are distinguished. 

4.4.1 Labyrinthulales 

Members of this order, especially of the genus 

Labyrinthula, can be readily isolated from marine 

angiosperms such as Zostera and Spartina or from 

seaweed by placing a small piece of one of these 

substrata directly on low-nutrient sea water agar 

augmented with penicillin and streptomycin 

(Porter, 1990). Within a few days, a fine network 

of strands can be seen extending over the agar 

surface (Fig. 4.6). Labyrinthula spp. can be kept in 

monoxenic culture with yeasts or bacteria as 

food source. These are presumably lysed by the 

enzymes contained in the slime net. 

A closer examination shows that the network 

consists of branched slime tubes within which 

spindle-shaped cells move backwards and 

forwards (Fig. 4.7a; see Webster, 2006a). 

Movement of a speed up to 100 mm min 1 has 

been reported and is due to a system of 

contractile actin-like proteins in the slime net 

(Nakatsuji & Bell, 1980). Cells occasionally aggregate 

to form sporangia containing numerous 

round cysts. Following meiosis, eight heterokont 

zoospores (Figs. 4.6a, 4.7b) are released by each 

cyst. These possess a pigmented eyespot not 

found in other types of heterokont zoospore 

(Porter, 1990). It is, however, unclear whether 

zoospores can establish new colonies (Porter, 

1990). Asexual reproduction occurs by division 

of spindle cells within the slime net, and 

fragments of such a colony can establish new 

colonies (Porter, 1972). Further details of the life 

cycle appear to be unknown at present. 

Labyrinthula spp. were implicated as pathogens 

in a wasting epidemic of eelgrass (Zostera 

marina) at the west coast of North America in the 

1930s (Young, 1943; Muehlstein et al., 1991), 

causing considerable disturbance to the littoral 

ecosystem and collateral damage to the 

local fisheries industry. However, although 

Labyrinthula spp. are still frequently associated 

with pieces of moribund Zostera shoots, no 

further epidemics seem to have occurred since. 

Instead, a new species, L. terrestris, has recently 

been identified as the cause of a rapid blight of 

Fig 4.6 Labyrinthula. (a) Zoospore with 

long anterior straminipilous flagellum 

and a short posterior whiplash flagellum 

with a pointed tip (after Amon & 

Perkins,1968). (b d) Portions of colonies 

at different magnifications. In (c) spindle 

cells are seen in swellings in the slime 

tracks.

LABYRINTHULOMYCOTA 

73 

Fig 4.7 Ultrastructural features of Labyrinthulomycota. (a) Spindle-shaped cells of Labyrinthula within their slime net. Each cell has 

mitochondria with tubular cristae (Mit),Golgi stacks (G), a single nucleus (N), and cortical lipid droplets (LD).The slime net is 

produced by several sagenogens (Sag) in each cell.The plasma membrane is continuous with the inner membrane of the slime net. 

Wall scales are released at the sagenogen point and accumulate between the plasma membrane and the inner membrane of the 

slime net. (b) Biflagellate heterokont zoospore of Labyrinthula showing an eyespot (E) close to the base of the whiplash flagellum. 

Note that eachTTH of the Labyrinthula zoospore produces only one terminal fibre. (c) Young thallus of Thraustochytrium. 

Mitochondria with tubular cristae, a Golgi stack, lipid droplets and larger vacuoles (Vac) are seen.The wall consists of scales 

pre-formed in Golgi-derived vesicles (Ves).The slime net is produced at the base of the thallus by a single sagenogen. All images 

schematic and not to scale; redrawn and modified from Porter (1990). ß1990 Jones and Bartlett Publishers, Sudbury, MA. 

www.jbpub.com. 

turf-grass on golf courses, infection presumably 

being brought about by irrigation with contaminated 

water of unusually high salinity (Bigelow 

et al., 2005). 

4.4.2 Thraustochytriales 

Thraustochytrids are probably ubiquitous in 

marine environments, occurring on organic 

debris as well as calcareous shells of invertebrates 

(Porter & Lingle, 1992). Like the labyrinthulids, 

they feed on organic matter, algae and 

bacteria (Raghukumar, 2002). Thraustochytrids 

can be baited by sprinkling pine pollen grains 

onto water samples or organic debris immersed 

in water. Within one to several days, the pollen 

grains become colonized by one or several thalli, 

the main bodies of which protrude beyond the 

grain surface (Figs. 4.8a,b). If colonized pollen 

grains are transferred to a suitable agar medium 

containing sea salts, yeast extract and sugar 

(Yokochi et al., 1998), thalli will grow on the agar 

surface and may be induced to release zoospores 

by mounting them in water. Thraustochytrids 

can be stored in pollen grain suspensions or on 

agar overlaid with sea water. They also possess 

the ability to survive in a dry state at room 

temperature for a year or longer (Porter, 1990). 

The thallus of thraustochytrids superficially 

resembles that of an epibiotic monocentric 

chytrid in having a roughly spherical shape 

with ‘rhizoids’ at its base (Fig. 4.8c). These 

‘rhizoids’ are, in fact, the slime net produced 

by one basal sagenogen (Fig. 4.7c). The thallus is 

surrounded by Golgi-derived scales forming 

a wall, but the slime net does not extend over 

the thallus. Sexual reproduction is unknown, 

but asexual biflagellate heterokont zoospores 

are released from the main body of the thallus,


Fig 4.8 Thraustochytriales. (a) Thallus of Thraustochytrium sp. growing on a pollen grain sprinkled onto seawater. (b) Thalli of 

Schizochytrium sp. growing on a pollen grain. (c) Thalli of Schizochytrium sp. growing on agar medium. Note the slime net extending 

away from the thalli. 

and these can settle onto a suitable substratum, 

giving rise to new thalli (Porter, 1990). 

Thus, these zoospores of Thraustochytriales 

are mitospores formed following mitosis, in 

contrast with those of Labyrinthulales which 

are meiospores, i.e. formed by meiosis. Although 

thraustochytrid zoospores lack a recognizable 

eye-spot, they are phototropic, reacting to light 

of blue wavelengths such as that produced by 

bioluminescent bacteria (Amon & French, 2004). 

Chemotropism has also been described for 

thraustochytrid zoospores (Fan et al., 2002), and 

both sensual responses may enable zoospores 

to locate potential food sources. 

Thraustochytrids, and especially the genera 

Thraustochytrium and Schizochytrium, have recently 

attracted attention as producers of polyunsaturated 

fatty acids (PUFAs). These are important 

as nutrient supplements, and thraustochytrid 

oils might eventually be able to compete with 

fish oils on the market (Yokochi et al., 1998; 

Lewis et al., 1999).

5 

Straminipila: Oomycota 


The phylum Oomycota, alternatively called 

Peronosporomycetes (Dick, 2001a), currently comprises 

some 800 1000 species (Kirk et al., 2001). 

The Oomycota as a whole have been resolved 

as a monophyletic group within the kingdom 

Straminipila in recent phylogenetic studies (e.g. 

Riethmüller et al., 1999; Hudspeth et al., 2000; 

see Fig. 4.2), although considerable rearrangements 

are still being performed at the level of 

orders and families. A scholarly treatment of the 

Oomycota has been published by Dick (2001a) 

and will remain the reference work for many 

years to come. Because of the outstanding significance 

of Oomycota, especially in plant pathology, 

we give an extended treatment of this group. 

5.1.1 The vegetative hypha 

Although some members of the Oomycota grow 

as sac-like or branched thalli, most of them 

produce hyphae forming a mycelium. Oomycota 

are now known to be the result of convergent 

evolution with the true fungi (Eumycota), and 

their hyphae differ in certain details. However, 

the overall functional similarities are so great 

that they provide a persuasive argument for 

the fundamental importance of the hypha in 

the lifestyle of fungi (Barr, 1992; Carlile, 1995; 

Bartnicki-Garcia, 1996). Much physiological work 

has been carried out on hyphae of Oomycota (see 

Chapter 1), and the results have a direct bearing 

on our understanding of the biology of the 

Eumycota. Like them, the hyphae of Oomycota 

display apical growth and enzyme secretion, 

ramify throughout the substratum by branching 

to form a mycelium, and can show morphogenetic 

plasticity by differentiation into specialized 

structures such as appressoria or haustoria. 

The hyphae of Oomycota are coenocytic, i.e. 

they generally do not form cross-walls (septa) 

except in old compartments or at the base of 

reproductive structures. The cytoplasm is generally 

coarsely granular and contains vacuoles, 

Golgi stacks, mitochondria and diploid nuclei. 

The apex is devoid of organelles other than 

numerous secretory vesicles. These are not, as 

in the Eumycota, arranged into a Spitzenkörper 

because the microvesicles which contain chitin 

synthase and make up the Spitzenkörper core are 

lacking. This is in line with the general absence, 

with a few exceptions, of chitin from the walls of 

Oomycota; instead, cellulose, a crystalline b-(1,4)- 

glucan, contributes the main fibrous component. 

As in the Eumycota, these structural fibres 

are cross-linked by branched b-(1,3)- and b-(1,6)- 

glucans, although the biochemical properties of 

the glucan synthases seem to differ fundamentally 

between those of Eumycota on the one hand 

and those of Oomycota and plants on the other 

(Antelo et al., 1998). Other biochemical differences 

include the lysine synthetic pathway (DAP 

in plants and Oomycota; AAA in true Fungi; 

see p. 67) and details of sterol metabolism (Nes, 

1990; Dick, 2001a). 

The mitochondria of Oomycota are indistinguishable 

by light microscopy from those of the 

Eumycota, but when viewed with the transmission 

electron microscope they have tubular

76 STRAMINIPILA: OOMYCOTA 

Fig 5.1 Asexual reproductive stages in Saprolegnia. 

(a) Auxiliary (primary) zoospore. (b) Principal 

(secondary) zoospore. Schematic drawings, based 

partly on Dick (2001a). 

rather than lamellate cristae (see Fig. 4.1). The 

vacuolar system of Oomycota is also unusual in 

containing dense-body vesicles or ‘fingerprint 

vacuoles’ (see Fig. 5.24b) which consist of deposits 

of a phosphorylated b-(1,3)-glucan polymer, mycolaminarin. 

Mycolaminarin may serve as a storage 

compound for carbohydrates as well as phosphate 

(Hemmes, 1983), and the polyphosphate 

storage deposits which are typically found within 

vacuoles of true Fungi are absent from vacuoles 

of Oomycota (Chilvers et al., 1985). Apart from 

that, however, vacuoles of Oomycota share many 

features with those of true Fungi, including the 

membranous continuities which often link adjacent 

vacuoles and provide a means of transport 

by peristalsis (Rees et al., 1994; see Fig. 1.9). 

Cytoplasmic glycogen granules, which are one 

of the major carbohydrate storage sites in 

Eumycota, are absent from hyphae of Oomycota 

(Bartnicki-Garcia & Wang, 1983). 

5.1.2 The zoospore 

The Oomycota are characterized by motile asexual 

spores (zoospores) which are produced in 

spherical or elongated zoosporangia. They are 

heterokont, possessing one straminipilous and 

one whiplash-type flagellum. Two types of zoospore 

may be produced and, if so, the auxiliary 

zoospore is the first formed. It is grapeseedshaped, 

with both flagella inserted apically 

(Fig. 5.1a), and it encysts soon after its formation. 

Encystment is by withdrawal of the flagella, 

so that a tuft of tripartite tubular hairs (TTHs; 

see p. 68) is left behind on the surface of the 

developing cyst (Dick, 2001b). The cyst germinates 

to give rise to the principal zoospore, which is 

by far the more common type and also the more 

vigorous swimmer. This typical and readily recognized 

oomycete zoospore is uniform in appearance 

across the phylum (Lange & Olson, 1983; 

Dick, 2001a). In species lacking auxiliary zoospores, 

the principal zoospore is usually produced 

directly from a sporangium. It is kidney-shaped, 

with the flagella inserted laterally in a kinetosome 

boss which in turn is located within the 

lateral groove (Fig. 5.1b). Encystment is initiated 

by the shedding, rather than withdrawal, of the 

flagella; no tufts of TTHs are left on the cyst 

surface (Dick, 2001a). Fascinating insights into 

the cytology of zoospore encystment have been

INTRODUCTION 

77 

Fig 5.2 Schematic drawing and terminology of sexual 

reproductive organs in the Oomycota. Modified from Dick 

(1995). 

obtained from several species (see Fig. 5.24). At 

the onset of encystment, adhesive and cell wall 

material is secreted by the synchronized fusion 

of pre-formed storage vesicles with the zoospore 

plasma membrane (Hardham et al., 1991; 

Hardham, 1995), thereby providing a rare example 

of regulated secretion in fungi. Constitutive 

secretion by growing hyphal tips is more commonly 

associated with their mode of life. 

Some members of the Oomycota have no 

motile spore stages but can be readily related 

to groups still producing them. 

5.1.3 Sexual reproduction 

The life cycle of the Oomycota is of the 

haplomitotic B type, i.e. mitosis occurs only 

between karyogamy and meiosis. All vegetative 

structures of Oomycota are therefore diploid 

(see Figs. 5.3 and 5.19). This is in contrast to the 

Eumycota in which vegetative nuclei are usually 

haploid, the first division after karyogamy being 

meiotic. Sexual reproduction in Oomycota is 

oogamous, i.e. male and female gametangia are 

of different size and shape (Fig. 5.2). Meiosis 

occurs in the male antheridia and in the female 

oogonia, and is followed by plasmogamy (fusion 

between the protoplasts) and karyogamy (fusion 

of haploid nuclei). Numerous meioses can occur 

synchronously, so that true sexual reproduction 

can actually happen within the same protoplast 

(Dick, 1990a). Heterothallic species of Oomycota 

display relative sexuality, i.e. a strain can produce 

antheridia in combination with a second 

strain but oogonia when paired against a third 

(see pp. 86 and 95). Steroid hormones play 

an important role in sexual reproduction (see 

Fig. 5.11). 

The mature oospore contains three major 

pools of storage compounds (Fig. 5.2; Dick, 1995). 

The oospore wall often appears stratified, and 

this is due in part to a polysaccharide reserve 

compartment, the endospore, which is located


Fig 5.3 Life cycle of Saprolegnia.Vegetative hyphae are diploid and coenocytic. Asexual reproduction is by means of diplanetic 

(auxiliary and principal) zoospores.The principal zoospore state is polyplanetic. Saprolegnia is homothallic, and sexual reproduction 

is initiated by the formation of antheridia and oogonia.For simplicity, only a single nucleus is shown in each of the oospheres and 

in the antheridium. Each oogonium contains several oospheres. Karyogamy occurs soon after fertilization of an oosphere by an 

antheridial nucleus.The oospore may germinate by means of a germ sporangium (not shown) or a hyphal tip.Open and closed circles 

represent haploid nuclei of opposite mating type; diploid nuclei are larger and half-filled. Key events in the life cycle are meiosis (M), 

plasmogamy (P) and karyogamy (K). 

between the plasma membrane and the outer 

spore wall (epispore). Upon germination, the 

endospore is thought to coat the emerging germ 

tube with wall material, and some material may 

also be taken up by endocytosis. A large storage 

vacuole inside the oospore protoplast is called 

the ooplast. It arises by fusion of dense-body 

vesicles and, like them, contains mycolaminarin 

and phosphate. Dick (1995, 2001a) speculated 

that the ooplast contributes membrane precursor 

material during the process of oospore germination. 

The third storage compartment consists 

of one or several lipid droplets which provide 

the endogenous energy supply required for germination. 

Ultrastructural changes during oospore 

germination have been described by Beakes 

(1981). 

5.1.4 Ecology and significance 

Oomycota have a major impact on mankind as 

pathogens causing plant diseases of epidemic 

proportions. Two events have had particularly 

far-reaching political and social consequences, 

and have shaped and interlinked the young 

disciplines of mycology and plant pathology in 

the nineteenth century. These were the great 

Irish potato famine of 1845 1848 caused by 

Phytophthora infestans (Bourke, 1991), and the 

occurrence of downy mildew of grapes caused 

by Plasmopara viticola (Large, 1940). The former

SAPROLEGNIALES 

79 

prepared the way for the then revolutionary 

theory that fungal infections can be the cause 

rather than the consequence of disease, whereas 

the latter stimulated research into chemical 

control of diseases which directly gave rise to 

the first fungicide, Bordeaux mixture (p. 119; 

Large, 1940). 

Although all members of Oomycota depend 

on moist conditions for the dispersal of their 

zoospores, they are cosmopolitan and ubiquitous 

even in terrestrial situations. In species adapted 

to drier habitats, the sporangia often germinate 

directly to produce a germ tube, with zoospores 

released as an alternative germination method 

only in the presence of moisture, or lacking 

altogether. Oomycota occur in freshwater, the 

sea, in the soil and on above-ground plant 

organs. Most are obligate aerobes, although 

some tolerate anaerobic conditions (Emerson & 

Natvig, 1981; Voglmayr et al., 1999), and one 

species (Aqualinderella fermentans) is obligately 

anaerobic and lacks mitochondria (Emerson & 

Weston, 1967). Oomycota live either saprotrophically 

on organic material, or they may be 

obligate (biotrophic) or facultative (necrotrophic) 

parasites of plants. Some can also cause diseases 

of animals, such as Aphanomyces astaci which has 

all but eliminated European crayfish from many 

rivers (p. 94), Saprolegnia spp. which cause serious 

infections of farmed fish, especially salmon 

(Plate 2a; Dick, 2003), or Pythium insidiosum 

causing equine phycomycosis (de Cock et al., 

1987). Yet other Oomycota, notably Lagenidium 

giganteum, parasitize insects and may prove 

valuable in the biological control of mosquito 

larvae (Dick, 1998). 

5.1.5 Classification 

As indicated above, the classification of 

Oomycota at the level below the phylum is still 

an ongoing process, and it is difficult at present 

to reconcile the different classification schemes 

that are being proposed. Kirk et al. (2001) listed 

eight orders in the phylum Oomycota, of which 

Dick (2001b) treated six within the class 

Peronosporomycetes, his equivalent to the 

Oomycota, considering the other two of 

uncertain affinity (incertae sedes). These groups 

are summarized in Table 5.1. 

5.2 Saprolegniales 

The order Saprolegniales is currently divided 

up into two families, the Saprolegniaceae 

(e.g. Achlya, Brevilegnia, Dictyuchus, Saprolegnia, 

Thraustotheca) and Leptolegniaceae (Aphanomyces, 

Leptolegnia, Plectospira), totalling 132 species in 

about 20 genera (Dick, 2001a; Kirk et al., 2001). 

The Saprolegniales are the best-known group of 

aquatic fungi, often termed the water moulds. 

Members of this group are abundant in wet soils, 

lake margins and freshwater, mainly as saprotrophs 

on plant and animal debris. Whilst some 

Saprolegniales occur in brackish water, most 

are intolerant of it and thrive best in freshwater. 

A few species of Saprolegnia and Achlya are economically 

important as parasites of fish and 

their eggs (Willoughby, 1994). Aphanomyces 

euteiches causes a root rot of peas and some 

other plants, whilst A. astaci is a serious parasite 

of the European crayfish Astacus (Alderman et al., 

1990). Algae, fungi, rotifers and copepods may 

also be parasitized by members of the group, and 

occasional epidemics of disease among zooplankton 

have been reported. 

Members of the Saprolegniales are characterized 

by coarse, stiff hyphae which branch 

to produce a typically fast-growing mycelium. 

The hyphae of Saprolegniales are coenocytic, 

containing a peripheral layer of cytoplasm 

surrounding a continuous central vacuole. 

Cytoplasmic streaming is readily observed in 

the peripheral cytoplasm. Numerous nuclei are 

present. Mitotic division is associated with the 

replication of paired centrioles and the development 

of an intranuclear mitotic spindle; the 

nuclear membrane remains intact throughout 

division (Dick, 1995). Filamentous mitochondria 

and lipid droplets can also be observed in 

vegetative hyphae. The mitochondria are orientated 

parallel to the long axis of the hypha and 

are sufficiently large to be seen in cytoplasmic 

streaming in living material. Important physiological 

work has been carried out on the


Table 5.1. Summary of the most important groups of Oomycota and their characteristic features. Only the 

last four groups are considered further in this book. Based on information provided by Dick (2001a,b) and 

Kirk et al. (2001). 

Order 

Number 

of species 

Thallus and 

reproduction 

Ecology 

Myzocytiopsidales 

(incertae sedes) 

Olpidiopsidales 

(incertae sedes) 

74 Holocarpic, later 

coralloid or breaking 

up into segments. 

Zoospores, oospores. 

21 Holocarpic, becoming 

converted into a 

sporangium. Zoospores, 

oospores. 

Rhipidiales 12 Eucarpic with rhizoids. 


Leptomitales 25 Constricted hyphae 

producing sporangia. 


Saprolegniales 

(see Section 5.2) 

Pythiales 


Peronosporales 


Sclerosporaceae 


132 Mycelium of wide stout 

hyphae. Zoospores, 

oospores. 

4200 Mycelium of relatively 

narrow hyphae. 


252 Intercellular mycelium with 

haustoria.Differentiated 

sporangiophores. 

Zoospores or‘conidia’, 

oospores. 

22 Mycelium of very narrow 

hyphae.Differentiated 


Zoospores or‘conidia’, 

oospores. 

Parasites of invertebrates or algae. 

Biotrophic parasites of Oomycota, 

Chytridiomycota and algae. 

Freshwater saprotrophs, facultatively 

or obligately anaerobic. 

Freshwater saprotrophs or parasites 

of animals. 

Saprotrophs or necrotrophic pathogens 

of animals, plants and other organisms. 

Saprotrophs or pathogens 

(often necrotrophic) of plants, fungi and 

animals. 

Biotrophic plant pathogens, causing 

downy mildews and other diseases. 

Biotrophic pathogens of grasses, causing 

downy mildews. 

For thallus terminology, see Fig.6.1. 

mechanisms of hyphal polarity and growth 

regulation in Achlya and Saprolegnia (see Heath, 

1995b; Hyde & Heath, 1997; Heath & Steinberg, 

1999). Like other Oomycota but in contrast to the 

Eumycota (Pfyffer et al., 1986; Rast & Pfyffer, 

1989), these fungi are unable to synthesize 

compatible osmotically active solutes such as 

glycerol, mannitol and other polyols to maintain 

their intrahyphal turgor pressure against fluctuating 

external conditions. Under conditions of 

water stress, the turgor pressure in hyphae of 

Achlya and Saprolegnia approaches zero, yet hyphal 

growth can still occur at least under laboratory 

conditions because of the enhanced secretion of


81 

cell wall-softening enzymes and the role of the 

cytoskeleton in pushing forward the growing tip 

(see pp. 6 9; Money & Harold, 1992, 1993; Money, 

1997; Money & Hill, 1997). 

The Saprolegniales are the only order within 

the Oomycota to produce both auxiliary and 

principal zoospores, although both forms are not 

produced in all genera. The production of two 

distinct motile stages is termed diplanetism. 

It has also been called dimorphism, but this 

term has several different meanings and is best 

avoided in the current context. Depending on 

environmental conditions, the cysts of principal 

zoospores may germinate either by means of a 

germ tube developing into a hypha or by the 

emergence of a new principal zoospore. The 

repetition of the same type of motile spore is 

called polyplanetism. 

Sexual reproduction in the Saprolegniales is 

oogamous, with a large, usually spherical oogonium 

containing one or several oospheres. 

Antheridial branches apply themselves to the 

wall of the oogonium and penetrate the wall 

by fertilization tubes through which a single 

nucleus is introduced into each oosphere. A 

feature of many Saprolegniales, especially when 

grown in culture, is the formation of thick-walled 

enlarged terminal or intercalary portions of 

hyphae which become packed with dense cytoplasm 

and are cut off from the rest of the 

mycelium by septa. These structures, which may 

occur singly or in chains (see Fig. 5.6g), are termed 

gemmae or chlamydospores, and their formation 

can be induced by manipulating the culture conditions. 

Morphologically less distinct but otherwise 

similar structures are frequently found in 

old cultures. Although it is known that chlamydospores 

cannot survive desiccation or prolonged 

freezing, they remain viable for long periods in 

less extreme conditions. They may function as 

female gametangia or as zoosporangia, but more 

frequently they germinate by means of a germ 

tube. Another feature of old cultures is the 

fragmentation of cylindrical pieces of mycelium 

cut off at each end by a septum. 

Members of the Saprolegniales can be isolated 

readily from water, mud and soil by floating split 

boiled hemp seeds or dead house flies in dishes 

containing pond water, or by covering soil 

samples or waterlogged twigs with water 

(Stevens, 1974; Dick, 1990a). Within about 4 days 

the fungi can be recognized by their stiff, 

radiating, coarse hyphae bearing terminal sporangia, 

and cultures can be prepared by transferring 

hyphal tips or zoospores to cornmeal agar 

or other suitable media. The most commonly 

encountered genera are Achlya, Dictyuchus, 

Saprolegnia, Thraustotheca and Aphanomyces. With 

the exception of a few obligately parasitic species, 

most of the Saprolegniales will grow readily in 

pure culture even on chemically defined media, 

and extensive studies of their nutritional physiology 

have been undertaken (summarized by 

Cantino, 1955; Gleason, 1976; Jennings, 1995). 

Most species examined have no requirement for 

vitamins. Organic forms of sulphur such as 

cysteine, cystine, glutathione and methionine 

are preferred, and most species are unable to 

reduce sulphate. Organic nitrogen sources such 

as amino acids, peptone and casein are preferred 

to inorganic sources. Ammonium is widely 

utilized, but nitrate is not. Glucose is the most 

widely utilized carbon source, but many species 

also degrade maltose, starch and glycogen. In 

liquid culture, Saprolegnia can be maintained in 

the vegetative state indefinitely if supplied with 

organic nutrients in the form of broth. When the 

nutrients are replaced by water, the hyphal tips 

quickly develop into zoosporangia. The formation 

of sexual organs can similarly be affected by 

manipulating the external conditions in some 

species, and the concentration of salts in the 

medium may play a decisive role (Barksdale, 

1962; Davey & Papavizas, 1962). 

5.2.1 Saprolegnia (Saprolegniaceae) 

Species of Saprolegnia are common in soil and in 

freshwater as saprotrophs on plant and animal 

remains. A few species such as S. parasitica and 

S. polymorpha cause disease in fish and their eggs 

(Plate 2a). Salmonid fish are particularly affected, 

and the disease can cause significant damage 

in fish farms around the world (Willoughby, 

1994, 1998a). Control by fungicides is difficult 

but possible (Willoughby & Roberts, 1992). The 

disease is also seen in wild salmon and other fish 

(Söderhäll et al., 1991; Bly et al., 1992). Pathogenic


strains or species may be closely related to nonpathogenic 

ones but can be distinguished by 

physiological characteristics, DNA sequencing 

(Yuasa & Hatai, 1996) and the length of the 

‘boat hook’ appendages on the cysts of principal 

zoospores (Figs. 5.5b,c; Beakes, 1983; Burr & 

Beakes, 1994). 

The life cycle of Saprolegnia is summarized in 

Fig. 5.3. A monographic treatment of the genus 

has been published by Seymour (1970). 

Asexual reproduction in Saprolegnia 

Sporangia of Saprolegnia develop when a hyphal 

tip, which is pointed in the vegetative condition, 

swells, rounds off and becomes club-shaped. It 

accumulates denser cytoplasm around the 

vacuole which remains clearly visible. A septum 

develops at the sporangial base and it is at first 

straight or convex with respect to the sporangium, 

i.e. it bulges into it (Figs. 5.4c,d). The 

sporangium contains numerous nuclei, and 

Fig 5.4 Saprolegnia. (a) Apex of vegetative hypha. (b d) Stages in the development of zoosporangia. (e) Release of zoospores. 

(f) Proliferation of zoosporangium. A second zoosporangium is developing within the empty one. (g) Auxiliary zoospore (first 

motile stage). (h) Cyst formed at the end of the first motile stage (auxiliary cyst). (i,j) Germination of auxiliary cyst to release a 

second motile stage (principal zoospores).These have the typical reniform shape. (k m) Principal zoospores. (n) Principal zoospore 

at the moment of encystment. Note the shed flagellum. (o) Principal cyst. (p) Principal cyst germinating by means of a germ tube. 

(a f) to same scale; (g p) to same scale. Note that the straminipilous flagellum cannot be distinguished from the whiplash flagellum 

at the magnification chosen.


83 

cleavage furrows separate the cytoplasm into 

uninucleate pieces, each of which differentiates 

into an auxiliary zoospore. As the zoospores are 

cleaved, the central vacuole disappears. The tip 

of the cylindrical sporangium contains clearer 

cytoplasm and a flattened protuberance, the 

papilla, develops at the apex. As the sporangium 

ripens and the zoospores become fully 

differentiated, they show limited movement 

and change of shape (Figs. 5.4b d). Shortly 

before discharge, there is evidence of a buildup 

of turgor pressure within the sporangium 

because the basal septum becomes concave, 

i.e. it is bent towards the lumen of the hypha 

beneath the sporangium. After cleavage, the 

positive turgor pressure is lost concomitantly 

with the loss of the sporangial plasma membrane 

which becomes part of the zoospore 

membranes, and the septum again bulges into 

the sporangium while the zoospores become fully 

differentiated. The sporangium undergoes a 

slight change of shape at this time and the 

sporangium wall breaks down at the papilla. The 

spores are released quickly, many zoospores 

escaping in a few seconds and moving as a 

column through the opening. Osmotic phenomena 

have been invoked to explain the rapidity 

of discharge, and the osmotically active substances 

must be large enough to be contained 

by the sporangial wall. Mycolaminarin, released 

from the central vacuole during zoospore differentiation, 

is the likely solute (Money & 

Webster, 1989). The whole process of sporangium 

differentiation takes about 90 min. The zoospores 

leave the sporangium backwards, with the blunt 

posterior end emerging first. The size of the 

zoospore is sometimes greater than the diameter 

of the sporangial opening so that the zoospores 

are squeezed through it. An occasional zoospore 

may be left behind, swimming about in the 

empty zoosporangium for a while before making 

its exit. Zoospores in partially empty sporangia 

orientate themselves in a linear fashion along the 

central axis of the sporangium. 

A characteristic feature of Saprolegnia is that, 

following the discharge of a zoosporangium, 

growth is renewed from the septum at its base so 

that a new apex develops inside the old sporangial 

wall by internal proliferation. This in 

turn may develop into a zoosporangium, discharging 

its spores through the old pore (Fig. 5.4f). 

The process may be repeated so that several 

empty zoosporangial walls may be found inside, 

or partially inside, each other. 

Upon release, the auxiliary zoospores slowly 

revolve and eventually swim somewhat sluggishly 

with the pointed end directed forwards. 

They are grapeseed- or pear-shaped (‘Conference’ 

pear; Dick, 2001a) and bear two apically attached 

flagella (see Figs. 5.1a, 5.4g). Each zoospore 

also contains a diploid nucleus, mitochondria, 

a contractile vacuole and numerous vesicles 

(Holloway & Heath, 1977a,b). The zoospores 

from a single sporangium show variation in 

their period of motility, the majority encysting 

within about a minute, but some remaining 

motile for over an hour. The zoospore then 

withdraws its flagella and encysts, i.e. the 

cytoplasm becomes surrounded by a distinct 

wall which is produced from pre-formed material 

stored in the cytoplasmic vesicles. Only the 

axonemes of the flagella are withdrawn, leaving 

the TTHs of the straminipilous flagellum at 

the surface of the cyst (see Fig. 5.5a). Following 

a period of rest (2 3h in S. dioica), the cyst 

germinates to release a further zoospore, the 

principal zoospore (Figs. 5.4i,j). This differs in 

shape from the auxiliary zoospore in being beanshaped, 

with the two flagella inserted laterally 

in a shallow groove running down one side of 

the zoospore (Fig. 5.1b). The principal zoospore 

may swim vigorously for several hours before 

encysting. Salvin (1941) compared the rates of 

movement of auxiliary and principal zoospores 

in Saprolegnia and found that the latter swam 

about three times more rapidly. The probable 

reason for this is that the lateral insertion of 

both flagella allows the straminipilous flagellum 

to point forward and the whiplash one to point 

backward, thereby improving the propulsion 

relative to the apical insertion in which both 

flagella point forward. 

Movement of principal zoospores is chemotactic 

and zoospores can be stimulated to 

aggregate on parts of animal bodies such as the 

leg of a fly, or the surface of a fish (Fischer & 

Werner, 1958; Willoughby & Pickering, 1977). 

When principal zoospores encyst, they shed


Fig 5.5 Surface features of Saprolegnia. (a) Detail of 

an auxiliary zoospore cyst of S. parasitica showing 

the tuft of TTHs (mt) at the point where the 

straminipilous flagellum was withdrawn. (b) Surface of 

a principal zoospore cyst of S. parasitica; the long boat 

hook spines are arranged in fascicles. (c) Surface of a 

principal zoospore cyst of S. hypogyna with discrete 

boat hooks of intermediate length. All bars ¼ 2 mm. 

All images kindly provided by M.W. Dick and I.C. 

Hallett; (b) reprinted from Hallett and Dick (1986), 

with permission from Elsevier. 

rather than withdraw their flagella. The first step 

in encystment is the fusion of vesicles called 

K-bodies with the plasma membrane. These are 

so called because they are located near the 

kinetosome. The material they secrete is involved 

in attachment of the zoospore to a substratum, 

which occurs in the region of the groove near the 

flagellar bases, designated the ventral region 

(Lehnen & Powell, 1989). The cyst wall and preformed 

boat hook spines are secreted by fusion of 

encystment vesicles with the plasma membrane 

(Beakes, 1987; Burr & Beakes, 1994). The length 

and arrangement of spines on the surface of a 

mature principal cyst are characteristic features 

of individual species (Figs. 5.5b,c). They probably 

mediate attachment of the cyst to the host, and 

pathogenic isolates of Saprolegnia have much 

longer spines than saprotrophic ones (Burr & 

Beakes, 1994). Alternatively, the boat hooks may 

mediate attachment to the water meniscus.


85 

Either way, attachment must be very effective 

because trout or char, placed in a water bath with 

principal zoospores of S. parasitica for 10 min and 

followed by 1 h in clean water, had an extremely 

high concentration of cysts attached to the skin 

(Willoughby & Pickering, 1977). 

Principal zoospore cysts can germinate either 

by means of a germ tube (Fig. 5.4p) or by 

releasing a further principal zoospore which in 

turn may germinate directly or by releasing yet 

another motile stage. Saprolegnia is therefore 

polyplanetic. The auxiliary and principal zoospores, 

as well as the cysts they form, differ 

morphologically from each other, i.e. they are 

diplanetic. 

Sexual reproduction in Saprolegnia 

All members of the genus Saprolegnia characterized 

to date are homothallic, i.e. a culture 

derived from a single zoospore will give rise to 

a mycelium forming both oogonia and antheridia. 

In contrast, Achlya also contains heterothallic 

species in which sexual reproduction occurs 

only when two different strains are juxtaposed, 

one forming oogonia, the other antheridia (see 

Fig. 5.10). 

Sexual reproduction follows a similar course 

in all members of the Saprolegniales. Oogonia 

containing one or several eggs are fertilized by 

antheridial branches. Fertilization is accomplished 

by the penetration of fertilization tubes 

into the oogonium. In some species, ripe oogonia 

are found without antheridia associated with 

them (Fig. 5.6f); this could be due either to the 

fusion of two haploid nuclei from adjacent 

meiotic events in a single oogonium (apomixis) 

or the formation of an oospore around a diploid 

nucleus that never underwent meiosis (parthenogenesis). 

Both processes are impossible to 

distinguish without detailed cytological evidence 

(Dick, 2001a). The typical arrangement of oogonia 

and antheridia in Saprolegnia is shown in 

Fig. 5.6. Antheridial branches arising from the 

stalk of the oogonium or the same hypha as the 

oogonium are said to be monoclinous whereas 

they are diclinous if they originate from different 

hyphae. 

Fig 5.6 Saprolegnia litoralis.(a d) Stages in the development of oogonia. (c) Oogonium showing furrowed cytoplasm indicative 

of centrifugal cleavage. (d) Outlines of two oospheres become visible. (e) Oogonium with two mature oospores. (f) Intercalary 

oogonium lacking antheridia.The oospores have developed by apomixis or parthogenesis. (g) Chain of chlamydospores.


The oogonial initial is multinucleate, and 

nuclear divisions continue as it enlarges. 

Eventually some of the nuclei degenerate, leaving 

only those nuclei which are included in the 

oospheres. From the central vacuole within the 

oogonium, cleavage furrows radiate outwards to 

divide the cytoplasm into uninucleate portions 

which round off to form oospheres. Oogonium 

differentiation is thus centrifugal, which is 

typical of the Saprolegniales. Cleavage of the 

oospheres from the cytoplasm is brought about 

by the coalescence of dense body vesicles which 

finally fuse with the plasma membrane of the 

oogonium so that the oospheres tumble into the 

centre of the oogonium (Dick, 2001a). The entire 

mass of cytoplasm within the oogonium is used 

up in the formation of oospheres and there is 

no residual cytoplasm (periplasm) as in the 

Peronosporales. The wall of the oogonium is 

often uniformly thick, but in some species it 

shows thin areas or pits through which fertilization 

tubes may enter (Fig. 5.6e). A septum at 

the base of the oogonium cuts it off from the 

subtending hypha. 

The antheridia are also multinucleate. The 

antheridial branch grows towards the oogonium 

and attaches itself to the oogonial wall. The tip of 

the antheridial branch is cut off by a septum, 

and the resulting antheridium puts out a fertilization 

tube which penetrates the oogonial wall 

and may branch within the oogonium. After the 

tube has penetrated an oosphere wall, a male 

nucleus eventually fuses with the single oosphere 

nucleus. The fertilized oosphere (oospore) undergoes 

a series of changes described by Beakes 

and Gay (1978a,b). The wall of the oospore 

thickens and oil globules become obvious. 

Mature oospores contain a membrane-bound 

vacuole-like body, the ooplast, surrounded by 

cytoplasm containing various organelles, with 

lipid droplets particularly prominently visible. 

In Saprolegnia, the ooplast contains particles in 

Brownian motion. The position of the ooplast in 

the oospore is used for species identification, and 

four types of oospore have been distinguished 

(Fig. 5.7; Seymour, 1970; Howard, 1971). Centric 

oospores have a central ooplast surrounded by 

one or two peripheral layers of small lipid 

droplets (e.g. S. hypogyna, S. ferax). Subcentric 

oospores have several layers of small lipid 

droplets on one side of the ooplast and only one 

layer or none at all on the other (e.g. S. unispora, 

S. terrestris). In subeccentric oospores, the small 

lipid droplets have fused into several large ones 

all grouped to one side, with the ooplast contacting 

the plasma membrane on the opposite side 

(e.g. S. eccentrica). The eccentric type (found, for 

example, in S. anisospora) is similar to the 

subeccentric type except that there is only one 

very large lipid drop. These descriptive terms are 

also used for many other species of Oomycota. 

5.2.2 Achlya (Saprolegniaceae) 

Phylogenetic analyses have shown that the 

genera Achlya and Saprolegnia as well as minor 

genera of the Saprolegniales are closely related 

to each other, with possible overlaps which may 

necessitate the re-assignment of some species in 

future (Riethmüller et al., 1999; Leclerc et al., 

2000; Dick, 2001a). Morphologically and ecologically, 

Achlya and Saprolegnia also share several key 

features. Both are common in soil and in waterlogged 

plant debris such as twigs, and certain 

species are pathogens of fish (Willoughby, 1994; 

Kitancharoen et al., 1995). Unlike Saprolegnia, 

some species of Achlya are heterothallic, but 

their life cycle is otherwise similar to that of 

Saprolegnia given in Fig. 5.3. Heterothallic strains 

of Achlya have been the subject of classical 

Fig 5.7 Possible arrangements of the 

ooplast (shaded organelle) and lipid 

droplets (empty circles or ellipses) in 

oospores of Saprolegnia. (a) Centric. 

(b) Subcentric. (c) Subeccentric. 

(d) Eccentric.


87 

studies on the nature of mating hormones 

(pheromones); additionally, more recent work 

has focused on zoospore release. Both aspects are 

described below. 

Asexual reproduction in Achlya 

The development of zoosporangia in Achlya is 

similar in all aspects to that in Saprolegnia but 

has been better researched. The central vacuole 

in the developing cylindrical sporangium is 

typical of the Saprolegniales and originates 

from the fusion of dense body vesicles containing 

mycolaminarin. The centrifugal cleavage of 

cytoplasm from the vacuole towards the plasma 

membrane, and the partitioning of individual 

spores, are controlled mainly by the actin 

cytoskeleton (Heath & Harold, 1992). In the 

Pythiales, vital roles of microtubules in the 

organization of differentiating cytoplasm have 

been described (see p. 102), and microtubules 

may have similar but as yet undescribed functions 

in the Saprolegniales. As the plasma 

membrane of the Achlya zoosporangium is 

breached, the zoosporangial volume decreases 

by about 10% due to the loss of turgor pressure. 

Since the membranes of the vacuole contribute 

to the zoospore plasma membrane, the vacuolar 

contents of water-soluble mycolaminarins (b-1,3- 

glucans) are released into the sporangium. These 

molecules are osmotically active but are too 

large to diffuse through the sporangial wall, thus 

causing the osmotic inward movement of water 

into the sporangium, which in turn pressurizes 

the sporangium and drives the rapid discharge of 

the auxiliary zoospores (Money & Webster, 1985, 

1988; Money et al., 1988). 

On discharge, the zoospores do not swim 

away but cluster in a hollow ball at the mouth of 

the zoosporangium and encyst there (Fig. 5.8a). 

In fact, it is doubtful whether the term ‘zoospore’ 

is altogether appropriate as functional flagella 

are probably not formed. Partial fragmentation 

of the cyst ball frequently occurs and may have 

ecological significance in the dispersal of cysts 

prior to the release of principal zoospores. Unlike 

certain species of Saprolegnia, Achlya cysts are 

normally found at the bottom of culture dishes, 

and presumably also at the water/bottom sediment 

interface in natural environments. Cysts of 

Fig 5.8 Achlya colorata. (a) Zoosporangium showing a clump 

of primary cysts at the mouth.Note the lateral proliferation of 

the hypha from beneath the old sporangium. (b) Full and empty 

auxiliary cysts. (c) Stages in the release of principal zoospores 

from an auxiliary cyst. (d) Principal zoospores. (e) Principal 

cyst. (f) Principal cyst germinating by means of a germ tube. 

A. klebsiana may remain viable for at least two 

months when stored aseptically at 5°C (Reischer, 

1951). However, most auxiliary cysts remain at 

the mouth of the sporangium for a few hours 

and then each cyst releases a principal zoospore 

through a small pore (Figs. 5.8b,c). After a period 

of swimming, principal zoospores encyst, and 

principal cysts germinate either by a germ tube 

or by releasing another principal zoospore. When 

the zoosporangium of Achlya has released its


Fig 5.9 Achlya colorata.(a d) Stages 

in the development of oogonia. 

(e) Six-month-old oospores 

germinating after 40 h in charcoal 

water. 

zoospores, growth is usually renewed laterally by 

the outgrowth of a new hyphal apex just beneath 

the first sporangium (Fig. 5.8a), rather than by 

internal proliferation. 

Sexual reproduction in Achlya 

Some species of Achlya are homothallic (Fig. 5.9) 

whereas others are heterothallic (Fig. 5.10). 

Achlya colorata, a homothallic species common 

in Britain, has oogonial walls which develop 

blunt, rounded projections so that the oogonium 

appears somewhat spiny (Fig. 5.9d). Otherwise, 

the process of sexual reproduction is similar to 

that of Saprolegnia litoralis (Fig. 5.6). Germination 

of oospores is often difficult to achieve with 

Oomycota, but can be stimulated in A. colorata by 

transferring mature oospores to freshly distilled 

water (preferably after shaking with charcoal 

and filtering). Germination occurs by means of a 

germ tube which grows out from the oospore 

through the oogonial wall. Here it may continue 

growth as a mycelium (Fig. 5.9e) or may give rise 

to a sporangium. 

The study of heterothallic species of Achlya by 

John R. Raper quickly revealed that the formation 

of oogonia and antheridia by compatible 

strains must be under hormonal control (Raper, 

1939, 1957). A particularly readable account of 

the classical series of experiments leading to the 

discovery of the steroid sex hormone, antheridiol 

(Fig. 5.11b), has been given by Carlile (1996b). 

Several reviews of the broader role of hormones 

in fungal reproduction have appeared recently 

(Gooday & Adams, 1992; Elliott, 1994). If isolates 

of Achlya bisexualis, A. ambisexualis or A. heterosexualis 

made from water or mud are grown singly


89 

Fig 5.10 Achlya ambisexualis. 

(a) Male and female mycelia grown 

on hemp seeds and placed together 

in water for 4 days. Note the 

formation of antheridial branches 

on the male and oogonial branches 

on the female. (b) Fertilization, 

showing the diclinous origin of the 

antheridial branch. 

Fig 5.11 Sterols from Achlya spp.Fucosterol (a) is one of the 

most abundant sterols in Oomycota and precursor to the sex 

hormones antheridiol (b) and oogoniol (c). 

on hemp seed in water, reproduction is entirely 

asexual, but when certain of the isolates are 

grown together in the same dish, it becomes 

apparent within 2 3 days that one strain is 

forming oogonia, and the other antheridia. The 

development of oogonia and antheridia occurs 

even when the two strains are held apart in the 

water or separated by a cellophane membrane or 

by agar. This suggests that one or more diffusible 

substances are responsible for the phenomenon. 

As compatible colonies approach each other, the 

first observable reaction is the production of fine 

lateral branches behind the advancing tips of the 

male hyphae. These are antheridial branches. 

By growing male (antheridial) strains in water 

in which a female (oogonial) strain had been 

grown previously, Raper (1939) showed that 

the vegetative female mycelium was capable 

of initiating the development of antheridial 

branches on the male. The reverse experiment 

showed no effect on female colonies in medium 

in which undifferentiated male colonies had 

been grown. The role of the vegetative female 

colony as initiator of the sequence of events 

leading to sexual reproduction was confirmed by 

ingenious experiments in micro-aquaria consisting 

of several consecutive chambers through 

which water flowed by means of small siphons. 

Male and female colonies were placed alternately 

in successive chambers, so that water from a 

male colony would flow over a female colony and 

so on. If a female colony was placed in the first 

chamber, the male colony in the second chamber 

reacted by developing antheridial hyphae. If, 

however, a male colony was placed in the first 

chamber, the male colony in the third chamber


was the first to react. Raper (1939) postulated that 

the development of the antheridial branches was 

in response to a hormone, termed Hormone A, 

secreted by vegetative female colonies. By further 

experiments of this kind, he showed that the later 

steps in the sexual process were also regulated 

by means of diffusible substances. He postulated 

that the antheridial branches secreted a second 

substance, Hormone B, which resulted in the 

formation of oogonial initials on the female 

colony. The oogonial initials in their turn 

secreted a further substance called Hormone C, 

which stimulated the antheridial initials to grow 

towards the oogonial initials and also resulted 

in the antheridia being delimited. Having made 

contact with the oogonial initials, the antheridial 

branches secreted Hormone D which resulted 

in the formation of a septum cutting off the 

oogonium from its stalk, and in the formation 

of oospheres. The original scheme (Table 5.2) 

therefore implicated four hormones, but confusion 

arose subsequently because the effect of 

Hormone A can be modulated by amino acids 

and other metabolites released from the hemp 

seeds (Barksdale, 1970; Schreurs et al., 1989). 

Since Hormone A is active at extremely low 

concentrations of 2 10 11 M (Barksdale, 1969), 

purification of this substance was extremely challenging, 

and 6000 l of culture fluid had to be 

extracted to obtain 20 mg crystalline Hormone A 

(Barksdale, 1967). It was eventually identified as 

the steroid antheridiol (Fig. 5.11b). Soon after, the 

structure of Hormone B was elucidated and 

found also to be a steroid, oogoniol (Fig. 5.11c), 

which is, in fact, present as three chemically 

closely related forms (McMorris et al., 1975). The 

effect postulated by Raper (1939) to be due to 

Hormone C is now thought to be mediated by 

antheridiol activity, whereas Hormone D may not 

exist (Carlile, 1996b). Both antheridiol and the 

oogoniols are derived from fucosterol (Fig. 5.11a), 

the principal sterol in Achlya (see Elliott, 1994). 

The physiological roles of antheridiol and 

the oogoniols are several-fold and include induction 

or suppression of sexuality (Thomas & 

McMorris, 1987), directional growth of gametangial 

tips (McMorris, 1978), and stimulation of 

the production of cell wall-softening enzymes 

(especially cellulase) at points of branching and 

contact between gametangia (Mullins, 1973; Gow 

& Gooday, 1987). A cytoplasmic receptor protein 

for antheridiol has been detected (Riehl et al., 

1984), and the hormone probably acts like 

its equivalents in mammalian cells, by the 

receptor hormone complex moving to the 

nucleus and binding specifically to DNA, increasing 

transcription rates of certain genes (Elliott, 

1994). 

There is evidence that the co-ordination of 

sexual reproduction by hormonal control is not 

confined to heterothallic forms of Achlya, but 

also takes place in homothallic species. The fact 

that it is possible to initiate sexual reactions 

between homothallic and heterothallic species 

of Achlya shows that some of the hormones are 

common to more than one species, although 

Table 5.2. Postulated effects of hormones on sexual reactions in Achlya ambisexualis. 

Hormone Produced by Affecting Specific action 

A Vegetative hyphae Vegetative hyphae Induces formation of antheridial branches. 

B Antheridial branches Vegetative hyphae Initiates formation of oogonial initials. 

C Oogonialinitials Antheridial branches (1) Attracts antheridial branches. 

(2) Induces thigmotropic response and 

delimitation of antheridia. 

D Antheridia Oogonialinitials Induces delimitation of oogonium 

by formation of basal septum. 

After Raper (1939). So far, only hormones A and C (antheridiol) and B (oogoniol) have been shown 

to exist.


91 

there is also evidence of some degree of 

specificity of the hormones of different species 

(Raper, 1950; Barksdale, 1965). 

One further interesting phenomenon which 

has been discovered in relation to heterothallic 

Achlya spp. is relative sexuality. If isolates of 

A. bisexualis and A. ambisexualis from separate 

sources are paired in all possible combinations, it 

is found that certain strains show a capacity to 

react either as male or as female, depending on 

the particular partner to which they are apposed. 

Other strains remain invariably male or invariably 

female, and these are referred to as true or 

strong males or females. The strains can be 

arranged in a series with strong males and 

strong females at the extremes, and intermediate 

strains whose reaction may be either male or 

female depending on the strength of their 

mating partner. Similar interspecific responses 

between strains of A. bisexualis and A. ambisexualis 

are also possible. Further, some of the strains 

which appear heterothallic at room temperature 

are homothallic at lower temperatures. 

Barksdale (1960) has postulated that the heterothallic 

forms are derived from homothallic ones. 

She argued that the most notable difference 

between strong males and strong females lies in 

their differential antheridiol production and 

response. Very little of this substance is found 

in male cultures, and these are much more 

sensitive in their response to the hormone than 

female cultures. Another important difference is 

in the uptake of antheridiol. Certain strains 

appear capable of absorbing it much more 

readily than others, and it is the strains with a 

high ability to absorb antheridiol that produce 

antheridial branches during conjugation with 

other thalli (Barksdale, 1963). If one assumes that 

heterothallic forms have been derived from 

homothallic ones, this might have occurred by 

mutations leading to increased sensitivity to 

antheridiol and hence to maleness. Conversely, 

mutations leading to enhanced extracellular 

accumulation of antheridiol should lead to 

increasing femaleness. 

Germination of the oospores of A. ambisexualis 

results in the formation of a multinucleate germ 

tube which develops into a germ sporangium 

if transferred to water, or into a coenocytic 

mycelium in the presence of nutrients. This 

mycelium can be induced to form zoosporangia 

when transferred to water. From zoosporangia of 

either source, single zoospore cultures can be 

obtained which can be mated with the parental 

male or female strains. All zoospores or germ 

tubes derived from a single oospore gave the 

same result with regard to their sexual interaction. 

This finding suggests that nuclear division 

on oospore germination is not meiotic, and is 

thus consistent with the idea that the life cycle is 

diploid (Mullins & Raper, 1965). Confirmation of 

these results, implying meiosis during gamete 

differentiation, has also been obtained with 

A. ambisexualis (Barksdale, 1966). 

5.2.3 Thraustotheca, Dictyuchus and 

Pythiopsis (Saprolegniaceae) 

In Thraustotheca clavata the sporangia are broadly 

club-shaped, and there is no free-swimming 

auxiliary zoospore stage. Encystment occurs 

within the sporangia and the auxiliary cysts are 

released by irregular rupture of the sporangial 

wall (Fig. 5.12a). After release, the angular cysts 

germinate to release bean-shaped principal zoospores 

with laterally attached flagella (Figs. 

5.12c,d). After a period of swimming, further 

encystment occurs, followed by germination by 

a germ tube (Figs. 5.12e,f), or by emergence of a 

further principal zoospore. The zoospores are 

thus monomorphic and polyplanetic. Sexual 

reproduction is homothallic, but formation of 

gametangia is stimulated by Achlya sex hormones 

(Raper, 1950). Oospores germinate either by a 

germ tube or by a germ sporangium (Fig. 5.12g). 

In Dictyuchus, there is again no free-swimming 

auxiliary zoospore stage. Commonly the entire 

zoosporangium is deciduous, and detached zoosporangia 

are capable of forming zoospores. 

Auxiliary zoospore initials are cleaved out but 

encystment occurs within the cylindrical sporangium. 

The cysts are tightly packed together 

and release their principal zoospores independently 

through separate pores in the sporangial 

wall (Fig. 5.13a). When zoospore release is 

complete, a network made up of the polygonal 

walls of the auxiliary cysts is left behind. After 

swimming, the laterally biflagellate zoospores


Fig 5.12 Thraustotheca clavata. 

(a) Zoosporangium showing formation of 

auxiliary cysts within the sporangium. 

Theauxiliarycystsarebeingreleasedthrough 

breakdown of the sporangial wall. 

(b) Auxiliary cyst. (c) Auxiliary cyst 

germinating to release a principal zoospore, 

the first motile stage in this species. 

(d) Principal zoospore. (e) Principal cyst. 

(f) Principal cyst germinating by means of 

a germ tube. (g) Sexual reproduction. 

Six-month-old oospore germinating after17 h 

in charcoal water.The germ tube is terminated 

by a germ sporangium. Bar¼20 mm(a)or 

10 mm(b) (g). 

encyst (Figs. 5.13b,c). Electron micrographs have 

shown that the wall of the secondary cyst of 

D. sterile bears a series of long spines looking 

somewhat like the fruit of a horse chestnut 

(Fig. 5.14; Heath et al., 1970). Following the 

formation of the first zoosporangium, a second 

may be produced immediately beneath it by the 

formation of a septum cutting off a subterminal 

segment of the original hypha, or growth may 

be renewed laterally to the first sporangium 

(Fig. 5.13a). 

Because there is only one motile stage in 

Thraustotheca and Dictyuchus (i.e. a zoospore of 

the principal type), they are said to be monomorphic. 

Pythiopsis cymosa (Figs. 5.13e i) is also 

monomorphic, but in this species the only 

motile stage is of the auxiliary type and principal 

zoospores are not formed. After swimming, 

the zoospore encysts and then 

germinates directly by means of a germ tube 

(Figs. 5.13g i). 

5.2.4 Aplanetic forms 

In certain cultures of Saprolegniaceae the zoosporangia 

produce cysts which do not release any 

motile stage. Instead, germ tubes are put out 

which penetrate the sporangial wall. Forms 

without motile spores are said to be aplanetic. 

The aplanetic condition is occasionally found 

in staling cultures of Saprolegnia, Achlya and


93 

Fig 5.13 (a d) Dictyuchus sterile. (a) Zoosporangium showing cysts within the sporangium and the release of principal zoospores 

through separate pores in the sporangium wall. Note the network of auxiliary cyst walls. (b) Principal zoospores. (c) Principal cyst. 

(d) Germination of principal cysts by means of germ tubes. (e i) Pythiopsis cymosa. (e) Zoosporangium. (f,g) Auxiliary zoospores. 

(h) Auxiliary cyst. (i) Auxiliary cyst germinating by means of a germ tube. Principal zoospores have not been described. 

(a c,e,f) to same scale; (g i) to same scale. 

Dictyuchus. Some species produce sporangia only 

rarely and the genus Aplanes has been erected for 

these forms. However, in very clean cultural 

conditions, all have been shown to behave as 

Achlya, and they are currently accommodated 

within that genus (Dick, 2001a). Two species of 

Saprolegniaceae are not known to form sporangia 

at all. They are common in soil, and have 

been placed in a separate genus, Aplanopsis. 

Another genus, Geolegnia, forms sporangia containing 

thick-walled aplanospores which never 

produce a flagellate stage. The final classification 

of these small genera of Saprolegniaceae will 

have to await the results of comparisons of 

suitable DNA sequences (see M. A. Spencer et al., 

2002).


Fig 5.14 Surface of a principal cyst of Dictyuchus 

sterile.Note the spines covering the surface.Image 

kindly provided by M.W. Dick and I.C. Hallett; 

reprinted from Hallett and Dick (1986), with 

permission from Elsevier. 

5.2.5 Aphanomyces (Leptolegniaceae) 

Aphanomyces is distinguished from Achlya by its 

thin, delicate hyphae and its narrow sporangia 

containing a single row of spores. Based on these 

morphological differences and DNA sequence 

analyses, the genus Aphanomyces has been 

removed from the Saprolegniaceae and classified 

in the family Leptolegniaceae, still within the 

Saprolegniales (Dick et al., 1999; Hudspeth et al., 

2000; Dick, 2001a). 

Asexual reproduction in Aphanomyces is variable. 

In A. euteiches, flagella do not develop on the 

first-formed spores. Protoplasts are cleaved out, 

move to the mouth of the sporangium, and 

encyst. Principal zoospores develop from the 

cysts and are the first true motile stage. Aphanomyces 

euteiches is thus monomorphic. In A. patersonii, 

the motility of the first-formed zoospore is 

controlled by variation in temperature. Below 

20°C, encystment of the auxiliary zoospores at the 

mouth of the sporangium occurs in a manner 

typical of the genus, but above this temperature 

the auxiliary zoospores swim away and encyst 

some distance away from the zoosporangium. 

The genus Aphanomyces has been monographed 

by Scott (1961). It has gained notoriety 

particularly because A. astaci is the cause of 

the plague of European crayfish. Having been 

introduced probably in the 1860s from America, 

where the local crayfish populations are fairly 

resistant to A. astaci infections, the fungus has 

now spread across Europe, severely damaging 

commercial production of the highly susceptible 

European crayfish, Astacus fluviatilis 

(Alderman & Polglase, 1986; Cerenius et al., 

1988; Alderman et al., 1990). Although it would 

be possible to introduce resistant stock of 

American crayfish into European river systems 

affected by the disease, resistant crayfish still 

harbour the pathogen, thereby making it impossible 

to restore the native crayfish populations 

in the future (Dick, 2001a). The difference in 

resistance between North American and European 

crayfish lies in the melanization reaction 

which arrests hyphal growth from encysted 

zoospores (Nyhlén & Unestam, 1980; Cerenius 

et al., 1988). In European crayfish, melanization 

occurs too slowly to prevent the spread of the 

fungus into the haemocoel which causes rapid 

death. Aphanomyces astaci can also cause epizootic 

ulcerative disease in fish, the symptoms often 

being very similar to those caused by Saprolegnia 

(Lilley & Roberts, 1997). 

Aphanomyces euteiches is a significant pathogen 

of roots of peas and other terrestrial plants 

(Papavizas & Ayers, 1974; Persson et al., 1997). 

Recently, methods have been developed to quantify 

the prevalence of the pathogen in infected 

plants by measuring the levels of specific fatty 

acids which are produced by A. euteiches but not by 

plants or pathogens belonging to the Eumycota 

(Larsen et al., 2000). Other species of Aphanomyces

PYTHIALES 

95 

are keratinophilic, occurring in the soil or in 

water on insect remains (Dick, 1970; Seymour & 

Johnson, 1973). 

5.3 Pythiales 

The order Pythiales includes two families, the 

Pythiaceae and Pythiogetonaceae (Dick, 2001a; 

Kirk et al., 2001). The Pythiogetonaceae are a small 

group of aquatic saprotrophs presently comprising 

one genus and six species. They occur in 

anoxic sediments at the bottom of freshwater 

lakes and are facultatively anaerobic as well as 

obligately fermentative, i.e. they break down 

sugars incompletely to give organic acids irrespective 

of the presence or absence of oxygen 

(Emerson & Natvig, 1981; Natvig & Gleason, 1983). 

Another member of the Pythiogetonaceae, 

Pythiogeton zeae, causes root and stalk rot in 

maize (Jee et al., 2000). The Pythiogetonaceae are 

clearly related to the Pythiaceae by DNA sequence 

homology (Voglmayr et al., 1999). 

Only the Pythiaceae will be considered 

further in this book. This is a large family of 

over 200 species in approximately 10 genera, of 

which 2 are of outstanding significance: Pythium 

and Phytophthora. Phytophthora species are primarily 

pathogenic to plants from which they can be 

isolated and grown in pure culture. The genus 

Pythium is best known for its saprotrophic soilinhabiting 

members, many of which are opportunistic 

pathogens especially in young plants. 

There are also obligately pathogenic Pythium 

spp. Generally, Pythium spp. parasitize a wider 

diversity of hosts than Phytophthora, including 

mammals, fungi and algae. 

5.3.1 Life cycle of Pythiaceae 

The life cycle of Phytophthora infestans is summarized 

in Fig. 5.19. Asexual reproduction in Pythium 

and Phytophthora is by means of sporangia 

which vary in shape from swollen hyphae or 

globose structures (Pythium) to lemon-shaped 

(Phytophthora). Sporangia are borne on more or 

less undifferentiated hyphae. In most cases, 

sporangia germinate to produce zoospores 

which are of the principal (kidney-shaped) type. 

In many Pythium spp., the final stages of zoospore 

differentiation take place outside the sporangium 

in a walled vesicle, followed by breakdown 

of the soft wall and release of the zoospores. In 

Phytophthora, in contrast, zoospores differentiate 

within the sporangium and are released directly 

or via a very short-lived vesicle which is surrounded 

only by a membrane. About 20% of 

the total respiratory activity within a released 

zoospore is used up to fuel propulsion (Hölker 

et al., 1993). The forward-directed straminipilous 

flagellum generates about 10 times more thrust 

than the posterior whiplash flagellum which acts 

mainly as a rudder (Erwin & Ribeiro, 1996). 

Zoospores can swim for several hours before they 

encyst. The process of encystment has been 

examined in great detail for Phytophthora (see 

p. 102). Cysts usually germinate by means of 

a germ tube, only rarely producing a further 

zoospore stage. In many species, sporangia can 

germinate either indirectly by releasing zoospores 

or directly by means of a germ tube, 

depending on environmental conditions and 

age of the sporangium. 

Sexual reproduction is oogamous. Each oogonium 

contains a single oosphere (except for 

Pythium multisporum in which there are several). 

The antheridial and oogonial initials are 

commonly multinucleate at their inception and 

further nuclear divisions may occur during 

development. Meiosis eventually takes place in 

the gametangia so that karyogamy occurs 

between haploid antheridial and oogonial 

nuclei. In many forms, there is only one functional 

male and female nucleus, but in others 

multiple fusions occur. Oospores germinate 

either by producing a single germ sporangium, 

or by sending out vegetative hyphae. 

Most members of the Pythiaceae are homothallic, 

although heterothallism and relative 

sexuality have been reported, e.g. for 

Phytophthora infestans (Fig. 5.19) and Pythium 

sylvaticum. Heterothallic species are thought to 

be derived from homothallic ones (Kroon et al., 

2004). The situation of mating in heterothallic 

strains is rather complex and still only incompletely 

understood. A system of two mating types 

(A1 and A2) seems to be superimposed on a 

hormonal control mechanism of mating akin to


that described for Achlya (p. 86). When two strains 

of Pythium or Phytophthora were separated by a 

membrane preventing hyphal contact but 

permitting the exchange of diffusible metabolites, 

oospores were formed by either or both 

strains (Ko, 1980; Gall & Elliott, 1985). Because 

the mycelia were separated by a membrane, 

oospores formed by selfing, whereas in direct 

contact they may form by hybridization 

(Shattock et al., 1986a,b). Oospore formation can 

also be induced by non-specific stimuli, such as 

volatile metabolites of the unrelated fungus 

Trichoderma stimulating reproduction in A2 but 

not A1 strains of Phytophthora palmivora (Brasier, 

1975a). This ‘Trichoderma effect’ may well have 

ecological implications, since Trichoderma spp. 

are very common, especially in soil. Oospore 

formation may be a defence reaction against 

antibiotics commonly produced by Trichoderma, 

and the ‘Trichoderma effect’ may actually enhance 

the survival of Phytophthora spp. in soil, since it 

stimulates production of the long-lived oospore 

stage even in the absence of a compatible mating 

type (Brasier, 1975b). It is not known why 

Trichoderma spp. do not stimulate oosporogenesis 

in A1 strains. 

Like Achlya, the Pythiaceae display relative 

sexuality, i.e. a strain can act as male in one 

pairing but as female in another. To complicate 

matters further, a given strain of Phytophthora 

parasitica can switch its mating type from 

predominantly male to predominantly female 

or vice versa, e.g. upon fungicide treatment 

(Ko et al., 1986). Clearly, despite substantial 

research efforts over many years the genetic 

basis of sexual reproduction in the Pythiaceae 

still poses numerous unresolved questions! 

By analogy with the hormones oogoniol and 

antheridiol of Achlya, a male strain needs to be 

induced to produce the oogonium-inducing 

hormone whereas female strains constitutively 

produce the antheridium-inducing hormone 

(Elliott, 1994). The ability of homothallic species 

to stimulate sexual reproduction in heterothallic 

species (Ko, 1980) indicates that these hormones 

may also fulfil a morphogenetic role in homothallic 

sexual reproduction. However, nothing 

seems to be known as yet about the chemical 

nature of these hormones. 

Sterols are neither synthesized nor strictly 

required by vegetatively growing Pythium or 

Phytophthora spp. (Nes et al., 1979). None the less, 

they are required for the formation of sexual 

reproductive organs (Elliott, 1994). It seems, 

therefore, that sterols especially sitosterol 

and stigmasterol which are normally taken up 

from the host plant are converted into as 

yet unidentified steroid hormones which initiate 

sexual morphogenetic events downstream of 

the action of the diffusible Achlya-like hormones 

(Elliott, 1994). An alternative hypothesis is that 

sterols interact with an as yet unknown membrane 

protein to transmit the hormonal signal 

and trigger the signalling cascade leading to 

sexual morphogenesis (Nes & Stafford, 1984). 

In Lagenidium giganteum, a member of the 

Pythiaceae parasitizing mosquito larvae (Cuda 

et al., 1997), this cascade seems to be carried by 

Ca 2þ and calmodulin (Kerwin & Washino, 1986). 

5.3.2 Pythium 

Species of Pythium grow in water and soil as 

saprotrophs, but under suitable conditions, e.g. 

where seedlings are grown crowded together in 

poorly drained soil, they can become parasitic, 

causing diseases such as pre-emergence killing, 

damping off and foot rot. Damping off of cress 

(Lepidium sativum) can be demonstrated by sowing 

seeds densely on heavy garden soil or garden 

compost which is kept liberally watered. Within 

5 7 days some of the seedlings may show brown 

zones at the base of the hypocotyl, and the 

hypocotyl and cotyledons become water-soaked 

and flaccid. In this condition the seedling 

collapses. A collapsed seedling coming into 

contact with other seedlings will spread the 

disease (Plate 2b). The host cells separate from 

each other easily due to the breakdown of the 

middle lamella, probably brought about by 

pectic and possibly cellulolytic enzymes secreted 

by the fungus. The enzymes diffuse from their 

points of secretion at the hyphal tips, so that 

softening of the host tissue actually occurs ahead 

of the growing mycelium. Pure culture studies 

suggest that species of Pythium may also secrete 

heat-stable substances which are toxic to plants. 

Within the host the mycelium is coarse and

PYTHIALES 

97 

Fig 5.15 Pythium mycelium in the rotting tissue of a cress 

seedling hypocotyl. Note the spherical sporangium initial and 

the absence of haustoria. 

coenocytic, with typically granular cytoplasmic 

contents (Fig. 5.15). At first there are no septa, 

but later cross walls may cut off empty portions 

of hyphae. Thick-walled chlamydospores may 

also be formed. There are no haustoria. 

Several species are known to cause damping 

off, e.g. P. debaryanum and, perhaps more 

frequently, P. ultimum. Pythium aphanidermatum 

is associated with stem rot and damping off of 

cucumber, and the fungus may also cause rotting 

of mature cucumbers. Pythium mamillatum 

causes damping off of mustard and beet seedlings 

and is also associated with root rot in Viola. 

Many Pythium spp. have a very wide host range; 

e.g. P. ultimum parasitizes over 150 plant species 

belonging to many different families (Middleton, 

1943; Hendrix & Campbell, 1973). Far from 

parasitizing only plant roots, several soil-borne 

species, e.g. P. oligandrum, P. acanthicum and 

P. nunn, are capable of attacking hyphae of 

filamentous fungi, including plant-pathogenic 

species and even other Pythium spp. (Foley & 

Deacon, 1986b; Deacon et al., 1990). Attack may 

be mediated by the secretion of wall-degrading 

b-1,3-glucanase, chitinase and cellulase, or by 

inducing the host to undergo autolysis (Elad 

et al., 1985; Laing & Deacon, 1991; Fang & Tsao, 

1995). In contrast to plant-pathogenic Pythium 

spp., the mycoparasitic species require thiamine 

for growth and are unable to utilize inorganic 

nitrogen sources. These deficiencies may 

explain their mycoparasitic habit (Foley & 

Deacon, 1986a). Other species of Pythium parasitize 

freshwater and marine algae (Kerwin et al., 

1992). 

The taxonomy of Pythium is somewhat 

confused at present due to the existence of 

numerous synonyms. Including a few varieties, 

Dick (2001a) listed 129 names in current use. 

Since the morphological characteristics traditionally 

used for diagnosis can be variable, the 

delimitation of species and their assignment to 

the genus Pythium will have to await the results 

of detailed molecular phylogenetic analyses 

which are in progress (Matsumoto et al., 1999; 

Lévesque & de Cock, 2004). Keys and descriptions 

have been published by Waterhouse (1967, 

1968), van der Plaats-Niterink (1981) and Dick 

(1990b). 

Asexual reproduction 

The mycelium within the host tissue or in 

culture usually produces sporangia, but their 

form varies. In some species, e.g. P. gracile,


Fig 5.16 Sporangia and zoospores of Pythium.(a)Pythium debaryanum. Spherical sporangium with short tube and a vesicle 

containing zoospores. (b k) Pythiumaphanidermatum. (b) Lobed sporangium showing a long tube and the vesicle, which is beginning 

to expand. (c g) Further stages in the enlargement of the vesicle, and differentiation of zoospores.Note the transfer of protoplasm 

from the sporangium to the vesicle in (c).The stages illustrated in (b g) took place in 25 min. (h) Enlarged vesicle showing the 

zoospores. Flagella are also visible. (i) Zoospores. (j) Encystment of zoospore showing a shed flagellum. (k) Germination of 

azoosporecyst.(b g) to same scale; (a) and (h k) to same scale. 

the sporangia are filamentous and are scarcely 

distinguishable from vegetative hyphae. 

In P. aphanidermatum, the sporangia are formed 

from inflated lobed hyphae (Fig. 5.16b). In many 

species, however, e.g. P. debaryanum, the sporangia 

are globose (Fig. 5.16a). A terminal or 

intercalary portion of a hypha enlarges and 

assumes a spherical shape, then becomes cut 

off from the mycelium by a cross wall. The 

sporangia contain numerous nuclei. Cleavage of 

the cytoplasm to form zoospores begins in the 

sporangium, but is completed within a thinwalled 

vesicle which is extruded from the 

sporangium. This is a homohylic vesicle because 

its glucan wall is continuous with one layer of 

the sporangial wall (Dick, 2001a). Within the 

sporangium, cleavage vesicles begin to coalesce 

to separate the cytoplasm into uninucleate 

portions; membrane-bound packets of TTHs 

are already present within the cytoplasm of the 

sporangium. In P. middletonii (Fig. 5.17), the 

fascinating process of differentiation from amorphous 

cytoplasm to motile zoospores takes about 

30 45 min (Webster, 2006a) and is readily 

demonstrated in the laboratory (Weber et al., 

1999). The sporangium is extended into an apical 

papilla capped by a mass of fibrillar material 

which is lamellate in ultrastructure (Lunney & 

Bland, 1976). Shortly before sporangial discharge, 

there is an accumulation of cleavage vesicles 

behind the apical cap and at the periphery of 

the cytoplasm close to the sporangium wall. The 

cleavage vesicles around the sporangial cytoplasm 

discharge their contents to form a loose, 

fibrous interface between the cytoplasm and the 

sporangial wall. 

Discharge of the sporangium occurs by the 

formation of a thin-walled vesicle at the tip of 

the papilla from the fibrillar material of the 

apical cap, and the partially differentiated 

zoospore mass is extruded into it. The movement 

of the cytoplasm from the sporangium into the

PYTHIALES 

99 

Fig 5.17 Pythium middletonii. Stages in zoospore discharge. (a) Sporangium shortly before discharge. Note the thickened tip of 

the papilla which consists of a cap of cell wall material. (b) Inflation of the vesicle begins. (c,d) Protoplasm is retreating from the 

sporangium.Note the shrinkage in sporangium diameter as compared with (a). (e) Zoospores have differentiated within the vesicle, 

with flagella visible between the vesicle wall and the zoospores. (f) Zoospores escape following the rupture of the vesicle wall. 

The whole process of discharge takes about 20 min. 

vesicle is probably the result of several forces 

including the elastic contraction of the sporangium 

wall and possibly surface energy (Webster 

& Dennis, 1967). Lunney and Bland (1976) have 

also suggested that the fibrillar material 

extruded from the cleavage vesicles at the 

zoosporangium periphery may imbibe water, 

resulting in a build up of turgor pressure. The 

vesicle enlarges as cytoplasm from the sporangium 

is transferred to it, and during the next few 

minutes the cytoplasm cleaves into 8 20 uninucleate 

zoospores which jostle about inside the 

sporangium, causing the thin vesicle wall to 

bulge irregularly (Fig. 5.17). Finally, about 20 min 

after the inflation of the vesicle, its wall breaks 

down and the zoospores swim away. Internal 

sporangial proliferation, i.e. the formation of a 

new sporangium inside an old discharged one, 

occurs in certain species, e.g. P. middletonii and 

P. undulatum.


In some forms, e.g. P. ultimum var. ultimum, 

sporangia do not release zoospores but germinate 

directly by producing a germ tube. 

Sporangia of P. ultimum var. ultimum may survive 

in soil, whether moist or air-dry, for several 

months, and are stimulated to germinate within 

a few hours by sugar-containing exudates from 

seed coats. The germ tubes grow very rapidly so 

that a host in the vicinity may be penetrated 

within 24 h (Stanghellini & Hancock, 1971). The 

oospore of P. ultimum var. ultimum can germinate 

either by means of a germ tube or by forming 

a zoosporangium which releases zoospores 

(Figs. 5.18d,e). 

The zoospore 

Zoospores of Pythium spp. are always of the 

principal type. They can swim for several hours 

in a readily recognizable manner of helical 

forward movement. Donaldson and Deacon 

(1993) have provided evidence that the zoospore 

swimming pattern is regulated by Ca 2þ and 

calmodulin; manipulations of Ca 2þ concentrations 

cause aberrations such as circular, straight, 

spirally skidding or irregular movement. Zoospores 

of Pythium are attracted towards host 

surfaces, usually roots. The Ca 2þ /calmodulin 

system may be the means by which the sensing 

of attractants is translated into directed movement. 

It is this directed movement (taxis), i.e. the 

ability to aim precisely at a suitable encystment 

site, rather than the ability to move per se, 

which represents the main benefit of zoospores 

to their producer (Deacon & Donaldson, 1993). 

Chemotaxis to root exudates is often nonhost-specific, 

being mediated by amino acids 

and other common metabolites ( Jones et al., 

1991). Other tactic movements also occur, such 

as phototaxis, electrotaxis or negative geotaxis 

(Dick, 2001a). In general, zoospores of Pythium 

spp. accumulate around the root cap, root 

elongation zone or sites of injury. 

Once the zoospore has alighted on a suitable 

surface, it encysts by shedding rather than 

withdrawing its flagella, and secreting a wall 

from pre-formed material. Much valuable ultrastructural 

work has been carried out on the 

encystment process of Phytophthora and is 

discussed on pp. 102 111. The cyst of Pythium 

spp. can germinate almost immediately, usually 

by emitting a germ tube which can directly 

penetrate the relatively soft root tissue. In P. 

marinum, which is parasitic on marine red algae, 

the germ tube forms a specialized infection 

structure termed an appressorium (Kerwin 

et al., 1992); this is also commonly formed by 

leaf-infecting Phytophthora spp. The entire process 

from zoospore encystment to successful penetration 

is called homing sequence and may take 

place in as little as 30 min (Deacon & Donaldson, 

1993). If a zoospore encysts on a non-host surface, 

the cyst may germinate by producing a further 

principal zoospore. 


Most species of Pythium are homothallic, i.e. 

oogonia and antheridia are readily formed in 

cultures derived from single zoospores. However, 

Fig 5.18 Oogonia and oospores of 

Pythium.(a)Pythium debaryanum. 

Note that there are several antheridia. 

(b) Pythium mamillatum.Oogonium 

showing spiny outgrowths of oogonial 

wall. (c) Pythium ultimum. 

(d, e) Germination of oospores of 

P. ultimum (after Drechsler,1960).

PYTHIALES 

101 

Fig 5.19 Life cycle of Phytophthora infestans.This fungus is heterothallic, and the asexual part of the life cycle (left of diagram) is 

shown only for one mating type (A1). Nuclei in vegetative states are diploid.When two compatible mycelia meet, multinucleate 

oogonia and antheridia are differentiated, and one meiotic event in each results in the transfer of one haploid nucleus from the 

gametangium to the oogonium. Karyogamy is delayed until shortly before oospore germination.Open and closed circles represent 

haploid nuclei of opposite mating type; diploid nuclei are larger and half-filled. Key events in the life cycle are meiosis (M), 

plasmogamy (P) and karyogamy (K). 

some heterothallic species are known, e.g. 

P. sylvaticum, P. heterothallicum and P. splendens. 

In these cases, mating is a complicated affair 

under hormonal control, and with relative 

sexuality (see p. 95). 

Oogonia arise as terminal or intercalary 

spherical swellings which become cut off from 

the adjacent mycelium by cross-wall formation. 

In some species, e.g. P. mamillatum, the oogonial 

wall is folded into long projections (Fig. 5.18b). 

The antheridia arise as club-shaped swollen 

hyphal tips, often as branches of the oogonial 

stalk (monoclinous) or sometimes from separate 

hyphae (diclinous). In some species, e.g. 

P. ultimum, there is typically only a single antheridium 

to each oogonium, whilst in others, e.g. 

P. debaryanum, there may be several (Fig. 5.18a). 

The young oogonium is multinucleate and 

the cytoplasm within it differentiates into a 

multinucleate central mass, the ooplasm from 

which the oosphere develops, and a peripheral 

mass, the periplasm, also containing several 

nuclei. The periplasm does not contribute to 

the formation of the oosphere. 

As soon as the gametangia have become 

delimited by the basal septum, mitotic divisions 

cease. Nuclei may be aborted at this stage, and 

in oogonia of P. debaryanum 1 8 nuclei undergo 

meiosis (Sansome, 1963). Meiotic divisions are 

synchronous in the antheridium and the oogonium, 

although no protoplasmic continuities 

exist at this stage (Dick, 1995). In the antheridium 

of P. debaryanum and P. ultimum, all nuclei 

but one degenerate prior to meiosis, so that four


haploid nuclei are present in each antheridium 

just prior to plasmogamy (Sansome, 1963; Win- 

Tin & Dick, 1975). The antheridium then attaches 

itself to the oogonial wall and penetrates it by 

means of a fertilization tube. Following penetration, 

only three nuclei were counted in the 

antheridium, suggesting that one had entered 

the oogonium. Later still, empty antheridia were 

found, and it is presumed that the three 

remaining nuclei enter the oogonium and join 

the oogonial nuclei degenerating in the periplasm. 

Fusion between a single antheridial and 

oosphere nucleus has been described. The fertilized 

oosphere secretes a double wall, and the 

ooplast appears in the protoplasm. Material 

derived from the periplasm may also be deposited 

on the outside of the developing oospore. 

Such oospores may need a period of rest (afterripening) 

of several weeks before they are 

capable of germinating. Germination may be 

by means of a germ tube, or by the formation of 

a vesicle in which zoospores are differentiated 

(Figs. 5.18d,e), or in some forms the germinating 

oospore produces a short germ tube terminating 

in a sporangium. 

Ecological considerations 

Pythium spp. can live saprotrophically and may 

survive in air-dry soil for several years. They 

are more common in cultivated than in natural 

soils (Foley & Deacon, 1985), and appear to be 

intolerant of highly acidic soils. As saprotrophs, 

species of Pythium are important primary colonizers, 

probably gaining initial advantage by 

virtue of their rapid growth rate. They do not, 

however, compete well with other fungi which 

have already colonized a substrate, and they 

appear to be rather intolerant of antibiotics. 

The control of diseases caused by Pythium is 

obviously rendered difficult by its ability to 

survive saprotrophically and as oospores in soil. 

Its wide host range means that it is not possible 

to control diseases by means of crop rotation. 

The effects of disease can be reduced by improving 

drainage and avoiding overcrowding of 

seedlings. Pythium infections are particularly 

severe in greenhouses and nurseries, where 

some measure of control can be achieved by 

partial steam sterilization of soil. Recolonization 

of the treated soil by Pythium is slow. The use of 

certain types of compost instead of peat in 

nurseries can provide good control (Craft & 

Nelson, 1996; Zhang et al., 1996). The fungicide 

metalaxyl (see Fig. 5.27) also gives good control 

of seedling blight. 

Pythium insidiosum 

This species is associated with algae in stagnant 

freshwater in tropical and subtropical regions. 

When horses or cattle come into contact with 

P. insidiosum-contaminated water, zoospores are 

attracted to wounds and can infect them, 

causing severe open lesions of skin and subcutaneous 

tissues known as pythiosis insidiosi (Meireles 

et al., 1993; Mendoza et al., 1993). If contaminated 

water is consumed, gastrointestinal or systemic 

infections may also arise. In addition to grazing 

animals, infections in dogs and humans have 

been reported. Pythium insidiosum is keratinophilic 

and survives well at 37°C. Infections can be 

treated successfully by immunotherapy in which 

horses are injected with killed fungal material, 

the immune response leading to healing of 

infections (Mendoza et al., 1992). Pythium insidiosum 

used to be known under different names, 

but its taxonomy has been clarified by de Cock 

et al. (1987). 

5.3.3 Phytophthora 

The name Phytophthora (Gr.: ‘plant destroyer’) is 

apt, most species being highly destructive plant 

pathogens. The best known is P. infestans, cause of 

late blight of potatoes (Plate 2e). This fungus is 

confined to solanaceous hosts (especially tomato 

and potato), but others have a much wider host 

range. For example, P. cactorum has been recorded 

from over 200 species belonging to 60 families of 

flowering plants, causing a variety of diseases 

such as damping off or rots of roots, fruits 

and shoots (Erwin & Ribeiro, 1996). Phytophthora 

cinnamomi has the widest host range of 

all species, being capable of infecting over 1000 

plants and causing serious diseases especially on 

woody hosts, including conifers and Eucalyptus 

(Zentmyer, 1980). Several other Phytophthora spp. 

and related Pythium spp. can also cause diebacks 

and sudden-death symptoms of trees, with

PYTHIALES 

103 

roots severely rotted by the time above-ground 

symptoms become apparent (Plate 2c,d). Other 

important pathogens are P. erythroseptica associated 

with pink rot of potato tubers (Plate 2f), 

P. fragariae causing red core of strawberries, 

and P. palmivora causing pod rot and canker of 

cocoa. The genus is cosmopolitan, although there 

are differences in the geographic distribution 

of individual species; for instance, P. cactorum, 

P. nicotianae, P. cinnamomi and P. drechsleri occur 

worldwide whereas P. fragariae and P. erythroseptica 

are found predominantly in Northern 

Europe and North America (Erwin & Ribeiro, 

1996). Many Phytophthora spp. are spreading 

actively at present, e.g. P. infestans which has 

been spread worldwide by human activity (Fry & 

Goodwin, 1997) or P. ramorum, a serious pathogen 

of oak trees and other woody plants (Henricot & 

Prior, 2004). To make matters worse, different 

Phytophthora species may hybridize in nature, 

producing strains with new host spectra. An 

example is the recent outbreak of wilt of Alnus 

glutinosa in Europe caused by P. alni, a tetraploid 

hybrid of species resembling P. cambivora and 

P. fragariae (Brasier et al., 2004). 

In accordance with the great importance of 

the genus Phytophthora in mycology and plant 

pathology, a vast amount of literature has been 

published, and some of it has been summarized 

by Erwin & Ribeiro (1996) and Dick (2001a). 

Several books on the genus have appeared, 

including those edited by Erwin et al. (1983), 

Ingram and Williams (1991) and Lucas et al. 

(1991), and the masterly compendium by Erwin 

and Ribeiro (1996). Keys to the genus have been 

produced by Waterhouse (1963, 1970) and 

Stamps et al. (1990). Including formae speciales, 

Dick (2001a) listed 84 names in current use. 

Phytophthora is closely related to Pythium and 

there are transitional species which may need to 

be re-assigned as more DNA sequences and other 

data become available (Panabières et al., 1997). 

In general, the two genera can be distinguished 

morphologically in that the sporangia of 

Phytophthora spp. are typically pear- or lemonshaped 

with an apical papilla (Fig. 5.20b), and 

ecologically by the predominantly saprotrophic 

existence of Pythium and the predominantly 

parasitic mode-of-life of Phytophthora. Probably 

all Phytophthora spp. are pathogenic on plants in 

some form, and they differ merely in the extent 

to which they have a free-living saprotrophic 

phase. All may survive in the soil at least in 

the form of oospores, or in infected host tissue. 

However, in contrast to the downy mildews 

(Peronosporales; Section 5.4), almost all pathogenic 

forms can be isolated from their hosts and 

can be grown in pure culture. Selective media, 

often incorporating antibiotics or fungicides 

such as pimaricin or benomyl, have been devised 

for the isolation of Phytophthora (Tsao, 1983; 

Erwin & Ribeiro, 1996). 

Vegetative growth 

Most species form an aseptate mycelium producing 

branches at right angles, often constricted 

at their point of origin. Septa may be present in 

older cultures. Within the host, the mycelium is 

intercellular, but haustoria may be formed. 

These are specialized hyphal branches which 

penetrate the wall of the host cell and invaginate 

its plasmalemma, thereby establishing a point of 

contact between pathogen and host membranes. 

Haustoria are typical of biotrophic pathogens 

such as the Peronosporales (see Fig. 5.29) but may 

also be formed during initial biotrophic phases 

of infections which subsequently turn necrotrophic. 

In P. infestans within potato tubers, the 

haustoria appear as finger-like protuberances 

(Fig. 5.20c). Electron micrographs of infected 

potato leaves show that the haustoria are not 

surrounded by host cell wall material, but by an 

encapsulation called the extrahaustorial matrix 

which is probably of fungal origin. This is 

delimited on the outside by the host plasma 

membrane, and on the inside by the wall and 

then the plasma membrane of the pathogen (Fig. 

5.21; Coffey & Wilson, 1983; Coffey & Gees, 1991). 

Haustoria of Phytophthora do not normally 

contain nuclei, although one may be situated 

near the branching point within the intercellular 

hypha (Fig. 5.21a). 


The sporangia of Phytophthora spp. are usually 

pear-shaped or lemon-shaped (Fig. 5.22a) and 

arise on simple or branched sporangiophores 

which are more clearly differentiated than


Fig 5.20 Phytophthorainfestans. 

(a) Sporangiophores penetrating a stoma of a 

potato leaf. (b) Zoospores and zoospore cysts, one 

formed inside a zoosporangium. (c) Intercellular 

mycelium from a potato tuber showing the 

finger-like haustoria penetrating the cell walls. 

Note the thickening of the cell walls around the 

haustorium. 

those of Pythium. On the host plant, the sporangiophores 

may emerge through the stomata, 

as in P. infestans (Fig. 5.20a). The first sporangium 

is terminal, but the hypha bearing it may push 

it to one side and form further sporangia by 

sympodial growth. Mature sporangia of most 

species have a terminal papilla which appears as 

a plug because it consists of material different 

from the sporangial wall (Coffey & Gees, 1991). 

In species of Phytophthora infecting aerial 

plant organs, the sporangia are detached, possibly 

aided by hygroscopic twisting of the sporangiophore 

on drying, and are dispersed by wind 

before germinating. In aquatic or soil-borne 

forms, zoospore release commonly occurs 

whilst the sporangia are still attached; internal 

proliferation of attached sporangia may occur. 

Whether deciduous or not, sporangia may 

germinate either directly by means of a germ 

tube, or by releasing zoospores. The latter seems 

to be the original route because undifferentiated 

sporangia contain pre-formed flagella within 

their cytoplasm, and these are degraded under 

unfavourable conditions leading to direct germination 

(Hemmes, 1983; Erwin & Ribeiro, 1996). 

The mode of germination is dependent on 

environmental parameters. For example, in 

P. infestans, uninucleate zoospores are produced 

below 15°C whilst above 20°C multinucleate 

germ tubes arise. Further, with increasing age 

sporangia lose their capacity to produce zoospores 

and tend to germinate directly. In 

P. cactorum, sporangia have been preserved for 

several months under moderately dry conditions.

PYTHIALES 

105 

Fig 5.21 TEM images of haustoria of P. infestans. (a) Mature haustorium within a leaf cell of potato. (b) The basal region of a 

haustorium.The haustorium contains fungal vacuoles (FV) and mitochondria (M) but no nuclei. However, a nucleus (NF) is located 

within the intercellular hypha close to the branch point.The plant tonoplast (T), plant extrahaustorial membrane (EM), 

extrahaustorial matrix (EX) and fungal wall (FW) are visible.The seemingly empty space surrounding the haustorium is the plant 

vacuole (V). Both images reprinted from Coffey and Wilson (1983) by copyright permission of the National Research Council of 

Canada.Original prints kindly provided by M.D.Coffey. 

When water becomes available again, such 

sporangia may germinate by the formation of 

a vegetative hypha, or a further sporangium. 

Thick-walled asexual spherical chlamydospores 

have also been described for many 

Phytophthora spp. and can survive in soil for 

several years (Ribeiro, 1983; Erwin & Ribeiro, 

1996). The morphological differences between 

sporangia, chlamydospores and oospores are 

illustrated in Fig. 5.22. 

Once formed, mature sporangia may remain 

undifferentiated for several hours or even days, 

but zoospore differentiation can be induced by 

suspending mature sporangia in chilled water or 

soil extract. Detailed methods to trigger zoospore 

release have been established for many species 

(Erwin & Ribeiro, 1996). Once cold-shock has 

been received, differentiation can be completed 

in less than 60 min and probably involves 

cAMP-mediated signalling cascades (Yoshikawa 

& Masago, 1977). The processes of differentiation 

of sporangial protoplasm into zoospores differ 

in certain details between Phytophthora and 

the Saprolegniales (see Hardham & Hyde, 1997). 

For instance, in Saprolegnia the central vacuole 

is prominent and its membrane as well as 

the plasma membrane contribute to the plasma 

membranes of the developing zoospores (p. 81). 

In contrast, in Phytophthora the central vacuole 

disappears from the young sporangium before 

cleavage of the cytoplasm begins, and the 

plasma membrane remains intact even after 

zoospores have become fully differentiated. The 

zoospore plasma membranes therefore mostly 

originate from Golgi-derived cleavage cisternae 

(Hyde et al., 1991). Detailed cytological studies


Fig 5.22 Reproductive structures in Phytophthora cactorum. (a) Sporangia. (b) Chlamydospore. (c) Oospore showing the 

paragynous mode of fertilization. (d) Oospore with amphigynous fertilization. (b d) to same scale. 

have revealed an important role of microtubules 

in organizing the distribution of nuclei 

during zoospore formation (Hyde & Hardham, 

1992, 1993). Cleavage of the cytoplasm of a 

zoospore begins close to that end of the nucleus 

which subsequently points towards the ventral 

groove. At this stage, three types of vesicle which 

become important during zoospore encystment 

also move into their positions: large peripheral 

vesicles, dorsal vesicles, and small ventral vesicles. 

When the pre-formed flagella have been 

inserted, the zoospores acquire their mobility 

(Hardham, 1995). Zoospores are either discharged 

directly through the plug after this has dissolved, 

or they are transferred into a very transient 

membranous vesicle which forms outside the 

opened plug upon discharge and bursts one or 

a few seconds later (Gisi, 1983). Since the plasma 

membrane of the sporangium has not become 

part of the zoospore membranes, the membranous 

vesicle is probably continuous with the 

plasma membrane. 

Encystment of zoospores 

Zoospores of Phytophthora swim for several hours, 

travelling distances of a few centimetres in water 

or wet soil, although they can be spread much 

further by passive movement within water 

currents (Newhook et al., 1981). They are 

attracted chemotactically to plant roots by 

non-specific root exudates such as amino acids, 

host-specific substances, or the electrical field 

generated by plant roots (Carlile, 1983; Deacon 

& Donaldson, 1993; Tyler, 2002). No equivalent 

studies seem to have been carried out for zoospores 

of Phytophthora infecting leaves. The 

process of zoospore encystment described below 

for Phytophthora seems to apply also to Pythium 

(Hardham, 1995). It is an act of regulated secretion, 

i.e. the release of pre-formed contents by 

synchronous fusion of vesicles with the plasma 

membrane. Regulated secretion is common in 

animal cells, e.g. in epithelial or neuronal 

systems, but in fungi it is probably confined to 

encysting zoospores. 

Zoospores of Phytophthora are kidney-shaped; 

both flagella arise from the kinetosome boss 

protruding from within the longitudinal groove 

at the ventral surface. The anterior end of the 

spore is indicated externally by the straminipilous 

flagellum and internally by the water 

expulsion vacuole; the nucleus is located in

PYTHIALES 

107 

Fig 5.23 Schematic drawings of a zoospore of Phytophthora (not to scale). (a) Longitudinal section. (b) Transverse section of the 

anterior region showing several types of vesicle, namely the water-expulsion vacuole (WEV), fingerprint vacuole (FPV), large 

peripheral vesicles (LPV), small ventral vesicles (SVV), small dorsal vesicles (SDV) and peripheral cisternae (PC). Mitochondria (Mit) 

with unusually lamellate cristae are also indicated. a modified from Dick (2001b); b based on the ultrastructural work of 

Hardham et al.(1991). 

the posterior half of the spore (Fig. 5.23a). 

The nucleus is associated with the microtubular 

roots of the flagella which force it into a 

somewhat conical shape, the pointed end pointing 

towards the kinetosome boss. Zoospores 

contain several vesicular compartments. Their 

positions are drawn schematically in Fig. 5.23, 

and electron micrographs are provided in 

Fig. 5.24. Fingerprint vacuoles, equivalent to the 

dense-body vesicles of Saprolegnia and Achlya, are 

defined by the lamellate structure of their 

contents, presumably deposits of b-1,3-glucan 

(mycolaminarin) and phosphate. Fingerprint 

vacuoles are located mainly in the interior of 

the zoospore and play no part in the encystment 

process but are thought to provide carbon and 

energy reserves during subsequent germination 

of the cyst (Gubler & Hardham, 1990). In zoospores 

of Phytophthora cinnamomi, there are 

several kinds of peripheral vesicle which have 

been distinguished morphologically (Fig. 5.23) 

and by labelling with specific antibodies. When 

zoospores approach a root, the groove of the 

ventral surface faces the root surface, initial 

contact presumably being made by the flagella. 

Attachment of the zoospore is achieved by means 

of a glue discharged by the synchronous fusion 

of the small ventral vesicles with the ventral 

plasma membrane (Hardham & Gubler, 1990). 

At the same time, the small dorsal vesicles 

also secrete their contents, leading to the 

deposition of the first cyst wall (Figs. 5.24c,d; 

Gubler & Hardham, 1988). The process of 

exocytosis is complete within 2 min of receiving 

the encystment trigger. In contrast, the large 

peripheral vesicles do not fuse with the plasma 

membrane but withdraw to the centre of the 

cyst. Their contents are proteinaceous and 

probably serve as reserves for the germination 

process. Peripheral cisternae, ultrastructurally 

distinct from the ER, line the inside of the 

zoospore plasma membrane and disappear 

during encystment (Hardham et al., 1991; 

Hardham, 1995).


Fig 5.24 Ultrastructure of Phytophthora cinnamomi zoospores as seen with theTEM. (a) Oblique section through a zoospore. 

Several kinds of vesicle are visible, as are mitochondria, the water-expulsion vacuole (arrow) and the conical nucleus with its 

prominent nucleolus. (b) Fingerprint vacuoles. (c,d) Immunogold labelling of wall material located within dorsal vesicles before 

(c) and in the cyst wall1min after (d) encystment of the zoospore. (a,b) reproduced from Hardham and Hyde (1997), with permission 

from Elsevier; (c,d) previously unpublished work. All images kindly provided by F.Gubler and A.R. Hardham. 

Zoospore encystment can be triggered by 

several stimuli, e.g. contact with host cell surface 

polysaccharides, change in medium composition, 

or presence of root exudates. Commitment 

to encystment occurs within 20 30 s of receiving 

the stimulus (Paktitis et al., 1986). Complex 

signalling cascades involving Ca 2þ and phospholipase 

D are involved (Zhang et al., 1992), and 

commitment to several future developmental 

processes is made before the onset of encystment, 

including the point of germ tube emergence 

(Hardham & Gubler, 1990). 

Zoospore cysts germinate quite rapidly after 

their formation, usually by means of a germ tube 

which infects the plant roots directly. In the case 

of hard surfaces such as leaves, the germ tube 

may form an appressorium which mediates 

infection (see pp. 378 381).

PYTHIALES 

109 

Fig 5.25 Oogonial 

development in 

Phytophthora. 

(a f) Stages of 


P. erythroseptica. 

(g i). Stages of 


P. cactorum. 


Oospore formation is dependent on sterols and 

mating hormones (p. 95) and may be homo- or 

heterothallic. Phylogenetic studies have indicated 

that the former is ancestral, heterothallism 

having arisen repeatedly within the genus 

Phytophthora (Kroon et al., 2004). Two distinct 

types of antheridial arrangement are found. 

In P. fragariae, P. megasperma and a number of 

other species, antheridia are attached laterally to 

the oogonium and are described as paragynous 

meaning ‘beside the female’ (Figs. 5.22c, 5.25g i). 

In other Phytophthora species such as P. infestans, P. 

cinnamomi and P. erythroseptica, the oogonium, 

during its development, penetrates and grows 

through the antheridium (Hemmes, 1983). The 

oogonial hypha emerges above the antheridium 

and inflates to form a spherical oogonium, with 

the antheridium persisting as a collar around its 

base (Figs. 5.25a f). This arrangement of the 

antheridium is termed amphigynous (‘around 

the female’). In some species (e.g. P. cactorum, 

P. clandestina, P. medicaginis), both types of arrangement 

may be found (Figs. 5.22c,d); one or the 

other may predominate, depending on strain 

and culture conditions (Erwin & Ribeiro, 1996). 

Both the oogonia and antheridia contain 

several diploid nuclei, but as the oosphere 

matures only a single nucleus remains at the 

centre while the remaining nuclei are included 

in the periplasm, i.e. the space between the 

oosphere and the oogonial walls (see Fig. 5.2). 

Meiosis occurs in the antheridium and oogonium 

(Shaw, 1983). Fertilization tubes have been 

observed and a single haploid nucleus is introduced 

from the antheridium into the oosphere 

(Fig. 5.26). Fusion between the oosphere nucleus 

and the antheridial nucleus is delayed. Even 

mature, dormant oospores may still be binucleate, 

karyogamy usually occurring after breakage 

of dormancy as a first step towards germination 

(Jiang et al., 1989). 

Following fertilization, the physiology 

and ultrastructure of the oospore change to


Fig 5.26 Phytophthora cactorum. 

Development of oogonium, antheridium 

and oospore. (a) Initials of oogonium 

and antheridium. (b) Oogonium and 

antheridium grown to full size: the 

oogonium has about 24 nuclei and the 

antheridium about 9. (c) Development 

of a septum at the base of each, and 

degeneration of some nuclei in each until 

the oogonium has 8 or 9 nuclei and the 

antheridium 4 or 5. (d) A simultaneous 

division of the surviving nuclei in 

oogonium and antheridium.The 

protoplast has large vacuoles. 

(e) Separation of oosphere from 

periplasm. Nuclei divide in the periplasm 

prior to degeneration.The oogonium 

presses into the antheridium. (f) Entry of 

one antheridial nucleus by a fertilization 

tube.The protoplasm and remaining 

nuclei of the antheridium degenerate. 

(g) Development of oospore wall. 

(h) The oospore enters its dormant 

period with exospore formed from dead 

periplasm, endospore deposited inside 

it, and paired nuclei in association but 

not yet fused. (a h) are composite 

drawings of eight stages in sequence 

(after Blackwell,1943). 

a resting state. Oospore differentiation proceeds 

from the outside inwards (centripetal development). 

The oospore has a thin outer wall 

(epispore) which is derived from the periplasm 

and appears to consist of pectic substances. The 

inner oospore wall (endospore) is rich in b-1,3- 

glucans which form a major storage reserve and 

are mobilized by glucanases just prior to germination 

(Erwin & Ribeiro, 1996). Within the 

developing oospore, the numerous small lipid 

droplets coalesce into a few large ones. Lipids are 

undoubtedly the major endogenous storage 

reserve in the spores of Oomycota (Dick, 1995) 

and many other fungi. Later, the dense body 

vesicles which are rich in mycolaminarin and 

phosphate fuse together, giving one large structure, 

the ooplast. Like the endospore, the ooplast 

is consumed during germination whereas some 

lipid droplets are saved and are translocated into 

the germ tube (Hemmes, 1983). Considering their 

thick walls and abundant storage reserves, it is 

not surprising that oospores are the longest-lived

PYTHIALES 

111 

propagule of Phytophthora, being capable of 

surviving in soil for many years. 

5.3.4 Phytophthora infestans,causeof 

potato late blight 

Late blight of potato caused by P. infestans is a 

notorious disease. In the period between 1845 

and 1848 it resulted in famine across much of 

Europe, and especially in Ireland where most 

people had come to depend on the potato as 

their major source of food. In Ireland alone, the 

population size dropped from over 8 million in 

1841 to 6.5 million in 1851 (Salaman, 1949). The 

history of the Great Famine has been ably 

documented by Large (1940), Woodham-Smith 

(1962) and Schumann (1991). The social and 

political repercussions of this tragedy have 

been immense and still reverberate today. 

An enormous amount of literature about 

P. infestans has been published over the past 

150 years, including several books (Ingram & 

Williams, 1991; Lucas et al., 1991; Dowley et al., 

1995). It has been estimated that about 10% of 

the entire phytopathological literature is concerned 

just with this one species. None the less, 

there are many uncomfortable gaps in our 

knowledge, and the fungus continues to provide 

unpleasant surprises to this day. 

Origin and spread 

The probable centre of evolution of most Solanum 

spp. and hence also their pathogens, notably 

P. infestans, lies in Mexico (Niederhauser, 1991), 

although the potato (S. tuberosum) was first 

cultivated in South America. There are several 

theories accounting for the spread of P. infestans 

round the world (Ristaino, 2002). In the early 

1840s P. infestans rapidly spread to North America, 

and it is generally assumed that it was introduced 

to Europe (Belgium) in June 1845 with a 

shipment of contaminated potatoes (Bourke, 

1991). Phytophthora infestans is heterothallic, and 

there is good evidence that in the first wave 

of migration in 1845 only the A1 mating type 

reached Europe (Goodwin et al., 1994a). Over the 

next century or more, the fungus probably 

survived entirely on an asexual life cycle, overwintering 

in tubers infected during the previous 

season and discarded together with shoots and 

other debris in the field. Despite the absence of 

sexual reproduction, P. infestans showed a considerable 

genetic adaptability, as documented by 

its ability to break the resistance bred into new 

potato cultivars (p. 114), and also the rapid 

emergence of strains resistant against newly 

introduced fungicides (p. 112). 

A second wave of P. infestans migration 

brought the A2 mating type from central 

Mexico to North America and Europe where it 

was first isolated in 1981 (Hohl & Iselin, 1984). 

It is now established worldwide (Spielman et al., 

1991; Fry et al., 1993; Gillis, 1993; Goodwin et al., 

1994b). The enhanced genetic recombination 

brought about by sexual reproduction is catalysing 

a change in the genetic make up of 

P. infestans, which may be leading to an explosive 

evolution of new P. infestans strains (Fry et al., 

1993; Goodwin et al., 1995). This situation is seen 

as the biggest threat posed by P. infestans since 

the 1840s (Fry & Goodwin, 1997). 

Epidemiology 

There is clear genetic evidence of sexual reproduction 

taking place in the field, and it is also 

possible that oospores contribute to the survival 

of P. infestans in soil during the winter (Andrivon, 

1995). Additionally, the fungus has a good 

capacity to survive the winter without oospores. 

A very low proportion of infected tubers left on 

the field gives rise to infected ‘volunteer’ plants 

in the following spring. In experimental plots, 

the proportion of infected plants developing 

from naturally or artificially infected tubers 

was found to be less than 1% (Hirst & Stedman, 

1960). Nevertheless, such infected shoots form 

foci within the crop from which the disease 

spreads. The sporangia of P. infestans are deciduous, 

and they are blown from diseased shoots 

to healthy leaves where they germinate either 

by the formation of germ tubes or zoospores. 

Zoospore production is favoured by lower 

temperatures (9 15°C). After swimming for a 

time, the zoospores encyst and then form germ 

tubes which usually penetrate the epidermal 

walls of the potato leaf, or occasionally enter the 

stomata. An appressorium is formed at the tip 

of the germ tube, attaching the zoospore cyst


firmly to the leaf. Penetration of the cell wall is 

probably achieved by a combination of mechanical 

and enzymatic action and can occur within 

2 h. Within the leaf tissue, an intercellular 

mycelium develops and haustoria are formed 

where hyphae contact host cell walls (Fig. 5.21). 

The resulting lesion acquires a dark green watersoaked 

appearance associated with tissue disintegration 

(Plate 2e). Such lesions are visible 

within 3 5 days of infection under suitable conditions 

of temperature and humidity. Around 

the margin of the advancing lesion on the lower 

surface of the leaf, a zone of sporulation is found 

in which sporangiophores emerge through the 

stomata (Fig. 5.20a). Sporulation is most prolific 

during periods of high humidity and commonly 

occurs at night following the deposition of dew. 

In potato crops, as the leaf canopy closes over 

between the rows to cover the soil, a humid 

microclimate is established which may result 

in extensive sporulation. As the foliage dries 

during the morning, the sporangiophore undergoes 

hygroscopic twisting which results in the 

flicking-off of sporangia. Thus the concentration 

of sporangia in the air usually shows a 

characteristic diurnal fluctuation, with a peak 

around 10 a.m. Although sporangia can survive 

drying if they are rehydrated slowly (Minogue & 

Fry, 1981), in practice the long-range spread of 

inoculum is probably by sporangia in contact 

with water drops (Warren & Colhoun, 1975). 

The destructive action of P. infestans is directly 

associated with the killing of photosynthetically 

active foliage. When about 75% of the leaf tissue 

has been destroyed, further increase in the 

weight of the crop ceases (Cox & Large, 1960). 

Thus, the earlier the onset of the epidemic, the 

more serious the consequences. To a certain 

extent, the crop reduction may be offset by the 

fact that epidemics are more common in rainy 

cool seasons which are conducive to higher crop 

yields. 

Phytophthora infestans can also cause severe 

post-harvest crop losses because tubers can be 

infected by sporangia falling onto them, either 

during growth or lifting. Such infected tubers 

may rot in storage, and the diseased tissue is 

susceptible to secondary bacterial and fungal 

infections. 

Chemical control 

By spraying with suitable fungicides, epidemic 

spread of the disease can be delayed. This results 

in a prolongation of photosynthetic activity of 

the potato foliage and hence an increase in yield. 

Fungicides developed against the Eumycota are 

often ineffective against Oomycota such as 

Phytophthora because the latter differ in fundamental 

biochemical principles, including many 

of the molecular targets of fungicides active 

against Eumycota (Bruin & Edgington, 1983; 

Griffith et al., 1992). In 1991, about 20% of the 

total amount of money spent on chemicals for 

controlling plant diseases worldwide was used 

for the control of Oomycota (Schwinn & Staub, 

1995). 

The first of all fungicides was Bordeaux 

mixture, an inorganic formulation containing 

copper sulphate and calcium oxide which was 

found to be effective against downy mildew 

of vines caused by Plasmopara viticola, another 

member of the Oomycota (see p. 119; Large, 1940; 

Erwin & Ribeiro, 1996). Oomycota in general are 

extremely sensitive to copper ions, and Bordeaux 

mixture is still widely used (Agrios, 2005). 

The dithiocarbamates such as zineb or 

maneb (Fig. 5.27a) were among the first organic 

fungicides to be developed. They act against 

a wide range of fungi, including Oomycota, 

because of their non-selective mode of action. 

The molecule is sufficiently apolar to diffuse 

across the fungal plasma membrane; once inside, 

it is metabolized, and the released isothiocyanate 

radical (Fig. 5.27b) reacts with the sulphydryl 

groups of amino acids (Agrios, 2005). 

The most important agrochemicals against 

Oomycota are the phenylamides such as metalaxyl 

(Fig. 5.27c) which are systemic fungicides, 

i.e. they can enter the plant and are translocated 

throughout it. Metalaxyl appears to inhibit the 

transcription of ribosomal RNA in Oomycota 

but not Eumycota (Davidse et al., 1983). This is 

an inhibition of a specific biochemical target, 

and the immense genetic variability of P. infestans 

enabled it to develop resistance against metalaxyl 

in the early 1980s shortly after this was 

released for agricultural use (Davidse et al., 

1991). Resistance is now widespread and has 

serious implications for future control of

PYTHIALES 

113 

Fig 5.27 Fungicides against P. infestans. (a) The dithiocarbamate maneb which is active against Oomycota and Eumycota. (b) The 

isothiocyanate radical released by metabolism of dithiocarbamates by fungal hyphae. (c) The phenylamide metalaxyl which is active 

only against Oomycota. (d) Aluminium ethyl phosphonate (fosetyl-Al). (e) Cyazofamid, a new fungicide specific against Oomycota. 

(f) Famoxadone, a new fungicide active against Oomycota and Eumycota. 

Phytophthora spp. (Erwin & Ribeiro, 1996). 

Phenylamides are now protected by being used 

in a cocktail, e.g. with the less-specific dithiocarbamates, 

and tailor-made application regimes 

are recommended for each year and each region 

(Staub, 1991). 

The phosphonates are a different type of 

fungicide against Phytophthora spp. Fosetyl Al 

(aluminium ethyl phosphonate; Fig. 5.27d) is 

readily taken up by plants in which it is broken 

down to release phosphorous acid (¼ phosphonate), 

which seems to be the active principle 

(Griffith et al., 1992). Fosetyl Al as well as phosphorous 

acid can move downwards through the 

phloem and upwards in the xylem, showing 

similar transport characteristics as sucrose 

(Ouimette & Coffey, 1990; Erwin & Ribeiro, 

1996). The mode of action of phosphonates is 

not known but is likely to be complex, with a 

stimulatory effect also on the host plant immune 

system (Molina et al., 1998). Although active 

only against potato tuber blight but not foliar 

blight caused by P. infestans (L. R. Cooke & Little, 

2002), phosphonates are effective against a wide 

range of root-infecting Phytophthora spp. and 

even show good curative properties (Erwin & 

Ribeiro, 1996). 

A useful introduction to current fungicides 

and their modes of action has been provided 

by Uesugi (1998). Because of the enormous 

economic significance of P. infestans and other 

Oomycota, new fungicide candidates are continually 

being developed and introduced into the 

market. Two recent examples are cyazofamid 

(Fig. 5.27e) and famoxadone (Fig. 5.27f). Both 

inhibit mitochondrial respiration. However, 

whilst the former is specific against Oomycota 

(Sternberg et al., 2001), famoxadone inhibits 

both Oomycota and Eumycota (Mitani et al., 

2002). Its molecular target is different from 

that of cyazofamid but probably the same as 

that of the strobilurins (see Figs. 13.15e,f), 

as indicated by the development of crossresistance 

in fungal pathogens against famoxadone 

and strobilurins. 

Disease forecast 

To avoid unnecessary spraying and to ensure 

that timely spray applications are made, it has 

proven possible to provide forecasts of the 

incidence of potato blight epidemics for certain 

countries. Beaumont (1947) analysed the incidence 

of blight epidemics in south Devon 

(England) and established that a ‘temperature 

humidity rule’ controls the relationship between 

blight epidemics and weather. After a certain 

date (which varies with the locality) and assuming 

that inoculum on volunteer plants is always


present, Beaumont (1947) predicted that blight 

would follow within 15 22 days of a period 

of at least 48 h during which the minimum temperature 

was not less than 10°C and the relative 

humidity was over 75%. The warm humid 

weather during this Beaumont period provides 

conditions suitable for sporulation and the 

initiation of new infections. Modified in the 

light of experience and adapted to regional 

climates, computerized forecasting systems are 

now used worldwide, limiting fungicide applications 

to situations in which they are necessary 

(Doster & Fry, 1991; Erwin & Ribeiro, 1996). After 

receipt of a blight warning, fungicide sprays are 

applied prophylactically by the farmer, irrespective 

of whether P. infestans is actually present in 

his field or not. 

Haulm destruction 

The danger of infection of tubers by sporangia 

falling onto them from foliage at lifting time can 

be minimized by ensuring that all the foliage is 

destroyed before lifting. This is achieved by 

spraying the foliage with herbicides 2 3 weeks 

before harvest time. The ridging of potato tubers 

also helps to protect the tubers from infection. 

Although sporangia may survive in the soil 

for several weeks, they do not penetrate deeply 

into it. 

Crop sanitation 

In principle, one infected volunteer plant per 

hectare is sufficent to initiate an epidemic. 

This is because late blight is a typical multicyclic 

disease, with numerous cycles of reproduction 

occurring in a single growing season under 

favourable conditions, leading to the rapid 

build up of inoculum. Crop sanitation, which is 

effective against single-cycle diseases, therefore 

has only limited value in the control of 

P. infestans (van der Plank, 1963). 

Breeding for major gene resistance 

A worldwide screening of Solanum spp. showed 

that a number of them have natural resistance to 

P. infestans. One species which has proven to be an 

important source of resistance is S. demissum 

which grows in Mexico, the presumed centre 

of origin of P. infestans. Although this species is 

valueless in itself for commercial cultivation, 

it is possible to cross it with S. tuberosum, and 

some of the progeny are resistant to the disease. 

Solanum demissum contains at least four major 

genes for resistance (R 1 , R 2 , R 3 and R 4 ), together 

with a number of minor genes which determine 

the degree of susceptibility in susceptible 

varieties (Black, 1952). The four genes may be 

absent from a particular host strain, or they may 

be present singly (e.g. R 1 ), in pairs, in threes, 

or all together, so that 16 host genotypes are 

possible representing different combinations of 

R genes. The identification of the R gene complex 

was dependent on the discovery that the fungus 

itself exists in a number of strains or physiological 

races. For each host R gene, the pathogen 

was assumed to carry a gene which enables it 

to overcome the effect of the R gene. This is 

the basis of the gene-for-gene hypothesis, and 

gene-for-gene interactions are common in 

many host pathogen interactions (Flor, 1971). 

Assuming a gene-for-gene situation for the 

interaction of P. infestans with S. tuberosum, 16 

races of P. infestans should theoretically be 

demonstrable. If the corresponding genes of 

the fungus are termed 1, 2, 3 and 4, then the 

different races can be labelled (0), (1), (2), etc., 

(1.1), (1.2), etc., (1.2.3), (1.2.4), etc., and (1.2.3.4). 

By 1953, 13 of the 16 races had been identified, 

the prevalent race being Race 4. By 1969, 11 R 

genes had been recognized in Britain 

(Malcolmson, 1969). Resistance based on a 

small number of defined genes of major effect 

has been termed major gene resistance or 

race-specific resistance. Because of the uncanny 

ability of P. infestans to break major gene resistance 

even before the arrival of the A2 mating 

type in Europe and North America, attempts at 

breeding fully resistant potato cultivars have 

now been abandoned (Wastie, 1991). 

The origin of physiological races is difficult to 

determine. The occurrence and spread of resistance 

genes before the arrival of the A2 mating 

type may have been due to mutation followed 

by selection imposed by the monoculture of 

a resistant host. Another possibility is that 

the mycelium of P. infestans is heterokaryotic, 

carrying nuclei of more than one race. Yet 

another scenario is vegetative hybridization

PERONOSPORALES 

115 

followed by parasexual recombination (see 

p. 230); by mixing sporangia of two different 

races, new races with a different pattern of 

virulence towards potato varieties have been 

obtained after several cycles of inoculation 

(Malcolmson, 1970). The parasexual cycle has 

been experimentally demonstrated for P. parasitica 

using fungicide resistance as a genetic 

marker (Gu & Ko, 1998). 

Within 1 2 days of infection, tissues of resistant 

hosts undergo necrosis so rapidly that 

sporulation and further growth of the fungus 

cannot occur. Such a reaction is sometimes 

termed hypersensitivity, and the function of 

the R genes is to accelerate this host reaction. 

When potato tubers are inoculated with an 

avirulent race of P. infestans, they respond by 

secreting antifungal substances called phytoalexins. 

Two of the phytoalexins formed by 

resistant tubers are rishitin and phytuberin. 

Rishitin, originally isolated from the potato 

variety Rishiri, is a bicyclic sesquiterpene. 

Tomiyama et al. (1968) showed that R 1 tuber 

tissue inoculated with an avirulent race of 

P. infestans produced over 270 times the amount 

of rishitin than when inoculated with a virulent 

race. The R genes of the potato probably determine 

the ability of host tissue to recognize 

and respond to avirulent races of P. infestans 

(Day, 1974). The detailed molecular interactions 

which determine race specificity are, however, 

complex and still only incompletely understood 

at present (Friend, 1991). 

Breeding for field resistance 

In addition to the major genes for resistance 

in potato, numerous other genes also exist 

which, although individually of small effect, 

may contribute to resistance if present together. 

Resistance of this kind is known as general 

resistance or field resistance, and some potato 

breeding programmes aim at producing varieties 

possessing it (Niederhauser, 1991). This is 

preferable to single-gene resistance because 

P. infestans is less likely to overcome the combined 

resistance of numerous minor genes 

simultaneously. Field resistance retards the 

infection process, e.g. by production of a particularly 

thick cuticle or by a leaf architecture 

unfavourable to infection, lowers the number of 

sporangia produced, and extends the time 

needed by the pathogen to initiate new infections 

(Wastie, 1991). Field resistance is equally 

effective against all physiological races of 

P. infestans, and it reduces the severity of an 

epidemic and consequently the need to apply 

fungicides (Erwin & Ribeiro, 1996). 

Tomato late blight 

P. infestans also causes significant worldwide crop 

losses of tomato (Lycopersicon esculentum) which, 

like potato, belongs to the Solanaceae. The 

general principles of control of tomato late 

blight are similar to those described above for 

potato, including fungicides used and blight 

forecasting (Erwin & Ribeiro, 1996). Many strains 

of P. infestans are capable of infecting both 

tomato and potato. However, since the resistance 

gene systems are different in these two hosts, 

correlations between virulence of a given strain 

on potato and tomato cannot be drawn (Legard 

et al., 1995). 

5.4 Peronosporales 

The Peronosporales are obligately biotrophic 

pathogens of a few groups of higher plants 

and are responsible for diseases mainly of 

aerial plant organs known collectively as 

downy mildews. The order currently comprises 

two families, the Peronosporaceae (Peronospora, 

Plasmopara, Bremia) and Albuginaceae (Albugo). 

There are about 250 species (Kirk et al., 2001). 

DNA sequencing data (Cooke et al., 2000; 

Riethmüller et al., 2002) are confusing at present 

because species of Phytophthora (Pythiales) and 

Peronospora (Peronosporales) seem to intergrade 

in phylogenetic analyses. Peronospora seems 

more closely related to Phytophthora than to 

other members of the Peronosporales such as 

Albugo, which in turn may have affinity with 

Pythium. Considerable rearrangements between 

the Peronosporales and Pythiales will therefore 

have to be carried out at some point in the 

future. However, we prefer to retain the conventional 

system for the time being because the 

downy mildews (Peronosporales) represent a


convincing biological entity (Dick, 2001a). The 

key features distinguishing them from the 

Pythiales are as follows. 

First, they are obligate biotrophs and cannot 

be grown apart from their living host. The 

mycelium in the host tissues is coenocytic and 

intercellular, with haustoria of various types 

penetrating the cell walls. No member of the 

Peronosporales has as yet been grown in axenic 

culture, although some can be propagated in 

dual culture with callus tissues of their plant 

hosts. None the less, some species (e.g. Plasmopara 

viticola) can cause cell damage to their hosts 

which leads to the leakage of cytoplasm (Lafon & 

Bulit, 1981). This is similar to the rots caused, for 

example, by Phytophthora erythroseptica (Plate 2f) 

and suggests an incomplete adaptation to the 

biotrophic habit, tying in with the likely origin 

of Peronosporales from within the Pythiales 

(Dick, 2001a). 

Second, whereas Pythium and Phytophthora spp. 

are typically able to attack a very wide range of 

host plants, Dick (2001a) has pointed out that 

Peronosporales parasitize a narrow range of 

angiosperm families, usually dicotyledons, and 

especially herbaceous plants which are either 

highly evolved or accumulate large amounts of 

secondary metabolites such as essential oils or 

alkaloids. Any one species of downy mildew is 

specific to only one or a few related host genera. 

Dick (2001a, 2002) has speculated that a coevolution 

of the downy mildews with herbaceous 

angiosperms occurred mainly in the Tertiary 

period, and as several independent events, 

whereby Phytophthora and downy mildews share 

common ancestors. The Peronosporaceae are 

relatively recent; Peronospora, along with its 

host plants, may have arisen in the mid to late 

Tertiary in the vicinity of Armenia and Iran. 

Plasmopara is probably of South American origin 

and dates back to the early Tertiary, whereas 

Bremia lactucae is a central European species. 

In contrast, the Albuginaceae (Albugo) are more 

ancient, with a late Cretaceous origin possibly in 

South America (Dick, 2002). 

A third major feature of the Peronosporales 

is the tendency of their sporangia to germinate 

directly, rather than by releasing zoospores. 

Many species have lost the ability to produce 

zoospores altogether, their sporangia being functional 

‘conidia’ which are disseminated by wind. 

The sporangiophores are well-differentiated, 

showing determinate growth and branching 

patterns which provide characteristic features 

for identification. The production of directly 

germinating sporangia on well-defined sporangiophores 

represents an adaptation to the terrestrial 

lifestyle and supports the postulated origin 

of the Peronosporales in the drier Tertiary period 

(Dick, 2002). The life cycle of Peronosporales is 

similar to that of Phytophthora (see Fig. 5.19). 

Sporangia infect directly or produce infective 

zoospores, leading to a new crop of sporangiophores 

and sporangia, and this asexual cycle 

spreads the disease during the vegetation period. 

Sexual reproduction is by means of oospores 

which are formed within the host tissue and 

survive adverse conditions after host death. 

Peronosporales cause economically significant 

diseases, and one of them Plasmopara 

viticola has had a major impact on agriculture 

and plant pathology because it led to the discovery 

of Bordeaux mixture (see p. 119). Overviews 

of the Peronosporales have been given by Spencer 

(1981), Smith et al. (1988) and Dick (2002). 

5.4.1 Peronospora (Peronosporaceae) 

Peronospora destructor causes a serious disease of 

onions and shallots whilst P. farinosa causes 

downy mildew of sugar beet, beetroot and 

spinach, but can also be found on weeds such 

as Atriplex and Chenopodium. Peronospora tabacina 

causes blue mould of tobacco. This name refers 

to the bluish purple colour of the sporangia, 

which is actually a feature of many species 

of Peronospora. Crop losses associated with 

P. tabacina can be up to 95%. This species was 

introduced into Europe in 1958 and has spread 

rapidly since (Smith et al., 1988). 

Peronospora parasitica attacks members of the 

Brassicaceae. Although many specific names 

have been applied to forms of this fungus on 

different host genera, it is now customary to 

regard them all as belonging to a single species 

(Dickinson & Greenhalgh, 1977; Kluczewski & 

Lucas, 1983). Turnips, swede, cauliflower, 

Brussels sprouts and wallflowers (Cheiranthus)


117 

Fig 5.28 Peronospora parasitica on Capsella bursa-pastoris. 

(a) Sporangiophore. (b) Sporangium germinating by means 

of a germ tube. (c) L.S. of host stem showing intercellular 

mycelium and coarse lobed haustoria. 

are commonly attacked, and the fungus is found 

particularly frequently on shepherd’s purse 

(Capsella bursa-pastoris). Diseased plants stand 

out by their swollen and distorted stems bearing 

a white ‘fur’ of sporangiophores (Plate 2g). On 

leaves the fungus is associated with yellowish 

patches on the upper surface and the formation 

of white sporangiophores beneath. Sections of 

diseased tissue show a coenocytic intercellular 

mycelium and branched lobed haustoria in 

certain host cells (Fig. 5.28c; Fraymouth, 1956). 

Following penetration of the host cell by 

P. parasitica, reactions are set up between the 

host protoplasm and the invading fungus. The 

haustorium becomes ensheathed by a layer of 

callose which is visible as a thickened collar 

around the haustorial base in susceptible host 

plants, whereas the entire haustorium may be 

coated by thick callose deposits in interactions 

showing a resistance response (Donofrio & 

Delaney, 2001). The general appearance of haustoria 

of Peronospora is very similar to that of 

Phytophthora shown in Fig. 5.21; the main body of 

the haustorium is surrounded by host cytoplasm, 

the host plasma membrane, an extrahaustorial 

matrix, the fungus cell wall, and the fungal 

plasma membrane (Fig. 5.29). Although the 

haustoria undoubtedly play a major role in the 

nutrient uptake of the fungus from the host 

plant, it should be noted that intercellular 

hyphae are also capable of assimilating nutrients 

in planta (Clark & Spencer-Phillips, 1993; Spencer- 

Phillips, 1997). 

The sporangiophores emerge singly or in 

groups from stomata. There is a stout main axis 

which branches dichotomously to bear eggshaped 

sporangia at the tips of incurved 

branches (Fig. 5.28a). Detachment of sporangia 

is possibly caused by hygroscopic twisting of the 

sporangiophores related to changes in humidity.


Fig 5.29 Peronospora manshurica. Diagram of host pathogen interface in the haustorial region.Fungal cytoplasm (FC) is bounded 

by the fungal plasma membrane (FP), lomasomes (LO) and the fungal cell wall (FW) in both the intercellular hyphae (right) and the 

haustorium (centre).The relative positions of the host cell vacuole (V), host cytoplasm (HC) and host plasmalemma (HP) are 

indicated.The host cell wall (HW) terminates in a sheath (S).The zone of apposition (Z) separates the haustorium from the host 

plasmalemma. Invaginations of the host plasmalemma and vesicular host cytoplasm are considered evidence for host secretory 

activity (sec). After Peyton and Bowen (1963). 

In P. tabacina, however, it has been suggested that 

changes in turgor pressure of the sporangiophores 

occur which parallel changes in the water 

content of the tobacco leaf. Sporangia may be 

discharged actively by application of energy at 

their point of attachment to the sporangiophore. 

In the Sclerosporaceae (see Section 5.5), violent 

sporangial discharge also occurs. Upon alighting 

on a suitable host, sporangia of P. parasitica 

germinate by the formation of a germ tube 

rather than zoospores. The germ tube penetrates 

the wall of the epidermis by means of an 

appressorium (Fig. 5.28b). 

Oospores of P. parasitica, like those of most 

other Peronosporales, are embedded in senescent 

leaf tissues and are found throughout the season. 

There is evidence that some strains of the fungus 

are heterothallic whilst others are homothallic 

(McMeekin, 1960). Both the antheridium and 

oogonium are at first multinucleate. Nuclear 

division precedes fertilization, and meiosis 

occurs in the oogonium and antheridium 

(Sansome & Sansome, 1974). Fusion between 

two nuclei is delayed at least until the oospore 

wall is partly formed. 

The wall of the oospore of P. parasitica is very 

tough, and it is difficult to induce germination. In 

P. destructor and some other species, germination 

occurs by means of a germ tube but in P. tabacina 

zoospores have been described. It is probable 

that oospores overwinter in soil and give rise 

to infection in subsequent seasons. Although 

oospores of P. destructor have been germinated 

after 25 years, it has not proven possible to infect 

onions from such material. Possibly in this case 

the disease is carried over by means of systemic 

infection of volunteer onion bulbs (Smith et al., 

1988). 

Peronospora parasitica and 

Arabidopsis thaliana 

The chance discovery of a P. parasitica infection in 

an Arabidopsis thaliana weed population in a 

Zurich garden showing haustoria, sporangia 

and oospores (Koch & Slusarenko, 1990) opened 

up the possibility of using this genetically 

well-characterized ‘model plant’ to investigate 

plant pathogen interactions involving downy 

mildews. The interaction between Arabidopsis 

and Peronospora is governed by a gene-for-gene 

relationship, i.e. it is a form of major gene 

resistance based on specific recognition of a 

pathogen avirulence gene (avr) product by the 

product of a matching host resistance (R) gene 

(e.g. Botella et al., 1998). Molecular aspects of 

the Arabidopsis immune response to infections by


119 

P. parasitica and other pathogens have been 

investigated in some detail. Infection of one 

leaf triggers a localized reaction, the hypersensitive 

response, leading to death of the plant 

cells in the vicinity of infection. Additionally, 

a systemic response is initiated, i.e. plant 

organs distal to the infected leaf become resistant 

against further attack. This phenomenon is 

called systemic acquired resistance and is active 

against attacks by the same as well as many 

other pathogens. It is triggered at the site of 

initial infection by various elicitor molecules of 

pathogen origin, e.g. fatty acids such as arachidonic 

acid, or by other substances. The signal is 

transmitted by signalling molecules such as 

salicylic acid (Lawton et al., 1995; Ton et al., 

2002) which itself has no antimicrobial activity. 

Salicylic acid-independent signalling events are 

probably also involved (McDowell et al., 2000). 

Salicylic acid is produced at sites of infection, 

diffuses through the plant and interacts with a 

signalling chain, leading to the expression of a 

set of pathogenesis-related (PR) genes. A whole 

subset of PR genes involved in resistance to 

P. parasitica (RPP genes) is now known (McDowell 

et al., 2000). The function of many PR genes is 

still obscure; those whose functions are known 

encode chitinases, b-1,3-glucanases, proteinases, 

peroxidases or enzymes involved in toxin 

biosynthesis (Kombrink & Somssich, 1997). By 

creating mutants of Arabidopsis or of crop plants 

which overexpress their own regulatory genes 

or PR genes, or express introduced genes 

encoding elicitor molecules of pathogen origin, 

constitutive resistance against pathogen attack 

may be generated. This is considered to hold 

great potential for agriculture (Cao et al., 1998; 

Maleck et al., 2002). 

Control of Peronospora 

Downy mildew infections caused by Peronospora 

spp. are controlled mainly by fungicide applications. 

Metalaxyl is very effective against all 

downy mildews, but resistance has arisen in 

several species, and thus this fungicide is now 

applied in a cocktail with dithiocarbamates 

(Smith et al., 1988). Fosetyl Al is also now 

widely used as a foliar spray, root dip or soil 

amendment (Agrios, 2005). 

The breeding of cultivars with resistance 

against Peronospora spp. has been successful in 

certain crops, e.g. in lucerne (Medicago sativa) 

against P. trifoliorum (Stuteville, 1981). In tobacco 

plants attacked by P. tabacina, this strategy is a 

useful component of integrated control but is 

not sufficient on its own to afford complete 

control (Schiltz, 1981). In the tobacco P. tabacina 

system, a disease warning system is also in 

operation in Europe; subscribing tobacco 

growers are informed of the occurrence of the 

pathogen, so that preventative measures can be 

taken (Smith et al., 1988). This is profitable 

because tobacco is a high-value crop. 

Because downy mildews infect aerial plant 

parts and produce air-borne propagules in large 

numbers, crop sanitation measures are generally 

not very effective. However, in the case of 

P. destructor which overwinters systemically in 

volunteer onion bulbs, removal of volunteers is 

essential. In P. viciae on peas and beans, deep 

ploughing of the crop residue is important as the 

pathogen survives on infected haulms (Smith 

et al., 1988). 

5.4.2 Plasmopara (Peronosporaceae) 

Although downy mildews caused by species of 

Plasmopara are rarely serious in temperate 

climates, P. viticola is potentially a very destructive 

pathogen of the grapevine. The disease, 

which was endemic in North America and not 

particularly destructive on the local vines, was 

introduced into France during the nineteenth 

century with disastrous results on the French 

vines which had never been exposed to the 

disease and were highly susceptible. Large (1940) 

has vividly recounted the moment when Alexis 

Millardet, walking past a heavily infected vineyard 

in 1882, noticed that vines close to the road 

appeared healthy and had been sprayed with a 

mixture of lime and copper sulphate to discourage 

passers-by from pilfering fruit. This led to 

the discovery of Bordeaux mixture, one of the 

world’s first fungicides and still effective against 

P. viticola and other foliar pathogens belonging to 

the Oomycota. 

Plasmopara nivea is occasionally reported in 

Britain on umbelliferous crops such as carrot


and parsnip, and it is also found on Aegopodium 

podagraria. Plasmopara pygmaea is found on 

yellowish patches on the leaves of Anemone 

nemorosa (Fig. 5.30b), whilst P. pusilla is similarly 

associated with Geranium pratense (Fig. 5.30a). 

The haustoria of Plasmopara are knob-like, 

the sporangiophores are branched monopodially 

and the sporangia are hyaline (Fig. 5.30). Two 

types of sporangial germination have been 

reported. In P. pygmaea there are no zoospores 

but the entire sporangium detaches and later 

produces a germ-tube. In other species the 

sporangia germinate by means of zoospores 

which encyst and penetrate the host stomata. 

Oospore germination in P. viticola is also by 

means of zoospores. 

Because the grapevine is such a highvalue 

crop, the fungicide market is lucrative. 

Bordeaux mixtures are still used today, and 

similar fungicide applications to those described 

for Peronospora are made. Resistance to metalaxyl 

has been observed in P. viticola. Disease forecasting 

systems are being developed (Lafon & Bulit, 

1981; Smith et al., 1988). Breeding for resistant 

cultivars is being carried out, but because of the 

long generation times of the crop, this will be a 

prolonged effort. 

5.4.3 Bremia (Peronosporaceae) 

Bremia lactucae causes downy mildew of lettuce 

(Lactuca sativa) and strains of it can be found on 

36 genera of the Asteraceae including Sonchus 

and Senecio (Crute & Dixon, 1981). Crossinoculation 

experiments using sporangia from 

these hosts have failed to result in infection of 

lettuce and it seems that the fungus exists as a 

number of host-specific strains (formae speciales). 

Although wild species of Lactuca can carry strains 

capable of infecting lettuce, these hosts are not 

sufficiently common to provide a serious source 

of infection. The disease can be troublesome both 

in lettuce grown in the open and under frames, 

Fig 5.30 Plasmopara. 

(a) Sporangiophores 

of P. pusilla on 

Geranium pratense. 

(b) Sporangiophores 

of P. pygmaea on 

Anemone nemorosa.


121 

and in market gardens there may be sufficient 

overlap in the growing of lettuce for the disease 

to be carried over from one sowing to the next. 

The damage to the crop caused by Bremia may 

not in itself be severe, but infected plants are 

prone to secondary infection by the more serious 

grey mould, Botrytis cinerea. Systemic infections 

can occur. The intercellular mycelium is coarse, 

and the haustoria are sac-shaped, often several of 

them being present in each host cell (Fig. 5.31d). 

The sporangiophores emerge singly or in small 

groups through the stomata and branch dichotomously. 

The tip of each branch expands to 

form a cup-shaped disc bearing short cylindrical 

Fig 5.31 Bremia lactucae from Senecio vulgaris. (a) Sporangiophore protruding through a stoma. (b) Sporangiophore apex. 

(c) Sporangium germinating by means of a germ tube which has produced an appressorium at its apex. (d) Cells of epidermis and 

palisade mesophyll, showing intercellular mycelium and haustoria. (a,c,d) to same scale.


sterigmata at the margin and occasionally in the 

centre, and from these the hyaline sporangia 

arise (Figs. 5.31a,b). Germination of the sporangia 

is usually by means of a germ tube which 

forms an appressorium to penetrate epidermal 

cells (Fig. 5.31c), or it enters through a stoma. 

Zoospore formation has been reported but 

not confirmed. Sexual reproduction is usually 

heterothallic, although homothallic strains also 

exist. The oospores are formed in leaf tissue and 

remain viable for 12 months (Michelmore & 

Ingram, 1980; Morgan, 1983). 

Chemical control of B. lactucae on lettuce is 

certainly possible although not necessarily desirable; 

hence, intensive efforts for major gene 

resistance breeding have been made. Integrated 

control based on resistant cultivars and fungicide 

applications using metalaxyl and dithiocarbamates 

is successful (Crute, 1984). However, 

resistance against metalaxyl arose in Britain as 

early as 1983. Fosetyl Al is not as effective as 

metalaxyl (Smith et al., 1988). 

5.4.4 Albugo (Albuginaceae) 

This family has only a single genus, Albugo, with 

about 40 50 species of biotrophic parasites of 

flowering plants which cause diseases known as 

white blisters or white rusts. The commonest 

British species is A. candida causing white blisters 

of crucifers such as cabbage, turnip, swede, 

horseradish, etc. (Plate 2h). It is particularly 

frequent on shepherd’s purse (Capsella bursapastoris). 

There is some degree of physiological 

specialization in the races of this fungus on 

different host genera. Albugo candida can infect 

Arabidopsis thaliana, and the host defence 

response is governed by resistance genes involved 

in the recognition of the pathogen (Holub et al., 

1995). The principle is similar to, although not as 

well researched as, the Arabidopsis Peronospora 

interaction described earlier (p. 116). It is also 

now possible to establish callus cultures of mustard 

plants (Brassica juncea) containing balanced 

infections of A. candida (Nath et al., 2001). This 

experimental system should facilitate studies 

of the physiology of host pathogen interactions. 

A less common species is A. tragopogonis, causing 

white blisters of salsify (Tragopogon porrifolius), 

goatbeard (T. pratensis) and Senecio squalidus. 

In A. candida on shepherd’s purse, diseased 

plants may be detected by the distorted stems 

and the shining white raised blisters on the stem, 

leaves and pods before the host epidermis is 

ruptured (Plate 2h). Later, when the epidermis 

has burst open, a white powdery pustule is 

visible. The distortion is possibly associated with 

altered auxin levels. The host plant may be 

infected simultaneously with Peronospora parasitica, 

but the two fungi are easily distinguishable 

microscopically both in the structure of the 

sporangiophores and by their different haustoria. 

In Albugo, the mycelium in the host tissues 

is intercellular with only small spherical haustoria 

(Fig. 5.32) which contrast sharply with the 

coarsely lobed haustoria of P. parasitica. The fine 

structure of A. candida haustoria has been 

described by Coffey (1975) and Soylu et al. 

(2003). They are spherical or somewhat flattened 

and about 4 mm in diameter, connected to the 

intercellular mycelium by a narrow stalk about 

0.5 mm wide. Inside the plasma membrane of the 

haustorium, lomasomes, i.e. tubules and vesicles 

apparently formed by invagination of the plasma 

membrane, are more numerous than in the 

intercellular hyphae. The cytoplasm of the haustorial 

head is densely packed with mitochondria, 

ribosomes, endoplasmic reticulum and occasional 

lipid droplets, but nuclei have not been 

observed. Since nuclei of Albugo are about 2.5 mm 

in diameter, they may be unable to traverse the 

constriction which links the haustorium to the 

intercellular hypha. Nuclei may (e.g. Peronospora 

pisi) or may not be present in the haustoria of 

other Oomycota. The base of the haustorium of 

A. candida is surrounded by a collar-like sheath 

which is an extension of the host cell wall, but 

this wall does not normally extend to the main 

body of the haustorium. Between the haustorium 

and the host plasma membrane is an encapsulation. 

Host cytoplasm reacts to infection by an 

increase in the number of ribosomes and Golgi 

complexes. In the vicinity of the haustorium 

the host cytoplasm contains numerous vesicular 

and tubular elements not found in uninfected 

cells. These structures have been interpreted


123 

Fig 5.32 Albugo candida on Capsella bursa-pastoris. (a) Mycelium, sporangiophores and chains of sporangia formed beneath the 

ruptured epidermis (right). (b) Germination of sporangia showing the release of eight biflagellate zoospores.The stages illustrated 

took place within 2 min. (c) Haustoria. 

as evidence of secretory processes induced in the 

host cell by the presence of the pathogen. 

The intercellular mycelium aggregates 

beneath the host epidermis to form a palisade 

of cylindrical or skittle-shaped sporangiophores 

which give rise to chains of spherical sporangia 

in basipetal succession i.e. new sporangia 

are formed at the base of the chain. The pressure 

of the developing chains of sporangia raises 

the host epidermis and finally ruptures it.


The sporangia are then visible externally as a 

white powdery mass dispersed by the wind. 

Sporangia reaching a suitable host leaf will 

germinate within a few hours in films of water 

to form biflagellate zoospores of the principal 

type, about eight per sporangium (Fig. 5.32b). 

After swimming for a time, a zoospore encysts 

and then forms a germ tube which penetrates 

the host epidermis. The asexual disease cycle 

may be completed within 10 days. Infections may 

be localized or systemic. Gametangia are formed 

in the intercellular spaces of infected stems and 

leaves. Both the antheridium and the oogonium 

are multinucleate at their inception, and during 

development two further nuclear divisions occur 

so that the oogonium may contain over 200 

nuclei. However, there is only one functional 

male and one functional female nucleus. In the 

oogonium all the nuclei except one migrate to 

the periphery and are included in the periplasm. 

Following nuclear fusion a thin membrane first 

develops around the oospore. Division of the 

zygote nucleus takes place and is repeated, so 

that at maturity the oospore may contain as 

many as 32 diploid nuclei. Sansome and 

Sansome (1974) reported that meiosis occurs 

within the gametangia. They also suggested 

that A. candida is heterothallic. The high incidence 

of oospores of Albugo in Capsella stems 

simultaneously infected with Peronospora 

parasitica may result from some stimulus 

towards self-fertilization in Albugo produced by 

Peronospora, a situation analogous to the 

Trichoderma-induced sexual reproduction in 

heterothallic species of Phytophthora (see p. 95). 

The mature oospore is surrounded by a brown 

exospore, thrown into warty folds (Fig. 5.33a). 

Germination of the oospores takes place only 

after a resting period of several months. Under 

suitable conditions the outer wall of the oospore 

bursts and the endospore is extruded as 

a thin, spherical vesicle, which may be sessile 

or formed at the end of a wide cylindrical tube. 

Within the thin vesicle 40 60 zoospores are 

differentiated and are released on its breakdown 

(Figs. 5.33b,c). 

The cytology of oospore development in 

some other species of Albugo differs from that 

of A. candida. InA. bliti, a pathogen of Portulaca 

in North America and Europe, the oogonia and 

antheridia are also multinucleate and two 

nuclear divisions take place during their development. 

Numerous male nuclei fuse with 

numerous female nuclei and the fusion nuclei 

Fig 5.33 Albugo candida oospores. (a) Oogonium and oospore 

from Capsella leaf. (b,c) Two methods of oospore germination 

(after Vanterpool,1959).

SCLEROSPORACEAE 

125 

pass the winter without further change. In 

A. tragopogonis, a multinucleate oospore develops 

and again there are two nuclear divisions 

involved in the development of the oogonium 

and antheridium, but finally there is a single 

nuclear fusion between one male and one 

female nucleus. This fusion nucleus undergoes 

repeated divisions so that the overwintering 

oospore is multinucleate. 

Albugo candida alone or in combination with 

co-infecting Peronospora parasitica can occasionally 

cause significant crop losses in cabbage 

cultivation. Fungicide treatment is possible, 

with copper-based or dithiocarbamate-type fungicides 

commonly used (Smith et al., 1988). 

5.5 Sclerosporaceae 

This family comprises the downy mildews of 

grasses and cereals. Although it is well defined as 

a biological group, its phylogenetic position is 

unclear, recent ribosomal DNA-based studies 

placing its members among the Peronosporales 

(Riethmüller et al., 2002). For reasons of their 

distinctly different biological features, we 

consider them briefly here. The principal 

genera are Sclerospora, with sporangia capable of 

germinating by releasing zoospores, and 

Peronosclerospora, whose sporangia show direct 

germination by germ tubes and are thus, 

functionally speaking, ‘conidia’. Sporangia or 

conidia are produced on repeatedly branching 

aerial structures which resemble those of 

Peronospora spp. In Peronosclerospora, the conidiophores 

project through stomata of the host and 

branch at their apices to produce up to 20 fingerlike 

tapering extensions which expand to form 

conidia (Figs. 5.34a c). The conidia are oval 

and hyaline. Unlike those of other Oomycota, 

conidia of Sclerosporaceae are projected actively 

by a sudden rounding-off of the conidiophore 

tip and conidial base, and this is visible as a 

Fig 5.34 Peronosclerospora sorghi. 

(a) Immature conidiophore showing 

conidium initials. (b) Mature conidiophore 

from which two conidia have become 

detached. (c) Old conidiophore; all conidia 

have become detached. (d) Discharged 

conidia. Note the small basal projection. 

Drawn from material kindly provided 

by K. Mathur.


Fig 5.35 Oospore of Peronosclerospora sorghi.Notethe 

thickened oogonial wall (arrow), within which the spherical 

oospore with its wall and ooplast is clearly visible. 

small projection at the base of discharged 

conidia (Fig. 5.34d). Oospores of Sclerosporaceae 

are distinctive in being surrounded by a thickened 

oogonial wall (Fig. 5.35), and this feature 

may enhance the longevity of the oospore. The 

most important species are Sclerospora graminicola 

infecting pearl millet (Pennisetum americanum), 

and Peronosclerospora sorghi pathogenic on 

sorghum and maize. Because of their similar 

biological features and great economic importance, 

these two species are often considered 

together. Thorough reviews have been written 

by R. J. Williams (1984) and Jeger et al. (1998). 

Downy mildews of grasses cause serious 

crop losses especially in dry subtropical and 

tropical zones in Africa, their putative centre of 

evolution, as well as Asia and, to a lesser extent, 

North and South America. The thick-walled 

oospores can survive on plant debris and in the 

soil for up to 10 years, and infections are usually 

initiated from oospores which germinate 

directly by means of a germ tube. The plant 

root may be the initial route of entry, although 

both S. graminicola and P. sorghi may also become 

seed-borne. Later infections are through the 

shoot surface, either by direct penetration of 

the epidermis by means of appressoria, or 

through stomata. Infections of host plants are 

obligately biotrophic and can become systemic 

if they reach the apical meristem. Sporangia 

or conidia are formed only on freshly infected 

living host tissues under moist conditions, and 

infections are therefore polycyclic only when 

sufficient moisture is available. In dry regions, 

infections may be carried exclusively by 

oospores, confining the pathogen to one disease 

cycle per growing season. Oospore production 

is buffered against environmental extremes by 

taking place within the tissue of aerial host 

organs. Like sporangia or conidia, oospores can 

be blown about by wind. 

Control of downy mildew of grasses is 

difficult. Metalaxyl gives good control both as a 

seed dressing and as a foliar spray but may 

not always be available. Numerous cultivars of 

sorghum and pearl millet show resistance 

against downy mildews, but this is usually 

based on one or a few major genes and can 

therefore be overcome by the pathogens if single 

cultivars are grown in large coherent areas. 

On small-scale farms, it may be possible to remove 

individual infected plants prior to the onset of 

sporulation (Gilijamse et al., 1997).

6 

Chytridiomycota 


The phylum Chytridiomycota comprises over 

900 species in five orders (D. J. S. Barr, 2001; Kirk 

et al., 2001). Fungi included here are colloquially 

called ‘chytrids’. Most chytrids grow aerobically 

in soil, mud or water and reproduce by zoospores 

with a single posterior flagellum of the whiplash 

type, although the zoospores of some members of 

the Neocallimastigales are multiflagellate. Some 

species inhabit estuaries and others the sea. 

Sparrow (1960) has given an extensive account 

of aquatic forms, Karling (1977) a compendium of 

illustrations, and Powell (1993) has provided 

examples of the importance of the group. Many 

members are saprotrophs, utilizing cellulose, 

chitin, keratin, etc., from decaying plant and 

animal debris in soil and mud, whilst species of 

Caulochytrium grow as mycoparasites on the 

mycelium and conidia of terrestrial fungi (Voos, 

1969). Saprotrophs can be obtained in crude 

culture by floating baits such as cellophane, 

hair, shrimp exoskeleton, boiled grass leaves 

and pollen on the surface of water overlying 

samples of soil, mud or pieces of aquatic plant 

material (Sparrow, 1960; Stevens, 1974; 

Willoughby, 2001). From such crude material, 

pure cultures may be prepared by streaking 

or pipetting zoospores onto agar containing 

suitable nutrients and antibiotics to limit contamination 

from bacteria. The growth and 

appearance of chytrids in pure culture is variable 

and often differs significantly from their natural 

habit. This has led to problems in classification 

systems based on thallus morphology (Barr, 1990, 

2001). The availability of cultures has, however, 

facilitated studies on chytrid nutrition and 

physiology (Gleason, 1976). 

Some chytrids are biotrophic parasites of 

filamentous algae and diatoms and may severely 

deplete the population of freshwater phytoplankton 

(see p. 139). Two-membered axenic 

cultures of diatom host and parasite have been 

prepared, making possible detailed ultrastructural 

studies of comparative morphology, zoospores, 

infection processes and reproduction. 

Other chytrids such as species of Synchytrium 

and Olpidium are biotrophic parasites of 

vascular plants. Synchytrium endobioticum is the 

agent of the potentially serious black wart 

disease of potato. Olpidium brassicae, common in 

the roots of many plants, is relatively harmless, 

but its zoospores are vectors of viruses such 

as that causing big vein disease of lettuce. 

Coelomomyces spp. are pathogens of freshwater 

invertebrates including copepods and the larvae 

of mosquitoes. The possibility of using them 

in the biological control of mosquitoes has 

been explored. The most unusual group are the 

Neocallimastigales, which grow in the guts of 

herbivorous mammals, are obligately anaerobic 

and subsist on ingested herbage. 

The cell walls of some chytrids have been 

examined microchemically by X-ray diffraction 

and other techniques. Chitin has been detected 

in many species (Bartnicki-Garcia, 1968, 1987), 

and in Gonapodya cellulose is also present 

(Fuller & Clay, 1993). The composition of the 

wall is of interest because chitin, a polymer of

128 CHYTRIDIOMYCOTA 

N-acetylglucosamine, is also found in the walls 

of other Eumycota (i.e. Zygomycota, Ascomycota 

and Basidiomycota), whilst the cell walls of 

members of the Oomycota contain cellulose. 

Cellulose and chitin occur together in the walls 

of species of Hyphochytrium and Rhizidiomyces, 

members of the Hyphochytriomycota (Fuller, 

2001; see Section 4.3). 

The form of the thallus in the 

Chytridiomycota is varied. In biotrophic species 

such as Olpidium and Synchytrium, where the 

whole thallus is contained within the host cell, 

there is no differentiation into a vegetative 

and a reproductive part. At maturity the entire 

structure, except for the wall which surrounds it, 

is converted into reproductive units, i.e. zoospores, 

gametes or resting sporangia. Such thalli 

are termed holocarpic (Fig. 6.1). More usually, the 

thallus is differentiated into organs of reproduction 

(sporangia and resting sporangia) arising 

from a vegetative part which often consists of 

rhizoids. These serve in the exploitation of the 

substratum and the assimilation of nutrients. 

Thalli of this type are eucarpic. Eucarpic thalli 

may have one or several sporangia and are then 

termed monocentric or polycentric, respectively 

(Fig. 6.1). In some species there are both monocentric 

and polycentric thalli, so that these terms 

have descriptive rather than taxonomic significance. 

A further distinction has been made, 

especially in monocentric forms, between those 

in which only the rhizoids are inside the host 

cell whilst the sporangium is external (epibiotic), 

in contrast with the endobiotic condition in 

which the entire thallus is inside the host cell 

(Fig. 6.1). In monocentric thalli, the rhizoids 

usually radiate from a single position on the 

sporangium wall, but in polycentric forms a 

more extensive, branched rhizoidal system, the 

rhizomycelium, develops. 

The zoosporangium is generally a spherical 

or pear-shaped sac bearing one or more discharge 

tubes or exit papillae. The method of 

zoospore release has been used in classification. 

Fig 6.1 Types of thallus structure in the 

Chytridiales, diagrammatic and not to scale.

INTRODUCTION 

129 

In the inoperculate chytrids such as Olpidium, 

Diplophlyctis and Cladochytrium, the sporangium 

forms a discharge tube which penetrates to the 

exterior of the host cell and its tip becomes 

gelatinous and dissolves away. In operculate 

chytrids such as Chytridium and Nowakowskiella, 

the tip of the discharge tube breaks open at a 

special line of weakness and is seen as a special 

cap or operculum after discharge (see Fig. 6.4b). 


The number of zoospores formed inside zoosporangia 

of chytrids varies with the size of the 

spore and sporangium. Although the zoospore 

size is roughly constant for a given species, the 

size of the sporangium may be very variable. In 

Rhizophlyctis rosea, tiny sporangia containing only 

one or two zoospores have been reported from 

culture media deficient in carbohydrate, whereas 

on cellulose-rich media large sporangia containing 

many hundred spores are formed. The release 

of zoospores is brought about by internal 

pressure which causes the exit papillae to burst 

open. In studies of the fine structure of mature 

sporangia of R. rosea and Nowakowskiella profusa 

(Chambers & Willoughby, 1964; Chambers et al., 

1967), it has been shown that the single 

flagellum is coiled round the zoospore like a 

watch spring. The zoospores are separated by a 

matrix of spongy material which may absorb 

water and swell rapidly at the final stages 

of sporangial maturation. When the internal 

pressure has been relieved by the ejection of 

some zoospores, those remaining inside the 

sporangium escape by swimming or wriggling 

through the exit tube. In some species the spores 

are discharged in a mass which later separates 

into single zoospores, but in others the zoospores 

make their escape individually. 

The form of the zoospore is similar in all 

chytrids (with the exception of the multiflagellate 

members of the Neocallimastigales). There 

is a spherical or ellipsoidal body which in some 

forms is capable of plastic changes in shape, and 

a long trailing flagellum. When swimming, the 

zoospores show characteristic jerky or ‘hopping’ 

movements; additionally, abrupt changes in 

direction are sometimes made. The internal 

structure of the zoospore as revealed by light 

and electron microscopy is variable, but characteristic 

of particular genera (Lange & Olson, 

1979). In view of the plasticity in morphology of 

the thallus under different growth conditions, 

zoospore ultrastructure is regarded as a more 

satisfactory basis of classification (D. J. S. Barr, 

1990, 2001). Two features are of taxonomic 

importance, the flagellar apparatus and an assemblage 

of organelles termed the microbody lipid 

globule complex (MLC) (D. J. S. Barr, 2001). 

The flagellar apparatus 

The whiplash flagellum resembles that of other 

eukaryotes, with a smooth membrane enclosing 

a cylindrical shaft, the axoneme, made up 

internally of nine doublet pairs of microtubules 

surrounding two central microtubules. As shown 

in Fig. 6.2, the base of the axoneme comprises 

three regions, the flagellum proper, the transitional 

zone and the kinetosome. The function 

of the kinetosome is to generate the flagellum. 

An interesting feature found in several species 

is a second kinetosome or the remainder of 

one, the dormant kinetosome. Its presence 

has led to the suggestion that the ancestors 

of the Chytridiomycota may have had biflagellate 

zoospores, the second flagellum having been 

lost in the course of evolution (Olson & Fuller, 

1968). 

In section, the kinetosome resembles a cartwheel 

(Fig. 6.2f), because to each of the nine 

outer microtubule doublets seen in the flagellum 

proper, a third microtubule is attached. 

This is called the C-tubule; in the doublets, 

that tubule with extended dynein arms is the 

A-tubule, and its partner is labelled B. These 

flagellar microtubules radiate as kinetosome 

props into the zoospore, perhaps providing 

structural support and anchorage of the flagellum 

(D. J. S. Barr, 2001). Microtubules may also be 

attached laterally to the kinetosome, contributing 

to the flagellar root system (Figs. 6.2c, 6.19). 

In the innermost (proximal) part of the transitional 

zone, the nine microtubule triplets of 

the kinetosome are converted into the doublets 

of the flagellum proper; concentric fibres, 

possibly arranged helically, surround the nine 

doublet pairs. Also within the transitional zone,

130 CHY TRIDIOMYCOTA 

Fig 6.2 Flagellar apparatus typical of zoospores of Chytridiomycota. (a) Median longitudinal section of the junction of the flagellum 

with the body of the zoospore.The labels indicate the flagellum proper (F), transitional zone (TZ), kinetosome (K), electron-dense 

region (ED), concentric fibres (CF), transitional fibres (TF), kinetosome props (KP), terminal plate (TP), kinetosome (K) showing a 

cartwheel-like organization (Cw), dormant kinetosome (DK), fibrillar material (Fi) found in some taxa, and microtubular roots (Mt) 

extending from the side or end of the kinetosome into the body of the zoospore. (b) Transverse section near the terminal plate 

showing nine kinetosome props extending from doublet microtubules to the cell membrane. (c) Transverse section in the lower 

part of the transition zone showing concentric and transitional fibres. (d) Transverse section of the flagellum proper showing two 

central microtubules and nine peripheral doublet microtubules enclosed in the flagellar membrane (FM). (e) Schematic drawing of 

the flagellum proper in transverse section.The arrowed line 0° 180° shows an imaginary plane which coincides with the plane of 

undulation of the flagellum, passing through doublet pair1and between the central microtubules and doublet pairs 5 and 6. 

The convention used in labelling the outer doublet pairs of microtubules is shown: the microtubule with dynein arms (d) is the 

A microtubule and its partner is the B microtubule. (f) Kinetosome in transverse section showing the triplet arrangement of the 

peripheral microtubules by the addition of a third microtubule (C). Redrawn from Barr and De¤saulniers (1988) by copyright 

permission of the National Research Council of Canada, Barr (1992). ßThe Mycological Society of America, and D. J. S. Barr (2001) 

with kind permission of Springer Science and Business Media. 

the two central microtubules arise near a 

terminal plate. The structure of the flagellum 

and kinetosome in transverse section is shown in 

Figs. 6.2e and f (Barr & Désaulniers, 1988). 

The microbody lipid complex 

The MLC (Fig. 6.3) is made up of a microbody 

which is often closely appressed to a large lipid 

globule and to simple membrane cisternae or 

a tubular membrane system, the rumposome. 

This is defined as a cisterna in which there is an 

area with hexagonally arranged, honeycomb-like 

pores called fenestrae (Fuller, 1976; Powell & 

Roychoudhury, 1992). The rumposome may 

be involved in signal transduction from the 

plasma membrane to the flagellum because it 

is known that this organelle sequesters calcium. 

Regulation of external calcium concentrations 

has an effect on the symmetry of flagellar beat 

and hence on the direction of zoospore movement 

(Powell, 1983). 

There are several distinct types of MLC (Powell 

& Roychoudhury, 1992) and Fig. 6.3 illustrates 

diagrammatically just one of them, that 

described for Rhizophlyctis harderi. In this species, 

the MLC includes several (3 5) lipid globules.

INTRODUCTION 

131 

Most zoospores are uninucleate. The nucleus 

is surrounded in many cases (but not all) by a 

nuclear cap of uneven thickness. The nuclear cap 

is especially prominent in zoospores of members 

of Blastocladiales such as Allomyces and 

Blastocladiella (Fig. 6.19). It is rich in RNA and 

protein and also contains ribosomes. 

Fig 6.3 Schematic diagram of the microbody lipid complex 

of the zoospore of Rhizophlyctis harderi as seen in a longitudinal 

section through the base of the zoospore and flagellum.The 

following organelles are drawn: mitochondrion (Mc), simple 

cisterna (C), lipid globule (L), microbody (Mi), flagellum (F) and 

rumposome (R). Redrawn from Powell and Roychoudhury 

(1992), by copyright permission of the National Research 

Council of Canada. 

Those at the anterior of the cell are embedded 

in an aggregation of ribosomes. The surfaces 

of lipid globules close to the plasma membrane 

are partially covered by one to several simple 

cisternae, sometimes with irregularly scattered 

pores. Towards the centre of the cell the 

lipid bodies are clasped by cup-shaped microbodies. 

At the posterior of the zoospore near 

the kinetosome, 1 3 smaller lipid globules 

are partially covered by a rumposome, linked 

to the plasma membrane by short bridges and 

to the kinetosome by a microtubule root. 

Other features 

Patches of glycogen are located in the peripheral 

cytoplasm of the zoospore and it is likely 

that these and the lipid globules represent 

sources of energy used in respiration and 

propulsion. Mitochondria tend to be concentrated 

in the posterior of the zoospore close 

to the kinetosome; in Allomyces and Blastocladiella 

(Blastocladiales), the base of the flagellum 

passes through the perforation of a single large 

mitochondrion (see Fig. 6.19). 

6.1.2 Zoospore encystment and 

germination 

The period of zoospore movement varies. Some 

flagellate zoospores seem to be incapable of 

active swimming and amoeboid crawling may 

take place instead, or swimming may last for 

only a few minutes. In other spores, motility 

may be prolonged for several hours. Prior to 

germination, the zoospore comes to rest and 

encysts. The flagellum may contract, it may be 

completely withdrawn or it may be cast off, 

but the precise details are often difficult to 

follow. The subsequent behaviour also differs 

in different species. In holocarpic parasites the 

zoospore encysts on the host surface and 

the cytoplasmic contents of the zoospore are 

injected into the host cell. In many monocentric 

chytrids rhizoids develop from one point on 

the zoospore cyst and the cyst itself enlarges to 

form the zoosporangium, but there are variants 

of this type of development in which the cyst 

enlarges into a prosporangium from which the 

zoosporangium later develops. In the polycentric 

types, the zoospore on germination may form 

a limited rhizomycelium on which a swollen 

cell arises, giving off further branches of rhizomycelium. 

Germination may be from a single 

point on the wall of the zoospore cyst (monopolar 

germination) or from two points, enabling 

growth to take place in two directions (bipolar 

germination). The mode of germination is an 

important character in distinguishing, for 

example, the Chytridiales (monopolar) from 

the Blastocladiales (bipolar). 

6.1.3 Life cycles of the Chytridiomycota 

Most chytrids have haploid zoospores and thalli 

but some Blastocladiales show an alternation 

of haploid (gametothallic) and diploid (sporothallic) 

generations. Apart from differences in


the reproductive organs, the morphology of the 

two types of thallus is very similar, a phenomenon 

known as isomorphic alternation of 

generations. 

Sexual reproduction, i.e. a life cycle which 

includes nuclear fusion and meiosis, may occur 

in several different ways (e.g. Figs. 6.6 and 6.22). 

In some chytrids it is by gametogamy, the fusion 

of gametes which are posteriorly uniflagellate. 

Isogamous conjugation occurs if there is no 

morphological distinction between the two 

fusing partners, but in some Blastocladiales (e.g. 

Allomyces) anisogamy takes place by fusion 

between a smaller, more actively motile male 

gamete with a larger, sluggish female gamete. 

Oogamy, fusion between an actively motile 

male gamete and a much larger, non-flagellate, 

immobile globose egg, is characteristic of 

Monoblepharidales. Somatogamy, the fusion 

of undifferentiated hyphae or rhizoids, has 

been well documented in cultures of the freshwater 

fungus Chytriomyces hyalinus by Moore 

and Miller (1973) and Miller and Dylewski 

(1981, 1987). As shown in Fig. 6.4, zoospores of 

C. hyalinus are released from the zoosporangium 

by the opening of a lid-like operculum. They 

germinate to form uninucleate rhizoidal thalli 

(contributory thalli) and the tips of the rhizoids 

from adjacent thalli, which are apparently not 

genetically distinct from each other, may fuse 

(Fig. 6.4c). At the point of fusion an incipient 

resting body develops (Fig. 6.4d) and swells 

while cytoplasm and a nucleus migrate into it 

from each contributory thallus. Nuclear fusion 

occurs in the resting body to form a diploid 

zygote nucleus. The resting body continues to 

enlarge and develops a thick wall. This type 

of sexual reproduction by somatogamous conjugation 

probably occurs in several genera of 

inoperculate and operculate chytrids (Moore & 

Miller, 1973). 

Fusion of gametangia (gametangiogametangiogamy) 

has been reported by Doggett 

and Porter (1996) for Zygorhizidium planktonicum, 

a parasite of the diatom Synedra. This species 

reproduces asexually by epibiotic zoosporangia. 

Germinating zoospores develop either new 

zoosporangial thalli or gametangial thalli of 

two sizes with globose uninucleate gametangia. 

Fig 6.4 Chytriomyces hyalinus somatogamy. (a,b) Epibiotic 

fruiting thallus seated on a pollen grain into which rhizoids 

have penetrated. In (a) the zoosporangium, containing 

numerous zoospores, is seen shortly before discharge with a 

bulging operculum (o). In (b) the operculum has lifted off and 

the zoospores are escaping. (c e) Stages in somatogamy. 

(c) Rhizoids from two uninucleate contributory thalli (c) have 

undergone anastomosis (arrow). (d) Cytoplasm and a nucleus 

from each contributory thallus have migrated towards the 

point of anastomosis, where the thallus swells to form a 

globose incipient resting body (i) which is binucleate and 

packed with cytoplasm, leaving the contributory thalli empty. 

(e) The two nuclei in the incipient resting body have fused. 

After C.E. Miller and Dylewski (1981). 

Conjugation occurs when a conjugation tube 

grows from the smaller donor to the larger 

recipient gametangium (Fig. 6.5a). Following 

nuclear fusion, the larger gametangium develops 

a thick wall and functions as a diploid resting 

spore. After a period of maturation the 

resting spore acts as a prosporangium, giving 

rise to a thin-walled meiosporangium. Meiosis, 

as evidenced by the presence of synaptonemal 

complexes, occurs here, followed by mitosis 

and cytoplasmic cleavage to form zoospores 

(Fig. 6.5b). A variant of this form of sexual 

differentiation (gametangio-gametogamy) has

INTRODUCTION 

133 

Fig 6.5 Sexual reproduction in Zygorhizidium planktonicum. (a) Empty donor gametangium to the left connected by a 

conjugation tube to a mature resting spore. (b) Near-median section of a fully formed meiosporangium which has developed 

from a germinating resting spore.The donor gametangium is on the right. Scale bar ¼ 4 mm. After Doggett and Porter (1996). 

been reported in species of Rhizophydium (Karling, 

1977); this involves copulation between the 

gametangium of a rhizoid-forming thallus and 

a motile gamete that encysts directly on the 

gametangium. 

Generally the product of sexual reproduction 

is a resting spore or resting sporangium with 

thick walls, but it is known that thick-walled 

sporangia may also develop asexually and in 

many chytrids sexual reproduction has not been 

described and possibly does not occur. Resting 

sporangia of some chytrids may remain viable 

for many years. 

6.1.4 Classification and evolution 

Fossil chytrids have been reported from the 

400 million-year-old Rhynie chert, a site known 

for the discovery of fossil remains of the 

earliest known vascular land plants. Clusters 

of holocarpic, endobiotic thalli resembling the 

present day Olpidium have been found inside 

cells of a coenobial alga preserved within the 

hollow axes of a vascular plant, and epibiotic 

sporangia with endobiotic rhizoids have been 

seen attached to meiospores of a vascular plant, 

much like those of extant chytrids like 

Rhizophydium which grow on pollen grains 

(Taylor et al., 1992). Chytrid-like fossils have also 

been found in strata of the 340 million-year-old 

Pennsylvanian (Carboniferous) era (Millay & 

Taylor, 1978) and from the more recent Eocene 

strata (Bradley, 1967). 

Formerly thought to have an affinity for 

the Oomycota, Hyphochytriomycota or protists, 

the Chytridiomycota are now accepted as 

members of the true fungi, the Eumycota. They 

are probably ancestral to other groups of true 

fungi, especially the Zygomycota (Cavalier-Smith, 

1987, 2001; D. J. S. Barr, 2001). The inclusion of the 

chytrids in the Eumycota is supported by several 

DNA-based phylogenetic analyses (e.g. Bowman 

et al., 1992; James et al., 2000), but the delimitation 

of orders within the Chytridiomycota is still 

problematic. Particularly puzzling is the grouping 

of the Blastocladiales with the Zygomycota on 

the basis of 18S ribosomal DNA sequences 

(see Fig. 1.26). 

D. J. S. Barr (2001) and Kirk et al. (2001) have 

classified the Chytridiomycota into five orders 

(Table 6.1) but the details of their distinguishing 

features need not concern us here. We shall 

study examples from each order.


Table 6.1. Orders of Chytridiomycota following D. J. S. Barr (2001) and Kirk et al. (2001). 

Order 

Number of 

described taxa 

Examples 

Chytridiales 


Spizellomycetales 


Neocallimastigales 


Blastocladiales 


Monoblepharidales 


80 genera Cladochytrium, Nowakowskiella, Rhizophydium, 

600 spp. 

Synchytrium 

13 genera Olpidium, Rhizophlyctis 

86 spp. 

5genera 

16 spp. 

Anaeromyces,Caecomyces, Neocallimastix, 

Orpinomyces, Piromyces 

14 genera Allomyces, Blastocladiella,Coelomomyces, 

179 spp. 

Physoderma 

4genera 

19 spp. 

Gonapodya, Monoblepharella, Monoblepharis 

6.2 Chytridiales 

This is by far the largest order, comprising more 

than 50% of the total number of chytrids 

described to date. It is difficult to characterize 

members of the Chytridiales because they lack 

any specific features by which species have been 

assigned to the other four orders. The classification 

of the Chytridiales has traditionally been 

based on thallus morphology (Sparrow, 1973) 

but, as pointed out by D. J. S. Barr (2001), this is 

unsatisfactory because of the great variability in 

thallus organization shown by the same fungus 

growing on its natural substratum and in 

culture. Future systems of classification will be 

based on zoospore ultrastructure and the 

comparison of several different types of DNA 

sequences, but too few examples have yet been 

studied to provide a definitive framework. 

Because of this we shall study genera which 

illustrate the range of morphology, life cycles 

and ecology of the Chytridiales without attempting 

to place them into families. 

6.2.1 Synchytrium 

In this genus the thallus is endobiotic and 

holocarpic, and at reproduction it may become 

converted directly into a group (sorus) of 

sporangia, or to a prosorus which later gives 

rise to a sorus of sporangia. Alternatively the 

thallus may turn into a resting spore which 

can function either directly as a sporangium 

and give rise to zoospores, or as a prosorus. The 

zoospores are of the characteristic chytrid type 

(Lange & Olson, 1978). Sexual reproduction is 

by copulation of isogametes, resulting in the 

formation of thalli which develop into thickwalled 

resting spores. Synchytrium includes 

about 120 species which are biotrophic parasites 

of flowering plants. Some species parasitize only 

a narrow range of hosts, e.g. S. endobioticum on 

Solanaceae, but others, e.g. S. macrosporum, have 

a wide host range (Karling, 1964). Most species 

are not very destructive to the host plant but 

stimulate the formation of galls on leaves, 

stems and fruits. 

Synchytrium endobioticum 

This is the cause of wart disease affecting 

cultivated potatoes and some wild species of 

Solanum. It is a biotrophic pathogen which has 

not yet been successfully cultured outside living 

host cells. Wart disease is now distributed 

throughout the main potato-growing regions 

of the world, especially in mountainous areas 

and those with a cool, moist climate. Lange 

(1987) has given practical details of techniques 

for studying the fungus but in most European 

countries handling of living material by

CHYTRIDIALES 

135 

unlicensed workers is illegal. Diseased tubers 

bear dark brown cauliflower-like excrescences. 

Galls may also be formed on the aerial shoots, 

and they are then green with convoluted leaf-like 

masses of tissue (the leafy gall stage; Plates 3a,b). 

Heavily infected tubers may have a considerable 

proportion of their tissues converted to warts. 

The yield of saleable potatoes from a heavily 

infected crop may be less than the actual weight 

of the seed potatoes planted. The disease is thus 

potentially a serious one, but fortunately varieties 

of potatoes are available which are immune 

from the disease, so that control is practicable. 

The possible life cycle of S. endobioticum is 

summarized in Fig. 6.6. 

The dark warts on the tubers are galls in 

which the host cells have been stimulated to 

divide by the presence of the fungus. Many 

of the host cells contain resting spores which 

are more or less spherical cells with thick dark 

brown walls folded into plate-like extensions 

(see Fig. 6.7a). The resting spores are released 

by the decay of the warts and may remain alive 

in the soil for over 40 years (Laidlaw, 1985). 

The outer wall (exospore) bursts open by an 

irregular aperture and the endospore balloons 

out to form a vesicle within which a single 

sporangium differentiates (Kole, 1965; Sharma 

& Cammack, 1976; Hampson et al., 1994). Thus 

the resting spore functions as a prosporangium 

on germination. Germination of the resting 

spore may occur spontaneously but can be stimulated 

by passage through snails. It is presumed 

that abrasion and digestion of the spore wall 

Fig 6.6 Schematic outline of the probable life cycle of Synchytrium endobioticum. Haploid and diploid nuclei are represented by 

small empty and larger split circles, respectively. Key events in the life cycle are plasmogamy (P), karyogamy (K) and meiosis (M). 

Resting spores within a warted potato contain a single nucleus which undergoes meiosis upon germination. Haploid zoospores 

are released from a single sporangium. If two zoospores pair up, a zygote is formed and penetration of a potato cell gives rise to 

a diploid thallus and, ultimately, a resting spore. Diploid infections cause host hyperplasia visible as the potato wart symptoms. 

If a zoospore infects in the haploid state, a haploidprosorus (summer spore) is formed, and hypertrophy of the infected and adjacent 

host cells ensues. A sorus of several sporangia is ultimately produced, with each sporangium releasing a fresh crop of haploid 

zoospores. Synchytrium endobioticum appears to be homothallic.


Fig 6.7 Synchytrium endobioticum. 

(a) Resting spores in section of wart. 

(b) Germinating resting spore showing 

the formation of a vesicle containing 

a single globose sporangium (after Kole, 

1965). (c) Section of infected host cell 

containing a prosorus.The prosorus 

is extruding a vesicle. Note the hypertrophy 

of the infected cell and adjacent 

uninfected cells. (d) Cleavage of vesicle 

contents to form zoosporangia. (e) Two 

extruded zoosporangia. (f) Zoospores. 

(g) Rosette of hypertrophied potato cells 

as seen from the surface.The outline 

of the infected host cell is shown dotted. 

(h) Young resting sporangium resulting 

from infection by a zygote. Note that 

the infected cell lies beneath the 

epidermis due to division of the 

host cells. 

in the snail gut causes breakdown of the thick 

wall which contains chitin and branched-chain 

wax esters, so overcoming dormancy related 

to the impermeability of the wall (Hampson 

et al., 1994). 

The zoospores are capable of swimming for 

about two hours in the soil water. If they alight 

on the surface of a potato ‘eye’ or some other 

part of the potato shoot such as a stolon or 

a young tuber before its epidermis is suberized, 

they come to rest and withdraw their flagellum. 

During penetration, the contents of the zoospore 

cyst are transferred to the host cell whilst the 

cyst wall remains attached to the outside. When 

a dormant ‘eye’ is infected, dormancy may 

be broken and the tuber may begin to sprout. If 

the potato variety is susceptible to the disease, 

the small fungal thallus inside the host cell 

will enlarge. The infected host cell as well as 

surrounding cells also enlarge so that a rosette 

of hypertrophied cells surrounds a central 

infected cell (Fig. 6.7c). The walls of these cells 

adjacent to the infected cell are often thickened 

and assume a dark brown colour. The infected 

cell remains alive for some time but eventually 

it dies. The pathogen thallus passes to the 

bottom of the host cell, enlarges and becomes 

spherical. A double-layered chitinous wall which

CHYTRIDIALES 

137 

is golden brown in colour is secreted around 

the thallus, now termed a prosorus or summer 

spore. Further development of the prosorus 

involves the protrusion of the inner wall through 

a pore in the outer wall, and its expansion as 

a vesicle which enlarges upwards and fills the 

upper half of the host cell (Fig. 6.7c). The 

cytoplasmic contents of the prosorus including 

the single nucleus are transferred to the vesicle. 

The process is quite rapid and can be completed 

in about 4 h. During its passage into the vesicle 

the nucleus may divide, and mitoses continue 

so that the vesicle contains about 32 nuclei. 

At this stage the cytoplasmic contents of the 

vesicle become cleaved into about 4 9 sporangia 

(Fig. 6.7d), forming a sorus. After the deposition 

of sporangial walls, further nuclear divisions 

occur in each sporangium, and finally each 

nucleus with its surrounding mass of cytoplasm 

becomes differentiated to form a zoospore. As 

the sporangia ripen, they absorb water and 

swell, causing the host cell containing them to 

burst open. Meanwhile, division of the host 

cells underlying the rosette has been taking 

place, and enlargement of these cells pushes 

the sporangia out onto the surface of the host 

tissue (Fig. 6.7e). The sporangia swell if water 

is available and burst open by means of a small 

slit through which the zoospores escape. There 

may be as many as 500 600 zoospores in a single 

large sporangium. The zoospores resemble those 

derived from resting sporangia and are capable 

of initiating further asexual cycles of reproduction 

throughout spring and early summer. 

Sometimes several zoospores succeed in penetrating 

a single cell so that it contains several 

fungal protoplasts. 

Alternatively, zoospores may function as 

gametes, fusing in pairs (or occasionally in 

groups of three or four) to form zygotes which 

retain their flagella and swim actively for a time. 

Since zoospores acting as gametes do not differ 

in size and shape, copulation can be described 

as isogamous. However, the gametes may differ 

physiologically. Curtis (1921) has suggested that 

fusion may not occur between zoospores derived 

from a single sporangium, but only between 

zoospores from separate sporangia. Köhler (1956) 

has claimed that the zoospores are at first 

sexually neutral. Later they mature and become 

capable of copulation. Maturation may occur 

either outside the sporangia or within, so that 

in over-ripe sporangia the zoospores are capable 

of copulation on release. At first the zoospores 

are ‘male’, and swim actively. Later the swarmers 

become quiescent (‘female’) and probably secrete 

a substance which attracts ‘male’ gametes. 

After swimming by means of its two flagella, 

the zygote encysts on the surface of the host 

epidermis and penetration may then follow by 

a process essentially similar to zoospore penetration. 

Multiple infections by several zygotes 

penetrating a single host cell can also occur. 

Nuclear fusion occurs in the young zygote before 

penetration. 

The results of zygote infections differ from 

infection by zoospores. The host cell reacts to 

zoospore infection by undergoing hypertrophy, 

i.e. increase in cell volume, and adjacent cells 

also enlarge to form the characteristic rosette 

which surrounds the resulting prosorus. In 

contrast, when a zygote infects, the host cell 

undergoes hyperplasia, i.e. repeated cell division. 

The pathogen lies towards the bottom of the 

host cell, adjacent to the host nucleus, and cell 

division occurs in such a way that the fungal 

protoplast is located in the innermost daughter 

cell. As a result of repeated divisions of the 

host cells, the typical gall-like potato warts are 

formed and fungal protoplasts may be buried 

several cell layers deep beneath the epidermis 

(see Fig. 6.7h). During these divisions of the 

host tissue the zygote enlarges and becomes 

surrounded by a two-layered wall, a thick outer 

layer which eventually becomes dark brown in 

colour and is thrown into folds or ridges which 

appear as spines in section, and a thin hyaline 

inner wall surrounding the granular cytoplasm 

(Lange & Olson, 1981). The host cell eventually 

dies and some of its contents are deposited on 

the outer wall of the resting sporangium, 

forming the characteristic brown ridges. During 

its development the resting spore remains uninucleate. 

Resting spores are released into the 

soil and are capable of germination within 

about 2 months. Before germination, the nucleus 

divides repeatedly to form the nuclei of the 

zoospores whose further development has


already been described. It has been claimed that 

the zygote and the young resting spore 

are diploid, and it has been assumed that meiosis 

occurs during germination of the resting sporangia 

prior to the formation of zoospores, so 

that these zoospores, the prosori and the soral 

zoospores are also believed to be haploid. 

These assumptions seem plausible in the light 

of knowledge of the life history and cytology 

of other species (e.g. Lingappa, 1958b), and an 

essentially similar life cycle has been described 

for S. lagenariae and S. trichosanthidis, parasitic on 

Cucurbitaceae, which differ from S. endobioticum 

in that their resting spores function as prosori 

instead of prosporangia (Raghavendra Rao & 

Pavgi, 1993). 

Control of wart disease 

Control is based largely on the breeding of 

resistant varieties of potato. It was discovered 

that certain varieties such as Snowdrop were 

immune from the disease and could be planted 

on land heavily infected with Synchytrium without 

developing warts. Following this discovery, 

plant breeders have developed a number of 

immune varieties such as Maris Piper. However, 

some potato varieties that are susceptible to 

the disease are still widely grown, including the 

popular King Edward. In most countries where 

wart disease occurs, legislation has been introduced 

requiring that only approved immune 

varieties be planted on land where wart disease 

has been known to occur, and prohibiting the 

movement and sale of diseased material. Within 

the British Isles, the growing of immune varieties 

on infested land has prevented the spread of 

the disease, and it is now confined to a small 

number of foci in the West Midlands, northwest 

England and mid and south Scotland. It has 

also persisted in Newfoundland. The majority of 

the outbreaks are found in allotments, gardens 

and smallholdings. 

The reaction of immune varieties to infection 

varies (Noble & Glynne, 1970). In some cases 

when ‘immune’ varieties are exposed to a heavy 

inoculum load of S. endobioticum in the laboratory, 

they may become slightly infected, but 

infection is often confined to the superficial 

tissues which are soon sloughed off. In the 

field such slight infections would probably pass 

unnoticed. Occasionally infections of certain 

potato varieties may result in the formation 

of resting spores, but without the formation 

of noticeable galls. Penetration of the parasite 

seems to occur in all potato varieties, but when 

a cell of an immune variety is penetrated it 

may die within a few hours, and since the fungus 

is a biotrophic parasite, further development is 

checked. In other cases the parasite may persist 

in the host cell for up to 2 3 days, apparently 

showing normal development, but after this 

time the fungal thallus undergoes disorganization 

and disappears from the host cell. 

Unfortunately, it has been discovered that 

new physiological races (or pathotypes) of 

the pathogen have arisen, capable of attacking 

potato varieties previously thought to be 

immune. About 20 pathotypes are now known, 

and the implications are obvious. Unless their 

spread can be prevented, much of the work of 

potato plant breeders over the past century will 

have to be started all over again. 

Other methods of control are less satisfactory. 

Attempts to kill the resting spores of the 

fungus in the soil have been made, but this is 

a costly and difficult process, requiring largescale 

fungicide applications to the soil. Copper 

sulphate or ammonium thiocyanate have been 

applied in the past at amounts of up to 1 ton 

acre 1 , and local treatment with mercuric 

chloride or with formaldehyde and steam has 

been used to eradicate foci of infection 

(Hampson, 1988). Control measures based on 

the use of resistant varieties seem more satisfactory. 

An interesting method of control developed 

in Newfoundland is the use of crabshell meal 

placed above seed tubers at the time of planting. 

This technique has resulted in significant 

and sometimes complete control (Hampson & 

Coombes, 1991) which may be due to selective 

enhancement of chitinolytic soil micro-organisms 

degrading the chitinous walls of the resting 

spores of S. endobioticum. 

Other species of Synchytrium 

Not all species of Synchytrium show the same kind 

of life cycle as S. endobioticum. Synchytrium fulgens, 

a parasite of Oenothera, resembles S. endobioticum

CHYTRIDIALES 

139 

in that both summer spores and resting spores 

are formed (Lingappa, 1958a,b), but in this 

species the zoospores from resting sporangia 

can also function as gametes and give rise 

directly to zygote infections from which further 

resting spores arise (Lingappa, 1958b). It has 

been suggested that the same phenomenon may 

occasionally occur in S. endobioticum. InS. taraxaci 

parasitic on Taraxacum (Fig. 6.8; Plate 3c), as 

well as a number of other Synchytrium spp., the 

mature thallus does not function as a prosorus 

but cleaves directly to form a sorus of sporangia, 

and the resting spore also gives rise to zoospores 

directly. In some species, e.g. S. aecidioides, 

resting sporangia are unknown, whilst in others, 

e.g. S. mercurialis, a common parasite on leaves 

and stems of Mercurialis perennis (Fig. 6.9), only 

resting sporangia are known and summer sporangial 

sori do not occur. Mercurialis plants 

collected from March to June often show 

yellowish blisters on leaves and stems. The 

blisters are galls made up of one or two layers 

of hypertrophied cells mostly lacking chlorophyll, 

surrounding the Synchytrium thallus 

during its maturation to form a resting 

sporangium. In this species the resting sporangium 

functions as a prosorus during the following 

spring. The undivided contents are extruded 

into a spherical sac which becomes cleaved into a 

sorus containing as many as 120 sporangia from 

which zoospores arise. The variations in the life 

histories of the various species of Synchytrium 

form a useful basis for classifying the genus 

(Karling, 1964). 

6.2.2 Rhizophydium 

Rhizophydium is a large, cosmopolitan genus of 

about 100 species (Sparrow, 1960) which grow 

in soil, freshwater and the sea. The thallus is 

eucarpic, with a globose epibiotic zoosporangium 

which develops from the zoospore cyst, 

and endobiotic rhizoids which penetrate the 

host. Whilst some species are saprotrophic, 

others are biotrophic pathogens of algae and 

can cause severe epidemics of freshwater phytoplankton. 

Saprotrophic forms such as R. pollinispini 

and R. sphaerocarpon colonize pollen grains 

and are easily isolated by sprinkling pollen onto 

the surface of water overlying soil (Fig. 6.10). 

Within 3 days, sporangia with exit papillae are 

Fig 6.8 Synchytrium taraxaci. 

(a) Undivided thallus in epidermal cell of 

scape of Taraxacum.Outline of host cell 

shown dotted. (b) Section of Taraxacum 

scape showing thallus divided into a sorus 

of sporangia. (c) A sorus of 

sporangia seen from above. 

Two sporangia are releasing zoospores. 

(d) A ripe sporangium. (e) Sporangium 

releasing zoospores. (f) Zoospores and 

zygotes.The triflagellate zoospore 

probably arose by incomplete 

separation of zoospore initials. 

(g) Section of host leaf showing a resting 

sporangium. (a e) and (g) to same scale.


Fig 6.9 Synchytrium mercurialis. 

(a) Section of stem of Mercurialis 

perennis showing hypertrophied cells 

surrounding a resting sporangium. 

(b) Germination of a resting 

sporangium to release a sorus of 

zoosporangia.Thus in S. mercurialis 

the resting sporangium functions as 

a prosorus (after Fischer,1892). 

Fig 6.10 Pine pollen grains 

colonized by Rhizophydium sp. 

(a) The rhizoid system attaching 

the epibiotic sporangium to the 

colonized pollen grain. (b) Mature 

sporangium; the cytoplasm has 

become cleaved into numerous 

zoospores. 

found in crude cultures on pine pollen. The 

zoospores are at first released into a hyaline 

vesicle which soon dissolves, allowing them to 

swim away. Gauriloff and Fuller (1987) have 

outlined techniques for growing R. sphaerocarpon 

in pure culture. This species can also grow 

parasitically on filaments of the green alga 

Spirogyra. 

Douglas Lake (Michigan, USA) is surrounded 

by conifers shedding pollen which floats on 

the lake and becomes colonized by Rhizophydium 

spp. Using the MPN (most probable number) 

technique, Ulken and Sparrow (1968) have 

estimated that the number of chytrid propagules 

in the surface waters (epilimnion) can rise to 

over 900 l 1 by late June. Some infected pollen 

grains sink through the hypolimnion to the mud 

at the floor of the lake. It is thought likely that 

these develop resting sporangia which survive 

the winter and provide inoculum to start off 

colonization of new pollen deposits in the 

following season. 

Rhizophydium planktonicum 

This species is the best-studied chytrid phytoplankton 

parasite. It is a biotrophic pathogen of

CHYTRIDIALES 

141 

the diatom Asterionella formosa, an inhabitant of 

eutrophic lakes. This alga forms cartwheel-like 

colonies, the diatom frustules making up the 

spokes, cemented together by mucilage pads at 

the hub of the wheel. Rhizophydium planktonicum 

may form one to many thalli on each host 

cell (Fig. 6.11a). Dual cultures of the host and 

parasite have been established (Canter & 

Jaworski, 1978) and from such cultures a detailed 

picture of infection, development and zoospore 

structure has been built up (Beakes et al., 1993). 

Zoospores are attracted to the alga and encyst 

on it, forming monocentric rhizoidal thalli. 

The rhizoids penetrate between the girdle lamellae 

of the host (Fig. 6.11b). The rhizoids may 

extend throughout the whole length of the 

host cell and infection is often accompanied 

by loss of photosynthetic pigment, failure of 

cells to divide, and ultimately early death of 

the host cell. The zoospore is uninucleate and the 

nucleus is retained within the zoospore cyst, 

the rhizoids being devoid of nuclei. The zoospore 

cyst enlarges to form the sporangium. 

Synchronous nuclear divisions result in the 

formation of several nuclei lying within the 

cytoplasm, followed by the development of 

cleavage furrows which divide up the sporangial 

contents into zoospores. A septum develops at the 

base of the sporangium and, prior to cleavage, the 

upper part of the sporangium wall develops a 

thickened apical papilla which balloons out to 

form a vesicle into which the immobile zoospores 

are released. The complete cycle from infection to 

zoospore release depends on temperature 

and can be as short as 2 3 days. About 1 30 

zoospores may be formed in a sporangium 

depending on the state of the host cells, in turn 

affected by external physical and chemical conditions. 

Breakdown of the vesicle allows the 

zoospores to swim away. No resting stage has 

been described for R. planktonicum. 

A striking feature of the zoospore ultrastructure 

is the presence of several paracrystalline 

bodies near the nucleus in the peripheral part 

of the cytoplasm (Beakes et al., 1993). They consist 

of parallel arrays of regularly arranged crystals 

interconnected to each other with fibrous 

material. They appear late in sporangial development 

but disappear following encystment 

of zoospores. Similar structures have been 

reported from the zoospores of a few other 

Chytridiomycota, but their composition and 

function are unknown. 

There have been several studies on the 

ecology of Asterionella subjected to parasitism by 

R. planktonicum (see Canter & Lund, 1948, 1953; 

Fig 6.11 Rhizophydium planktonicum 

growing parasitically on the 

frustules of the colonial diatom 

Asterionella formosa. (a) Heavily 

infected colony from a dual-clone 

culture showing encysted 

zoospores. (b) Scanning electron 

micrograph of Asterionella cells 

showing heavy infection and 

zoospore cysts which have 

germinated and penetrated the 

host cells via the girdle lamellae. 

From Beakes et al. (1993), with 

permission from Elsevier; original 

images kindly provided by G.W. 

Beakes.


Canter & Jaworski, 1981; van Donk & Bruning, 

1992). Asterionella is also parasitized by two 

other chytrids, Zygorhizidium planktonicum and 

Z. affluens, and some of the early studies in freshwater 

lakes may well have included a mixture 

of species. 

Studies on the epidemiology of infection of 

Asterionella by R. planktonicum in lakes have 

shown that there are peak periods of Asterionella 

population density both in spring and in autumn, 

related to the availability of dissolved nutrients, 

water temperature, thermal stratification and its 

breakdown, daylength and light intensity. 

Asterionella cells infected with Rhizophydium can 

occur throughout the year, but epidemics in 

which a high proportion of cells are infected only 

occur at concentrations of around 10 host cells 

ml 1 (Holfeld, 1998). Interpretation of the conditions 

conducive to the occurrence of epidemics 

has been aided by experiments using dual 

cultures of pathogen and host in which effects 

such as light intensity, temperature and phosphorus 

concentration have been varied (van Donk 

& Bruning, 1992). The effects of light are complex. 

Although Rhizophydium zoospores are not phototropic, 

they are quiescent and incapable of 

infection in the dark or at low light intensity. 

Experiments by Canter and Jaworski (1981) have 

indicated that a light intensity below 200 lx is 

inadequate for zoospore settlement on host cells. 

In light-limited cultures of Asterionella, the sporangia 

of the pathogen and hence the number of 

zoospores produced are smaller than when light 

is not limiting (Bruning, 1991a). Similarly, zoospore 

production is also reduced when the 

concentration of phosphorus limits growth of 

the host (Bruning, 1991b). Temperature affects 

the rate of sporangium development and the 

size of sporangia, with maximum dimensions 

at 2°C at fairly high light intensities (Bruning, 

1991a). It also affects the duration of swimming of 

zoospores and therefore their infective lifetime 

which can vary from about 10 days at 3°C to only 

2 days at 20°C. Epidemic development may result 

from a combination of factors and there is a 

remarkable interaction between the effects of 

light intensity and temperature (Bruning, 1991c). 

At higher temperatures, optimal conditions for 

epidemic development occur at high light 

intensities, but at temperatures below 5 6°C 

epidemic development is encouraged by lower 

light intensities. This may explain why, in nature, 

epidemics can occur both in summer (high light 

intensity, high temperature) and winter (low 

light intensity, low temperature). 

Rhizophydium planktonicum is a specialized 

parasite infecting only Asterionella. It is more 

compatible with certain clones of host cells 

than others, and cells from incompatible clones 

show hypersensitivity, undergoing rapid death 

following infection (Canter & Jaworski, 1979). 

6.2.3 Cladochytrium 

There are about a dozen species of Cladochytrium 

(Sparrow, 1960) which are widespread saprotrophs, 

mostly of aquatic plant debris. The 

thallus is eucarpic and polycentric and the 

vegetative system may bear intercalary swellings 

and septate turbinate cells (sometimes termed 

spindle organs). The sporangia are inoperculate. 

Cladochytrium replicatum is a common representative 

in decaying pieces of aquatic vegetation 

and can be distinguished from other chytrids 

by the bright orange lipid droplets found in the 

sporangia. It is frequently isolated if moribund 

aquatic vegetation is placed in a dish of water 

and baited with boiled grass leaves or cellulosic 

materials such as dialysis tubing. Lucarotti (1987) 

has given details of its isolation and growth 

in culture. The bright orange sporangia which 

are visible under a dissecting microscope 

appear on baits within about 5 days, arising 

from an extensively branched hyaline rhizomycelium 

bearing two-celled intercalary swellings. 

Sporangium development is encouraged by 

exposure to light. On release from the sporangium, 

the zoospores each contain a single orange 

lipid droplet and bear a single posterior flagellum. 

Lucarotti (1981) has described the fine 

structure of the zoospore. After swimming for 

a short time, the zoospore attaches itself to 

the surface of the substratum and puts out 

usually a single germ tube which can penetrate 

the tissues of the host plant. The germ tube 

expands to form an elliptical or cylindrical 

turbinate cell which is often later divided into 

two by a transverse septum (Fig. 6.12d). The

CHYTRIDIALES 

143 

zoospore is uninucleate and during germination 

the single nucleus is transferred to the 

swollen turbinate cell which becomes a vegetative 

centre from which rhizoids are put out 

which in turn produce further turbinate cells 

(see Figs. 6.12b,d). Nuclear division is apparently 

confined to the turbinate cells, and although 

nuclei are transported through the rhizoidal 

system they are not resident there. The thallus 

so established branches profusely, and at certain 

points spherical zoosporangia form, 

either terminally or in intercalary positions. 

Sometimes one of the cells of a pair of turbinate 

cells swells and becomes transformed into a 

sporangium. In culture, both cells may 

be modified in this way. The spherical to pearshaped 

zoosporangium undergoes progressive 

nuclear division, and the contents of the sporangium 

acquire a bright orange colour due 

to accumulation of lipid droplets containing 

the carotenoid lycopene. These lipid reserves are 

later found in the zoospores. Cleavage of the 

cytoplasm to form uninucleate zoospore initials 

follows. The zoospores escape through a narrow 

Fig 6.12 Cladochytriumreplicatum. 

(a) Rhizomycelium within the epidermis 

of an aquatic plant bearing the 

two-celled hyaline turbinate cells and 

globose orange zoosporangia. (b) 

Rhizomycelium and turbinate cells from 

a culture. (c) Zoosporangia from a 

two-week-old culture. One 

zoosporangium has released zoospores, 

each of which contains a bright orangecoloured 

globule. (d) Germinating 

zoospores on boiled wheat leaves. 

The empty zoospore cysts are spherical. 

The germ tubes have expanded to form 

turbinate cells. (e) A zoosporangium 

which has proliferated internally to form 

a second sporangium. (f) Rhizomycelium 

within a boiled wheat leaf bearing a 

thick-walled, spiny resting sporangium.


exit tube which penetrates to the exterior of 

the substratum and becomes mucilaginous at 

the tip. There is no operculum. Sometimes 

zoosporangia may proliferate internally, a new 

zoosporangium being formed inside the wall of 

an empty one. Resting sporangia with thicker 

walls and a more hyaline cytoplasm are also 

formed either terminally or in an intercalary 

position on the rhizomycelium. In some cases 

the wall of the resting sporangium is reported 

to be smooth and in others spiny, and it has 

been suggested (Sparrow, 1960) that the two 

kinds of resting sporangia may belong to different 

species. However, studies by Willoughby 

(1962) of a number of single-spore isolates have 

shown that the presence or absence of spines is 

a variable character. The contents of the resting 

sporangia divide to form zoospores which also 

have a conspicuous orange droplet, and escape 

by means of an exit tube as in the thin-walled 

zoosporangia. Whether the resting sporangia are 

formed as a result of a sexual process is not 

known. Pure cultures of C. replicatum have been 

studied by Willoughby (1962), Goldstein (1960) 

and Lucarotti (1981). The fungus is heterotrophic 

for thiamine. Biotin, while not absolutely 

required, stimulates growth. Nitrate and sulphate 

are utilized, as are a number of different 

carbohydrates; a limited amount of growth takes 

place on cellulose. 

6.2.4 Nowakowskiella 

Species of Nowakowskiella are widespread saprotrophs 

in soil and on decaying aquatic plant 

debris, and can be obtained by baiting aquatic 

plant remains in water with boiled grass 

leaves, cellophane, dialysis tubing and the like. 

Nowakowskiella elegans is often encountered in 

such material, and pure cultures can be obtained 

and grown on cellulosic materials overlying 

agar, or directly in liquid culture media 

(Emerson, 1958; Johnson, 1977; Lucarotti, 1981; 

Lucarotti & Wilson, 1987). In culture, considerable 

variation in growth habit and morphology 

can result from changing the concentration of 

nutrients and the availability of water (Johnson, 

1977). In boiled grass leaves the fungus forms an 

extensive rhizomycelium with turbinate cells 

(Fig. 6.13c). Zoosporangia are formed terminally 

or in an intercalary position (Fig. 6.13c) and 

are globose or pear-shaped with a subsporangial 

swelling (apophysis), and granular or refractile 

hyaline contents. At maturity some sporangia 

develop a prominent beak, but in others this 

is not present. When an operculum becomes 

detached, zoospores escape and initially remain 

clumped together at the mouth of the sporangium 

(Figs. 6.13b,c). The fine structure of the 

zoospore is very similar to that of Rhizophydium 

but paracrystalline bodies have not been observed 

(Lucarotti, 1981). It also has close resemblance 

to the zoospore ultrastructure of the inoperculate, 

polycentric Cladochytrium replicatum. 

Yellowish resting sporangia (Fig. 6.13e) have 

been described (Emerson, 1958; Johnson, 1977; 

Lucarotti & Wilson, 1987). They develop as 

spherical to fusiform swellings in the rhizomycelium 

which become delimited by septa, develop 

thick walls and a large central vacuole 

surrounded by dense cytoplasm with small 

spherical lipid droplets. The resting sporangium 

is at first binucleate. After nuclear fusion the 

diploid nucleus divides meiotically. Further 

nuclear divisions are mitotic and the contents 

of the resting sporangium cleave into zoospores 

which may be released through a papilla in 

the sporangium wall. Alternatively, the resting 

sporangium may give rise to a thin-walled zoosporangium 

from which the zoospores are 

released, i.e. the resting sporangium may function 

as a prosporangium as in some other chytrids 

( Johnson, 1977). 

In N. profusa, which is probably synonymous 

with N. elegans (Johnson, 1977), three kinds of 

sporangial dehiscence have been described: 

exo-operculate, in which the operculum breaks 

away to the outside of the sporangium; endooperculate, 

in which the operculum remains 

within the sporangium; and inoperculate, 

where the exit papilla opens without any clearly 

defined operculum (Chambers et al., 1967; 

Johnson, 1973). Such variations within a single 

chytrid strain add emphasis to criticisms of 

the value of dehiscence as a primary criterion in 

classification. 

Goldstein (1961) has reported that N. elegans 

requires thiamine and can utilize nitrate,

SPIZELLOMYCETALES 

145 

Fig 6.13 Nowakowskiella elegans. 

(a) Polycentric mycelium bearing 

zoosporangia. (b) Empty zoosporangia 

showing opercula. (c) Mycelium showing 

turbinate cells and zoosporangia. 

(d) Zoospores from culture. (e) Resting 

sporangium from culture. 

sulphate and a number of carbohydrates including 

cellulose, but cannot utilize starch. 

6.3 Spizellomycetales 

Members of this order differ from the 

Chytridiales in possessing zoospores which 

contain more than one lipid droplet and are 

capable of limited amoeboid movement. Thalli 

are generally monocentric. The order takes its 

name from the genus Spizellomyces which in turn 

was named in honour of the chytrid pioneer 

F. K. Sparrow after Spizella, a genus of North 

American sparrows (Barr, 1980). Some 86 species 

of Spizellomycetales are currently recognized. 

6.3.1 Olpidium 

About 30 species of Olpidium are known, but 

the genus is in need of revision and possibly


some of the species should be classified elsewhere. 

Typical species are holocarpic. Some are 

parasitic on fungi and aquatic plants or algae, 

or saprotrophic on pollen (Sparrow, 1960). 

Others parasitize rotifers (Glockling, 1998), 

nematodes and their eggs (Tribe, 1977; Barron 

& Szijarto, 1986), moss protonemata or leaves 

and roots of higher plants (Macfarlane, 1968; 

Johnson, 1969). Olpidium bornovanus (¼ O. radicale) 

develops on various monocotyledonous and 

dicotyledonous plant roots following inoculation 

(Lange & Insunza, 1977). Olpidium brassicae is 

common on the roots of cabbages, especially 

when growing in wet soils, and is also found on 

a wide range of unrelated hosts, but some 

host specialization has been reported. Both 

O. bornovanus and O. brassicae are vectors of a 

number of plant viruses (Barr, 1988; Adams, 

1991; Hiruki, 1994; Campbell, 1996) and this 

topic is discussed more fully below. Weber and 

Webster (2000a) have given practical details of 

how to grow O. brassicae for observation on 

Brassica seedlings. A film featuring O. brassicae is 

also available (Webster, 2006a). 

Epidermal cells and root hairs of infected 

cabbage roots contain one or more spherical or 

cylindrical thalli, sometimes filling the whole 

cell (Fig. 6.14a). The cytoplasm of the thallus 

is granular and the entire contents divide into 

numerous posteriorly uniflagellate zoospores 

that escape through one or more discharge 

tubes which penetrate the outer wall of the 

host cell (Temmink & Campbell, 1968). Release of 

the zoospores takes place within a few minutes 

of washing the roots free from soil. The tip of 

the discharge tube breaks down and zoospores 

rush out and swim actively in the water. The 

zoospores are very small, tadpole-like, with 

Fig 6.14 Olpidium brassicae in cabbage 

roots. (a) Two ripe sporangia and one 

empty sporangium in an epidermal cell. 

Each sporangium has a single exit tube. 

(b) Empty sporangium showing three exit 

tubes. (c) Zoospores. (d) Zoospore cysts 

on a root hair. Note that some cysts are 

uninucleate and some are binucleate. 

(e) Resting sporangia. (a,b,d,e) to same 

scale.


147 

Fig 6.15 Olpidium brassicae. 

Diagrammatic representation of 

L.S. of zoospore (afterTemmink & 

Campbell,1969a). 

a spherical head and a long trailing flagellum. 

The fine structure of the zoospore is summarized 

in Fig 6.15. A distinctive feature is the banded 

rhizoplast which connects the kinetosome to 

the nucleus (Temmink & Campbell, 1969a; 

Lange & Olson, 1976a,b; Barr & Hartmann, 

1977). This structure has also been reported 

from the zoospore of the eucarpic chytrid 

Rhizophlyctis rosea (see p. 148; Barr & Hartmann, 

1977). 

The zoospores swim actively in water for 

about 20 min. If roots of cabbage seedlings are 

placed in a suspension of zoospores, these settle 

on the root hairs and epidermal cells, withdraw 

their flagella and encyst. The cysts are attached 

by a slime-like adhesive (Temmink & Campbell, 

1969b). The cyst wall and the root cell wall at 

the point of attachment are dissolved and 

the root cell is penetrated. The cyst contents 

are transferred to the inside of the host cell, 

probably by the enlargement of a vacuole which 

develops inside the cyst, whilst the empty cyst 

remains attached to the outside. The process 

of penetration can take place in less than 

one hour (Aist & Israel, 1977). Within 2 days of 

infection, small spherical thalli can be seen in 

the root hairs and epidermal cells of the root, 

carried around the cell by cytoplasmic streaming. 

The thalli enlarge and become multinucleate. 

Within 4 5 days discharge tubes develop 

and the thalli are ready to release zoospores. 

In some infected roots, stellate bodies with 

thick folded walls, lacking discharge tubes, 

are also found (Fig. 6.14e). These are resting 

sporangia. There is no evidence that they are 

formed as a result of sexual fusion either in 

O. brassicae or in O. bornovanus (Barr, 1988). 

Although biflagellate zoospores may occur in 

O. brassicae, these possibly result from incomplete 

cleavage (Temmink & Campbell, 1968) and 

zoospores with as many as 6 flagella have been 

observed (Garrett & Tomlinson, 1967). The resting 

sporangia are capable of germination 

7 10 days after they mature, and germinate by 

the formation of one or two exit papillae 

through which the zoospores escape. 

Virus transmission by Olpidium 

Several plant viruses are transmitted by zoospores 

of Olpidium. By analogy with plant virus 

transmission by aphids, Adams (1991) arbitrarily


distinguished viruses with non-persistent and 

persistent transmission by fungi, although 

Campbell (1996) objected to the use of these 

terms, distinguishing instead between viruses 

which can be acquired in vitro (i.e. outside the 

plant) and those that can only be acquired in vivo 

(within the host cell). 

Tobacco necrosis virus (TNV) and cucumber 

necrosis virus (CNV) are non-persistent viruses 

which can be acquired in vitro by zoospores 

of O. brassicae or O. bornovanus (respectively). 

Virus particles (virions) are adsorbed onto the 

plasmalemma of the zoospore and onto the 

flagellar axonemal sheath which is continuous 

with it (Temmink et al., 1970). Binding seems to 

occur between the virus coat and specific molecules 

at the zoospore surface, possibly oligosaccharide 

side chains of proteins (Kakani et al., 

2003; Rochon et al., 2004). When the flagellum is 

withdrawn into the body of the zoospore at 

encystment, virus particles are introduced into 

the fungal cytoplasm and are then transmitted 

into the plant upon infection. Air-dried roots 

containing TNV virus and O. brassicae resting 

sporangia, or living virus-infected roots with 

resting sporangia treated with 5N HCl, were 

incapable of transmitting virus even though 

the resting sporangia survived these treatments, 

indicating that TNV is not carried inside the 

resting sporangia (Campbell & Fry, 1966). 

Lettuce big vein virus, LBVV, in contrast, is 

an example of the persistent type (Grogan 

et al., 1958). In this case it has been shown that 

the virus can persist in air-dried resting sporangia 

for 18 20 years (Campbell, 1985). Here 

the virions are acquired in vivo and they are 

present inside the zoospores which emerge from 

sporangia and resting sporangia (Campbell, 

1996). 

Classification of Olpidium 

Although previously classified within the 

family Olpidiaceae in the order Chytridiales, 

D. J. S. Barr (2001) has placed Olpidium in the 

order Spizellomycetales along with Rhizophlyctis 

on the basis of similarities in zoospore structure. 

Ribosomal DNA sequence comparisons are 

inconclusive in that they do not show any close 

similarity between Olpidium and either Chytridium 

or Spizellomyces (Ward & Adams, 1998). 

6.3.2 Rhizophlyctis 

There are about 10 known species of Rhizophlyctis 

with monocentric eucarpic thalli, growing as 

saprotrophs on a variety of substrata in soil, 

freshwater and the sea. Rhizophlyctis rosea grows 

on cellulose-rich substrata in soil, and it probably 

plays an active but currently underestimated 

role in cellulose decay (Powell, 1993). It can 

survive for prolonged periods in dry soil, even 

when this is heated to 90°C for two days (Gleason 

et al., 2004) and, in fact, the recovery of R. rosea 

is greatly enhanced if soil samples are air-dried 

prior to isolation experiments (Willoughby, 

2001). Willoughby (1998b) has estimated that 

over 1000 thallus-forming units could be recovered 

per gram of air-dry soil or leaf humus 

fragments from Provence, France. These numbers 

may arise from one or a few sporangia, since 

a single sporangium about 100 mm in diameter 

may discharge up to 30 000 zoospores. Mitchell 

and Deacon (1986) have shown that zoospores 

of R. rosea accumulate preferentially on cellulosic 

materials. 

The fungus is readily isolated and grown 

in culture, and details of techniques have 

been provided by Stanier (1942), Barr (1987), 

Willoughby (1998b) and Weber and Webster 

(2000a). The placing of a small crumb of soil 

onto moist tissue paper or cellophane overlying 

agar containing mineral salts, or the floating 

of squares of cellophane on water containing 

a soil sample, are followed within a few days 

by the development of thalli with bright pink 

sporangia. The sporangia are attached to coarse 

rhizoids which arise at several points on the 

sporangial wall and extend throughout the 

cellulosic substratum, tapering to fine points. 

Extensive corrosion of the substrate underneath 

the thallus and rhizoids points at the secretion 

of powerful cellulases (Fig. 6.17). 

Although the fungus is usually monocentric, 

there are also records of some polycentric 

isolates. When ripe, the sporangia have pink 

granular contents which differentiate into 

numerous uninucleate posteriorly uniflagellate


149 

zoospores (Fig. 6.16a). One to several discharge 

tubes are formed, and the tip of each tube 

contains a clear mucilaginous plug which, prior 

to discharge, is exuded in a mass from the tip of 

the tube (Fig. 6.16c). While the plug of mucilage 

dissolves, the zoospores within the sporangium 

show active movement and then escape by 

swimming through the tube. In some specimens 

of R. rosea it has been found that a membrane 

may form over the cytoplasm at the base of 

the discharge tubes. If the sporangia do not 

discharge their spores immediately, the membrane 

may thicken. When spore discharge 

occurs, these thickened membranes can be seen 

floating free within the sporangia, and the term 

endo-operculum has been applied to them. The 

genus Karlingia was erected for forms possessing 

such endo-opercula, including R. rosea, which 

is therefore sometimes referred to as Karlingia 

rosea, but the validity of this separation is 

questionable because the presence or absence 

of endo-opercula is a variable character 

(Blackwell & Powell, 1999). 

Zoospores of R. rosea are capable of swimming 

for several hours. The head of the zoospore is 

often globose, but can become pear-shaped or 

show amoeboid changes in shape. It contains a 

prominent lipid body, several bright refringent 

globules, and bears a single trailing flagellum. 

Ultrastructural details resemble those of 

Olpidium brassicae in the presence of a striated 

rhizoplast connecting kinetosome and nucleus 

(Barr & Hartmann, 1977). On coming to rest on 

a suitable substratum, the flagellum is withdrawn 

and the body of the zoospore enlarges 

to form the rudiment of the sporangium, whilst 

rhizoids appear at various points on its surface. 

Within the sporangium, the flagella are tightly 

wrapped around the zoospores (Chambers 

& Willoughby, 1964). 

Resting sporangia are also found. They are 

brown, globose or angular and have a thickened 

Fig 6.16 Rhizophlyctisrosea. (a) Zoospores. (b) Young thallus formed on germination of zoospore.The zoospore cyst has enlarged 

and will form the sporangium. (c) Older sporangium showing three discharge tubes. (d) Sporangium showing mucilage plugs at the 

tips of the discharge tubes and thickenings of the cell membrane at the bases of the tubes. Such thickenings are termed 

endo-opercula. (e) Globose sporangium and seven visible papillae. (f) Resting sporangium formed inside an empty zoosporangium. 

(a,b) to same scale; (c f) to same scale.


Fig 6.17 Scanning electron 

micrograph of two thalli of 

Rhizophlyctisrosea on a cellophane 

membrane. Pit corrosion is visible 

where a thallus has been lifted 

from the substratum (arrows). 

wall (Fig. 6.16f ). Whether they are formed 

sexually in R. rosea is not known. Couch (1939) 

has, however, put forward evidence that the 

fungus is heterothallic because single isolates 

grown in culture failed to produce resting 

sporangia whereas these structures did form 

when certain cultures were paired. Stanier (1942) 

has reported the occurrence of biflagellate zoospores, 

but whether these represented zygotes 

seemed doubtful. In the homothallic chitinophilic 

fungus Rhizophlyctis oceanis, Karling (1969) 

has described frequent fusions between zoospores. 

These fusions are possibly sexual, but 

unfortunately Karling was unable to cultivate 

the resulting thalli to the stage of resting spore 

development. 

On germination, the resting sporangium of 

R. rosea functions as a prosporangium, although 

it is uncertain whether resting sporangia are 

important for survival in nature. Willoughby 

(2001) has shown that R. rosea could be recovered 

from cellophane baits in as little as 5 6 h after 

placing air-dried soil samples in water, and it 

was concluded that these zoospores were derived 

from sporangia instead of resting spores which 

need a longer time to produce zoospores. 

The nutritional requirements of R. rosea are 

simple. It shows vigorous growth on cellulose 

as the sole carbon source but it can utilize 

a range of carbohydrates such as glucose, 

cellobiose and starch. The pink colour of the 

sporangia is due to the presence of carotenoid 

pigments such as g-carotene, lycopene and a 

xanthophyll. 

6.4 Neocallimastigales 

(rumen fungi) 

A very interesting and unusual group of zoosporic 

fungi inhabits the rumens (foreguts) of 

ruminants (herbivorous mammals which regurgitate 

and masticate previously ingested food) 

like cows, sheep and deer. They have also been 

found in some non-ruminants such as horses and 

elephants and probably occur in the guts of 

many large herbivores. These fungi are obligate 

anaerobes which can flourish in the rumen 

because oxygen is depleted there by the intense 

respiratory activity of a dense population of 

protozoa and bacteria, some of which are 

facultative anaerobes capable of scavenging free 

oxygen. Their zoospores were at first thought to 

be protozoa and were not recognized as belonging 

to fungi because obligately anaerobic fungi

NEOCALLIMASTIGALES (RUMEN FUNGI) 

151 

were not believed to exist. Further, microbiologists 

working on microbes from the ruminant 

gut studied only strained rumen fluid and 

therefore failed to see the thalli of fungi attached 

to herbage fragments. The view that the motile 

cells swimming in rumen fluid belonged to 

flagellates was challenged by Orpin (1974), who 

observed that there was an enormous increase in 

the concentration of ‘flagellates’ in the rumen of 

sheep within a short time of feeding. The ratio of 

minimum (pre-feeding) to maximum concentration 

of motile cells could vary between 1:15 and 

1:296 (average 1:47), and if these were organisms 

reproducing by binary fission it would be 

necessary for them to undergo six successive 

cell divisions in 15 min. The explanation for the 

rapid increase in motile cells is that sedentary 

fungal thalli, anchored by rhizoids to partially 

digested food fragments floating in the rumen, 

are stimulated to release zoospores by soluble 

substances such as haems released from the 

newly ingested food material. The zoospores 

attach themselves in large numbers to the 

herbage fragments, and germinate to form 

rhizoidal or rhizomycelial thalli with sporangia 

capable of releasing further zoospores within 

about 30 h. 

Some 5 genera and 15 species have now been 

distinguished (Theodorou et al., 1992, 1996; 

Trinci et al., 1994). They include Caecomyces 

which has mono- and polycentric thalli, 

Anaeromyces and Orpinomyces with polycentric 

thalli, and Piromyces and Neocallimastix which 

are monocentric. The zoospores of Anaeromyces, 

Caecomyces and Piromyces are uniflagellate 

whilst those of Neocallimastix and Orpinomyces 

are multiflagellate (see Fig. 6.18). They were 

classified within the order Spizellomycetales, 

family Callimasticaceae by Heath et al. (1983) 

and Barr et al. (1989) but are now placed in a 

separate order Neocallimastigales (Li et al., 1993; 

D. J. S. Barr, 2001). Special techniques and media 

are needed for isolating and handling anaerobic 

fungi, but the life cycle details of several have 

now been followed in pure culture. One of the 

best known is N. hurleyensis, isolated from sheep 

(Fig. 6.18). Minutes after the arrival of fresh 

food, globose ripe zoosporangia on previously 

colonized grass fragments release zoospores 

through an apical pore and these attach themselves 

to herbage fragments and germinate to 

produce rhizoids which penetrate and digest the 

ingested plant material. The walls of the thallus 

contain chitin. A single zoosporangium develops 

and is cut off from the rhizoidal system by 

a septum. The rhizoidal part is devoid of nuclei, 

but within the zoosporangium repeated nuclear 

divisions occur before the cytoplasm cleaves 

to form 64 128 zoospores. The life cycle of 

N. hurleyensis from zoospore germination to the 

release of a fresh crop of zoospores lasts about 

29 31 h at 39°C (Lowe et al., 1987a). The 

zoospores bear 8 16 whiplash flagella inserted 

posteriorly in two rows. 

The ultrastructure of zoospores has been 

described for several species of Neocallimastix, 

including N. patriciarum (Orpin & Munn, 1986), 

N. frontalis (Munn et al., 1981; Heath et al., 1983) 

and N. hurleyensis (Webb & Theodorou, 1988, 

1991). There are differences in detail. For 

example, the zoospore of N. frontalis has a waistlike 

constriction, with the majority of the cytoplasmic 

organelles concentrated in the posterior 

portion near the insertion of the flagella. 

Characteristic organelles known from zoospores 

of aerobic chytridiomycetes such as mitochondria, 

Golgi bodies, lipid droplets or gamma 

particles (seen in zoospores of Blastocladiella 

emersonii; Fig. 6.19) are absent. In the posterior 

portion of the zoospore of N. hurleyensis near the 

point of insertion of the flagella, an irregularly 

shaped complex structure interpreted as a 

hydrogenosome has been reported in place of a 

mitochondrion. In zoospores of N. patriciarum 

there are many presumed hydrogenosomes 

concentrated around the region of flagellar 

insertion. Hydrogenosomes are organelles 

capable of the anaerobic metabolism of hexoses 

to acetic and formic acids. Protons (H þ ) act as 

electron acceptors, so that gaseous H 2 is released 

by the activity of the enzyme hydrogenase 

(Müller, 1993; Boxma et al., 2004). The hydrogen, 

in turn, is used by anaerobic methanogenic 

bacteria to reduce CO 2 to CH 4 (methane) which 

escapes in profusion through the front and hind 

exits of the ruminant digestive tracts. 

Hydrogenosomes are found in several anaerobic 

lower eukaryotes and are believed to be derived


Fig 6.18 Neocallimastix hurleyensis. (a) Rhizoidal 

thallus with zoosporangium. (b) Release of 

zoospores. (c) Tracing of T.E.M. of zoospore 

with 14 flagella in longitudinal section. 

Diagrams based on Webb and 

Theodorou (1991). 

from mitochondria (Embley et al., 2002). Whereas 

mitochondria of most fungi contain a limited 

amount of DNA, hydrogenosomes of rumen 

chytrids seem to have lost their genome altogether 

(Bullerwell & Lang, 2005). 

Granular inclusion bodies which contain 

aggregates of ribosome-like particles and also 

free ribosome-like arrays are found anterior to 

the nucleus. Rosettes of glycogen represent the 

energy reserve of the zoospore. The shafts of 

the flagella contain the familiar eukaryotic 9 þ 2 

arrangement of microtubules, but in N. frontalis 

the microtubules do not extend into the tips 

of the flagella which are narrower than the 

proximal part. 

Ecologically, these anaerobic fungi play an 

important role in the early colonization of 

ingested herbage and have a wide range of 

enzymes which enable them to utilize monosaccharides, 

disaccharides and polysaccharides 

such as xylan, cellulose, starch and glycogen 

(Theodorou et al., 1992). They may play an active 

role in fibre breakdown. It is likely that colonization 

of straw particles by these fungi aids further 

attack by bacteria. The survival of anaerobic 

fungi outside the unusual and protective environment 

of the herbivore gut occurs in dried 

faeces in the form of cysts or as melanized 

thick-walled thalli whilst transmission to young 

animals takes place in saliva during licking

BLASTOCLADIALES 

153 

and grooming (Lowe et al., 1987b; Wubah et al., 

1991; Theodorou et al., 1992). 

6.5 Blastocladiales 

6.5.1 Introduction 

Species belonging to the Blastocladiales are 

mostly saprotrophs in soil, water, mud or aquatic 

plant and animal debris, and some are pathogens 

of plants, invertebrate animals or fungi. Most 

are obligate aerobes, but Blastocladia spp. are 

facultatively anaerobic, requiring a fermentable 

substrate and growing on submerged fleshy 

fruits, twigs or other plant materials rich in 

soluble carbohydrates (Emerson & Robertson, 

1974). The life cycles of Blastocladiales show 

great variations and in some forms there is an 

alternation of distinct haploid gametothallic 

and diploid sporothallic generations. These 

terms are used in preference to the botanical 

terms gametophytic and sporophytic. Species 

of Physoderma, previously grouped with the 

Chytridiales (Lange & Olson, 1980), are biotrophic 

parasites of higher plants (Karling, 1950). They 

include P. maydis, the cause of brown spot of 

maize, and P. alfalfae (Lange et al., 1987). One 

genus, Coelomomyces, consists of obligate parasites 

of insects, usually mosquito larvae (Couch & 

Bland, 1985). This genus is unusual in that 

the vegetative thallus is a wall-less plasmodiumlike 

structure lacking rhizoids. The life cycle 

is completed in unrelated alternate animal 

hosts, sporothalli occurring in mosquito larvae 

(Insecta) and gametothalli in a copepod 

(Crustacea) (Whisler et al., 1975; Federici, 1977). 

Attempts are being made to use Coelomomyces 

in the biological control of mosquitoes. Catenaria 

anguillulae, a facultative parasite of nematodes 

and their eggs, liver fluke eggs and some other 

invertebrates, can be grown in culture (Couch, 

1945; Barron, 1977; Barstow, 1987), whilst 

Catenaria allomycis is a biotrophic parasite of 

Allomyces (Couch, 1945; Sykes & Porter, 1980). 

With the exception of Coelomomyces, the 

thallus of members of the Blastocladiales is 

eucarpic. The morphologically simpler forms 

such as Blastocladiella (Fig. 6.22) are monocentric, 

with a spherical or sac-like zoosporangium or 

resting sporangium arising directly or on 

a short one-celled stalk from a tuft of radiating 

rhizoids. These simpler types show considerable 

similarity to monocentric Chytridiales of 

other orders such as Rhizophlyctis rosea (Figs. 6.16 

and 6.17), and in the vegetative state they 

may be difficult to distinguish. The more 

complex organisms such as Allomyces are polycentric, 

and the thallus is differentiated into 

a trunk-like portion which has rhizoids below 

whilst branching above, often dichotomously, 

and bearing sporangia of various kinds at the 

tips of the branches. Chitin has been demonstrated 

in the walls of Allomyces and Blastocladiella 

(Porter & Jaworski, 1966; Youatt, 1977; Maia, 

1994). 

The zoospore of Blastocladiales 

The zoospore of Blastocladiales has a single 

posterior flagellum of the whiplash type. 

Details of the fine structure of this kind of 

zoospore have been reviewed by Fuller (1976) 

and Lange and Olson (1979). The best known 

are Blastocladiella emersonii (Cantino et al., 1963; 

Reichle & Fuller, 1967) and Allomyces macrogynus 

(Fuller & Olson, 1971). The structure of the 

zoospore of B. emersonii is summarized diagrammatically 

in Fig. 6.19. The zoospore is tadpolelike 

with a pear-shaped head about 7 9 mm and 

a single, trailing flagellum about 20 mm long. 

Under the light microscope, the most conspicuous 

internal structure is the dense crescentshaped 

nuclear cap which surrounds the more 

transparent nucleus. The nuclear cap is rich in 

RNA and protein, and is filled with ribosomes. 

The zoospore of B. emersonii is unusual in that 

it contains only a single large mitochondrion, 

situated near the flagellar kinetosome. 

The organization of the flagellum is essentially 

as described on p. 129. The nine triplet 

microtubules extend in a funnel-shaped manner 

from the proximal end of the kinetosome 

towards the nucleus and nuclear cap, maintaining 

its conical shape. Extending into the mitochondrion 

and linking up the kinetosome


Fig 6.19 Blastocladiella emersonii zoospore, 

fine structure, diagrammatic and not to scale. 

(a) L.S. of zoospore along the axis of the 

flagellum. (b) T.S. of kinetosome showing nine 

triplets of microtubules. (c) T.S. of kinetosome 

at a slightly lower level showing the origin of 

two of the banded rootlets which extend 

into the mitochondrion.The cristae of the 

mitochondrion are close to the membrane 

which surrounds the banded rootlets. 

(d) T.S. of axoneme showing the nine paired 

peripheral microtubules and the two central 

microtubules. 

with it are three striated bodies variously 

referred to as flagellar rootlets, striated rootlets 

or banded rootlets. They are contained within 

separate channels, and each is surrounded by 

a unit membrane. Since the energy for propulsion 

is generated within the mitochondrion, it is 

possible that the banded rootlets are, in some 

way, responsible for transmitting energy to the 

base of the axoneme. It is also possible that the 

banded rootlets serve to anchor the flagellum 

within the body of the zoospore. 

There are two other obvious kinds of organelle 

within the body of the Blastocladiella zoospore. 

The lipid sac attached to the mitochondrion 

contains a group of lipid droplets which is 

surrounded by a unit membrane. It is not 

known whether lipid forms the energy reserve 

used in swimming, cytoplasmic glycogen deposits 

being a more plausible alternative (Cantino 

et al., 1968). In the anterior of the zoospore 

between the nuclear cap and the plasma 

membrane, there is a group of granules about 

0.5 mm in diameter, called gamma particles. 

They consist of an inner core, shaped like 

an elongated cup and bearing two unequal 

openings at opposite sides of the cup. This cupshaped 

structure is enveloped in a unit membrane 

(Myers & Cantino, 1974). Gamma particles 

are only present in developing and motile 

zoospores but disappear as the zoospore encysts. 

Formerly thought to represent the chytrid 

equivalent of the chitosome found in higher 

fungi (see p. 6), this notion has now been 

discarded (Hohn et al., 1984).


155 

The zoospore of Allomyces macrogynus broadly 

resembles that of B. emersonii (Fuller & Olson, 

1971). Gamma particles are present in the 

zoospore and, during encystment, these form 

vesicles which fuse with the plasma membrane. 

Fusion coincides with the appearance of 

wall material around the cyst (Barstow & 

Pommerville, 1980). The zoospore of Allomyces 

differs from that of Blastocladiella in some other 

ways. Although there is a large basal mitochondrion, 

many smaller mitochondria are also 

present, generally located along the membrane 

of the nuclear cap in the anterior part of the 

cell. A complex structure situated laterally at 

the base of the body of the zoospore, between 

the nucleus and the zoospore membrane, has 

been termed the side body complex by Fuller 

and Olson (1971). It consists of two closely 

appressed membranes separated by an electronopaque 

material. These membranes subtend 

numerous electron-opaque, membrane-bound 

bodies, lipid bodies and a portion of the basal 

mitochondrion. In addition, there are membrane-bound 

non-lipid bodies termed Stüben 

bodies by Fuller and Olson (1971), whose function 

and composition are uncertain. 

The zoospore is propelled forward by rhythmic 

lashing of the flagellum, and it can swim 

for a period even under anaerobic conditions. 

It is also capable of amoeboid changes of shape. 

On coming to rest, the flagellum is retracted 

into the body of the zoospore. There are different 

interpretations of the manner in which flagellar 

retraction is achieved. Cantino et al. (1968) 

have suggested that the flagellum is retracted 

by a revolving action of the nucleus, whereas 

in the ‘lash-around’ mechanism the flagellum 

coils around the body of the spore, the flagellar 

membrane fuses with the plasmalemma of 

the spore and the axoneme enters the spore 

cytoplasm (Olson, 1984). In Allomyces, the zoospore 

cyst produces, at one point, a narrow germtube 

which branches to form the rhizoidal 

system. At the opposite pole, the zoospore cyst 

forms a wider germ tube which gives rise to 

hyphae which branch and later bear sporangia. 

This bipolar germination pattern is a point 

of difference between the Blastocladiales and 

the Chytridiales, in which germination is 

typically unipolar. The rhizoids are strongly 

chemotropic and specialize in nutrient uptake 

and transport. An inwardly directed electrical 

current has been detected around the rhizoids, 

and an outwardly directed current around 

the hyphae and hyphal tips. The inward current 

at the rhizoids may be the consequence of 

localized proton-driven solute transport 

(de Silva et al., 1992). 

Life cycles of Blastocladiales 

A number of distinct life history patterns are 

found. In Allomyces arbuscula, for example, isomorphic 

alternation of haploid gametothallic 

and diploid sporothallic generations has been 

demonstrated. In A. neo-moniliformis (¼ A. cystogenes) 

there is no free-living sexual generation, 

but this stage is represented by a cyst (see 

below). In A. anomalus, only the asexual stage 

has been found in normal cultures, but experimental 

treatments may result in the development 

of sexual thalli. Similar variations in life 

cycles have been found in other genera such 

as Blastocladiella. A characteristic feature of 

the asexual thalli of the Blastocladiales is the 

presence of resting sporangia with chitinous, 

pitted walls impregnated with a dark brown, 

melanin-type pigment. The pits are inwardly 

directed conical pores in the wall. The inner 

ends of the pores abut against a smooth, colourless 

inner layer of wall material surrounding 

the cytoplasm (Skucas, 1967, 1968). The resting 

sporangia of Allomyces can remain viable for up 

to 30 years in dried soil. The ease with which 

certain members of the group can be grown 

in culture has facilitated extensive studies of 

their nutrition and physiology, and the results 

of some of these investigations are discussed 

below. 

Four families have been recognized 

Coelomomycetaceae, Catenariaceae, Physodermataceae 

and Blastocladiaceae but of these we 

shall study only Allomyces and Blastocladiella, 

both representatives of the Blastocladiaceae. 

6.5.2 Allomyces 

Species of Allomyces are found in mud or soil of 

the tropics or subtropics, including desert soil,


and if dried samples of soil are placed in water 

and ‘baited’ with boiled hemp seeds, the baits 

may become colonized by zoospores. From such 

material, it is possible to obtain pure cultures by 

streaking or pipetting zoospores onto suitable 

agar media and to follow the complete life 

history of these fungi in the laboratory. Olson 

(1984) has given a full account of the taxonomy, 

life cycles, morphogenesis and genetics of 

different species of Allomyces, with practical 

details of how to grow and handle them. Good 

growth occurs on a medium containing yeast 

extract, peptone and soluble starch (YPsS), but 

chemically defined media have also been used. 

There is a requirement for thiamine and organic 

nitrogen in the form of amino acids. 

Emerson (1941) isolated species of Allomyces 

from soil samples from all over the world. He 

distinguished three types of life history, represented 

by three subgenera. 

Sub-genus Eu-Allomyces 

The Eu-Allomyces type of life history is exemplified 

by A. arbuscula and A. macrogynus (Fig. 6.21; for 

a film, see Webster & Hard, 1998a). Resting 

sporangia are formed on asexual diploid thalli. 

They contain about 12 nuclei which undergo 

meiosis during the early stages of germination 

(Olson, 1974). The cytoplasm cleaves around the 

48 haploid nuclei to form the zoospores. Since 

meiosis occurs in the resting sporangia, these 

have been termed meiosporangia, and the 

haploid zoospores meiospores. The meiospores 

are released when the outer wall of the brown 

pitted resting sporangium cracks open by a slit 

and the inner wall balloons outwards and 

eventually opens by one or more pores. The 

meiospores swim by movement of the trailing 

flagellum and, on coming to rest, encyst and 

germinate as described above to form a rhizoidal 

system and a trunk-like region which bears 

dichotomous branches. 

The tips of the branches have been claimed 

to resemble the Spitzenkörper of higher fungi 

in being actin-rich, although secretory vesicles 

and/or microvesicles (chitosomes) have not been 

clearly shown (Srinivasan et al., 1996). Repeated 

nuclear division occurs to form a coenocytic 

structure, and finger-like ingrowths from the 

walls of the trunk-region and branches form 

incomplete septa, sometimes termed pseudosepta, 

with a pore in the centre through which 

cytoplasmic connections can be seen (Fig. 6.20d; 

Meyer & Fuller, 1985). The haploid thalli which 

develop from the meiospores are gametothallic, 

i.e. sexual. They are monoecious, and the tips 

of their branches swell to form paired sacs the 

male and female gametangia. The male gametangia 

can be identified by the presence of 

a bright orange pigment, g-carotene, whilst the 

female gametangia are colourless. In A. arbuscula 

the male gametangium is subterminal or 

hypogynous, i.e. beneath the terminal female 

gametangium, but in A. macrogynus the positions 

are reversed and the male gametangium is 

terminal or epigynous (Figs. 6.20e,i). The gametangia 

bear a number of colourless papillae on 

their walls, blocked by pulley-shaped plugs 

which eventually dissolve. 

The contents of the gametangia differentiate 

into uninucleate gametes which differ in size 

and pigmentation. The female gametangium 

forms larger, colourless motile gametes (swarmers) 

whilst the male gametangium releases 

smaller, more active, orange-coloured swarmers. 

After escaping through the papillae in the walls 

of the gametangia, the gametes swim for a time 

and then pair off. A female gamete which fails 

to pair can function as a zoospore by germinating 

to form a new sexual thallus. A hormone, 

sirenin, is secreted by female gametangia during 

gametogenesis and by the released female 

gametes, and this stimulates a chemotactic 

response in male gametes at the extremely low 

concentration of 8 10 11 M (Machlis, 1972; 

Carlile, 1996a). The chemical structure of sirenin 

has been determined (Fig. 6.22), and both d- and 

l-forms have been synthesized. Only l-sirenin is 

active. It is a bicyclic sesquiterpene, probably 

derived from the parent hydrocarbon sesquicarene 

(Nutting et al., 1968; Plattner & Rapoport, 

1971). A second hormone, parisin, which attracts 

female gametes, is secreted by male gametes. 

Its structure has not been determined, although 

it may well be related to sirenin (Pommerville 

& Olson, 1987). 

The biflagellate zygote resulting from the 

fusion of two gametes may swim for a while


157 

Fig 6.20 (a h) Allomyces arbuscula. (a) Zoospores (haploid meiospores). (b) Young gametothalli, 24 h old. (c) Young sporothalli,18 h 

old. (d) Sporothallus, 30 h old. Perforations are visible in some of the septa. (e) Gametangia at the tips of the branches of the 

gametothallus. Note the disparity in the size of the gametes (anisogamy).The smaller male gametes are orange in colour whilst 

the larger female gametes are colourless.Compare the hypogynous arrangement of the male gametangia with the epigynous 

arrangement in A. macrogynus shown at (i). (f) Meiosporangia (resting sporangia, R.S.) and mitosporangia (zoosporangia, Z.S.) on a 

sporothallus. (g) Release of mitospores from zoosporangia (¼ mitosporangia) on sporothallus. (h) Rupture of meiosporangium 

(¼ resting sporangium). (i) Allomyces macrogynus. Branch tip from gametothallus showing the arrangement of gametangia with 

terminal, epigynous male gametangia and anisogamous gametes. 

before it encysts and casts off the flagella. 

Nuclear fusion then follows (Pommerville & 

Fuller, 1976). The zygote develops immediately 

into a diploid asexual thallus which differs 

from gametothalli in bearing two types of 

zoosporangia instead of gametangia. The first 

formed are thin-walled papillate zoosporangia 

formed singly or in rows at the tips of the


Fig 6.21 Life cycle diagram of Eu-Allomyces as exemplified by A. macrogynus. A diploid sporothallus may produce diploid mitospores 

from a colourless, thin-walled papillate mitosporangium, and haploid meiospores from a thick-walled pitted meiosporangium in 

which meiosis occurs. Meiospores germinate to form a haploid gamethothallus which produces two different gametangia and 

releases haploid gametes of two kinds, small carotenoid-rich (shaded) ‘male’gametes and larger colourless ‘female’ones.Upon 

copulation, a diploid zygote gives rise to a sporothallus. Alternatively, if failing to pair up, the female gametes may function as 

zoospores, in which case they give rise to a new gametothallus. Small open circles represent haploid nuclei whereas diploid nuclei 

are drawn larger and split. It should be noted that many field strains of A. macrogynus have a higher ploidy level, e.g. alternating 

between diploid (small circles) and tetraploid (large split circles) conditions. Key events in the life cycle are plasmogamy (P), 

karyogamy (K) and meiosis (M). 

branches (Fig. 6.20g). Within these thin-walled 

sporangia the nuclei undergo mitosis. Initially 

the nuclei are arranged in the cortical region 

of the cytoplasm, but later they migrate and 

become uniformly spaced apart. Movement of 

the nuclei is controlled by forces generated by 

actin microfilaments whilst their spacing and 

positioning is controlled by microtubules (Lowry 

et al., 1998). Cleavage of the cytoplasm around 

the nuclei to form diploid colourless zoospores 

is initiated by the formation of membranes seen 

first at the plasmalemma, then extending into 

the cortex to form a complex membranous 

network (Fisher et al., 2000). The process of 

cytokinesis, i.e. the extension and fusion of 

Fig 6.22 Chemical structure of the hormone l-sirenin which 

attracts male gametes of Allomyces macrogynus.The structure 

of parisin, attractive to female gametes, does not seem to have 

been elucidated as yet. 

membranes, seems to be mediated principally 

by the actin component of the cytoskeleton 

(Lowry et al., 2004). According to Barron and 

Hill (1974), the development of the cleavage


159 

membranes is induced by the availability of free 

water. Zoospores are released from the sporangia 

after dissolution of the plugs blocking the exit 

papillae. Since nuclear division in the thinwalled 

sporangia is mitotic, these are termed 

mitosporangia, and the diploid swarmers they 

release are mitospores. The mitospores, after a 

swimming phase, encyst and are capable of 

immediate germination, developing into a 

further diploid asexual thallus. 

The second type of zoosporangium is the dark 

brown, thick-walled, pitted resting sporangium 

(meiosporangium), formed at the tips of the 

branches. Meiotic divisions within these sporangia 

result in the formation of the haploid 

meiospores, which develop into sexual thalli. 

The life cycle of a member of the subgenus 

Eu-Allomyces is thus an isomorphic alternation 

of gametothallic and sporothallic generations 

(Fig. 6.21). Comparisons of the nutrition and 

physiology of the two generations show no 

essential distinction between them up to the 

point of production of gametangia or sporangia. 

Emerson and Wilson (1954) have made cytological 

and genetic studies of a number of 

collections of Allomyces. Interspecific hybrids 

between A. arbuscula and A. macrogynus have 

been produced in the laboratory, and it has 

been shown that the fungus earlier described 

as A. javanicus is a naturally occurring hybrid 

between these two species. Cytological examination 

of the two parent species and of artificial 

and natural hybrids showed a great variation 

in chromosome number. In A. arbuscula the 

basic haploid chromosome number is 8, but 

strains with 16, 24 and 32 chromosomes have 

been found. In A. macrogynus the lowest haploid 

number encountered is 14, but strains with 

28 and 56 chromosomes are also known. The 

demonstration that these two species each 

represent a polyploid series was the first to 

be made in fungi. The wild-type strain of 

A. macrogynus appears to be an autotetraploid 

which, after meiosis, produces diploid gametothalli 

(Olson & Reichle, 1978). 

The behaviour of the hybrid strains is of 

considerable interest. As seen above, the parent 

species differ in the arrangement of the primary 

pairs of gametangia, A. arbuscula being 

hypogynous whilst A. macrogynus is epigynous. 

Following fusion of gametes derived from different 

parents, zygotes formed, germinated and 

gave rise to sporothalli. The meiospores from the 

hybrid sporothalli had a low viability (0.1 3.2%), 

as compared with a viability of about 63% for 

A. arbuscula meiospores, but some germinated 

to form gametothalli. The arrangement of the 

gametangia on these F 1 gametothalli showed 

a complete range from 100% epigyny to 100% 

hypogyny. Also, in certain gametothalli the ratio 

of male to female gametangia (normally about 

1:1) was very high, with less than one female 

per 1000 male gametangia. It was concluded 

from these experiments that, since intermediate 

gametangial arrangements are found in hybrid 

haploids, this arrangement is not under the 

control of a single pair of non-duplicated allelic 

genes, but that a fairly large number of genes 

must be involved. Hybridization in some way 

upsets the mechanism which controls the 

arrangement of gametangia in the parental 

species. By treating meiospores of A. macrogynus 

with DNA extracted from gametothallic cultures 

of A. arbuscula, Ojha and Turian (1971) have 

demonstrated an inversion of the normal gametangial 

arrangement, i.e. a proportion of the 

DNA-treated meiospores developed colonies 

with hypogynous antheridia instead of the 

normal epigynous arrangement. Similar inversions 

were also obtained in converse experiments. 

In an isolate of the naturally occurring 

hybrid A. javanicus, Ji and Dayal (1971) have 

shown that although copulation between anisogamous 

gametes results in the formation of 

sporothalli bearing thin-walled and thick-walled 

sporangia, the swarmers from the thick-walled 

sporangia rarely develop into gametothalli, but 

into sporothalli. This is not surprising for a 

hybrid, and is possibly due to a failure of meiosis 

in the thick-walled sporangia. 

Sub-genus Cystogenes 

A life cycle different from Eu-Allomyces is found 

in Allomyces moniliformis and A. neo-moniliformis. 

There is no independent gametothallic generation, 

but this stage is probably represented by 

a cyst (C. M. Wilson, 1952). The asexual thalli 

resemble those of subgenus Eu-Allomyces, bearing


both thin-walled mitosporangia and brown, 

thick-walled, pitted meiosporangia. The mitospores 

encyst and germinate to form a further 

crop of asexual thalli. In the meiosporangium, 

meiosis takes place, but before cytoplasmic 

cleavage occurs, the haploid nuclei pair, the 

paired nuclei being united by a common nuclear 

cap. When cleavage does occur it therefore 

results in the formation of some 30 binucleate 

cells. When the meiosporangial wall cracks open, 

the binucleate cells are released as amoeboid 

bodies which may or may not bear flagella, and 

it is these cells which form the cysts. A mitotic 

division in each cyst results in four haploid 

nuclei, and cytoplasmic cleavage gives rise to 

four colourless uniflagellate isogametes. These 

copulate to form biflagellate zygotes, each of 

which can develop into an asexual sporothallus. 

In the Cystogenes life cycle there is thus a freeliving 

diploid asexual sporothallic generation, 

whereas the haploid generation is reduced to the 

cysts and gametes. 

Sub-genus Brachy-Allomyces 

In certain isolates of Allomyces which have been 

placed in a ‘form species’ A. anomalus, there are 

neither sexual thalli nor cysts. Asexual thalli 

bear mitosporangia and brown resting sporangia. 

The spores from the resting sporangia 

develop directly to give asexual thalli again. 

The cytological explanation proposed by C. M. 

Wilson (1952) for this unusual behaviour is that, 

due to complete or partial failure of chromosome 

pairing in the resting sporangia, meiosis 

does not occur and nuclear divisions are mitotic. 

Consequently the zoospores produced from resting 

sporangia are diploid, like their parent thalli 

and, on germination, give rise to diploid asexual 

thalli again. Similar failures in chromosome 

pairing were also encountered in the hybrids 

between A. arbuscula and A. macrogynus leading to 

very low meiospore viability from certain crosses. 

In view of this it seemed possible that some of 

the forms of A. anomalus might have arisen 

through natural hybridization. In a later study, 

Wilson and Flanagan (1968) showed that there 

is a second way in which the life cycle of 

this fungus is maintained without a sexual 

phase. In certain isolates, meiosis does occur in 

the resting sporangia, followed by apomixis, 

i.e. the fusion of two meiosis-derived nuclei in 

the same thallus. Propagules from the resting 

sporangia are therefore diploid and the cysts 

develop into sporothalli. By germinating resting 

sporangia in dilute K 2 HPO 4 , a small percentage 

of zoospores were produced which developed 

into gametothalli, some of which were identified 

as A. macrogynus and some as A. arbuscula. No 

hybrids were found. Thus A. anomalus is not 

a single species, but represents sporothalli of 

these two species in which the normal alternation 

of generations has been upset by cytological 

deviations. 

6.5.3 Blastocladiella 

About a dozen species of Blastocladiella have been 

isolated from soil or water, and one is parasitic 

on the cyanobacterium Anabaena (Canter & 

Willoughby, 1964). The form of the thallus is 

comparatively simple, resembling that of some 

monocentric chytrids. There is an extensive 

branched rhizoidal system which is attached 

either to a sac-like sporangium or to a cylindrical 

trunk-like region bearing a single sporangium 

at the tip. In B. emersonii it has been shown that 

the rhizoids are chemotropic and function 

not only in attachment, but in absorption and 

selective translocation of nutrients (Kropf & 

Harold, 1982). 

Different species of Blastocladiella have life 

cycles resembling those of the three subgenera 

of Allomyces, and Karling (1973) has proposed 

that Blastocladiella should similarly be divided 

into three subgenera, i.e. Eucladiella corresponding 

to Eu-Allomyces, Cystocladiella corresponding 

to Cystogenes, and Blastocladiella corresponding 

to Brachy-Allomyces. In some species there is an 

isomorphic alternation of generations, probably 

matching in essential features the Eu-Allomyces 

pattern, but cytological details are needed to 

confirm this. For example, in Blastocladiella 

variabilis two kinds of asexual thallus are found. 

One bears thin-walled zoosporangia which 

release posteriorly uniflagellate swarmers. 

These swarmers may develop to form thalli 

resembling their parents or may give rise to 

the second type of asexual thallus bearing


161 

a thick-walled dark-brown sculptured resting 

sporangium within the terminal sac. The resting 

sporangium releases posteriorly uniflagellate 

swarmers which, after swimming, germinate 

to form sexual thalli of two kinds. About half 

of the sexual thalli are colourless (‘female’), 

and about half are orange-coloured (‘male’). 

However, in contrast to the anisogamy of 

Eu-Allomyces, inBlastocladiella there is no distinction 

in size between the gametes. The orange 

and colourless gametes pair to produce zygotes, 

which germinate directly to produce asexual 

thalli. In other species (e.g. B. cystogena) the life 

cycle is of the Cystogenes type, i.e. there are no 

gametothalli. 

In yet other species there is no clear evidence 

of sexual fusion. In B. emersonii (Fig. 6.23), the 

resting sporangial thallus contains a single 

globose, dark reddish brown resting sporangium 

with a dimpled wall. Meiosis occurs during 

development of the resting sporangium (Olson 

& Reichle, 1978). After a resting period, the wall 

cracks open and one to four papillae protrude 

from which swarmers are released. The swarmers 

germinate to form two types of thallus bearing 

thin-walled zoosporangia. About 98% of the 

swarmers give rise to thalli bearing colourless 

sporangia (Fig. 6.23a), and about 2% to thalli 

with sporangia coloured orange due to the 

presence of g-carotene. The colourless thalli 

develop rapidly and are ready to discharge 

zoospores within 24 h. These have about twice 

the DNA content as the swarmers released from 

resting sporangia (Horgen et al., 1985). Thus 

young colourless thalli are at first haploid, but 

release diploid zoospores. The manner in which 

the diploid state of the colourless thalli or of the 

resting sporangia is brought about is not known. 

The life cycle of B. emersonii thus corresponds 

to that of the sub-genus Brachyallomyces. 

Blastocladiella emersonii has a number of other 

unusual features. If zoospore suspensions are 

pipetted onto yeast peptone glucose (YPG) 

agar, the majority of thalli which develop will 

be of the thin-walled colourless type. On the 

same medium containing 10 mM bicarbonate, 

resting sporangial thalli develop. The addition 

of 40 80 mM KCl, NaCl or NH 4 Cl, or exposure 

of cultures to ultra-violet light, will similarly 

induce the formation of resting sporangia 

(Horgen & Griffin, 1969). Thus, by means of 

simple manipulation of the environment it is 

possible to switch the metabolic activities of 

the fungus into one of two morphogenetic 

Fig 6.23 Blastocladiella emersonii. (a) Thin-walled thallus releasing zoospores. (b) Three-day-old thallus with immature resting 

sporangium. (c) Thallus with germinating resting sporangium showing the cracked wall and four exit tubes. (d) Zoospores from 

thin-walled thallus.


pathways. There are important differences in the 

activities of certain enzymes (Cantino et al., 1968; 

Lovett, 1975). In the absence of bicarbonate, 

there is evidence for the operation of a tricarboxylic 

acid cycle, whereas in the presence of 

bicarbonate, part of this cycle is reversed, leading 

to alternative pathways of primary carbon 

metabolism. In addition, a polyphenol oxidase, 

absent in the thin-walled thallus, replaces the 

normal cytochrome oxidase. There is also 

increased synthesis of melanin and of chitin in 

the presence of bicarbonate. The effect of 

bicarbonate can be brought about by increased 

levels of CO 2 . 

Another unusual feature is that B. emersonii 

fixes CO 2 more rapidly in the light than in the 

dark. In the presence of CO 2 , light-grown thalli 

show a number of differences when compared 

with dark-grown controls. Illuminated thalli take 

about three hours longer to mature, and are 

larger than dark-grown thalli. They also have an 

increased rate of nuclear division and a higher 

nucleic acid content. The most effective wavelengths 

for this increased CO 2 fixation (or 

lumisynthesis) lie between 400 and 500 nm, i.e. 

at the blue end of the spectrum. This suggests 

that the photoreceptor should be a yellowish 

substance. Attempts to identify the photoreceptor 

have as yet been unsuccessful, but it is known 

not to be a carotenoid. 

6.6 Monoblepharidales 

This group includes about 20 species and is 

represented by 5 genera, namely Monoblepharis, 

Monoblepharella, Gonapodya, Oedogoniomyces and 

Harpochytrium. Fungi belonging to this order 

can be isolated from soil samples or from twigs 

or fruits submerged in freshwater, sometimes 

under anoxic conditions (Karling, 1977; Fuller 

& Clay, 1993). Whisler (1987) has given details 

of isolation techniques. Most species are saprotrophs 

and several are available in culture. In all 

genera the thallus is eucarpic either with 

rhizoids or a holdfast, and with branched or 

unbranched filaments. The walls contain 

microfibrils of chitin (Bartnicki-Garcia, 1968), 

but the walls of G. prolifera also contain cellulose 

(Fuller & Clay, 1993). A characteristic feature is 

the frothy or alveolate appearance of the 

cytoplasm caused by the presence of numerous 

vacuoles often arranged in a regular pattern. 

Asexual reproduction is by posteriorly uniflagellate 

zoospores which are borne in terminal, 

cylindrical or flask-shaped sporangia. Sexual 

reproduction, where known, is unique for fungi 

in being oogamous with a large egg and a 

smaller, posteriorly flagellate spermatozoid. The 

egg may be retained within the oogonium or 

may move to its mouth by amoeboid movement 

in some species of Monoblepharis, or propelled by 

the lashing of the flagellum of the spermatozoid 

in Monoblepharella and Gonapodya. 


The fine structure of zoospores is similar in 

representatives of all five genera (Fig. 6.24; see 

Mollicone & Longcore, 1994, 1999). In all cases 

the body of the zoospore is oval, the narrow 

part facing forward and with a long whiplash 

flagellum trailing from the wider posterior. 

Amoeboid changes of shape may occur and 

swimming zoospores may develop pseudopodia 

anteriorly. The body of the zoospore is differentiated 

into three regions: an anterior region 

which is often devoid of organelles apart from 

lipid globules, a few vacuoles and tubular 

cisternae; a central region which contains the 

nucleus, surrounded by ribosomal aggregations 

(sometimes termed the nuclear cap), microbodies 

and spherical mitochondria with flattened 

cristae; and a posterior ‘foamy’ region at 

the base of which are the functional kinetosome, 

a non-functional kinetosome and a rumposomal 

complex. The functional kinetosome is surrounded 

by a striated disc, apparently anchored 

to annular cisternae. From an electron-dense 

region of the striated disc, about 31 34 microtubules 

extend outwards into the body of the 

zoospore. Water expulsion vacuoles have been 

identified in the anterior part of the zoospore 

of G. prolifera. Another distinctive feature in this 

fungus is the presence of a pair of paraxonemal 

structures, solid cylindrical fibres which are

MONOBLEPHARIDALES 

163 

Fig 6.24 Summary diagram of zoospore ultrastructure 

of Monoblepharis polymorpha. Abbreviations: angular cisternae 

(ac), endoplasmic reticulum (er), kinetosome (K), lipid globule 

(L), mitochondria (M), microbody (mb), microtubule (mt), 

nucleus (N), non-flagellated centriole (nfc), transition zone 

plug (O), kinetosome prop (P), ribosomal aggregate (R), 

rumposome (Ru), striated disc (sd), vacuole (V).The diameter 

of the zoospore is about 6 mm. Reprinted with permission 

from Mollicone and Longcore (1994), Mycologia. 

ß The Mycological Society of America. 

smaller in diameter than the axonemal microtubules, 

running parallel to them within the 

axoneme and connected at intervals to doublets 

3 and 8 (Mollicone & Longcore, 1999). 

6.6.2 Monoblepharis 

Species of Monoblepharis occur in quiet silt-free 

pools containing neutral or slightly alkaline 

water (i.e. pH 6.4 7.5) on waterlogged twigs on 

which the bark is still present. Twigs of birch, 

ash, elm and especially oak are suitable substrata, 

and although samples taken at varying 

times throughout the year may yield growths 

of the fungus, there are two main periods of 

vegetative growth, one in spring and another 

in autumn, with resting periods during the 

summer and winter months. Low temperatures 

appear to favour asexual development and good 

growth can be obtained on twigs incubated in 

dishes of distilled water at temperatures around 

3°C. The mycelium is delicate and vacuolate. 

The hyphae are multinucleate. During the 

formation of a sporangium, a multinucleate 

tip is cut off by a septum. The cytoplasm cleaves 

around the nuclei to form zoospore initials 

which are at first angular and then later pearshaped. 

The ripe sporangium is cylindrical or 

club-shaped and may not be much wider than 

the hypha bearing it. A pore is formed at 

the tip of the sporangium through which the 

zoospores escape by amoeboid crawling. The 

free zoospores swim away. On coming to rest, 

a zoospore encysts and germinates by emitting 

a germ tube. The single nucleus of the zoospore 

cyst divides and further nuclear divisions occur 

as the germ tube elongates. 

Sexual reproduction can be induced by 

incubating twigs at room temperature. Light 

also affects reproduction in M. macrandra. 

Cultures of this fungus incubated in the dark 

produced only gametothalli whilst those grown 

in light formed only sporothalli (Marek, 1984). 

In M. polymorpha and related species, the antheridia 

are epigynous, becoming cut off by a basal 

septum. Beneath the antheridium the hypha 

becomes swollen somewhat asymmetrically so 

that the antheridium is displaced into a lateral 

position. The swollen subterminal part becomes 

spherical and is then cut off by a basal septum 

to form the oogonium. In M. sphaerica and 

some other species, the arrangement of the sex 

organs is the reverse of that in M. polymorpha, 

i.e. hypogynous. In M. macrandra the antheridia 

and oogonia may grow as solitary organs at the


Fig 6.25 Monoblepharis macrandra reproduction. (a) Terminal 

zoosporangium containing cleaved zoospores. (b) Solitary 

terminal antheridium. (c) Solitary terminal oogonium with 

apical receptive area. (d) Oogonium with hypogynous 

antheridium. (e) Spermatozoid release from solitary terminal 

antheridium. (f) Exogenous oospore on empty oogonium with 

bullations on the wall of the oogonium and lipid inclusions 

in the cytoplasm. (a e) to same scale.Traced from Whisler 

and Marek (1987), with permission by Southeastern Publishing 

Corporation. 

tips of the hyphae (Figs. 6.25b,c) or in pairs, 

with the antheridium in a hypogynous position 

(Fig. 6.25d). The antheridium often releases 

sperm before the adjacent oogonium is ripe. 

Each antheridium forms about four to eight 

posteriorly uniflagellate swarmers which resemble, 

but are somewhat smaller than, the zoospores. 

The oogonium contains a single spherical 

uninucleate oosphere, and when this is mature 

an apical receptive papilla on the oogonial wall 

breaks down. A spermatozoid approaching the 

receptive papilla of the oogonium becomes 

caught up in mucus and fusion with the 

oosphere then follows, the flagellum of the 

spermatozoid being absorbed within a few 

minutes. Following plasmogamy, the oospore 

secretes a golden-brown wall around itself 

and nuclear fusion later occurs. In some species, 

e.g. M. sphaerica, the oospore remains within 

the oogonium (endogenous) but in others, e.g. 

M. macrandra and M. polymorpha, the oospore 

begins to move towards the mouth of the 

oogonium within a few minutes of fertilization, 

and remains exogenous, i.e. attached to it 

(Fig. 6.25f). In the exogenous species, nuclear 

fusion is delayed but finally fusion occurs and 

the oospore becomes uninucleate. In some 

species the oospore wall remains smooth, but 

in others such as M. macrandra the wall may be 

ornamented by hemispherical warts or bullations 

(Fig. 6.25f). The oospore germinates after 

a resting period which coincides with frozen 

winter conditions or summer drought by producing 

a single hypha which branches to form 

a mycelium. The cytological details of the life 

cycle are not fully known but it seems likely 

that reduction division occurs during the germination 

of the overwintered oospores.

7 

Zygomycota 


The phylum Zygomycota comprises the first 

group of fungi considered in this book which 

lacks any motile stage. Asexual reproduction is 

by spores which are called aplanospores because 

they are non-motile, and sporangiospores 

because they are typically contained within 

sporangia. They are dispersed passively by wind, 

insects and rain splash, although violent liberation 

of entire sporangia (e.g. Pilobolus) or individual 

spores (e.g. Basidiobolus, Entomophthora) can 

also occur. Sexual reproduction is by gametangial 

copulation which is typically isogamous and 

results in the formation of a zygospore. The 

mycelial organization is coenocytic, and the 

cell wall contains chitin and its deacetylated 

derivative, chitosan (Bartnicki-Garcia, 1968, 1987; 

see Fig. 1.5). As in the Chytridio-, Asco- and 

Basidiomycota, the mitochondria possess lamellate 

cristae, and the Golgi system is reduced to 

single cisternae. Lysine is synthesized by the 

a-aminoadipic acid (AAA) route, as it appears to 

be in all Eumycota. 

General accounts of the Zygomycota have 

been given by Benjamin (1979), Benny (2001) and 

Benny et al. (2001). Molecular evidence indicates 

that the group may have diverged from the 

Chytridiomycota early in the history of terrestrial 

life. The Zygomycota, in turn, probably 

gave rise to the Asco- and Basidiomycota, i.e. 

the ‘higher fungi’ (Jensen et al., 1998; Schüssler 

et al., 2001). Two classes are included in the 

Zygomycota, namely Zygomycetes comprising 

870 species in 10 orders, and Trichomycetes 

with 218 species in 3 orders (Kirk et al., 2001). 

The most prominent orders of the Zygomycetes 

are the Mucorales, Entomophthorales and 

Glomales. Mucorales are ubiquitous in soil and 

dung mostly as saprotrophs, although a few are 

parasitic on plants and animals. Entomophthorales 

include a number of insect parasites, but 

some saprotrophic forms also exist. Glomales 

are mutualistic symbionts associated with 

almost all kinds of terrestrial plants as arbuscular 

and vesicular arbuscular mycorrhiza. Trichomycetes 

are mostly commensal in the guts of 

arthropods, e.g. millipedes and the larvae of 

aquatic insects. 

The Zygomycetes are almost certainly polyphyletic, 

but the precise evolutionary relationships 

within this class are still controversial 

(O’Donnell et al., 2001; Schüssler et al., 2001; 

Tanabe et al., 2004, 2005), and comparisons of 

numerous representative organisms with several 

different DNA sequences, e.g. genes encoding 

ribosomal RNA, cytochrome oxidase or cytoskeletal 

proteins, will be required before a satisfactory 

natural arrangement can be found. A recent 

phylogenetic scheme is presented in Fig. 7.1. 

7.2 Zygomycetes: Mucorales 

In most members of the Mucorales, numerous 

spores are contained in globose sporangia borne 

at the tips of aerial sporangiophores (Fig. 7.2). 

Within the sporangium the spores may surround

166 ZYGOMYCOTA 

Fig 7.1 Recent phylogenetic scheme of 

the Zygomycota based on partial 

sequences of the gene encoding a subunit 

of RNA polymerase II.Orders discussed in 

detail in this book include Mucorales 

(Sections 7.2 7.3), Zo opagales 

(Section 7.4), Entomophthorales 

(Section 7.5) in the Zygomycetes, and 

Harpellales (Section 7.7) in the 

Trichomycetes.The Glomales (Section 7.6), 

only distantly related to other 

Zygomycota, were not included in this 

analysis. Redrawn and modified from 

Tanabe et al. (2004), with permission 

from Elsevier. 

a central core or columella, although in some 

species (e.g. Mortierella spp.) the columella is 

greatly reduced. Some species possess fewspored 

sporangia, termed sporangiola, which 

are often dispersed as a unit, and in some groups 

the spores are arranged as a single row inside a 

cylindrical sac termed a merosporangium. Yet 

other Mucorales reproduce by means of unicellular 

propagules which are sometimes termed 

conidia, but Benjamin (1979), in his consideration 

of asexual propagules formed in the 

Zygomycota, has recommended the use of the 

term ‘sporangiolum’ instead of ‘conidium’ in 

this context. It is believed that ‘conidia’ may have 

evolved several times within different groups of 

Mucorales from forms with monosporous sporangiola. 

A distinction between sporangiospores 

and conidia is that germinating sporangiospores 

lay down a new wall, continuous with the germ 

tube, within their original spore wall, whilst 

within germinating conidia there is no new wall 

layer formed. 

The Mucorales are mostly saprotrophic and 

are abundant in soil, on dung and on other 

organic matter in contact with the soil. They may 

play an important role in the early colonization 

of substrata. Sometimes, however, they can 

behave as weak pathogens of soft plant tissues, 

e.g. Rhizopus stolonifer can cause a rot of sweet 

potatoes or fruits such as apples, tomatoes and 

strawberries (Plate 3d). Such infections may 

cause spoilage of food (Samson et al., 2002). 

Some species are parasitic on other fungi, a 

common example being Spinellus fusiger which 

forms a tuft of sporangiophores on the caps of 

moribund fruit bodies of Mycena spp. (Plate 3e). 

Others cause diseases of animals including 

man, especially patients suffering from diabetes, 

leukaemia and cancer. Lesions may be localized 

in the brain, lungs or other organs, or may be 

disseminated, e.g. at various points in the 

vascular system (Kwon-Chung & Bennett, 1992). 

Species of Rhizopus and Mucor are reported from 

human lesions, and these genera together with

ZYGOMYCETES: MUCORALES 

167 

species of Absidia may also infect domestic 

animals. 

A number of species have been used in the 

production of oriental foods such as sufu, 

tempeh and ragi (Nout & Aidoo, 2002) and 

some are used as starters in the saccharification 

of starchy materials before fermentation to 

alcohol (Hesseltine, 1991). In modern biotechnology, 

many mucoralean fungi are employed in 

biotransformation processes (for references, see 

Kieslich, 1997). Further, a number of species are 

oleaginous, i.e. they are able to synthesize and 

accumulate lipids to over 20% (dry weight) of 

their biomass. Because these lipids (principally 

triacylglycerides) may be enriched in polyunsaturated 

fatty acids (PUFAs), oleaginous members 

of the Mucorales are of current biotechnological 

interest (Certik & Shimizu, 1999). 

Extensive studies of nutrition and physiology 

have been made. A wide variety of sugars can be 

used, and whilst starch can be decomposed by 

some species, cellulose is generally not utilized. 

Under anaerobic conditions, ethanol and numerous 

organic acids are produced. Many Mucorales 

need an external supply of vitamins for growth 

in synthetic culture. Thiamine is a common 

requirement, and the amount of growth of 

Phycomyces has been used as an assay for the 

concentration of thiamine. 

Zycha et al. (1969) have given a general 

account of the taxonomy of the Mucorales, 

including keys to genera and species. Benny 

et al. (2001) recognized 13 families and 57 genera. 

Classification and identification are based 

largely on the morphology of the anamorph. 

However, DNA sequence comparisons indicate 

that several families and even some larger 

genera are polyphyletic (O’Donnell et al., 2001), 

meaning that the traditional family-level classification 

scheme is artificial. We retain it here 

because it presents an accessible framework 

of morphological features within which the 

Mucorales can be understood, and because 

convincing alternative schemes have not yet 

been put forward. 

7.2.1 Growth and asexual reproduction 

The mycelium is coarse, coenocytic and 

richly branched, the branches tapering to fine 

Fig 7.2 Mucor mucedo. (a) Mycelium and young 

sporangiophores with globules of liquid attached. (b) Immature 

sporangium with the columella visible through the sporangial 

wall. (c) Dehisced sporangium showing the columella, the frill 

representing the remains of the sporangial wall, and 

sporangiospores. 

points (Fig. 7.2). Later, septa may appear. 

Thick-walled mycelial segments (chlamydospores) 

may be cut off by such septa (Benjamin, 

1979) and in certain species, e.g. Mucor racemosus, 

the presence of chlamydospores in sporangiophores 

may be a useful diagnostic feature 

(Fig. 7.14b). In anaerobic liquid culture, especially 

in the presence of CO 2 , several species of 

Mucor (e.g. M. rouxii) grow in a yeast-like instead 

of a filamentous form (Fig. 7.3) but revert to 

filamentous growth in the renewed presence 

of O 2 . The cell walls of Mucorales are chemically 

complex (Ruiz-Herrera, 1992; Gooday, 1995). 

Chitin microfibrils are present but are often


Fig 7.3 Mucor rouxii. (a) Yeast-like growth in liquid medium 

under anaerobic conditions 24 h after inoculation with spores. 

(b) Filamentous growth from spores in liquid medium under 

aerobic conditions 4 h after inoculation. 

deacetylated to chitosan. Other compounds such 

as poly-D-glucuronides, polyphosphates, proteins, 

lipids, purines, pyrimidines, magnesium and 

calcium have also been detected. Comparison of 

the structure and composition of yeast-like and 

filamentous cells of Mucor rouxii shows that the 

yeast-like cells have much thicker walls. They 

also have a mannose content about five times 

as great as that of filamentous cell walls. The 

synthesis of chitin microfibrils takes place 

within chitosomes which have been described 

from sporangiophores of Phycomyces (Herrera- 

Estrella et al., 1982; Gamow et al., 1987) and 

from a number of other fungi with chitinous 

walls (see p. 6). 

Asexual reproduction is by aplanospores 

(sporangiospores) contained in globose or pearshaped 

sporangia, which are borne singly at 

the tip of a sporangiophore or on branched 

sporangiophores. In Absidia (Fig. 7.17), the 

sporangia are arranged in whorls on aerial 

branches, and in many species of Rhizopus the 

sporangiophores arise in groups from a clump 

of rhizoids (Fig. 7.16). Sporangiophores are 

often phototropic, and several studies on the 

phototropism of the strikingly large sporangiophores 

of Phycomyces blakesleeanus have been 

undertaken (see p. 169) and have been summarized 

in elegant and stimulating reviews of the 

biology of this fungus (Bergman et al., 1969; 

Cerdá-Olmedo & Lipson, 1987; Cerdá-Olmedo, 

2001). ‘The sporangiophore of the fungus 

Phycomyces is a gigantic, single-celled, erect, 

cylindrical aerial hypha. It is sensitive to at 

least four distinct stimuli: light, gravity, 

stretch, and some unknown stimulus by which 

it avoids solid objects. These stimuli control a 

common output, the growth rate, producing 

either temporal changes in the growth rate or 

tropic responses’ (Bergman et al., 1969). The 

avoidance by the sporangiophore of solid 

objects is termed the avoidance response or 

fugitropism. Despite its obvious fascination, the 

mechanisms behind the avoidance response are 

still not understood. Because, under certain 

conditions, P. blakesleeanus may also develop 

much smaller sporangiophores (microsporangiophores 

or microphores), the larger sporangiophores 

are sometimes termed macrophores. 

Despite their remarkable height (Fig. 7.4), for 

much of their length the macrophores are 

a constant 100 mm in diameter. The wall, about 

0.6 mm thick, encloses a peripheral layer of 

cytoplasm of about 30 mm surrounding a 

central vacuole about 40 mm in diameter 

(Fig. 7.5). The mature sporangium is spherical 

and some 500 mm across. 

The sporangiophore of Phycomyces develops 

as a conical outgrowth from the vegetative


169 

mycelium. Elongation of the sporangiophore is 

confined to a yellow-pigmented growing zone 

(about 1 cm long) beneath the apex. In the 

absence of light, sporangiophores grow vertically 

as a negative response to gravity. Schimek et al. 

(1999) have suggested that gravity may be 

detected by a combination of at least two 

mechanisms. Proteinaceous crystals located 

inside vacuoles have a higher density than the 

vacuolar sap and therefore sediment in response 

to gravity, whereas a cluster of buoyant lipid 

droplets less dense than the cytoplasm floats to 

the apex of the sporangiophore. Both mechanisms 

would be different from that found in 

the fruit bodies of basidiomycetes such as 

Flammulina, in which nuclei denser than the 

surrounding cytoplasm seem to be the organelles 

involved in graviperception (see p. 546). 

7.2.2 Phototropism in Phycomyces 

If a sporangiophore is subjected to unilateral 

illumination it bends towards the light, 

especially blue light. Phototropism in Phycomyces 

is extremely sensitive, the lower threshold being 

1nWm 2 , which is equivalent to the light 

emitted by a single star at night (Cerdá- 

Olmedo, 2001). Bending is the consequence of 

a deceleration of about 6% in the growth rate 

of the side proximal to the direction of light, 

and an increase by the same rate on the distal 

side (Fig. 7.4). Because the refractive index of 

the sporangiophore contents exceeds that of air, 

the sporangiophore functions as a cylindrical 

lens, focusing unilateral light on the distal 

wall of the sporangiophore, resulting in more 

intense illumination of that side. Evidence in 

support of the lens effect is the demonstration 

that sporangiophores immersed in mineral oil 

with a higher refractive index than that of the 

sporangiophore contents function as a diverging 

lens and bend away from the light. The illumination 

of the edge of a sporangiophore by a narrow 

beam of light from a laser is followed by bending 

of the sporangiophore in a direction perpendicular 

to the light beam (Meistrich et al., 1970). 

Photoreceptors are located in the plasma 

membrane (Fukshansky, 1993), and the transmission 

of the signal leads to localized wall 

softening and the synthesis of new cell wall 

Fig 7.4 Sporangiophore development of Phycomyces 

blakesleeanus in standard test tubes (about1.5 cm diameter). 

The tubes were wrapped except for the tip of tube (a) or a 

square on the right-hand side near the top of tube (b) In tube 

(a), the sporangiophores have grown straight towards the 

light, whereas in tube (b) they have bent towards the lateral 

light source. 

material (Herrera-Estrella & Ruiz-Herrera, 1983; 

Ortega, 1990). 

A central problem in studies of photoresponses 

is the nature of the photoreceptor(s). 

Two photoreceptors one for low and the 

other for high light intensities are involved 

in determining the phototropism in Phycomyces, 

and there are also two receptors each for 

light-induced microphore formation, macrophore 

formation, and carotenoid biosynthesis 

(Cerdá-Olmedo, 2001). A clue to the possible


Fig 7.5 Sporangiophore of 

Phycomyces as a cylindrical lens. 

Upper portion: light ray L impinges 

from the left and is refracted at 

the first surface.The ratio of 

‘path length’of the light ray in 

the proximal part of the 

sporangiophore to the path length 

in the distal part is PM/DM.The 

maximum value of the angle b is 

about 20°.Lowerportion: 

sporangiophore in section to show 

the peripheral layer of cytoplasm 

surrounding the central vacuole. 

The values are estimates of the 

refractive index of cytoplasm and 

vacuolar sap. Diagram modified 

from Bergman et al. (1969). 

nature of the photoreceptors can be obtained by 

studying the action spectrum of the response 

over a range of light wavelengths. The phototropic 

curvature of Phycomyces sporangiophores 

has a similar action spectrum to the growth 

response of the vegetative mycelium, which is 

also stimulated by light. There are several clearly 

defined peaks at 485, 455, 385 and 280 nm, i.e. 

mostly in the blue part of the spectrum. 

Although b-carotene is present in large amounts 

in the growing zone of the sporangiophore, the 

photoreceptor system is more likely to comprise 

a flavin-type molecule and a pterin-type protein 

(Flores et al., 1999; Galland & Tölle, 2003). 

Mutants with less than 0.1% of the wild-type b- 

carotene content remain fully photosensitive. 

However, b-carotene is involved in the other 

light-induced responses. The signalling chains 

involved in transduction of the light signal are 

only partially unravelled at present (Cerdá- 

Olmedo, 2001). 

Moss and Baker (2002) have described a 

technique for demonstrating the phototropic 

response of P. blakesleeanus in the laboratory. 

7.2.3 Sporangiophore development in 

Phycomyces 

As the sporangiophore of Phycomyces develops it 

rotates. Castle (1942) followed the growth and 

rotation of the sporangiophore by attaching 

Lycopodium spores as markers and tracking the 

displacement of the markers. His findings are 

illustrated in Fig. 7.6. After a period of apical 

growth of the tubular sporangiophore (stage I), 

the sporangium appears as a terminal swelling 

and growth ceases. During this period (stage II), 

growth is limited to sporangial enlargement. 

In the next period (stage III) no further enlargement 

of the sporangium occurs, and elongation 

is also at a standstill. During stages IVA and IVB, 

elongation of the sporangiophore is resumed and 

growth is mainly localized in a zone somewhat 

below the sporangium. During stage I the tip of 

the sporangiophore rotates clockwise (as seen 

from above looking down) through a maximum 

angle of about 90°. There is no rotary movement 

during stages II and III. When sporangiophore 

elongation recommences in stage IVA, the direction 

of rotation is now anti-clockwise (as seen from


171 

Fig 7.6 Diagram of developmental stages of 

the sporangiophore of Phycomyces. Regions 

in which growth is taking place are stippled. 

The rotary component of growth is indicated. 

During stage I the axis of growth is directed 

sinistrally, in stages II and III growth is 

unoriented. In Stage IVA dextral spiralling 

occurs and in Stage IVB sinistral spiralling again 

takes place. 

above). During this stage, which lasts about an 

hour, markers attached to the growth zone may 

make up to two complete revolutions around the 

axis. During stage IVB the direction of rotation 

reverses once more. The reasons for the spiral 

growth are far from clear (see Ortega et al., 2003). 

It is known that the chitin microfibrils which 

make up the wall of the sporangiophore show 

a right-handed or Z-spiral orientation. One 

possible explanation is that the laying down of 

the fibrils in this way is responsible for the 

rotation. A second is that the extension due to 

turgor pressure of a cylinder whose walls are 

composed of spirally arranged fibrils would 

naturally result in a passive rotation. The 

phenomenon of spiral growth is not peculiar to 

Phycomyces, occurring also during elongation of 

the sporangiophores of other members of the 

Mucorales such as Thamnidium and Pilobolus, and 

in various cylindrical plant cells. 

The mechanical properties of the sporangiophore 

of Phycomyces change during development. 

During stage II, when no elongation of the 

sporangiophore is taking place, the sporangiophore 

shows elastic deformation when small 

loads are applied to it, i.e. the fractional change 

in length is directly proportional to the applied 

load, and on removal of the load, the 

sporangiophore returns to its original length. 

During stage IV, although the sporangiophore 

changes in length in response to applied loads, 

upon unloading the sporangiophore does not 

return to its original length. 

There is evidence that the spores secrete 

one or more unknown substances which control 

elongation of the sporangiophore. If mature 

sporangia are removed, growth of the sporangiophore 

ceases. Replacement of the detached 

sporangium with a substitute sporangium, 

with a suspension of spores, or with a drop 

of supernatant liquid from a centrifuged spore 

suspension, results in resumption of growth. 

Another effect of the removal of a ripe sporangium 

is that branching is induced in the 

sporangiophore, and this phenomenon has been 

likened to the breaking of apical dominance 

upon removal of the terminal bud in shoots of 

angiosperms. 

7.2.4 Sporangium development 

The tip of the sporangiophore expands to form 

the sporangium initial containing numerous 

nuclei which continue to divide. A dome-shaped 

septum is laid down and cuts off a distal portion 

which will contain the spores, from a cylindrical 

or subglobose spore-free core, the columella.


The columella is curved from its inception. 

Cleavage planes separate the nuclei within the 

sporangium, and finally the spores are cleaved 

out. They may be uninucleate or multinucleate 

according to the species, e.g. M. hiemalis and 

Absidia glauca have predominantly uninucleate 

spores (Storck & Morrill, 1977) whilst M. mucedo, 

P. blakesleeanus, Rhizopus stolonifer and Syzygites 

megalocarpus have multinucleate spores 

(Hammill & Secor, 1983). The number of spores 

formed is very variable. On nutrient-poor media 

minute sporangia containing very few spores 

may be formed, but in P. blakesleeanus the number 

of spores may be as high as 50 000 100 000 in a 

single sporangium of normal size. 

The ultrastructure of developing sporangia 

of Gilbertella has been studied by Bracker 

(1968a) and is essentially similar in multisporous 

columellate sporangia of other Mucorales, 

e.g. M. mucedo (Hammill, 1981) and Zygorhynchus 

heterogamus (Edelman & Klomparens, 1994). One 

difference is that in M. mucedo mitotic division 

continues during sporangial development, which 

has not been reported from the other species 

studied. The cleavage of the sporangial cytoplasm 

to form spores is accomplished by the 

fusion of membranous cleavage vesicles lined by 

electron-opaque granules. The vesicles are at first 

globose but coalesce and become flattened to 

form cleavage furrows. A three-dimensional network 

of cleavage furrows envelops the individual 

spore protoplasts, radiating outwards until they 

fuse with the sporangial plasma membrane. 

After cleavage, the flattened membrane which 

bounded the cleavage vesicle persists as the 

plasma membrane of the sporangiospore, 

whereas the electron-opaque granules make up 

part of the spore wall (Fig. 7.7). The columella 

is delimited from the rest of the sporangium by 

a process similar to that which cuts out the 

spores. Edelman and Klomparens (1994) noted 

that in Z. heterogamus the wall of the sporangium 

contains chitin, but the walls of the sporangiospores 

and columella do not. They have suggested 

that the columella may be a source of 

chitinase which causes enzymatic degradation of 

the mature sporangial wall whilst not affecting 

the walls of the spores or the columella itself. 

Fig 7.7 Zygorhynchus heterogamus. Diagrammatic interpretation of ultrastructural transition from cleavage furrows isolating spore 

protoplasts (a) to post-cleavage spores (b). (a) shows the cleavage furrow membrane (1), an electron-translucent layer (2), a layer of 

fusing electron-opaque granules (3), an electron-transparent zone (5) and the electron-translucent matrix of the cleavage furrow 

(6). (b) shows the spore plasma membrane which was initially the cleavage furrow membrane (1), an electron-translucent layer (2), 

the electron-opaque layer which originated from the fusing granules of the cleavage furrows (3), an additional electron-translucent 

layer which had no corresponding layer within the cleavage furrows (4), a uniform zone of electron transparency, similarly placed in 

the cleavage furrows (5), and a non-uniform granular matrix separating the spores (6).Redrawn with permission from Edelmann and 

Klomparens (1994), Mycologia. ßThe Mycological Society of America.


173 

The sporangial wall is sometimes colourless 

or yellow, but it often darkens and develops a 

spiny surface due to the formation of crystals of 

calcium oxalate dihydrate (weddellite) beneath 

the surface layer (Fig. 7.14c; Jones et al., 1976; 

Urbanus et al., 1978; Whitney & Arnott, 1986). In 

some species similar crystals may develop on the 

sporangiophore. A possible function ascribed to 

these structures is that they form a barrier 

against grazing arthropods. 

Despite the apparent similarity in sporangial 

structure across members of the Mucorales, 

spore liberation may be brought about by two 

different mechanisms (Ingold & Zoberi, 1963; 

Zoberi, 1985). In many of the commonest species 

of Mucor (e.g. M. hiemalis), the sporangium wall 

dissolves and the sporangium becomes converted 

at maturity into a ‘sporangial drop’ adhering to 

the columella. Sporangial walls which dissolve in 

this way are said to be diffluent. In large 

sporangia, for example of M. plasmaticus, M. 

mucedo and Phycomyces, the spores are embedded 

in mucilage. The sporangial wall does not break 

open spontaneously, but the slimy contents 

exude when the wall is touched. Such sticky 

spore masses are distributed by insects or rain 

splash, or by wind after drying. In the second 

spore liberation mechanism, the sporangial wall 

breaks into pieces, and here air currents or 

mechanical agitation readily liberate spores. An 

example of this is Mucor plumbeus (Figs. 7.14c,d). 

In M. plumbeus the columella terminates in 

one or more finger-like or spiny projections 

(Fig. 7.14d), and in some Absidia spp. the 

columella may also bear a single nipple-like 

projection (Fig. 7.17b). In Rhizopus stolonifer the 

columella is large, and as the sporangium dries 

the columella collapses so that it appears like a 

basin balanced at the end of the sporangiophore 

(Fig. 7.16d). Associated with these changes in 

columella shape, the sporangium wall breaks up 

into many fragments and the dry spores can 

escape in air currents. 

7.2.5 Sexual reproduction 

The Mucorales reproduce sexually by a process of 

gametangial conjugation resulting in the formation 

of zygospores. By strict definition, what we 

describe as a zygospore is actually a zygosporangium, 

the dark warty ornamentation representing 

its outer wall (Benny et al., 2001). 

According to this definition the zygosporangium 

contains a single globose zygospore, sometimes 

referred to as the zygospore proper. For convenience, 

we continue to use the term ‘zygospore’ 

in a wide sense. 

Some species are homothallic, zygospores 

being formed in cultures derived from a 

single sporangiospore (e.g. Rhizopus sexualis, 

Syzygites megalocarpus, Zygorhynchus moelleri and 

Absidia spinosa). However, the majority of species 

are heterothallic and only form zygospores 

when compatible strains are mated together. 

It is believed that homothallic species are derived 

from heterothallic ancestors (O’Donnell et al., 

2001). There is, in reality, no absolute distinction 

between the homothallic and heterothallic 

conditions because some species normally 

homothallic or heterothallic are ambivalent, i.e. 

they can change their mating behaviour under 

certain conditions (Schipper & Stalpers, 1980). 

Zygospore formation is affected by environmental 

conditions, being generally favoured by 

darkness (Hesseltine & Rogers, 1987; Schipper, 

1987). The effects of temperature are variable. In 

Mucor piriformis lower temperatures (0 15°C, 

optimum 10°C) favour zygospore formation, 

whilst for Choanephora cucurbitarum the optimum 

is 20°C (Michailides et al., 1997). 

In heterothallic species, if the appropriate 

strains are inoculated at opposite sides of a Petri 

dish, the mycelia grow out and a line of 

zygospores develops where they meet (Fig. 7.8). 

The two compatible strains rarely differ from 

each other in any obvious morphological or 

physiological features, although there may be 

slight differences in growth rate and carotenoid 

content. Because it was not possible to designate 

one strain as male and the other as female, 

Blakeslee (1906) labelled them (þ) and ( ). 

The two compatible strains are said to differ in 

mating type. The morphological events preceding 

zygospore formation are sufficiently similar 

to allow a general description of the process. 

When two compatible strains approach each 

other, three reactions can be distinguished.


Fig 7.8 Phycomyces blakesleeanus.Maltagarplate5days 

after inoculation with a (þ)anda( )strain.Alineof 

black zygospores has been produced where the two 

mycelia have met. 

(1) A ‘telemorphotic reaction’ which involves 

the formation of aerial (or occasionally 

submerged) swollen hyphal tips. These are 

called zygophores or, when they have made 

contact with each other, progametangia. They 

are often coloured yellow due to a high b- 

carotene content. (2) A ‘zygotropic reaction’, in 

which directed growth of zygophores of (þ) and 

( ) mating partners towards each other is 

observed. (3) A ‘thigmotropic reaction’, i.e. 

a touch response involving the events which 

occur after contact of the respective zygophores, 

such as gametangial fusion and septation of 

the progametangia to form gametangia and 

suspensors. 

Hormonal control of sexual reproduction 

The mating process is under the control of 

mating hormones (sex hormones, gamones, 

pheromones), and the hormones involved are 

effective in all members of the Mucorales studied 

(see Gooday, 1994; Gooday & Carlile, 1997). Early 

evidence of the involvement of pheromones 

was the demonstration that in Mucor mucedo the 

mating process can be initiated between mycelia 

of different mating types separated by a collodion 

membrane. The effect of the mating 

hormone is to switch the vegetative mycelium 

from asexual to sexual development. Other 

effects are the accumulation of carotenoids in 

cultures containing both mating types and, in 

Phycomyces, of a marked reduction in the growth 

rate of the vegetative mycelia as they approach 

each other (Drinkard et al., 1982). The mating 

hormones have been identified as trisporic acid, 

actually a family of structurally related molecules, 

and its precursors. Trisporic acid was so 

named after Blakeslea trispora (see Fig. 7.27) from 

which this substance was first isolated (Austin 

et al., 1969; Sutter, 1987). Liquid media inoculated 

with a mixture of (þ) and ( ) spores of 

B. trispora developed more intense yellow pigmentation 

than unmated cultures due to a 

massive stimulation of b-carotene synthesis. 

Trisporic acid itself is derived from b-carotene 

(see Fig. 7.9) and is synthesized by collaborative 

metabolism of the two different mating type 

strains. Each strain has an incomplete enzyme 

pathway for the synthesis of trisporic acid so that 

intermediates accumulate which can only be 

metabolized further by mycelium of the opposite 

mating type. As shown in Fig. 7.9, the enzymatic 

steps in the conversion of b-carotene (I) to 

4-dihydrotrisporol (III) via retinal (II) are 

common to both mating types. The (þ) strain 

can convert 4-dihydrotrisporol to methyl-4-dihydrosporate 

(IV), whereas the ( ) strain converts 

4-dihydrotrisporol to trisporol (V). Thus IV and V 

function as two complementary prohormones, 

each of which is inactive in its own mycelium


175 

but is converted to the active hormone trisporic 

acid after diffusion into the mycelium of the 

complementary strain (Gooday, 1994). Trisporic 

acid stimulates further synthesis of b-carotene 

and of the two prohormones, leading to amplification 

of its own synthesis by a ‘cascade’ 

mechanism. The 15 20-fold enhanced synthesis 

of b-carotene upon mating of two compatible 

strains of B. trispora holds potential for commercial 

production of this substance (Lampila et al., 

1985; Sandmann & Misawa, 2002). 

The role of the trisporic acid in inducing 

b-carotene synthesis and zygophore formation is 

widespread in the Mucorales, having been 

characterized in Blakeslea, Phycomyces, Mucor and 

even Mortierella (Schimek et al., 2003). It is also 

known that trisporic acid is involved in the 

sexual response of some homothallic Mucorales 

such as Zygorhynchus moelleri, Mucor genevensis and 

Syzygites megalocarpus (Lampila et al., 1985). The 

common nature of the hormones of homothallic 

and heterothallic species could also be inferred 

from earlier observations of attempted matings 

between such forms, either at the interspecific or 

intergeneric level. 

Zygophores show directional growth towards 

each other in response to volatile hormones. 

Gooday (1994) has suggested that these may be 

the mating type-specific prohormones, methyl- 

4-dihydrosporate of the (þ) strain and trisporol of 

the ( ) strain. 

Thigmotropic reactions 

When compatible zygophores make contact, they 

become firmly attached to each other and 

develop into progametangia. In Mucor mucedo 

there is evidence that the cell wall chemistry of 

the zygophores is distinct from that of the 

vegetative mycelium and that the (þ) and ( ) 

zygophores are bound together by lectins, i.e. 

glycoproteins exhibiting specific binding for 

polysaccharides (Jones & Gooday, 1977). In 

Fig 7.9 Collaborative biosynthesis of trisporic acid 

by cross-feeding of intermediates between (þ)and 

( ) mating types of Blakeslea trispora. b-Carotene 

(I) is metabolizedby both (þ)and( ) mating-types 

via retinal (II) to 4-dihydrotrisporol (III).This is 

metabolized by (þ)strainsto 

4-dehydrosporic acid and its methyl ester (IV)and 

by ( ) strains to trisporol (V).These are converted 

to trisporic acid (VI) only after diffusing to the ( ) 

and (þ) strains, respectively. Redrawn from 

Gooday (1994), with kind permission of Springer 

Science and Business Media.


Phycomyces, after arrest of the growth of vegetative 

hyphae, certain submerged hyphal tips 

develop short branches called ‘knobbly knots’ 

(Fig. 7.18) which break through the surface of the 

agar and become progametangia (O’Donnell 

et al., 1976; Sutter, 1987). The progametangia 

become tightly appressed and their close contact 

is enhanced by the formation of extracellular 

fimbriae whose presence appears to be essential 

for further development in Phycomyces (Yamakazi 

& Ootaki, 1996) as well as in other groups of 

fungi (see p. 652). Fimbriae may be the lectinbearing 

structures. In other Mucorales the 

zygophores are aerial and club-shaped. The tip 

of each progametangium becomes cut off by a 

septum to separate a distal multinucleate gametangium 

from the subterminal suspensor (see 

Fig. 7.10). 

The walls separating the two gametangia 

break down so that the numerous nuclei from 

each cell become surrounded by a common 

cytoplasm. The fusion cell, or zygote, swells and 

develops a dark warty outer layer to become the 

zygospore. 

Cytology of zygospore formation 

There have been numerous accounts of the 

cytology of zygospore formation. Meiosis usually 

occurs before zygospore germination, so that the 

zygospore can be regarded as a meiosporangium. 

Four main types of nuclear behaviour can be 

distinguished. 

(1) In Mucor hiemalis, Absidia spinosa and some 

other species, all the nuclei fuse in pairs within a 

few days, then quickly undergo meiosis so that 

the mature zygospore contains only haploid 

nuclei. 

(2) In Rhizopus stolonifer and Absidia glauca, 

some of the nuclei entering the zygospore do not 

pair, but degenerate. The remainder fuse in 

pairs, but meiosis is delayed until germination 

of the zygospore. 

(3) In Phycomyces blakesleeanus, the haploid 

nuclei continue to divide mitotically in the 

young zygospore and then become associated in 

groups, with occasional single nuclei also 

present. Before germination some of the nuclei 

pair up, and in the germ sporangium diploid 

nuclei and also haploid nuclei are found; some of 

these may be products of meiosis, others may 

represent the scattered solitary nuclei which 

failed to pair up. 

(4) In Syzygites megalocarpus mitotic nuclear 

divisions continue in the young zygospore, but 

nuclear fusion and meiosis apparently do not 

occur. This fungus can therefore be described as 

amictic (Burnett, 1965). 

The fine structure of zygospore development 

has been studied in the homothallic Rhizopus 

sexualis (Hawker & Beckett, 1971; Ho & Chen, 

1998). Following contact of the tips of the two 

zygophores, their walls adhere to each other and 

become flattened (Figs. 7.10a c) to form the 

fusion septum. On either side of the fusion 

septum, each cell becomes distended to form 

a progametangium. In each progametangium, 

an oblique septum, concave to the developing 

zygospore, develops by gradual inward extension 

mediated by the coalescence of vesicles. When 

the septum is complete, it separates the terminal 

gametangium from the progametangial base 

now called the suspensor. However, cytoplasmic 

continuity between the suspensor and the 

gametangium persists through a series of pores 

which probably enable nutrients to flow into the 

developing zygospore from the surrounding 

mycelium. Numerous nuclei congregate on 

either side of the fusion septum. It has been 

estimated that there may be over 150 nuclei in 

a pair of progametangia, but the number 

may rise to over 300 in a pair of completely 

delimited gametangia, reflecting further nuclear 

divisions. 

The breakdown of the fusion septum is 

associated with an accumulation of vesicles in 

the vicinity of the dissolving wall. These may 

contain wall-degrading enzymes. The fusion 

septum is completely dissolved, and once the 

cytoplasmic contents of the two gametangia are 

continuous, the nuclei become arranged in the 

periphery of the cytoplasm. In R. sexualis, itis 

probable that most of the gametangial nuclei 

fuse in pairs immediately, and that the fusion 

nuclei then quickly divide. 

Even before dissolution of the fusion wall is 

complete, the primary outer wall of the zygote 

thickens, and beneath this original wall, the 

warts (which will eventually ornament the wall


177 

Fig 7.10 Rhizopus sexualis.(a g) Successive stages in the 

formation of zygospores.The fungus is homothallic. 

of the mature zygospore) are initiated as widely 

separated patches shaped like inverted saucers 

(Fig. 7.11c). The cytoplasm fills the domes of the 

‘saucers’ and also balloons out between them, 

enveloped by the plasmalemma. As the zygospore 

continues to enlarge, the saucers change in 

shape and size to resemble inverted flower pots 

which increase in size by the addition of new 

material at their rims until they are contiguous. 

From this moment onwards, electron microscopy 

fixatives can no longer penetrate, explaining 

why cytological studies of later stages of 

zygospore development have proven difficult. 

Eventually, the tips of the warts become pushed 

through the original primary wall. At least three 

wall layers are deposited beneath the original 

primary wall (Fig. 7.11g). The darkening of the 

wall is probably due to the deposition of 

melanin. The sculpturing of the zygospore wall 

of other members of the Mucorales, as seen by 

scanning electron microscopy, shows different 

patterns, ranging from circular or conical warts 

to branched stellate warts. Essentially similar 

zygospore development has been reported in 

the heterothallic Gilbertella persicaria (O’Donnell 

et al., 1977a). 

In M. mucedo and P. blakesleeanus, the wall of 

the zygospore is rich in sporopollenin (Gooday 

et al., 1973; Furch & Gooday, 1978). This substance, 

which is also present in the walls of 

pollen grains, is extremely resistant to degradation 

and enables zygospores to remain dormant 

but undamaged in the soil for long periods. 

Sporopollenin is formed by oxidative polymerization 

of b-carotene, and this may explain the 

high content of this pigment in developing 

zygophores. However, b-carotene and sporopollenin 

appear to be absent from the zygospore 

walls of R. sexualis (Hocking, 1963). 

Zygospore investment 

In Phycomyces and Absidia, the suspensors may 

bear appendages which arch over the zygospore. 

In Phycomyces the suspensor appendages are black


Fig 7.11 Development of the zygospore wall in Rhizopus sexualis (diagrammatic, after Hawker & Beckett,1971). (a) Primary wall 

before inflation of zygospore, showing thin electron-dense outer layer, thicker less electron-dense inner one, and scattered 

lomasome-like bodies. (b) Blocks of secondary material (wart initials) developing locally on inner surface of primary wall. (c) Wart 

initials growing by deposition of secondary material at the rims to give saucer-shapedpigmentedmasses. (d) Warts becoming flower 

pot shaped by further growth at rims, inner layer of primary wall becoming gelatinous and swollen. Note pockets of cytoplasm 

between warts. (e) Rims of warts nearly touching, inner layer of primary wall showing stress lines, pockets of cytoplasm between 

warts much reduced. (f) Edges of warts touching, warts lined with tertiary smoothing layer, outer layer of primary wall torn. 

(g) Thick stratified impermeable layer of quaternary material laid down inside smoothing layer, inner gelatinous layer of primary 

wall has collapsed as a horny skin enveloping the warts. 

and forked, whilst in Absidia they are hyaline 

and coiled or curved inwards (see Figs. 7.17, 7.18). 

The function of such appendages is unknown; 

possibly they assist in attaching zygospores to 

passing animals. The forked appendage tips 

of Phycomyces bear a drop of liquid, and they 

have been interpreted as hydathodes (i.e. watersecreting 

structures). In the homothallic species 

A. spinosa the appendages arise on only one 

suspensor. 

Mating behaviour 

Analysis of the results of crosses involving several 

genes suggest that there is a single mating type 

locus with two alternative alleles, (þ) and ( ), 

which segregate at meiosis. However, no DNA 

sequences of this locus have as yet been 

published, and there are also a number of 

anomalous results for which a full cytological 

explanation is still awaited. 

Hybridization experiments have been 

conducted between different species and genera 

of Mucorales, and in some cases imperfect 

zygospores are formed. Attempted copulation 

has also been observed between homothallic and 

heterothallic strains. An unusual type of mating 

behaviour has been discovered in Mucor pusillus 

which is predominantly heterothallic but in 

which homothallic strains are known. It has 

been possible to induce a (þ) strain to mutate 

to a ( ) strain, and also to a homothallic strain 

by g-irradiation (Nielsen, 1978). 

7.2.6 Zygospore germination 

After a resting period the zygospore may germinate 

by developing a germ sporangium which 

resembles an ordinary sporangium and contains 

sporangiospores of the normal type. In some 

cases vegetative mycelium develops from the 

germinating zygospore. The conditions for zygospore 

germination are, in many cases, imperfectly 

known, but a protocol for germination 

has been established for Phycomyces blakesleeanus 

(Eslava & Alvarez, 1987). Mature zygospores


179 

collected from 6-week-old cultures and placed on 

moist filter paper at 22°C under alternating 

light/dark illumination will germinate after 

about 8 days, reaching maximum germination 

after a further 8 10 days. In Mucor piriformis, the 

germination rate is highest in fresh zygospores 

(Guo & Michailides, 1998), a vigorous germ tube 

emerging through one of the suspensors or 

through a crack in the zygospore wall. The 

germ tube may continue development as mycelium 

or grow into the air and form a germ 

sporangium at the tips of single or branched 


Mating-types represented in germ sporangia 

The distribution of mating types amongst the 

germ spores which are present in germ sporangia 

falls into three categories. 

1. Pure germinations in which all the spores 

are homothallic, e.g. in Mucor genevensis, 

Zygorhynchus dangeardi and Syzygites megalocarpus. 

2. Pure germinations in which all sporangiospores 

are of one mating type, i.e. all (þ) 

or all ( ). Mucor mucedo, M. hiemalis and 

P. blakesleeanus generally behave in this way. In 

P. blakesleeanus, the analysis of progeny from 

crosses involving up to four unlinked factors 

which included mating type were best explained 

on the basis of the survival of a single diploid 

nucleus from the thousands which are present 

in the young zygospore (Cerdá-Olmedo, 1975; 

Eslava et al., 1975a,b). This single diploid nucleus 

undergoes meiosis and one or more of the 

resultant nuclei divide mitotically to provide 

nuclei for the germ sporangium (Fig. 7.12). 

Occasionally two or three diploid nuclei may 

survive and undergo meiosis. In some germ 

sporangia heterokaryotic spores are present. If 

these are heterokaryotic for mating type, the 

mycelium which develops from them may be 

abnormal and ‘neuter’, i.e. it is unable to mate 

with (þ) as well as ( ) strains. 

3. Mixed germinations. In Phycomyces nitens, 

the same germ sporangium sometimes contains 

(þ), ( ) and homothallic (i.e. self-fertile) spores. 

The finding that diploid nuclei enter the 

germ sporangia may be the explanation for the 

presence of homothallic spores which should 

properly be described as secondarily 

homothallic. Mixed germinations have also 

been reported by Gauger (1961) for Rhizopus 

stolonifer in which both (þ) and ( ) spores were 

present in some germ sporangia, whereas others 

contained spores of either mating type. For this 

type of mixed germination to occur, it would 

be necessary only to postulate the survival of 

more than one meiotic product so that both 

mating types are represented in the sporangium. 

‘Neuter’ spores were found in some germ 

sporangia. Thus, in Choanephora cucurbitarum 

mixed germinations have been reported in 

which the majority (usually all) of the germ 

sporangia contained only either (þ) or( ) spores, 

but a low proportion gave heterokaryotic spores 

of mating-type (þ/ ). A characteristic feature of 

C. cucurbitarum cultures derived from heterokaryotic 

(þ/ ) germ spores or fusion of (þ) with ( ) 

protoplasts is that they produce azygospores 

(Yu & Ko, 1996, 1999; see below). 

7.2.7 Azygospores 

In some Mucorales, if gametangial copulation 

fails to take place normally, one or both 

gametangia may give rise parthenogenetically 

to a structure morphologically similar to the 

zygospore, termed an azygospore (azygosporangium). 

Azygospores therefore usually appear as 

warty spherical structures borne on a single 

suspensor-like cell, or occasionally on a sporangiophore. 

They are formed regularly in cultures 

of Mucor bainieri and M. azygospora (Fig. 7.13), both 

of which are obligately azygosporic and do not 

form true zygospores (Benjamin & Mehrotra, 

1963), and they have also been reported in 

Rhizopus azygosporus (Yuan & Yong, 1984). The 

development of azygospores of M. azygospora 

resembles that of normal zygospores in other 

Mucorales (O’Donnell et al., 1977b; Ginman & 

Young, 1989). Azygospore formation may occur 

in intergeneric and interspecific crosses, for 

example in crosses between a (þ) strain of 

Gilbertella persicaria and a ( ) strain of Rhizopus 

stolonifer (O’Donnell et al., 1977c) and between 

different species of Rhizopus (Schipper, 1987). 

Azygospore development has also been seen 

in intraspecific crosses, e.g. in certain isolates 

of M. hiemalis (Gauger, 1966, 1975). These azygosporic 

isolates of M. hiemalis were derived from


Fig 7.12 Life cycle of Phycomyces blakesleeanus (diagrammatic and not to scale). From a coenocytic haploid mycelium of either 

mating type (þ)or( ), sporangiophores develop. Sporangia are columellate and contain numerous sporangiospores which, in 

P. blakesleeanus, are multinucleate.When hyphae of both mating types meet, sexual reproduction is initiated by the formation of 

knobbly zygophores which develop into progametangia. Each progametangium divides into a gametangium and a suspensor, the 

latter ornamented by black forked appendages. Plasmogamy (P) occurs by lysis of the wall separating the two multinucleate 

gametangia.This is followed by mass karyogamy (K), but only one of the numerous diploid fusion nuclei seems to undergo 

meiosis (M), and only one of the resulting tetrad nuclei survives in the zygospore during dormancy, so that the sporangiospores 

in the germ sporangium are usually of either one or the other mating type.Open and closed circles represent haploid nuclei of 

opposite mating type; diploid nuclei are larger and half-filled. 

spores of germ sporangia developed from normal 

zygospores. If the azygosporic strains are subcultured, 

either from single sporangiospores or by 

mass transfer, they show a tendency to ‘break 

down’ to strains of (þ) or ( ) mating type of 

normal appearance. It seems that azygosporic 

strains of M. hiemalis are typically diploid and 

heterozygous for mating type, i.e. the diploid 

nucleus carries both (þ) and ( ) mating type 

alleles. The breakdown to the normal (þ) or( ) 

mating type condition may be brought about 

by somatic (i.e. non-meiotic) reduction leading to 

aneuploid intermediates, and finally to haploids. 

The germination of azygospores is unknown. 

7.3 Examples of Mucorales 

As mentioned before, the traditional family 

classification within the Mucorales is artificial 

(see Benny et al., 2001; Tanabe et al., 2004), 

and we use it here solely for convenience of 

presentation. 

7.3.1 Mucoraceae 

Mucor 

About 50 species of Mucor are currently known 

(Kirk et al., 2001). The genus is cosmopolitan, with

EXAMPLES OF MUCORALES 

181 

Fig 7.13 Azygospore of Mucor azygospora.Originalimage 

kindly provided byT.W.K.Young. 

many species being widespread in soil or 

on substrates in contact with soil. Most species 

are mesophilic (growing at 10 40°C with an 

optimum 20 35°C), but some, e.g. M. miehei or 

M. pusillus (sometimes classified as species of 

Rhizomucor; see Mouchacca, 1997, 2000) are 

thermophilic, with a minimum growth temperature 

of about 20°C and a maximum extending up 

to 60°C (Cooney & Emerson, 1964; Maheshwari 

et al., 2000). Mucor indicus and M. circinelloides are 

used as starters in food processing to break down 

starchy polysaccharides in rice, cassava and 

sorghum, releasing simple sugars for the 

preparation of fermented foods or alcohol 

production (Hesseltine, 1991). 

Most species of Mucor grow rapidly on agar 

at room temperature, filling a Petri dish in 

2 3 days with their coarse aerial mycelium. 

When incubated in liquid culture under semianaerobic 

conditions, several species grow in 

a yeast-like state. The ability to switch between 

the yeast-like and filamentous state is termed 

dimorphism, a phenomenon which has been 

studied in greatest detail in M. rouxii (see 

Fig. 7.14), but also occurs in M. circinelloides, 

M. fragilis, M. hiemalis, M. lusitanicus and in other 

Mucorales (Orlowski, 1991, 1995). Sporangia are 

globose and borne on branched and unbranched 

sporangiophores growing into the air. The 

columella is large and typically elongated 

(Figs. 7.2 and 7.3). Zygospores are rarely formed 

in agar culture because most species are heterothallic. 

Amongst the most common species from 

soil are M. hiemalis, M. racemosus and M. spinosus 

(Domsch et al., 1980). Several species of Mucor, 

e.g. M. mucedo, fruit on dung (Ellis & Ellis, 1998; 

Richardson & Watling, 1997), and they are the 

earliest fungi to appear in the succession of 

fungal fruit bodies on this substrate (Dix & 

Webster, 1995). The sporangiospores of coprophilous 

Mucor spp. survive digestion by herbivorous 

mammals. 

A few species of Mucor are human pathogens. 

The term mucormycosis, however, usually refers 

to conditions caused by Mucorales generally 

rather than the genus Mucor (Rinaldi, 1989; 

Eucker et al., 2001) because it is not possible to 

identify species by the microscopic appearance 

of their coenocytic mycelium within diseased 

tissue. Diagnosis is dependent on the isolation 

and identification of the suspected pathogen in 

culture, sometimes post mortem. By these means, 

several ubiquitous species of Mucor have been 

associated with disease symptoms, including 

M. circinelloides, M. hiemalis and M. racemosus. 

Infections are opportunistic, derived from sporangiospores 

present in the soil or air, and are 

usually associated with patients suffering from 

other diseases such as diabetes, leukaemia, 

AIDS and post-operative conditions. There are 

no records of person-to-person transmission. 

Mucormycoses are serious, even fatal in immunocompromised 

patients, although some can be 

successfully treated by surgery and antibiotics 

such as amphotericin B (Kwon-Chung & Bennett, 

1992). 

Schipper (1978) has given a key to 49 species 

of Mucor, and Watanabe (1994) has described the 

six homothallic and two azygosporic species.


Fig 7.14 Mucor racemosus (a,b) and M. plumbeus (c,d). (a) Tip of a sporangiophore which has formed a sporangium.The columella 

(arrow) is visible. (b) Lower region of sporangiophores showing intercalary thick-walled chlamydospores which are typical of the 

species. (c) Sporangium with a spiny surface of calcium oxalate crystals. (d) Exposed columellae with finger-like projections. (a,b) to 

same scale; (c,d) to same scale. 

Zygorhynchus 

There are about six species, mostly reported from 

soil, often from considerable depth (Hesseltine 

et al., 1959). All species are homothallic and, 

unusually, form heterogametangic zygospores 

(Fig. 7.15). The sporangiophores are commonly 

branched and the columella is often broader than 

high. The most frequently encountered species is 

Z. moelleri, which has been isolated worldwide 

from a range of soils and from the rhizosphere of 

numerous plants (Domsch et al., 1980). Most 

species are mesophilic, but Z. psychrophilus forms 

zygospores readily at 5°C. Sporangium development 

in Z. heterogamus has been studied by 

Edelmann and Klomparens (1994) (see p. 171). 

Zygospore development and structure in several 

species of Zygorhynchus have been described by 

O’Donnell et al. (1978a). The warts on the outside 

of the zygosporangia often appear as interlocking, 

starfish-like pointed thickenings. The inner 

wall of the zygosporangium is ornamented by a 

network of ridges and grooves radiating from 

centres corresponding to the points of the warts. 

The outer wall of the zygospore proper, lying 

within the zygosporangium, is similarly 

ornamented by a pattern of radiating grooves 

and ridges which are a template of the lining 

of the zygosporangial wall. 

Rhizopus 

There are about 10 species which grow in soil 

(Domsch et al., 1980) and on fruits, other foods 

and all kinds of decaying materials. Rhizopus spp. 

also occur frequently as laboratory contaminants. 

Rhizopus stolonifer (syn. R. nigricans) grows 

rapidly. It is often found on ripe fruits, especially 

if these are incubated in a moist atmosphere (see 

Plate 3d). Characteristic features of Rhizopus are 

the presence of rhizoids at the base of the 

sporangiophores (which may grow in clusters), 

and the stoloniferous habit (Fig. 7.16). An aerial 

hypha grows out, and where it touches on the 

substratum it bears rhizoids and sporangiophores. 

Growth in this manner is repeated. The 

sporangium wall is brittle and the sporangiospores 

are dry and wind-dispersed. Some species 

of Rhizopus, e.g. R. oryzae, R. microsporus and its 

allies, are used as starters in ragi fermentations 

of rice (Hesseltine, 1991). Several species 

(R. arrhizus, R. microsporus, R. rhizopodiformis) are


183 

Fig 7.15 Zygorhynchus moelleri. 

(a) Zygospore and sporangium. 

(b) Young sporangiophores. 

(c) Dehisced sporangia. (d g) Stages 

in zygospore formation. Note that 

the fungus is homothallic and that the 

suspensors are unequal. 

human pathogens associated with mucormycosis 

(Rinaldi, 1989). Most species of Rhizopus are 

heterothallic, but R. sexualis is homothallic and 

forms zygospores freely within 2 days in the 

laboratory (see Fig. 7.10). 

Rhizopus microsporus causes rice seedling 

blight in which root growth is strongly impaired 

by a toxin, rhizoxin, excreted by the soil-borne 

pathogen. The toxin binds to b-tubulin, thereby 

interfering with mitosis. Intriguingly, it is 

synthesized not by R. microsporus but by bacteria 

(Burkholderia spp.) living endosymbiotically 

within the cytoplasm of Rhizopus hyphae 

(Partida-Martinez & Hertweck, 2005). Bacterial 

endosymbionts have been reported only rarely 

from fungi, e.g. in the zygomycete Geosiphon 

pyriforme (p. 221), or within hyphae of the 

ascomycete Morchella elata (p. 427) and the 

basidiomycete Laccaria bicolor (p. 552). 

Absidia 

There are some 20 species growing in soil 

(Domsch et al., 1980). Characteristic features are 

pear-shaped sporangia arising in partial whorls 

along stolon-like branches which produce 

rhizoids at intervals but not opposite the


that many workers confused the two and much 

of the early literature on P. nitens probably refers 

to P. blakesleeanus. Neither species is particularly 

common, but likely substrata are fatty products 

and empty oil casks. Bread, dung and decaying 

hops are other recorded substrata. The zygospores 

are unusual in that they are overarched 

by black, forked suspensor appendages (see 

Fig. 7.18; O’Donnell et al., 1976, 1978b). Great 

interest has been focused on the development 

and sensory perception of the spectacularly 

large sporangiophore, especially to light (see 

pp. 169 171), and on the genetics of Phycomyces 

(Eslava & Alvarez, 1987). The genus has been 

classified in the family Phycomycetaceae by 

Benny et al. (2001). 

Fig 7.16 Rhizopus stolonifer. (a) Habit sketch, showing 

stolon-like branches which develop rhizoids and tufts of 

sporangiophores. (b) Two sporangiophores showing basal 

rhizoids. (c) Dehisced sporangium showing the columella 

with attached spores. (d) Invaginated columella. 

sporangiophores. The zygospores are surrounded 

by curved unbranched suspensor appendages 

which may arise from either or both suspensors 

(Fig. 7.17). Most species are heterothallic but 

A. spinosa is homothallic. Absidia glauca and 

A. spinosa are amongst the most commonly 

isolated species. Absidia corymbifera is a human 

pathogen. 

Phycomyces 

The two best-known species are P. blakesleeanus 

and P. nitens. The sporangiospores of P. nitens are 

larger than those of P. blakesleeanus, but it is likely 

Syzygites 

Syzygites megalocarpus (¼ Sporodinia grandis; see 

Hesseltine, 1957) is found on the decaying 

basidiocarps of various toadstools, especially 

Boletus, Lactarius and Russula. It grows readily in 

culture and is homothallic. Probably because of 

this fact it was the first member of the Mucorales 

for which sexual reproduction was described in 

detail (Davis, 1967). The sporangiophores are 

dichotomous and bear thin-walled sporangia 

(Fig. 7.19a). In culture, light is essential for the 

development of sporangiophores but has no 

effect on zygospore formation. Lowering of the 

osmotic potential markedly stimulates zygospore 

development and this is possibly significant 

ecologically in that the drying out of basidiocarp 

tissue on which the fungus grows might induce 

the development of the zygosporic (resting) state 

(Kaplan & Goos, 1982). 

7.3.2 Pilobolaceae 

There are two common genera, Pilobolus and 

Pilaira, which grow on the dung of herbivores. 

Both genera have evolved mechanisms to ensure 

that their sporangia escape from the vicinity of 

the dung patch on which they were produced. In 

Pilobolus the sporangiophore is swollen and 

the sporangium is shot away violently by a jet 

of liquid, whilst in Pilaira the sporangiophore 

is elongated and the sporangium becomes 

converted into a sporangial drop, breaking off


185 

Fig 7.17 Absidia glauca. (a) Habit showing whorls of 

pear-shaped sporangia. (b) Intact and dehisced sporangia. 

Note the single pointed projection on certain columellae. 

(c) Zygospore showing the arching suspensor appendages. 

upon contact with an object. The sporangia are 

black and melanized, presumably as a protection 

against UV irradiation. Grove (1934) has written 

a monograph of the family which has stood 

the test of time. 

Pilobolus 

The generic name means literally the ‘hat 

thrower’, referring to the sporangial discharge 

mechanism. If fresh herbivore (e.g. rabbit, 

sheep, deer, horse) dung is incubated in light, 

the characteristic bulbous sporangiophores of 

Pilobolus appear after a preliminary phase of 

fruiting of Mucor which may last for 4 7 days 

(Fig. 7.20, Plate 3f). Nine Pilobolus spp. previously 

recognized have been reduced to five, but 

including a number of varieties (Hu et al., 1989). 

Common species are P. crystallinus, P. kleinii (¼ 

P. crystallinus var. kleinii), and P. umbonatus (¼ 

P. roridus var. umbonatus). Here we adopt the 

nomenclature proposed by Grove (1934). As far as 

is known all members of the Pilobolaceae are 

heterothallic. 

A full account of the development and 

discharge of the sporangium has been given by 

Buller (1934) and Ingold (1971). Discharged 

sporangia of Pilobolus become attached to vegetation 

surrounding the dung on which they were 

produced. When the vegetation is eaten by a 

herbivore, the spores are released into the gut. 

In the voided faeces, the spores germinate to 

form a mycelium. After about 4 days, the 

mycelium near the surface of the dung pellet 

forms trophocysts, swollen hyphal segments 

coloured yellow by carotenoids (Fig. 7.20). 

Sporangiophores develop from the trophocysts 

in a regular daily sequence, and the stage of 

development can be correlated with the time of 

day. During the late afternoon the sporangiophore 

grows away from the trophocyst towards 

the light and during the night its tip enlarges to 

become the sporangium. The swelling of the 

subsporangial vesicle takes place mainly between 

midnight and the early morning. Young sporangiophores 

are highly phototropic even before 

their sporangia are differentiated, and the 

clear tip of the developing sporangiophore is


Fig 7.18 Phycomyces blakesleeanus.Stagesin 

zygospore formation.The fungus is 

heterothallic. (a) Zygophores consisting of 

knobbly hyphal branch tips which become 

closely appressed. (b) Paired club-shaped 

progametangia which develop from the 

appressed zygophores. (c) Septation of the 

progametangia to form terminal gametangia 

and subterminal suspensors. Appendages 

are developing on the suspensor to the right. 

(d) Young zygospore overarched by 

dichotomous suspensor appendages. 

the sensitive region. Despite the bright yellow 

carotenoid deposits in the trophocysts and young 

sporangiophores, studies of the phototropic 

response to light of various wavelengths suggest 

that the photoreceptor in the sporangiophore is 

more likely to be a flavonoid than a carotenoid 

(Page & Curry, 1966). Fully developed sporangiophores 

are also highly phototropic. Light 

projected along the axis of the sporangiophore 

is brought to a focus at a point beneath the 

swollen vesicle termed the ocellus. In this region, 

there is an accumulation of carotenoid-rich 

cytoplasm which glows orange when illuminated 

(Plate 3f). When light falls asymmetrically onto 

the sporangiophore, it is focused onto the back of 

the subsporangial vesicle near its base, and some 

stimulus is probably transmitted to the cylindrical 

part of the sporangiophore, resulting in 

more rapid growth of the wall facing away from 

the light. Curvature of the whole sporangiophore 

thus occurs until it is again orientated parallel 

to the incident light (see Fig. 7.21). 

The structure of the sporangium differs in a 

number of ways from that of the Mucoraceae. 

The sporangium is hemispherical, and its wall is 

dark black, shiny, tough and unwettable. At the 

base of the sporangium is a conical columella, 

which is separated from the spores by a pad of 

mucilage. During late morning the sporangium 

cracks open by a suture running around the 

base, just above the columella. The spores are 

prevented from escaping by the mucilaginous 

pad which protrudes through the crack in 

the sporangium wall as a ring of mucilage 

(Figs. 7.20e,f). The subsporangial vesicle is 

turgid, and the osmotic pressure of the liquid 

has been estimated to be around 5.5 bars (Buller, 

1934). Drops of liquid decorate the outside of


187 

Fig 7.19 Syzygites megalocarpus. 

(a) Sporangiophore. (b) Germinating 

zygospore.The fungus is homothallic. 

Fig 7.20 Asexual reproduction in Pilobolus 

kleinii. (a) Developing trophocyst which is 

becoming distended by carotenoid-rich 

cytoplasm. (b) Trophocyst with immature 

sporangiophore.The clear tip of the 

sporangiophore is light-sensitive. 

(c) Trophocyst bearing a developing 

sporangium.The upper part of the sporangium 

is beginning to darken.Globules of liquid 

accumulate on the sporangiophore surface 

(9.00 p.m.). (d) Trophocyst with sporangium 

which has not yet dehisced (9.00 a.m.). 

The arrow (o) points to a carotenoid-rich band 

of cytoplasm called the ocellus. 

(e) Sporangiophore bearing a 

sporangium which has dehisced near its base. 

Spores have extruded and are held in place by 

a ring of mucilage (11.30 a.m.). (f) Sporangium 

showing dehiscence line at its base 

(d). (g) Discharged sporangium surrounded 

by dried-out vesicular sap.The spores are 

enclosed in mucilage. (a e) to same scale; 

(f,g) to same scale.


the sporangiophore of Pilobolus, as they do in 

many zygomycetes. Eventually, usually about 

midday, the sporangial vesicle explodes at a line 

of weakness just beneath the columella. Due to 

the elasticity of the vesicle wall the liquid 

contents are squirted out, projecting the entire 

sporangium forward in the direction of the light. 

Photographs of the jet show that it is at first 

cylindrical but eventually breaks up into fine 

droplets (Fig. 7.22c; Page, 1964). In P. kleinii, the 

velocity of projection varies between wide limits 

of 4.7 27.5 m s 1 with a mean of 10.8 m s 1 

(Page & Kennedy, 1964). The sporangia can be 

projected vertically upwards for as much as 

2 m and horizontally for up to 2.5 m. On striking 

a grass blade or other herbage, the sporangium 

becomes attached in such a way that the 

mucilaginous ring adheres to it, with the black 

sporangium wall facing outwards. Buller (1934) 

has suggested that the projectile contains a 

drop of liquid attached to the sporangium 

(Fig. 7.22a). When the projectile strikes an 

object the liquid flows around the sporangium, 

but because the sporangium wall is hydrophobic 

and the base of the sporangium is surrounded 

by the wettable mucilaginous ring, the sporangium 

turns round in the liquid so that its wall 

faces outwards (Fig. 7.22b). The non-wettable 

nature of the sporangial wall may be related to 

the presence on its surface of hollow, blunttipped 

spines and crystals as seen by electron 

microscopy (Bland & Charles, 1972). As the 

mucilage dries, the sporangium becomes 

cemented onto the surface which it struck. The 

spores of Pilobolus are released only after the 

sporangium has been ingested by an animal. 

They survive gut passage and are voided with 

the faeces. A film featuring the life cycle of 

Pilobolus has been made (Webster & Hard, 1999). 

An unexpected consequence of the attachment 

of Pilobolus sporangia to herbage is that the 

sporangia may act as vectors for parasitic 

nematodes such as Dictyocaulus spp., which multiply 

on dung and, when ingested, cause lungworm 

disease in sheep, cattle and some wild 

mammals. 

The physiology of Pilobolus shows a number 

of interesting features possibly related to its 

coprophilous habit. Spores germinate best above 

Fig 7.21 Pilobolus kleinii. Diagrammatic L.S. of sporangiophore 

showing the path of light rays falling parallel to the axis of the 

sporangiophore which are brought to a focus beneath the 

subsporangial vesicle.The sporangiophore illustrated is 

orientated symmetrically with respect to the incident light. 

Note the mucilaginous ring extruded through the sporangial 

wall at its base (after Buller,1934). 

pH 6.5, and can be induced to germinate by 

treatment with alkaline pancreatin. Germination 

can also be triggered by hexoses such as 

glucose and mannose. Mycelial growth occurs 

over a wide range of temperatures, with optimum 

temperatures at 25 35°C. Growth on 

synthetic media with asparagine and acetic acid


189 

Fig 7.2 2 Projectiles of Pilobolus (diagrammatic). (a) Sporangium with adherent drop of sporangiophore sap about to strike an 

obstacle. (b) Sporangium after striking the obstacle.The sporangiophore sap has flowed round the sporangium which has turned 

outwards so that the mucilage ring adheres to the surface of the obstacle (after Buller,1934). (c) Sporangiophore releasing a 

sporangium. Note the jet of liquid and the bending of the narrow base of the sporangiophore under the recoil of the discharge 

(after Page,1964). 

as nutrients is stimulated by the addition 

of thiamine, haemin and coprogen, an organoiron 

compound produced by various fungi 

and bacteria (Hesseltine et al., 1953; Page, 1960; 

Levetin & Caroselli, 1976). Sporangium formation 

is stimulated by ammonia, and in dual 

cultures Mucor plumbeus may release sufficient 

gaseous ammonia to induce asexual reproduction 

in Pilobolus spp. (Page, 1959, 1960). 

Pilaira 

Pilaira (Fig. 7.23) also appears early in the 

succession of coprophilous fungi, i.e. the order 

in which their fruit bodies appear on herbivore 

dung incubated under moist conditions. It has 

not been found in the tropics (Kirk, 1993). The 

structure of the melanized sporangium closely 

resembles that of Pilobolus in that the spores are 

separated from the columella by a mucilaginous 

ring which extrudes from the base of the 

sporangium. There are, however, no trophocysts 

or subsporangial vesicles, and sporangial release 

is non-violent. The cylindrical sporangiophores 

are phototropic, and when mature, especially 

under moist conditions, they elongate rapidly 

to a length of several centimetres (H. J. Fletcher, 

1969, 1973). Their development essentially 

resembles that of Phycomyces. In a moist atmosphere, 

the mucilaginous ring may absorb water 

and swell considerably so that a large sporangial 

drop is formed (Ingold & Zoberi, 1963). When the 

mucilaginous ring at the base of the sporangium


makes contact with adjacent herbage it becomes 

firmly attached to it. The sporangium slips off its 

columella and dries down onto the herbage. 

Pilaira anomala forms zygospores resembling 

those of Pilobolus. On germination, a germ 

sporangium is produced (Fig. 7.23g). 

Nutritional studies on P. anomala indicate a 

preference for NH 4 þ and urea over NH 3 or 

asparagine as nitrogen sources, and a biotin 

and thiamine requirement, but no requirement 

of haem compounds for either growth or fruiting, 

in contrast to the related genus Pilobolus. In 

culture, of the simple carbon sources tested only 

glucose and fructose supported good growth, 

and there was no evidence of enzymatic ability to 

degrade starch, cellulose, pectin or proteins 

(Wood & Cooke, 1987). These nutritional characteristics 

support the idea that P. anomala is a 

typical ruderal fungus, its activities constrained 

by the availability of simple soluble nutrients 

which would be depleted rapidly in decomposing 

dung. 

7.3.3 Thamnidiaceae 

In this family two kinds of asexual reproductive 

structure are found, namely columellate sporangia 

of the Mucor type and smaller, few-spored, 

usually non-columellate sporangia termed sporangiola, 

which are often borne in whorls or at 

the tips of branches. The branches bearing 

the sporangiola may be borne laterally on the 

columellate sporangiophores or may arise separately. 

In some cases the branch system bearing 

the sporangiola is terminated by a spine. Benny 

et al. (2001) have recognized 10 genera but we 

shall consider only Thamnidium. 

Fig 7.23 Pilaira anomala. (a) Sporangiophore 

from rabbit dung showing rupture of the 

sporangial wall at the base of the sporangium. 

(b) Sporangium with extruded mucilage ring 

adhering to an adjacent hypha. (c) Columella 

after sporangium has been detached. 

(d) Detached sporangium showing basal 

mucilage ring. (e) Zygospore. (f,g) Stages in 

zygospore germination (e g) after Brefeld, 

1881).


191 

Thamnidium 

The only species is T. elegans (Fig. 7.24), which 

grows in soil in cold and temperate regions, and 

on the dung of many different animals (Benny, 

1992). It is psychrophilic, continuing to grow 

at 1 2°C, with an optimum 18°C and a maximum 

at 27 31°C (Domsch et al., 1980). It has 

been reported from meat in cold storage. 

In culture, large terminal columellate sporangia 

are produced on tall sporangiophores which 

may also have repeatedly dichotomous lateral 

branches bearing fewer-spored columellate or 

non-columellate sporangiola. The sporangiola 

may also be borne on separate branch systems. 

Low temperature and light induce the formation 

of sporangia as opposed to sporangiola. During 

the development of the sporangiophores, spiral 

growth occurs as in Phycomyces (see Fig. 7.6). 

Electron microscopy studies of the development 

of sporangia and sporangiola show that 

they develop in essentially the same way 

(J. Fletcher, 1973a,b). At maturity the columellate 

sporangia become converted into sticky sporangial 

drops. In contrast, the sporangiola are easily 

detached in wind tunnel experiments. A change 

from damp to dry air leads to increased liberation 

of sporangiola (Ingold & Zoberi, 1963). 

Thamnidium elegans is heterothallic and forms 

zygospores resembling those of Mucor or Rhizopus, 

but they are produced best at low temperatures 

such as 6 7°C and not at 20°C (Hesseltine & 

Anderson, 1956). 

7.3.4 Chaetocladiaceae 

The family Chaetocladiaceae contains two 

genera, the facultatively mycoparasitic Chaetocladium 

and the saprotrophic Dichotomocladium. 

Their fertile hyphae are branched and bear 

monosporous sporangiola on fertile vesicles. 

The main branches terminate in sterile spines 

(Benny & Benjamin, 1993). Whilst species of 

Chaetocladium are believed to be psychrophilic 

and are rarely collected within the tropics, all 

known species of Dichotomocladium have been 

recorded only in tropical areas (Kirk, 1993). 

Chaetocladium 

In Chaetocladium (Fig. 7.25) there are no Mucor-like 

sporangia. Sporangiola, each containing a single 

spore, are borne on lateral branches which 

end in spines. Such monosporous sporangiola 

are sometimes termed conidia. There are two 

species, C. jonesii and C. brefeldii, both parasitic 

on other Mucorales (Benny & Benjamin, 1976), 

especially on Mucor or Pilaira growing on dung. 

At the point of attachment to the host there 

are numerous yellow galls. These are unique 

bladder-like outgrowths which contain nuclei 

of both the host and the parasite in a common 

cytoplasm. Chaetocladium does not form haustoria 

and has been described as a fusion biotroph 

(Jeffries & Young, 1994). Both Chaetocladium spp. 

can, however, be cultured on standard agar 

media in the absence of a host. They are 

heterothallic. Chaetocladium brefeldii is heterogametangic, 

forming zygospores resembling 

Zygorhynchus. Burgeff (1920, 1924) has claimed 

that a given strain of Chaetocladium can only 

parasitize one of the two mating type strains 

of heterothallic Mucor spp., suggesting that the 

parasitic habit of fungi such as Chaetocladium 

may have originated from attempted copulation 

with other members of the Mucorales. Jeffries 

and Young (1994) believed that contact is truly 

mycoparasitic and not pseudosexual. 

7.3.5 Choanephoraceae 

This is probably the only current family in the 

Mucorales to be monophyletic (O’Donnell et al., 

2001). Members of the Choanephoraceae are 

essentially tropical in their distribution. There 

are three genera of which the best-known are 

Blakeslea and Choanephora (Kirk, 1984). Asexual 

reproduction is by sporangia and sporangiola. 

The sporangia which have brown persistent walls 

are usually columellate and often hang downwards. 

They contain dark brown sporangiospores 

with a striate wall and bristle-like appendages at 

each end. The sporangiola contain one or a few 

spores, also with brown striate walls and with 

(Blakeslea) or without (Choanephora) polar appendages. 

The dark sporangium walls and the dark 

walls of the sporangiospores (due to melanin 

and carotenoid pigments), both unusual features 

in the Mucorales, may have evolved as a protection 

against the mutagenic and oxidizing UV 

light and may help to explain the tropical


Fig 7.24 Thamnidium elegans. 

(a) Sporangiophore showing terminal 

sporangium and lateral branches bearing 

sporangiola. (b) Dehisced sporangium 

showing columella and spores. (c) Immature 

terminal sporangium showing the columella. 

(d) Base of sporangiophore with dichotomous 

branches bearing sporangiola. 

(e) Sporangiola. Note the absence of 

a columella in these sporangiola. (b d) to 

same scale. 

Fig 7.25 Chaetocladium brefeldii. (a) Habit 

sketch to show branches ending in spines 

and bearing lateral sporangiola. 

(b) Branch showing spine and sporangiola. 

(c) Hypha of Pilaira anomala bearing 

bladder-like outgrowths following 

parasitism by Chaetocladium.


193 

distribution of these fungi (Kirk, 1993). The 

zygospores proper, when extruded from their 

zygosporangia, also have striate walls. 

Choanephora 

Choanephora cucurbitarum is a weak pathogen 

causing soft rot and wet rot diseases of a wide 

range of tropical and subtropical plants such as 

okra, chilli pepper, cowpea and Amaranthus. It 

also grows on decaying flowers of various kinds. 

Infection of male inflorescences of Artocarpus 

integer (Moraceae) by Choanephora attracts gall 

midges which feed on the mycelium and build 

up large populations on the decaying flesh of the 

inflorescence. The gall midges are probably 

involved in pollination of the female inflorescences 

of Artocarpus (Sakai et al., 2000). 

Asexual reproduction is by two types of 

structure, drooping multisporous sporangia and 

monosporous sporangiola (‘conidia’) borne on 

separate sporangiophores (Fig. 7.26). The development 

of sporangia is stimulated by growth on 

carbon-limited media and temperatures around 

30°C, whilst the optimum temperature for 

sporangiolum formation is around 25°C. Light 

is essential for sporulation. The sporangia are 

columellate or non-columellate and dehisce into 

two halves along a line of weakness. The 

sporangiospores have brown walls with longitudinal 

grooves appearing as striations, and 

bear a group of hyaline tapering appendages at 

each pole. These appendages may play a role in 

the dispersal of the spores in water films since 

they only become extended if the sporangium 

dehisces in water (Higham & Cole, 1982). 

Sporangiola develop on globose vesicles at the 

tips of separate sporangiophores, each of which 

may bear about 100 sporangiola. The sporangiolum 

is multinucleate and the spore within 

it develops a separate thick, brown, ridged 

Fig 7.26 Choanephora cucurbitarum. 

(a) Sporangiophore with drooping sporangium. 

(b) Sporangiophore (‘conidiophore’) with 

numerous monosporous sporangiola (‘conidia’). 

(c) Apex of conidiophore showing swollen 

vesicles bearing conidia. (d) Dehisced 

sporangium showing striate spores with 

terminal appendages. (e) Conidium. 

(f) Sporangiospore. (c) and (d) to same scale.


(i.e. striate) wall inside the thin sporangiolum 

wall which clings to it and conforms to its shape, 

making it difficult to discern that the spore 

wall is distinct (Higham & Cole, 1982). The spore 

inside the sporangiolum has no appendages. 

Choanephora cucurbitarum is heterothallic. Its 

zygosporangia develop from intertwined zygophores 

and are held in place between tongs-like 

suspensors (Kirk, 1977; Chang et al., 1984). The 

zygosporangial wall is thin and may flake off 

or fracture to reveal the striate wall of the 

enclosed zygospore. 

Blakeslea 

Blakeslea trispora, which has been isolated from 

cowpeas, tobacco and cucumber leaves, forms 

two kinds of asexual reproductive structure in 

culture: nodding columellate or non-columellate 

sporangia with brown, faintly striate spores 

which usually bear bristle-like appendages, and 

non-columellate sporangiola borne in large 

numbers on globose vesicles (Fig. 7.27). The 

sporangiola contain 2 5 (typically 3) distinctly 

striate, dark brown spores which also have 

bristle-like appendages. The production of the 

Fig 7.27 Blakeslea trispora. 

(a) Sporangiophores with globose 

terminal vesicles bearing 

sporangiola containing three or 

four spores. (b) A dehisced 

sporangiolum showing two spores 

released from it. Note the striate 

wall, the polar spore appendages 

and the splitting of the 

sporangiolum wall into two halves. 

(c) Sporangiophore with a drooping 

sporangium. No columella was 

observed. (d) Dehisced sporangium 

also lacking a columella. Note the 

split sporangial wall and the 

sporangiospores with striate walls 

and polar appendages.


195 

nodding sporangia is enhanced in culture by 

growth at a temperature of 30°C and that of 

sporangiola by a temperature of 26°C, with 

mixed sporulation at 28°C (Tereshina & 

Feofilova, 1995). The number of spores within 

sporangiola is affected by nutrition, and when 

grown on media with limiting nutrient content 

the sporangiola may contain only a single spore, 

thus resembling Choanephora. InB. unispora the 

sporangiola generally contain only one spore, 

rarely two. The sporangiola of B. trispora are 

readily detached by wind and break open in 

water like the two halves of a bivalve shell to 

release the spores which are carried by insects 

from one plant to another (Fig. 7.27b). Blakeslea 

trispora is heterothallic and has brown striate 

zygospores resembling those of Choanephora 

(Mistry, 1977). 

The Choanephoraceae have been the subject 

of physiological investigations. An interesting 

phenomenon observed in intra- and inter-specific 

crosses is that the production of b-carotene is 

markedly enhanced when (þ) and ( ) strains are 

mated on liquid media, as compared with 

production from either strain grown singly. 

Commercial production of b-carotene and lycopene 

from fermentations of mixed cultures of 

(þ) and ( ) strains of B. trispora is possible (Mehta 

et al., 2003). The discovery that b-carotene 

production can be stimulated by an acid fraction 

of culture filtrates from mixed cultures of 

B. trispora led to the discovery of trisporic acid 

as the sex hormone of Mucorales (see p. 173). 

Syncephalastrum 

Syncephalastrum racemosum (Fig. 7.28) can be 

isolated from soil and dung in tropical and 

subtropical areas (Domsch et al., 1980). It grows 

rapidly in culture over a wide range of temperatures 

(7 40°C) and is mainly saprotrophic, but 

has been implicated in mucormycosis in human 

and animal hosts. It has also been isolated from 

foodstuff, cereal grains, other seeds and spices. 

In culture it forms aerial branches terminating 

in club-shaped or spherical vesicles. The vesicles 

are multinucleate and bud out all over their 

surface to form cylindrical outgrowths, the merosporangial 

primordia. Into these outgrowths 

one or perhaps several nuclei pass, and nuclear 

division continues. The cytoplasm in the merosporangium 

cleaves into a single row of 5 10 

7.3.6 Syncephalastraceae 

A characteristic feature of this family is that 

asexual reproduction occurs by means of cylindrical 

sporangia containing typically a single row 

of sporangiospores. Such sporangia are termed 

merosporangia and are formed in groups on 

inflated vesicles (Benjamin, 1966). Merosporangia 

appear to have evolved independently in the 

Piptocephalidaceae (Zoopagales) (see p. 201). 

There is only a single genus, Syncephalastrum, in 

the Syncephalastraceae. DNA sequence analysis 

indicates close relationships with certain genera 

traditionally classified in Mucoraceae and 

Thamnidiaceae (O’Donnell et al., 2001). 

Fig 7.28 Syncephalastrum racemosum. (a) Sporangiophore 

bearing a vesicle and numerous merosporangia. 

(b) Merosporangia and merospores.


sporangiospores, each with 1 3 nuclei. The 

cleavage process is similar to that found in 

other Mucorales (Fletcher, 1972). The sporangial 

wall shrinks at maturity so that the spores 

appear in chains reminiscent of Aspergillus. 

Occasionally the merospores may lie in more 

than a single row. The spore heads remain dry 

and entire rows of spores (spore rods) are 

detached by wind (Ingold & Zoberi, 1963). 

Syncephalastrum racemosum is heterothallic and 

forms zygospores resembling those of other 

Mucorales. 

7.3.7 Cunninghamellaceae 

In this family, asexual reproduction is entirely by 

means of monosporous sporangiola. Sporangia 

are not formed. There is a single genus. 

Cunninghamella 

There are about 12 species of Cunninghamella, 

found in soil in the warmer regions of the world, 

e.g. the Mediterranean and subtropics (Domsch 

et al. 1980; Zheng & Chen, 2001). Cunninghamella 

elegans and C. echinulata are saprotrophs but C. 

bertholettiae is a serious, sometimes fatal, human 

pathogen. Cunninghamella echinulata may also be 

a destructive mycoparasite of Rhizopus arrhizus. 

Cunninghamella elegans and C. echinulata have been 

used in a wide range of biotransformations of 

pharmaceutical products (Kieslich, 1997). DNA 

sequence studies have grouped C. echinulata with 

some of the genera traditionally classified in 

Mucoraceae (O’Donnell et al., 2001), but comparisons 

of fatty acid and cell wall composition of 

Cunninghamella japonica and Blakeslea trispora 

have suggested that Cunninghamella is related to 

members of the Choanephoraceae, a conclusion 

reached also on morphological criteria by some 

other workers. 

The sporangiola of Cunninghamella are hyaline 

and clustered on globose vesicles (ampoules) 

on branched or unbranched sporangiophores 

(Fig. 7.29). They are sometimes referred to as 

conidia, but details of their development indicate 

that they are best interpreted as one-spored 

sporangiola. Khan and Talbot (1975) have studied 

sporangiolum development in C. echinulata. The 

ampoules are club-shaped, globose or pearshaped 

and bear spherical sporangiola, each 

arising from a tubular denticle. Localized areas 

of weakness in the ampoule wall, yielding to 

turgor pressure, blow out to form the denticles. 

The wall is two-layered in the ampoule and 

denticle, but single in the developing sporangiolum 

where it develops hollow spines all over the 

surface. Within the sporangiolum wall a twolayered 

wall develops around the multinucleate 

protoplast. Hawker et al. (1970) have studied the 

structure and germination of sporangiola in 

a species of Cunninghamella. Here, too, the wall 

Fig 7.29 Cunninghamella echinulata. (a) A 

simple and a branched sporangiophore. 

(b,c) Apices of sporangiophores showing 

expanded vesicles developing 

sporangiola. (d) Apex of mature 

sporangiophore with cluster of 

attached and two detached 

spiny-walled sporangiola. Scale bar (a) ¼ 

25 mm, (b d) ¼ 10 mm.


197 

of the ungerminated sporangiolum consisted of 

at least two layers, the outermost layer relatively 

thin, enclosing a distinct thicker inner layer. On 

germination only the inner layer extends as a 

germ tube. 

The zygospores of Cunninghamella resemble 

those of Mucor. 

7.3.8 Mortierellaceae 

The distinctive feature of this family is that the 

sporangiophore produces only a rudimentary 

columella or lacks it altogether. In the most 

frequently encountered genus, Mortierella, zygospores 

are often heterogametangic and may be 

naked or enclosed in a weft of mycelium. The 

family, which includes about seven genera, has 

been monographed by Zycha et al. (1969). DNA 

sequence analyses indicate relationships to 

certain genera usually placed in Mucoraceae 

(O’Donnell et al., 2001; Tanabe et al., 2004; 

see Fig. 7.1), although many authors regard 

Mortierella and its allies as a separate order, 

Mortierellales. 

Mortierella 

About 90 species of Mortierella are known mainly 

from soil, the rhizosphere, and plant or animal 

remains in contact with soil (Gams, 1977; 

Domsch et al., 1980). These fungi can be isolated 

readily on nutrient-poor media which prevent 

the growth of more vigorous moulds. Many 

species are psychrophilic and may comprise the 

bulk of fungal isolates from soil if the isolation 

media are incubated near 0°C (Carreiro & Koske, 

1992). Mortierella wolfii is associated with mycotic 

abortion in cattle and can be isolated from the 

placenta and foetal stomach contents and from 

liver. In nature it grows in warm soils, overheated 

silage and rotten hay and can grow well 

at 40 42°C (Austwick, 1976; Domsch et al., 1980). 

Certain species of Mortierella, e.g. M. alpina, have 

been used in fermentations as catalysts of 

biotransformations in the production of pharmaceuticals 

(Kieslich, 1997). Another focus 

of biotechnological interest is their accumulation 

of lipid, notably polyunsaturated fatty 

acids (PUFAs) which are of nutritional value 

(Dyal & Narine, 2005). These are also produced 

by thraustochytrids (see p. 73). The genus 

Mortierella is polyphyletic, and many of the 

best-known species, including M. isabellina, 

M. ramanniana and M. vinacea, are now placed 

in other genera such as Micromucor or Umbelopsis 

(Meyer & Gams, 2003). 

The mycelium of most species of Mortierella 

is fine and, in agar culture, often shows a 

characteristic series of fan-like zones. Cultures 

frequently have a garlic-like odour. The sporangia 

are borne on branched or unbranched tapering 

sporangiophores (Fig. 7.30a). The sporangium wall 

is delicate and may collapse around the spores. 

There is no protruding columella (Fig. 7.30b). 

Frequently the entire sporangium is detached. In 

a number of species, and also dependent upon 

environmental conditions, there may be only 

one or a few spores per sporangium (Figs. 7.30c,d). 

Asexual reproduction may also include the 

formation of sessile, intercalary chlamydospores 

which are not dispersed but remain in 

the soil when their subtending mycelium 

breaks down (Fig. 7.30e). Stylospores are also 

produced; unfortunately this term has been used 

for two different, non-homologous structures. In 

its original application by van Tieghem, it 

referred to aerial chlamydospores, i.e. relatively 

thick-walled, stalked spores as seen, for example, 

in M. polycephala (Domsch et al., 1980). In other 

species, classified in the section Stylospora, e.g. M. 

humilis and M. zonata (Gams, 1977), single-spored 

sporangiola (Fig. 7.31a) have been termed stylospores. 

On detachment of the sporangiolum, the 

remnants of the sporangiolum wall can often be 

seen at the tip of the sporangiophore (Domsch 

et al., 1980). In some species, e.g. M. stylospora and 

M. zonata, only sporangiola are present and true 

sporangia are lacking. Mortierella chlamydospora 

also lacks true sporangia, reproducing asexually 

by intercalary smooth or stalked echinulate 

chlamydospores and sexually by zygospores 

(Ansell & Young, 1982). 

The zygospores of Mortierella spp. may be 

naked or surrounded by a partial or complete 

investment of sterile hyphae (see Figs. 7.31b,c). 

Of the 90 species, 26 are known to form zygospores, 

half of which are homothallic (Watanabe 

et al., 2001). It is likely that the majority of the 

remaining species will prove to be heterothallic.


Fig 7.30 Mortierella hyalina. (a) Branched sporangiophore as viewed with the dissection microscope. (b) Intercalary chlamydospore. 

(c) One-spored sporangium (sporangiolum) showing separate walls, the outer belonging to the sporangium and the inner to the 

sporangiospore. (d) Multi-spored sporangium with the sporangial wall disintegrating. (e) Apex of a sporangiophore in which the 

sporangium has dehisced, leaving fragments of the sporangial wall as a frill. Note the absence of a bulging columella. (b e) to same 

scale. Reprinted from Weber and Tribe (2003), with permission from Elsevier. 

Zygospore production takes place in culture, 

often embedded in the agar, on media with a 

relatively poor nutrient content which 

discourages profuse development of aerial mycelium. 

A common feature is that zygospores are 

heterogametangic, one suspensor being considerably 

larger than the other. The smaller progametangium 

or gametangium does not enlarge 

and may disappear soon after plasmogamy. The 

early development of such heterogametangic 

zygospores is illustrated in the heterothallic 

M. umbellata (Fig. 7.32; Degawa & Tokumasu, 

1998). In this species, hyphal coiling occurs at the 

point of contact of compatible mycelia, followed 

by the development of club-shaped progametangia 

which grow parallel and closely appressed to 

each other. One, the macroprogametangium, 

soon becomes much larger than the other, the 

microprogametangium. In each progametangium 

a septum delimits a terminal gametangium 

from a suspensor. The macrogametangium 

and macrosuspensor both enlarge considerably,


199 

Fig 7.31 (a) Mortierella zonata sporangiola, one germinating. (b,c) Mortierellarostafinskii (after Brefeld,1876). (b) Developing zygospore. 

(c) Older zygospore surrounded by a weft of hyphae. (d) Mortierella epigama zygospore with unequal suspensors arising 

from a common branch showing that this fungus is homothallic and heterogametangic.The zygospore proper, lying within the 

zygosporangium, has a thick undulating wall. 

appearing as two contiguous spheres (Figs. 

7.32e,f). Eventually the macrogametangium 

becomes a zygosporangium, its wall ornamented 

with small warts, and containing a smooth, 

thick-walled zygospore. 

The heterothallic M. indohi is also heterogametangic, 

one progametangium being blunter 

and more rounded than the other. A cross wall 

develops only in this larger progametangium to 

cut off a gametangium which enlarges and


Fig 7.32 Mortierella umbellata, stages in zygospore 

development (traced from Degawa & Tokumasu,1998). 

(a) Developing progametangia with 

micro-progametangium on the left. (b) Swelling of 

progametangia. (c) Septum formation in 

micro-progametangium, arrowed. (d) Septa have formed 

in both progametangia to delimit the terminal gametangia 

from sub-terminal suspensors. (e) The macrogametangium 

and macrosuspensor have enlarged. (f) Mature 

zygosporangium containing a thick-walled zygospore. 

becomes converted into a subspherical zygosporangium 

with a dimpled wall. The narrower progametangium 

does not enlarge appreciably. It is 

not divided by a septum and remains as a lateral 

attachment to the zygosporangium (Ansell & 

Young, 1983, 1988). Delimitation of the zygosporangium 

by means of a single wall in only one of 

the fusing progametangia occurs in several other 

species of Mortierella (Kuhlman, 1972). 

Mortierella capitata shows an unusual mode of 

zygospore development (Degawa & Tokumasu, 

1997). It is heterothallic and heterogametangic, 

with two mating types designated A and B. When 

compatible vegetative hyphae meet in culture, 

their tips swell to form progametangia. The 

hyphal tips from strain B are always larger 

than those from A and are designated as macroprogametangia. 

The narrower hyphae from 

strain A (microprogametangia) coil around the 

macroprogametangia, branch dichotomously 

and become septate, resulting in the formation 

of microsuspensors and microgametangia. A 

septum divides the terminal macrogametangium 

from its macrosuspensor. The macrogametangium 

becomes the zygosporangium and eventually 

contains a thick-walled hyaline zygospore. 

The macrosuspensor elongates and persists so 

that the mature zygosporangium appears at the 

end of a long stalk surrounded at its base by the 

coiled microsuspensors. Apart from the other 

unusual features of this developmental process, 

M. capitata is distinctive in that the morphology 

of its gametangia is linked to mating type, i.e. 

the formation of macrogametangia occurs only 

in the B strain and microgametangia in the A 

strain. This condition, termed morphological 

heterothallism, is comparatively rare in 

Zygomycota and in fungi generally. 

Complete investment of the zygospore by 

branching hyphae is a feature of M. rostafinskii 

(see Figs. 7.31b,c) and M. ericetorum (Kuhlman, 

1972). The zygospores proper in Mortierella are 

hyaline with thick smooth walls, sometimes 

showing coarse, undulating folds (see Fig. 

7.31d). Little is known about the germination of 

zygospores. 

7.4 Zoopagales 

The order Zoopagales contains soil- and dunginhabiting 

parasites of fungi and small terrestrial 

animals such as protozoa and nematodes. 

Reproduction is by conidia, merosporangia 

and zygospores. Benny et al. (2001) recognized

ZOOPAGALES 

201 

5 families and 20 genera but we shall study only 

the Piptocephalidaceae, earlier classified in the 

Mucorales. 

7.4.1 Piptocephalidaceae 

This family includes Piptocephalis and Syncephalis, 

both mycoparasites. DNA sequence analysis 

suggest that these two genera are not closely 

related (Tanabe et al., 2000). Piptocephalis is a 

biotrophic haustorial parasite which needs the 

presence of a susceptible host for good growth 

and reproduction (Manocha, 1975), although on 

certain agar media Piptocephalis spores will 

germinate and give rise to a limited mycelium 

producing dwarf sporangiophores. The spores so 

formed are unable to germinate if transferred to 

fresh agar, but they do germinate and infect a 

suitable host fungus if one is present. Syncephalis 

develops intrahyphal hyphae within the host 

mycelium and can be grown more readily in 

culture if supplied with appropriate nutrients 

(Jeffries & Young, 1994). 

Piptocephalis 

Most of the 20 or so known species of Piptocephalis 

(Gr. pipto ¼ to fall, kephale ¼ head) parasitize the 

mycelium of Mucorales, with P. xenophila exceptional 

in its ability to infect members of the 

Ascomycota. Species of Piptocephalis are most 

abundant in the surface layers of soils where 

there is a rapid recycling of organic matter, 

such as in woodland and in grazed grassland 

(Richardson & Leadbeater, 1972). They also parasitize 

Mucorales on dung. A characteristic habitat 

for P. freseniana is herbivore dung towards the 

end of the fruiting phase of Mucor and Pilaira. 

From an infected host mycelium Piptocephalis 

develops an erect dichotomous sporangiophore 

(Fig. 7.33a). Swollen nodulose (knobbly) head 

cells form at the tips of the branches (see 

Fig. 7.33c), and from these cylindrical merosporangia 

radiate outwards. The merosporangia are 

thin-walled and usually contain from one to 

several multinucleate merospores, arranged in 

a single row. Piptocephalis unispora is unusual in 

that its merosporangia contain only a single 

sporangiospore. Its merosporangial wall encloses 

the sporangiospore which has a two-layered wall 

and may contain 1 3 nuclei (Jeffries & Young, 

1975). At maturity Piptocephalis merosporangia 

behave in two different ways (Ingold & Zoberi, 

1963). In some species the thin sporangial wall 

collapses around the spores which remain 

attached together as spore rods, appearing as 

short chains (see Fig. 7.33c). Alternatively, as in 

P. freseniana, the merosporangial wall becomes 

diffluent and all the spores in a head collapse 

to form a spore drop. In some species the whole 

head cell with its attached merospores becomes 

detached at maturity. All types of propagule can 

be dispersed by wind. 

On germination sporangiospores swell and 

emit one to several germ tubes (McDaniell & 

Hindal, 1982). There is a chemotropic attraction 

Fig 7.33 Piptocephalis virginiana. (a) Habit 

sketch to show dichotomous sporangiophore. 

(b) Head cell and intact merosporangia. 

(c) Head cells showing breakdown of 

merosporangia to form chains of spores. 

(d) Spore germination and formation of 

appressorium on a host hypha. 

(e) Appressorium and branched 

haustorium on host hypha.The parasite 

mycelium is branched and extending to other 

host hyphae. (f) Zygospore.The fungus is 

homothallic. (b e) to same scale.


of germ tubes towards host hyphae (Fig. 7.33d), 

with preferential growth towards the hyphal 

tips. On agar the chemotropic stimulus can be 

detected over distances as great as 5 mm (Evans 

& Cooke, 1982). Fimbriae extending outwards for 

up to 25 mm from the cell walls of potential host 

fungi may play a role in directing the growth of 

Piptocephalis germ tubes towards the host hyphae 

(Rghei et al., 1992). At the point of contact an 

appressorium develops, but in some combinations 

the parasite hyphae may coil around those 

of their host and several appressoria form. In 

successful host parasite combinations, the host 

wall is penetrated beneath the appressorium by 

mechanical and possibly also enzymatic means. 

An infection peg penetrates the host wall. 

Enclosed by the plasmalemma of the host cell, 

the tip of the penetration peg expands to form a 

haustorium which may branch inside the host 

hypha. The haustoria of Piptocephalis have close 

similarity to those of biotrophic haustorial parasites 

of plants (Manocha & Lee, 1971; Jeffries & 

Young, 1976). Nutrients taken up by the haustorium 

are translocated to the germinating spore 

and its germ tubes may then grow out to form 

a mycelium which extends over the host hypha, 

producing further haustoria. The distinctive 

biochemical features of the Mucorales which 

are correlated with their ability to support the 

growth of these mycoparasites are that their 

walls contain chitosan and that their cytoplasm 

is rich in the polyunsaturated fatty acid 

g-linolenic acid which is essential for growth 

of the mycoparasite (Manocha, 1975, 1981; 

Manocha & Deven, 1975). 

Recognition between the mycoparasite and 

its hosts operates on at least two levels, the cell 

wall and the protoplast surface (Manocha et al., 

1990). There are qualitative and quantitative 

differences in the carbohydrates present at the 

hyphal surface of host and non-host species. 

Attachment is favoured by the presence of two 

distinctive glycoproteins in the wall of susceptible 

host hyphae. These two glycoproteins act as 

subunits of an agglutinin which may serve as 

receptor to a complementary protein in the 

mycoparasite (Manocha et al., 1997). 

Piptocephalis virginiana readily infects young 

but not old cultures of Choanephora cucurbitarum. 

This is correlated with the fact that the wall of 

young hyphae of C. cucurbitarum is single-layered 

whilst that of older hyphae is double-layered. 

Although appressoria and penetration pegs 

develop on older hyphae, penetration of the 

inner layer of the cell wall is rarely successful. 

The inner wall layer develops a papilla opposite 

the point of attempted penetration (Manocha, 

1981). Similar findings were made when 

P. virginiana failed to penetrate the resistant 

species P. articulosus (Manocha & Golesorkhi, 

1981). Where successful penetration of a susceptible 

host occurs, the mycoparasite P. virginiana 

can suppress wall synthesis by the host in the 

vicinity of infection points, so overcoming one 

of its defence reactions (Manocha & McCullough, 

1985; Manocha & Zhonghua, 1997). 

The effects of Piptocephalis spp. on the growth 

of their hosts are very variable (Curtis et al., 1978). 

In some combinations the rate of growth of 

dual cultures was not significantly different 

from that of uninfected hosts, in others it was 

reduced, whilst in yet others it was enhanced. 

These effects are temperature-dependent. Growth 

and sporulation of the coprophilous fungus 

Pilaira anomala were reduced in culture when 

infected by P. fimbriata or P. freseniana (Wood & 

Cooke, 1986). A curious effect was found in 

culture when P. fimbriata challenged its normally 

susceptible host Mycotypha microspora. In the 

presence of P. fimbriata the host grew in a yeastlike 

state which was not infected. In contrast, 

the mycelial state of this fungus is readily 

infected (Evans et al., 1978). 

Most species of Piptocephalis are homothallic 

(Leadbeater & Mercer, 1957). In culture zygospores 

are usually formed within the agar. The 

mature zygospore is a spherical dark brown 

sculptured globose cell held between two tongshaped 

suspensors. 

7.5 Entomophthorales 

Many Entomophthorales are parasites of insects 

and other animals, whilst some parasitize 

desmids, nematodes or fern prothalli, or grow 

saprotrophically in plant litter, dung or soil.

ENTOMOPHTHORALES 

203 

An illustrated account of entomopathogenic 

species has been provided by Samson et al. 

(1988) and a key to genera by Humber (1997). 

The major entomopathogenic genera are Batkoa, 

Conidiobolus, Entomophaga, Entomophthora, Erynia, 

Furia, Massospora, Neozygites, Pandora and 

Zoophthora. Some of these insect pathogens hold 

promise for the control of insect pests, not least 

because many of them can be grown in culture, 

albeit on complex media containing ingredients 

such as sugars, egg yolk, yeast extract and milk 

(Wolf, 1981; Papierok & Hajek, 1997). The cells of 

Entomophthorales are uninucleate or coenocytic 

with chitinous walls, or they may exist in 

the bodies of insects as wall-less protoplasts. 

The absence of a wall presumably reduces the 

elicitation of immune responses in their hosts 

(Dunphy & Nolan, 1982). Asexual reproduction in 

most genera is by means of forcibly discharged 

conidia, and on germination such conidia may 

develop a variety of secondary conidia. Sexual 

reproduction is by isogamous or anisogamous 

conjugation between uni- or multinucleate 

gametangia, to give a thick-walled zygospore. 

Azygospores may also be formed without conjugation, 

but it is likely that nuclear fusion and 

reduction division occur during their development 

(McCabe et al., 1984). 

Fossil evidence indicates that, as insect 

pathogens, members of the group were extant 

at least 25 million years ago. A well-preserved 

specimen of a winged termite probably infected 

with a species of Entomophthora has been found 

embedded in amber dated around the 

Oligocene Miocene border in the Dominican 

Republic (Poinar & Thomas, 1982). 

According to Benny et al. (2001), the order 

Entomophthorales consists of six families including 

the Basidiobolaceae. If this family is 

excluded, the remaining Entomophthorales 

appear to be monophyletic by DNA-based analysis 

(Jensen et al., 1998). In many phylogenetic 

schemes, Basidiobolus ranarum seems to be more 

closely related to Chytridiales and Neomastigales 

than to Entomophthorales (see Figs. 1.26, 7.1), 

and Cavalier-Smith (1998) has placed it in a 

separate order, the Basidiobolales. In the current 

context, we sacrifice these taxonomic details in 

favour of a better understanding of the 

Zygomycota as a whole, and therefore retain 

Basidiobolus in the Entomophthorales. 

Important criteria in the classification of 

Entomophthorales are the branched or unbranched 

nature of the conidiophores, whether 

the conidia are uninucleate or multinucleate, 

whether the wall of the conidium is single 

(unitunicate) or separates into two layers 

(bitunicate), and the presence or absence of 

secondary conidia and their morphology 

(Humber, 1989). 

7.5.1 Basidiobolaceae: Basidiobolus 

Basidiobolus is the only genus in the 

Basidiobolaceae. The best-known species is B. 

ranarum, which has a worldwide distribution. It 

fruits on the dung of frogs, toads, lizards, some 

insectivorous fish and mammals such as bats. It 

has also been found on the dung of kangaroos 

and wallabies (Speare & Thomas, 1985). If a frog 

is captured and placed in a jar with a little water, 

it will defaecate in due course and its dung can 

be filtered off. If the damp filter paper is placed 

in the lid of an inverted Petri dish containing a 

suitable agar medium (e.g. 1% peptone agar, 

potato-dextrose agar, or cornmeal agar), conidia 

of B. ranarum will be shot upwards from the dung 

onto the agar surface, and within a few days 

coarsely septate colonies will become visible on 

the agar (Weber & Webster, 1998a). The presence 

of Basidiobolus and other ballistosporic fungi such 

as Conidiobolus in surface soil and litter can 

also be disclosed by the ‘canopy’ technique. 

A suspension of soil is filtered and the filter 

paper, bearing a thin layer of soil, is placed in the 

lid of a Petri dish facing downwards over a 

suitable agar medium. The dish is illuminated 

from below and this encourages the discharge of 

conidia onto the agar (Smith & Callaghan, 1987; 

Callaghan, 2004). 

In agar cultures of Basidiobolus, the cytoplasm 

in the mycelium moves towards the hyphal apex 

so that only a few terminal segments contain 

cytoplasm and a single large, prominent nucleus 

whilst the older segments are empty, being 

isolated by retraction septa (Fig. 7.34d). The 

cytoplasm-filled mycelial segments are termed 

hyphal bodies. Branching occurs immediately


Fig 7.34 Basidiobolus ranarum. (a) Gut-stage cell from 

fresh frog dung. (b) Germination of gut-stage cells 

producing a coarse septate mycelium. (c) Hyphal apex 

with the terminal cells full of cytoplasm.The prominent 

nucleus in the apical cell is arrowed. (d) Apex of an older 

hypha in which only the two terminal cells contain 

cytoplasm; those behind are empty. (e) Branches arising 

beneath the septa of three subterminal cells. Scale bar: 

(a,b) ¼ 25 mm, (c) ¼ 50 mm, (d,e) ¼ 100 mm. 

behind the septum delimiting the apical 

segment, after mitotic division of the nucleus 

(Fig. 7.34e). The conidiophores, which develop in 

a few days, are phototropic and resemble the 

sporangiophores of Pilobolus but bear a colourless 

pear-shaped to globose ballistosporic conidium 

(Fig. 7.35a). O’Donnell (1979) interpreted the 

conidium as a monosporous sporangiolum but 

since it can, under certain conditions, cleave to 

form endospores it may also be regarded as a 

modified sporangium. The conidium is uninucleate. 

A conical columella projects into it. Beneath 

is a swollen sub-conidial vesicle containing liquid 

under turgor pressure. This is probably generated 

by a single large vacuole which fills most of 

the sub-conidial vesicle at maturity. A line of 

weakness can be detected as a slight constriction 

around the base of the vesicle, and when this 

ruptures the conidium and vesicle fly forward for 

a distance of 1 2 cm. The elastic upper portion 

of the vesicle contracts and the vacuolar sap 

within it squirts out backwards, so that it 

behaves as a minute rocket (Ingold, 1971). 

During their flight the conidium and the rocket 

motor (i.e. the vesicle) may be separated or the 

two parts remain attached to each other until 

landing (Figs. 7.35c,d). 

Conidium germination in B. ranarum 

Primary ballistosporic conidia can germinate in a 

number of different ways depending on external 

conditions (Zahari & Shipton, 1988; Waters & 

Callaghan, 1999). 

(1) By direct germination, producing one to 

several germ tubes from which the vegetative 

mycelium develops (Fig. 7.35e). Germination of 

this type requires a nutrient concentration above 

that of 0.1% malt extract agar.


205 

(2) Germination by repetition to form a secondary 

conidiophore with a ballistosporic conidium. 

This is essentially similar to the primary 

conidium (Fig. 7.35a) and is produced under 

conditions of high water availability and low 

nutrient concentration. Secondary conidia may 

germinate by further repetition or in other ways. 

(3) Discharged ballistosporic conidia formed 

in culture on certain media or located within 

the gut of the frog may cleave to form many 

endospores (sporangiospores, sometimes termed 

meristospores), and these are released by dissolution 

of the original conidial wall (Fig. 7.36a; 

Dykstra, 1994). 

(4) Germination under somewhat drier conditions 

with a water activity at or below 0.995 

stimulates the development of capilliconidia 

or capillispores (Fig. 7.36c). The body of the 

capilliconidium may cleave by transverse and 

longitudinal septa to form endogenous segments 

(endospores, meristospores) which are released 

by breakdown of the wall of the capilliconidium 

(Fig. 7.36d; Drechsler, 1956). 

Capilliconidia are so called because they are 

formed on long (over 0.3 mm), slender conidiophores. 

The conidia themselves are spindleshaped 

and apically beaked with a terminal 

globose adhesive droplet or haptor. The material 

making up the haptor is extruded through a 

narrow channel within the beak of the conidium. 

The droplet has unusual properties because it is 

not affected by water but rapidly spreads out to 

form a film when in contact with a solid surface 

(Dykstra & Bradley-Kerr, 1994). The capilliconidia 

are easily detached from their conidiophores 

and may be dispersed by mites (Blackwell & 

Fig 7.35 Basidiobolus ranarum. (a) Conidiophore from 

culture. Note the conical columella and the swollen 

vesicle with a line of weakness around its base. 

(b) Primary conidium germinating to produce a 

secondary conidiophore and ballistosporic conidium. 

(c) Discharged conidium with remnant of the vesicle 

attached. (d) Discharged conidium separated from the 

remnant of the vesicle. (e) Conidium germinating directly 

to form a septate mycelium.


Fig 7.36 Basidiobolusranarum. (a) Stages in the 

development of endospores by primary 

ballistoconidia. Above: cytoplasmic contents cleaving 

to form two protoplasts.Centre: sporangium 

containing over a dozen sporangiospores. Below: 

sporangium showing breakdown of sporangium wall 

(traced from Dykstra,1994). (b) Successive cleavage 

of protoplasts from a primary ballistosporic conidium 

placed on a rich agar medium to form the‘Palmella’ 

stage. (c) Germination of a primary ballistoconidium 

to form a uninucleate secondary capilliconidium with 

a terminal beak which has extruded a sticky haptor. 

(d) Capilliconidium which has divided to produce 

several endospores, some of which have been 

released following breakdown of its wall.One of the 

endospores is germinating. Scale bars: (a,b) ¼ 20 mm, 

(c,d) ¼ 12.5 mm. 

Malloch, 1989). Mites are ingested by beetles, the 

main vectors of B. ranarum, but other insects, 

spiders, millipedes, woodlice, worms and snails 

may also acquire conidia. These are ingested by 

vertebrate insectivores. Within the vertebrate 

gut, endospores are released from ballistosporic 

conidia and capilliconidia. 

Endospores germinate in the vertebrate gut 

to form spherical, large, uninucleate, hyaline 

cells up to 20 mm. These were called the ‘Darm- 

Form’ (gut-stage) of B. ranarum by Levisohn (1927) 

who showed that a single ingested primary 

conidium can give rise to 50 60 division 

products (meristospores) forming gut-stage cells 

(Fig. 7.34a). The concentration of Basidiobolus 

propagules builds up in the guts of the vertebrate 

vectors, and the fungus can be isolated 

from faeces of lizards up to 18 days after the 

animals are deprived of infected prey (Coremans- 

Pelseneer, 1973; Okafor et al., 1984). The gut-stage 

cells are voided with the faeces and can survive 

for several months under dry conditions. Under 

moist warm conditions they germinate to form a 

mycelium from which ballistosporic conidiophores 

develop, whereas on certain media they 

enlarge and their contents undergo successive 

binary fission to form globose thick-walled cells. 

This state is sometimes termed the ‘Palmella’ 

state (Fig. 7.36b) because of its superficial 

resemblance of a genus of green algae.


207 

Basidiobolus microsporus, which grows in 

deserts in California, has a method of asexual 

reproduction not found in B. ranarum. Primary 

conidia can germinate directly or by repetition 

as in B. ranarum, but capilliconidia have not 

been found. However, under relatively dry 

conditions primary conidia may produce large 

numbers of exogenous obclavate spores (microspores) 

each attached by a separate pedicel to 

the wall of the primary conidium. They have 

been interpreted as modified sporangiospores 

(Benjamin, 1962). 

In culture it has been found that light, 

especially blue light of wavelength 440 480 nm, 

stimulates conidial development and discharge 

in B. ranarum. The effect of light is to stimulate 

aerial growth from hyphal bodies within the 

medium, and the aerial hyphae which develop 

in the light become modified as conidiophores 

(Callaghan, 1969a,b). 

Sexual reproduction in B. ranarum 

Zygospores are formed following conjugation. 

The fungus is homothallic and development can 

be seen on certain agar media (e.g. Czapek-Dox 

agar) within 4 5 days in cultures derived from a 

single conidium. Zygospore development appears 

to occur most readily in the dark, and under these 

conditions the hyphal bodies become bicellular 

prior to developing into zygospores (Callaghan, 

1969b). On either side of a septum, beak-like 

projections develop, and the single nucleus 

within each hyphal segment migrates into the 

tip and divides there. One daughter nucleus is cut 

off by a septum in the terminal cell of the beak 

and later disintegrates, whereas the second 

nucleus migrates back into the parent cell. 

Following this, one of the parent cells enlarges 

to several times the volume of the adjacent cell 

and a pore is formed connecting the two cells 

through the original septum separating them. 

A nucleus from the smaller cell passes through 

the pore and lies close to the nucleus of the larger 

cell. Nuclear fusion may occur directly or after 

a further division. The enlarged parent cell forms 

the zygospore which has a thick wall when 

mature (Fig. 7.38). Meiosis occurs within the 

mature zygospore to give four haploid nuclei, of 

which three usually degenerate. The mature 

zygospores of some isolates of B. ranarum have 

thick undulating walls of variable thickness, 

but in others the wall may be smooth. On germination 

the zygospore forms a germ tube 

or a conidiophore terminated by a ballistosporic 

conidium. Capilliconidia may also develop from 

germinating zygospores (Dykstra & Bradley-Kerr, 

1994). The complicated and unusual life cycle 

of B. ranarum is illustrated in Fig. 7.37. 

Basidiobolus ranarum is an atypical zygomycete 

in that its mycelium becomes divided into uninucleate 

segments. The nucleus is also unusually 

large, up to 25 mm, and this fact has led to several 

investigations of its cytology (e.g. Robinow, 1963; 

Tanaka, 1970; Sun & Bowen, 1972). The number 

of chromosomes has been estimated to be as high 

as 900, and the nucleus may be polyploid. 

Pathogenicity of B. ranarum 

Basidiobolus is probably not harmful to most 

insects and mites, although it has been isolated 

as a mass infection of mosquitoes, from termites 

and from larvae of Galleria (Krejzová, 1978). It was 

earlier thought to be harmless to reptiles and 

amphibians and there is no evidence of intestinal 

lesions in them. However, an epizootic cutaneous 

infection caused by B. ranarum has been reported 

from the dwarf African clawed frog, Hymenochirus 

curtipes (Groff et al., 1991). There are many reports 

of the isolation of B. ranarum from man and 

domestic animals such as horses (see Gugnani, 

1999; Ribes et al., 2000). Although several specific 

names have been applied to isolates pathogenic 

to humans and other mammals, the consensus is 

that they should be regarded as synonyms 

of B. ranarum (McGinnis, 1980). This view is 

supported by ribosomal DNA analysis (Nelson 

et al., 1990). Isolates from humans, unsurprisingly, 

are capable of growing at 37°C (Cochrane 

et al., 1989). Human disease caused by B. ranarum 

is more common in tropical and subtropical 

regions than in temperate zones. Infection is 

associated with subcutaneous swellings of 

affected areas of the lower limbs but rare intestinal 

infections are also known. It is assumed that 

the inoculum is usually soil-borne, and the use 

of fallen leaves in place of toilet paper has 

sometimes been implicated as the cause of


Fig 7.37 The eventful life cycle of Basidiobolus ranarum, not to scale. A beetle with attached or ingested ballistoconidia and 

capilliconidia is eaten by a frog. In the gut of the frog, both conidial types can undergo cleavage to form endospores, which germinate 

by enlargement to form the gut stage. After defaecation, gut-stage cells germinate to produce ballistoconidia or cleave to give the 

Palmella stage. Discharged ballistoconidia may germinate by repetition, by forming capilliconidia, or by emitting a hypha. Zygospore 

formation is initiatedby conjugation between two adjacent hyphal cells. Small open circles represent haploid nuclei; diploid nuclei are 

larger and split. Basidiobolusranarum is homothallic. Key events in the life cycle are plasmogamy (P), karyogamy (K) and meiosis (M). 

infections. In horses, infection of the nasal 

mucosa is again most probably from soil. 

7.5.2 Ancylistaceae: Conidiobolus 

There are about 30 species of Conidiobolus, the 

‘conidium thrower’. King (1977) has given keys 

and descriptions. Most of them grow saprotrophically 

in soil and litter and can be readily 

isolated by the canopy technique described for 

Basidiobolus (see p. 203) because they forcefully 

project their conidia. Several species have been 

isolated from basidiocarps of the Jew’s Ear 

fungus, Auricularia auricula-judae. Some are pathogenic 

to insects such as aphids and termites, and 

certain species cause disease in mammals 

including man. The characteristic feature of 

Conidiobolus is the formation of globose multinucleate 

primary conidia surrounded by a twolayered 

wall whose layers do not separate (Latgé 

et al., 1989). The primary conidia are projected 

by an eversion mechanism in which the inner 

wall of the double-walled conidiophore apex 

(‘columella’) suddenly rounds off because of 

different mechanical properties of the two wall 

layers. The force responsible is turgor pressure. 

After discharge, the tip of the columella can be 

seen projecting outwards as a conical papilla, 

and the base of the discharged conidium ends 

in a similar projection (Fig. 7.39b). Spores may 

be shot away for up to 4 cm. Germination of 

primary conidia may be by repetition producing 

the same spore type, by germ tubes (direct


209 

Fig 7.38 Basidiobolus ranarum. Successive 

stages in the formation of zygospores. 

(a) Progametangia. (b) Young zygospore. 

(c) Mature zygospore. 

germination), by the formation, in some species, 

of numerous microconidia, or by the development 

of capilliconidia resembling those of 

Basidiobolus. Zygospores or azygospores have 

been reported and all species which reproduce 

sexually in this way are homothallic. It is 

believed that the cytological condition of the 

nuclei is haploid, as it is in other Zygomycota, 

and that karyogamy and meiosis are involved in 

the formation of zygospores and azygospores 

(McCabe et al., 1984). 

The best-known species of Conidiobolus is the 

cosmopolitan C. coronatus, a fungus which has 

been referred to under various names, e.g. 

Entomophthora coronata, Delacroixia coronata and 

Conidiobolus villosus. It grows readily and rapidly 

in agar culture, forming a septate mycelium and 

numerous phototropic conidiophores (Fig. 7.39) 

which shoot off conidia onto the lid of the Petri 

dish. Conidial discharge takes place both in the 

light and in the dark, but is enhanced by light 

(Callaghan, 1969a). 

The behaviour of a conidium on germination 

depends on pH, humidity, availability of light, 

and nutrients. If the conidium falls on a medium 

containing nutrients, it germinates by means of a 

germ tube, but on nutrient-poor media, such as 

water agar, it may develop into a secondary 

conidiophore, forming a slightly smaller conidium 

(Fig. 7.39c). The secondary conidiophore 

develops from the illuminated side of a primary 

conidium, and the conidiophore which develops 

is phototropically orientated, but not very 

precisely (Page & Humber, 1973). Under conditions 

of reduced humidity the primary conidia 

may develop a cluster of globose microconidia 

(Fig. 7.39f). The entire cytoplasm of the primary 

conidium is evacuated by the expansion of a large 

vacuole into numerous buds formed by localized 

softening of the primary conidium wall. At


Fig 7.39 Conidiobolus 

coronatus. (a) Conidiophore 

with attached primary 

conidium. Note the columella 

which protrudes into the body 

of the conidium. (b) Apex of 

conidiophore and conidium 

after discharge by eversion of 

the columella from inside the 

spore. (c) Primary conidium 

germinating by repetition to 

produce a secondary conidium 

of similar type. (d) Conidium 

germinating directly, forming 

several germ tubes. 

(e) Conidium germinating to 

produce a villose secondary 

conidium. (f) Conidia 

germinating to produce 

numerous secondary 

microconidia which are 

discharged by columellar 

eversion. 

maturity each microconidium is supported on a 

two-ply columella and projected by the eversion 

mechanism. In older cultures, primary conidia 

may form short conidiophores terminating in 

pear-shaped spiny-walled (villose) conidia, which 

are also projected by columellar eversion. The 

precise conditions under which spiny conidia are 

formed are not known. They have been interpreted 

as resting spores, and they germinate to 

form a coarse septate mycelium. The possession of 

both microconidia and villose conidia is a 

combination unique to C. coronatus. Another 

type of resting spore may develop from ungerminated 

primary conidia which swell and form 2 3


211 

layered thickened walls. Such conidia have been 

termed loriconidia (Gindin & Ben-Ze’ev, 1994). 

No zygospores have been reported for C. coronatus, 

structures resembling zygospores being interpreted 

as aerial chlamydospores. 

Conidiobolus coronatus is a parasite of aphids, 

termites and whiteflies attacking tobacco, cotton 

and sweet potato, as well as of waxmoths and 

some other insects (Gindin & Ben-Ze’ev, 1994; 

Bogus & Szczepanik, 2000). It should be regarded 

as a relatively primitive opportunistic pathogen. 

Infection of termites can occur by penetration of 

germ tubes through the exoskeleton, or via the 

oesophagus after ingestion of germinated conidia 

(Yendol & Paschke, 1965). Following infection 

of insects, death can occur within 2 days, probably 

by the production of toxins (Evans, 1989). 

A highly insecticidal 30 kDa protein has been 

found in mycelium and culture filtrates of 

C. coronatus (Bogus & Scheller, 2002). This and 

possibly other toxins induce damage to blood 

cells or early death in several insects when 

injected into the haemocoel. In artificially 

infected waxmoths (Galleria mellonella), infection 

is followed by melanization of the host cuticle 

and damage to the Malpighian tubules with 

no evidence of tissue penetration (Bogus & 

Szczepanik, 2000). Conidiobolus coronatus and 

C. obscurus are being investigated as potential 

agents of biological control of insect pests. 

Conidiobolus coronatus is also pathogenic to 

mammals such as horses, llama, chimpanzee 

and man. Human infections are most common in 

the moist tropics and subtropics, especially in 

male outdoor workers from the rain forests of 

West Africa. Although the mode of transmission 

has not been established it is probably by inhalation 

of spores which germinate in the nasal 

mucosa. Other species of Conidiobolus known to 

infect vertebrates are C. incongruus and C. 

lamprauges. Isolates pathogenic to vertebrates 

grow readily at 37°C (Gugnani, 1992; Ribes 

et al., 2000). 

7.5.3 Entomophthoraceae 

Benny et al. (2001) included 12 entomopathogenic 

genera in the family Entomophthoraceae 

(Gr. ‘insect destroyer’), of which we shall study 

the three most important, i.e. Erynia, 

Entomophthora and Furia. 

Erynia 

There are about 12 species of Erynia parasitic 

on terrestrial insects such as aphids and 

Lepidoptera, but some attack the aquatic larval 

stages of Diptera such as Simulium spp. (river 

blackflies), stone flies and caddis flies. 

Characteristic features of the genus are branched 

conidiophores bearing uninucleate, bitunicate 

primary conidia which are discharged by septal 

eversion. Germination of primary conidia is by 

the production of various types of secondary 

conidia. Tertiary conidia may also develop. 

Resting bodies (azygospores and zygospores) 

occur in some, but not all species. Attempts are 

being made to use Erynia neoaphidis to control 

aphid populations in field crops (Pell et al., 2001). 

Erynia neoaphidis 

This species, synonymous with Entomophthora 

aphidis, Pandora neoaphidis and Zoophthora neoaphidis, 

is the most widespread aphid pathogen of 

temperate regions and has been found on over 

70 species of aphids on annual and perennial 

crops. It also attacks aphids on non-cultivated 

plants, a common example being the nettle 

aphid, Microlophium (Fig. 7.40). Infected aphids 

are cream to brown in colour. They are attached 

on the ventral side to their plant host by fungal 

rhizoids and their bodies are distended. Within 

the body of an infected aphid there are numerous 

closely packed, wide, septate hyphal bodies 

(Fig. 7.41a). Widely spaced, thick-walled, long, 

awl-shaped pseudocystidia (Fig. 7.41b) pierce 

the cuticle and, surrounding them, numerous 

tightly packed, branched conidiophores emerge, 

usually made up of uninucleate segments 

(Figs. 7.41b,d; Brobyn & Wilding, 1977). The tip 

of the conidiophore is cut off by a two-ply 

septum to form a uninucleate primary conidium 

with a two-layered wall (Figs. 7.41d,e). 

Under humid conditions (relative humidity 

495%), primary conidia are discharged by 

septal eversion for a distance of about 1 cm, 

and detached conidia show a bulging papilla 

at their base. Violent discharge projects the 

conidia through the boundary layer of still air


Fig 7.4 0 Carcass of a nettle aphid (Microlophium) incubated 

on tap water agar for12 h. Note the halo of discharged conidia 

of Erynia neoaphidis. 

surrounding the host so that they come under 

the influence of wind and gravity, falling at a 

velocity of about 1 cm s 1 (Hemmati et al., 2002). 

About 200 000 conidia are produced per cadaver 

of adult pea aphid over a period of 2 3 days. 

Immediately after discharge, primary conidia 

may germinate to produce secondary conidia 

which are wider and more ovate than the 

primary conidia (see Figs. 7.41e,f). Direct germination 

by the production of a germ tube from 

one or both ends of primary and secondary 

conidia also occurs (Fig. 7.41c). As in many 

Entomophthorales, cytoplasm is concentrated 

into a few terminal cells, leaving empty intercalary 

segments cut off by retraction septa 

(Fig. 7.41c). 

Brobyn and Wilding (1977) and Butt et al. 

(1990) have described the process of infection of 

the pea aphid Acyrthosiphon pisum. Conidia adhere 

to any point on the aphid cuticle, often in 

clumps, and may germinate by forming secondary 

conidia or germ tubes. The tip of a germ tube 

can penetrate any part of the cuticle. Clavate or 

globose appressoria develop at the tips of the 

germ tubes. After penetrating the cuticle and 

epidermis, the hyphal tips branch and fragment 

to form multinucleate protoplasts which become 

rapidly dispersed throughout the haemocoel 

within about 12 24 h. The protoplasts may 

increase in number by budding (Butt et al., 

1981). It is believed that the switch to the 

protoplast form is in response to contact with 

the nutrient-rich haemolymph. Later, as the 

nutrients in the haemolymph are exhausted, 

the protoplasts develop cell walls and are 

transformed into hyphal bodies. Protoplasts 

and hyphal bodies colonize fat bodies, nerve 

ganglia and muscle tissue. Infected aphids die 

some 72 h after inoculation, and shortly before 

death rhizoids develop from enlarged hyphal 

bodies and emerge from the ventral side of the 

abdomen, making contact with the leaf on which 

the aphid has been feeding, then branching by 

bifurcation to form digitate holdfasts. About 

15 30 rhizoids may develop from a single aphid 

before it dies. Soon after death, pseudocystidia 

and conidiophores emerge. Under natural conditions, 

infected aphids die in the late afternoon 

and sporulation begins at night. The moist 

conditions and dew formation after sunset play 

a role in enhancing spore production and 

discharge. Hemmati et al. (2001) found that 

concentrations of air-borne conidia among 

wheat crops were usually highest at night and 

in the early morning and relatively low during 

the day, peak concentrations being correlated 

with high relative humidity. 

It is rare for an infected aphid to produce 

both conidia and resting bodies. Germinating 

resting bodies form branched or unbranched 

germ tubes bearing retraction septa. They are 

terminated by an apical conidium, followed by 

one or two lateral conidia. These conidia closely 

resemble those which develop on infected 

aphids, and they are discharged by septal eversion 

(Tyrell & MacLeod, 1975). The germination 

of resting bodies is markedly stimulated by longday 

conditions of more than 14 h of light per 

day (Wallace et al., 1976). In the pea aphid, 

E. neoaphidis does not form resting bodies, surviving 

instead as hyphal bodies in aphid cadavers. 

Artificially infected cadavers can be stored and


213 

Fig 7.41 Erynianeoaphidis.(a)Hyphalbodyfrom 

within an infected aphid. (b) Pointed 

pseudocystidium projecting above a layer of 

conidiophores at the surface of a dead aphid. 

(c) Direct germination of a secondary conidium. 

Cytoplasm is confined by a retraction septum to 

the tip of the germ tube. (d) Branched 

conidiophore with terminal primary conidia. 

The wall surrounding the conidium is bitunicate 

with a thin outer envelope. (e) Discharged 

uninucleate primary conidium. (f) Discharged 

secondary conidium.Compare its more ovoid 

shape with the shape of the primary conidium. 

(g) A discharged secondary conidium has 

germinated by repetition to form a further 

conidium of the same type. Note the bulging 

septum on the empty conidium and at the 

base of the newly developed conidium. 

(h) Primary conidium germinating to form 

a secondary conidium. Both are bitunicate. 

(i) Secondary conidium germinating to form 

a tertiary conidium with a single large lipid body. 

(j) Tertiary conidium germinating by 

repetition. (a,b) ¼ 20 mm; (c j) ¼ 12.5 mm. 

used as inoculum to introduce the parasite 

into field populations of aphids pathogenic to 

crops, such as Aphis fabae, the common blackfly 

of broad beans. It is also possible to grow 

E. neoaphidis in agar culture and to introduce 

inoculum into aphid-infested crops in this form 

(Shah et al., 2000). 

Erynia conica 

Whilst E. neoaphidis shows some versatility in its 

asexual reproduction, a more extreme example 

is E. conica, which forms four distinct types 

of conidium, some of them primary and some 

secondary (Descals et al., 1981; Hywel-Jones & 

Webster, 1986a). Erynia conica is a parasite of the 

blackfly Simulium (Diptera) and some other insect 

hosts associated with aquatic habitats. Simulium 

spp. have aquatic larval stages generally found in 

rapidly flowing streams. The larvae are attached 

to stones, twigs and aquatic plants, feeding by 

the ingestion of particulate matter collected 

by modified branched mouthparts (head rakes). 

After pupation, winged adults emerge, mate, and 

the females take a blood meal from a mammal. 

Gravid females lay egg masses amongst algae and 

mosses on water-splashed boulders kept continuously 

wet by trickling water. At such sites the 

white swollen bodies of dead females infected 

by E. conica, attached by rhizoids, may sometimes 

be found in large numbers. Conidiophores 

project from the carcass, bearing conidia of two 

types. From conidiophores which develop in air, 

i.e. at the surface of the insect’s body projecting 

out of water, boat-shaped bitunicate conidia


develop. These are termed primary cornute (type 1) 

conidia and are illustrated in Fig. 7.42a. They are 

discharged from the conidiophores by septal 

eversion. If a type 1 conidium floats on the 

water surface, it will germinate to produce a 

balloon-shaped secondary globose (type 2) conidium 

on its upper side, projecting into the air. 

The type 2 conidium contains a single large lipid 

body and a two-ply septum capable of discharge 

by eversion (see Fig. 7.42b). 

When primary cornute conidia become 

submerged in water, they germinate to produce 

a secondary conidium of a different type. Its body 

has four branches (i.e. it is tetraradiate) and the 

position of attachment of this conidium to the 

short conidiophore is the central point from 

where the four arms radiate (see Fig. 7.42c). 

This type of spore is termed a secondary stellate 

(type 3) conidium. If a dead infected insect is 

continuously bathed in water or is submerged, 

the conidiophores emerging from it will develop 

primary conidia which are also tetraradiate, 

but these are attached at the tip of the main 

arm from which three upper arms radiate 

(see Fig. 7.42d). This type of conidium is a primary 

coronate (type 4) conidium. So types 1 and 2 are 

aerial conidia, formed and discharged into air, 

whilst types 3 and 4 are aquatic conidia, formed 

and released under water. Tetraradiate conidia 

are a typical adaptation of fungi to dispersal in 

aquatic environments and are produced also by 

aquatic hyphomycetes (see p. 685). 

Most of the four types of conidium can 

germinate by repetition, by germinating to 

form conidia of one of the other types, or by 

the formation of germ tubes. For example, a type 

1 conidium can germinate by repetition to 

form a secondary conidium morphologically 

identical to itself, i.e. another type 1 conidium. 

This is described in shorthand as 1 1 

Fig 7.42 Erynia conica.The four types of conidia. (a) Primary cornute conidium (type1). Note the bitunicate wall. (b) Primary 

cornute conidium germinating to produce a secondary globose conidium (type 2). (c) Secondary stellate conidium (type 3) which has 

developed from a submerged primary cornute conidium.The point of attachment of the conidium is between the three backwardly 

directed arms (arrow). (d) Primary coronate conidium (type 4) with the point of attachment at the end of the main, vertical, arm 

(arrow).The single large nucleus is visible below the point of branching.Bar ¼ 20 mm, all images to same scale.From Webster (1992), 

with kind permission of Springer Science and Business media.


215 

germination (Webster et al., 1978). Type 1 conidia 

may show 1 1, 1 2 and 1 3 germination. Of the 

16 (i.e. 4 4) possible interconversions, 12 have 

been observed so far (Webster, 1987). The only 

type of conidium shown to be infective is the 

secondary globose, i.e. type 2, conidium (Hywel- 

Jones & Webster, 1986b). It is sometimes termed 

an invasive conidium. This kind of conidium 

only develops from cornute conidia, although 

these may be primary or secondary. When a 

secondary globose conidium is in contact with an 

insect cuticle, a short germ tube develops with 

an appressorium at its tip. Penetration of the 

cuticle seems to be mainly by enzymatic means 

and is followed by the formation of multinucleate, 

branched hyphal bodies in the haemocoel. 

It is presumed that the other kinds of 

conidia function as dispersal rather than infection 

units, and they can be found in appreciable 

numbers trapped in foam near infected flies. It 

appears that only adult flies are infected through 

the cuticle. Although all types of conidia are 

known to be present in larval guts, there is no 

evidence that larvae are infected from ingested 

conidia. Survival over winter, when adult insects 

are not available, is by globose, thick-walled 

zygospores which are formed within the dead 

body of an insect, surrounded by a network of 

brown hyphae. 

The precise physical conditions associated 

with the different types of germination in 

E. conica are not known and most attention has 

been devoted to the germination of the primary 

cornute (type 1) and secondary globose (type 2) 

conidia (Nadeau et al., 1995, 1996). Germination 

of the latter, resulting in appressorium formation 

and cuticular penetration on wings of the 

susceptible host S. rostratum, occurs over the 

temperature range of 15 25°C with an optimum 

at 20°C. Germination occurs within 2 h and 

penetration within 9 h. The development of 

appressoria is related to the presence of a coating 

of lipid on the host cuticle. In experiments in 

which lipids were removed from susceptible 

blackfly wings, there was no discernible appressorium 

formation or cuticular penetration. On 

the non-susceptible host S. decorum, germination 

is delayed and appressorium formation and 

cuticular penetration do not occur. Instead, a 

high level (26%) germination of the 2 1 type 

takes place. 

The plasticity of asexual reproduction shown 

by E. conica is not unique. Similar versatility 

is shown by some other members of the 

Entomophthoraceae which grow on insects 

with aquatic larval stages such stoneflies 

(Plecoptera) and crane flies (Tipulidae) (Descals 

& Webster, 1984). 

Entomophthora muscae 

There are about a dozen species of Entomophthora, 

occurring as widespread insect pathogens 

(Samson et al., 1988; Humber, 1997). They are 

characterized by unbranched conidiophores and 

multinucleate primary conidia which are 

projected by a squirt mechanism. Secondary 

conidia may form on germination of the primary 

conidia, but these are discharged by a septal 

eversion mechanism similar to that described 

above for Erynia and Conidiobolus. Sexual reproduction 

is by the formation of zygospores and 

azygospores. 

The best-known taxon is E. muscae which is, in 

fact, a complex of about five species with similar 

morphology and spore dimensions (MacLeod 

et al., 1976). This fungus is a parasite of houseflies 

and other Diptera. Disease is apparent in summer 

to autumn and is more frequent in wet weather. 

In the field, epizootics occur in places where there 

are dense populations of potential hosts, for 

example dung flies (Scatophaga spp.) on farms, or 

hoverflies (Melanostoma spp.) attracted to the 

honeydew secreted by Claviceps (see Fig. 12.26b) 

on the moor grass Molinia. Diseased flies can 

occasionally be found attached to the glass of a 

window pane surrounded by a white halo about 

2 cm in diameter made up of discharged conidia 

(Plate 3g). 

The dead fly shows a distended abdomen with 

white bands of conidiophores projecting between 

the segments of the exoskeleton. The unbranched 

multinucleate conidiophores arise from the 

coenocytic mycelium which plugs the body of 

the dead fly. The conidia are also multinucleate 

(Fig. 7.43b). They are projected by a forwardly 

directed jet of cytoplasm from the elastic conidiophores. 

On impact, the bitunicate nature of 

the wall of the primary conidium becomes


apparent (Fig. 7.43e). Recently discharged conidia 

have a dried out drop around them which 

represents the cytoplasm squirted from the 

conidiophore (Figs. 7.43d f). This cytoplasmic 

coating may act as a protective agent against 

desiccation and may possibly help in attaching 

the primary conidium to the cuticle of an insect. 

If the conidium impinges on the body of a fly, it 

develops an adhesive pad which attaches it firmly 

to the cuticle (Fig. 7.43h). Penetration of the 

cuticle is probably brought about by a combination 

of mechanical and enzymatic means (Brobyn 

& Wilding, 1983). A few hours after infection, triradiate 

fissures can be seen in the cuticle beneath 

attached conidia. When the cuticle in such a 

region is examined from the inside, a thin-walled 

bladder-like expansion can be seen. From this cell 

mycelial branches develop. The hyphae grow 

towards the fatty tissues, and as these are 

consumed the hyphae break up to form wall-less 

protoplasts which are carried by the circulatory 

system to all parts of the body. Eventually the 

protoplasts secrete walls and become converted 

into hyphal bodies (Fig. 7.43c). Infected flies show 

behavioural changes, often crawling to the top of 

a grass stem and clasping it or adhering to walls 

or window panes by the proboscis (Maitland, 

1994). The sexual behaviour of the host may also 

be affected (Moller, 1993). Males attempting to 

mate with diseased females may themselves 

Fig 7.43 Entomophthora muscae. 

(a) House fly adhering to a window pane, 

surrounded by a halo of discharged 

conidia. (b) L.S. house fly showing palisade 

of unbranched conidiophores projecting 

between segments of the exoskeleton. 

The conidiophores and conidia are 

multinucleate. (c) Hyphal bodies from 

recently dead fly extending to form 

conidiophores. (d) Primary conidium 

immediately after discharge surrounded 

by cytoplasm from the conidiophore. 

(e,f) Germination of primary conidia to 

form secondary conidia which are 

discharged by bouncing off (septal 

eversion). (g) Germination of secondary 

conidium by germ tubes. (h) Attachment 

of primary conidium to integument 

of a fly. (i) Two primary conidia 

attached to integument and penetrating 

it by a tri-radiate fissure. (j) View of 

penetration from within the integument. 

Note the bladder-like expansion within 

the tri-radiate fissure. (b g) to same 

scale, (h j) to same scale.

GLOMALES 

217 

become infected with E. muscae, making it a 

sexually transmitted pathogen. Although it was 

previously generally accepted that there are no 

rhizoids in E. muscae, Balazy (1984) has shown that 

rhizoids do develop from hyphal bodies within 

the head, growing through the proboscis and 

forming a network of branched hyphae with 

short irregular holdfasts. A few days after infection 

the fly dies and the hyphal bodies within 

the abdomen then grow out into coenocytic 

hyphae which penetrate between the abdominal 

segments and develop into conidiophores. 

Discharge of primary conidia begins within 

about 5 h, reaching a maximum about 10 12 h 

after death. Over 8000 conidia may develop from 

a single cadaver (Mullens & Rodriguez, 1985). 

The primary conidia remain viable for only 

3 5 days. If they fail to penetrate a fly, they may 

produce secondary conidia within 3 h. The 

secondary conidia are released from the tips of 

short conidiophores by septal eversion. They may 

germinate by a germ tube or by producing the 

same type of conidium by repetition. 

Within the body of the dead fly, multinucleate 

spherical resting bodies (azygospores) are formed. 

In the wheat bulb fly Leptohylemia coarctata it has 

been observed that a much higher proportion of 

infected female flies contain resting bodies as 

compared with infected males. This is probably 

associated with the longer lifespan of females 

than males (Wilding & Lauckner, 1974). Resting 

bodies may develop terminally or in an intercalary 

position from short hyphae, or by budding 

from hyphal bodies. They germinate by developing 

a germ conidiophore. Germination is stimulated 

by the action of chitin-decomposing 

bacteria on the resting spore wall. It is from 

such resting bodies that infection probably 

begins each year (Goldstein, 1923). 

The onion fly Delia antiqua has maggots which 

pupate in the soil and overwinter there. Adults 

become infected as they emerge through the 

soil the following season, presumably from germ 

conidia which develop from resting spores 

(Carruthers et al., 1985). In some members of 

the Entomophthorales, e.g. Entomophthora sepulchralis, 

zygospores develop following conjugation 

between hyphal bodies (see Fig. 7.44). 

Entomophthora muscae, like many other 

entomopathogenic Entomophthorales, can be 

grown in complex media such as those used in 

tissue culture (Wolf, 1981; Papierok & Hajek, 

1997). Yeast extract and ingredients of animal 

origin such as egg yolk, fat and serum or blood 

are also used. Growth is markedly stimulated by 

glucosamine, a breakdown product of chitin. 

Successful cultures have also been established 

on a medium containing wheat grain extract, 

peptone, yeast extract and glycerol (Srinivasan 

et al., 1964). 

Furia 

Some of the species formerly placed in the 

genus Entomophthora have features distinct 

from E. muscae and have been re-classified into 

different genera. An example is Furia americana 

(Plate 3h, Fig. 7.45), a fungus found on blowflies 

in the autumn, especially around corpses of dead 

animals or stinkhorns. In wet weather severe 

epidemics may occur, greatly affecting the 

blowfly population. Distinctive features are the 

conidiophores which branch close to the conidiogenous 

cells; uninucleate, bitunicate clavate 

conidia with a rounded apex and basal papilla; 

and discharge by septal eversion. Dead flies are 

often attached to adjacent plants by filamentous 

rhizoid-like hyphae. The conidiophores form 

yellowish pustules between the abdominal 

segments and the branched tips bear conidia. 

The two layers of the conidium wall are 

frequently separated from each other by liquid 

(Figs. 7.45a c). These conidia are projected for 

several centimetres from the host and, on germination, 

may form germ tubes, or may produce 

secondary conidia which are projected by the 

rounding off of a two-ply septum. Within the dry 

body of the dead fly numerous smooth hyaline 

thick-walled resting spores (azygospores) are 

formed by budding from the lateral walls of 

parent hyphae (Fig. 7.45f). 

7.6 Glomales 

The roots of most terrestrial plants grow in 

a mutualistic symbiosis with fungi, i.e. an 

association in which both partners benefit.


mycorrhiza (AM). These fungi are particularly 

well-known as mycorrhizal associates of herbaceous 

plants, but they may also associate with 

trees, especially in the tropics. 

Fig 7.4 4 Entomophthora sepulchralis.Three stages in 

zygospore formation.Two hyphal bodies conjugate and the 

zygospore arises as a bud from the fusion cell (afterThaxter, 

1888). 

Such symbiotic associations are termed mycorrhiza 

(Gr. ‘fungus root’). There are several 

different kinds of mycorrhiza, including vesicular 

and arbuscular mycorrhiza, ectomycorrhiza 

(sheathing mycorrhiza, pp. 21 and 526), ericoid 

mycorrhiza (p. 442), and orchid mycorrhiza 

(p. 596) (Smith & Read, 1997; Peterson et al., 

2004). It is important to realize that the nature of 

the relationships between the fungi and their 

host plants in these distinct types of association 

is not the same. In this section we shall look 

at the Glomales, a group of zygomycetous 

fungi causing the development of vesicular 

arbuscular mycorrhiza (VAM) and arbuscular 

7.6.1 General features of VAM and AM 

A coarse, intercellular, aseptate coenocytic mycelium 

within the root tissues may develop large, 

balloon-shaped intercalary or terminal thickwalled 

vesicles (intraradical vesicles) which are 

multinucleate and contain large amounts of 

lipid (Figs. 7.46c,d). In some plants, e.g. the 

roots of Paris, the mycelium emits branches 

which penetrate the cortical root cells, forming 

extensive intracellular coils. More commonly, 

hyphae penetrating host cells fork repeatedly to 

form richly branched arbuscules (Fig. 7.46c) 

which invaginate the plasmalemma. Plant and 

fungal plasma membranes are separated by an 

apoplastic compartment, the periarbuscular 

space. The arbuscule is therefore a type of 

haustorium, and there is an interchange of 

nutrients and water across the periarbuscular 

space. Arbuscules have a relatively short active 

life, lasting only a few days. After this time the 

fine tips of the arbuscules are digested by the 

host cell so that only irregular clumps of fungal 

material remain (Fig. 7.46c). 

A coarse, angular and often thick-walled 

mycelium extends outwards from infected 

roots, sometimes for several cm, and penetrates 

into the surrounding soil. It may bear large 

(4100 mm dia.) globose multinucleate thickwalled 

spores which are sometimes termed 

chlamydospores. These spores contain thousands 

of nuclei as well as energy reserves including 

lipid droplets, glycogen, protein and trehalose. 

These spores may be borne singly or in clusters 

and are often naked, but in some species, 

e.g. Glomus mosseae, they are enveloped in a weft 

of hyphae to form a sporocarp (Figs. 7.46a,b). 

Chlamydospores are asexual reproductive structures 

and are known to survive in dry soil for 

many years. For most members of the group only 

asexual reproduction is known, but in Gigaspora 

decipiens zygospores and azygospores have been 

reported in addition to chlamydospores. 

This species is heterothallic (Tommerup &

GLOMALES 

219 

Fig 7.45 Furia americana from blowfly. 

(a) Branched conidiophore. (b) Single 

conidiophore and conidium. Note that the 

wall of the conidium is bitunicate. (c) Conidia 

after discharge. (d) Conidium germinating by 

means of a germ tube. (e) Primary conidia 

germinating to produce secondary conidia. 

(f) Spherical resting bodies from dead fly. 

Sivasithamparam, 1990). Sporocarps may form 

part of the diet of some mammals and chlamydospores 

can be dispersed by soil animals, including 

invertebrates and some rodents as well as 

larger hoofed mammals. Chlamydospores can 

survive in their faeces and are also dispersed in 

wind-borne soil dust (Allen, 1991; Allen et al., 

1997; Linderman, 1997). 

The spores of Glomales can be extracted from 

soil by wet sieving and decanting from soil 

slurries using a series of sieves in the 

2000 60 mm size range (Gerdemann & Nicolson, 

1963). After surface sterilization, single chlamydospores 

placed near the roots of susceptible host 

plants such as Trifolium and Sorghum germinate, 

produce hyphae which make contact with the 

root surface and form appressoria before infecting 

the root (Hepper, 1984; Menge, 1984). In this 

way, dual cultures have been established and can 

be maintained by the addition of freshly 

extracted spores or infected root pieces to pots 

containing a suitable host plant. Viable spores 

derived from dual cultures maintained on potted 

plants are available from the International 

Collection of Vesicular Arbuscular Mycorrhizal 

Fungi (Morton et al., 1993). Spores have also been 

produced under aseptic conditions in association 

with hairy root cultures (Mugnier & Mosse, 1987; 

Bécard & Fortin, 1988). Limited extension of germ 

tubes takes place after germination in vitro, but 

sustained growth in the absence of living root 

tissues does not occur, so the fungi causing this


Fig 7.4 6 Vesicular arbuscular mycorrhiza. (a) Glomus mosseae sporocarp in which chlamydospores are embedded.There are also 

naked chlamydospores attached to external hyphae. (b) Chlamydospores dissected from a sporocarp, borne on single subtended 

hyphae. (c) Onion root cells infected with Glomus mosseae.The cell to the left contains a nucleus with two nucleoli and a branched 

haustorium or arbuscule. In the cell to the right the arbuscule has degenerated. (d) Vesicles from roots of Arum maculatum.

GLOMALES 

221 

kind of mycorrhiza are obligate mutualistic 

symbionts. Glomalean fungi are generally nonspecific 

in their host range. The roots of most 

groups of vascular land plants are associated with 

this type of mycorrhiza, as are the gametophytic 

stages of Bryophyta and Pteridophyta. 

7.6.2 Taxonomy and evolution of Glomales 

Fungi in this group were originally classified in 

the Endogonales but are currently placed in a 

separate order, the Glomales, with the 

Endogonales now reduced to a single genus, 

Endogone, with subterranean fleshy sporocarps 

which contain zygospores. Each zygospore is 

formed after conjugation of two gametangia 

(Pegler et al., 1993). One species, E. flammicorona, 

forms ectomycorrhizae with some Pinaceae (Fassi 

et al., 1969). The fruit bodies of Endogone spp. are 

colloquially called ‘pea truffles’ (Plate 3i; Pegler 

et al., 1993). 

The order Glomales was proposed by Morton 

and Benny (1990) to include all soil-borne fungi 

which form arbuscules in obligate mutualistic 

associations with terrestrial plants. Sexual reproduction 

is rare. There are about 150 species and 

6 genera in 2 suborders, the Glomineae with 

2 families (Glomaceae and Acaulosporaceae), 

and the Gigasporineae with a single family 

(Gigasporaceae). Members of the Glomineae 

(such as Glomus, Acaulospora) form intraradical 

vesicles (VAM type), whilst members of the 

Gigasporineae have no intraradical vesicles and 

are of the AM type. The separation of genera 

within the Glomales is based partly on different 

patterns of chlamydospore development, and 

partly on the structure of the spore wall which 

may be complex and multilayered (Hall, 1984; 

Morton & Bentivenga, 1994). Schüssler et al. 

(2001) have suggested that the Glomales are not 

closely related to the Zygomycota and should 

be considered as a separate phylum, the 

Glomeromycota. 

VAM and AM associations are very ancient, 

and structures resembling extant arbuscules 

have been discovered in the fossilized rhizome 

tissues of early vascular plants, including 

Devonian psilophytes such as Rhynia (Pirozynski 

& Dalpé, 1989; Taylor et al., 1995). Even older are 

the fossilized chlamydospores found among 

bryophytes of the Ordovician period (some 

460 million years old; Redecker et al., 2000a). It 

is believed that the origin and evolution of land 

plants was dependent on symbiotic associations 

of the VAM and AM type (Pirozynski & Malloch, 

1975; Malloch, 1987; Simon et al., 1993). 

An interesting non-mycorrhizal relative of 

the Glomales is the fungus Geosiphon pyriforme, 

which is unusual in harbouring a mutualistic 

endosymbiont, the cyanobacterium Nostoc. When 

the hyphal tip of Geosiphon encounters a suitable 

symbiont, this is taken up and the hypha 

swells to form a so-called bladder cell. The 

Geosiphon Nostoc symbiosis resembles cyanolichens 

(see p. 451) in being autotrophic both for 

carbon and nitrogen (Schüssler & Kluge, 2001). 

Geosiphon reproduces by forming chlamydospores 

similar to those of Glomus. Molecular studies 

show that Geosiphon is closely related to the 

Glomales and may be ancestral to the group 

(Gehrig et al., 1996; Redecker et al., 2000b). 

7.6.3 Physiological and ecological studies 

The immense current interest in AM and VAM 

mycorrhiza has its origins in the demonstration 

of the improved growth of mycorrhiza-infected 

host plants compared to uninfected controls. 

Literature on the physiology of this relationship 

has been reviewed by Hause and Fester (2005). 

The arbuscule is the main interface for nutrient 

exchange between the plant and its fungal 

partner, although the latter may also be able to 

take up nutrients through intercellular hyphae. 

The periarbuscular space is a highly acidic 

compartment (Guttenberger, 2000) due to the 

outward-directed pumping of protons by H þ 

ATPases located in the plasma membranes of 

both partners. This sets up proton gradients 

which may be used for active uptake of sucrose 

hydrolysis products (fructose and glucose) by the 

fungus, and phosphate and other mineral nutrients 

by the plant. Proton-dependent transport 

proteins have been localized in both plant and 

fungal perihaustorial membranes (see Hause & 

Fester, 2005). 

The ecology of VAM and AM fungi in crop 

plants and natural communities is of particular


interest (Allen, 1991; Smith & Read, 1997; Leake 

et al., 2004). There are numerous reports of 

significant improvements in growth rate, dry 

weight and mineral content following infection 

especially of plants growing on nutrient-deficient 

soils. Emphasis has been placed on phosphate 

nutrition. The supply of phosphate (as 

2 

HPO 4 or H 2 PO 4 , depending on soil pH) is often a 

limiting factor to plants growing in natural soils. 

It is usually present in low concentrations and 

diffuses through soil very slowly. Its influx may 

increase 3 4-fold in infected plant roots but 

there are also significant increases in other 

minerals such as Zn, Cu, and ammonium. The 

water relations and resistance of infected plants 

to infections by pathogens may also be improved. 

Increased uptake of minerals is largely due to the 

exploration of larger volumes of soil by the 

extramatrical hyphae which can extend beyond 

the depletion zone surrounding plant roots. 

The depletion zone is a region in which minerals 

are taken up by plant roots at a rate greater than 

can be replenished by diffusion through the soil. 

For many plants the depletion zone is only 

1 2 mm wide whilst the extramatrical hyphae 

may extend for several centimetres and can 

penetrate into soil cavities too fine to be 

explored by roots. Moreover, phosphate can be 

translocated through fungal hyphae towards 

the host root at much faster rates than is possible 

by diffusion through soil. The improved growth 

of host plants associated with increased supply 

of minerals obtained through the hyphae of the 

mycorrhizal symbiont is achieved at a cost to 

the plant, i.e. the drain of photosynthate taken 

up by the fungus whose biomass, achieved 

largely at the expense of the host, may amount 

to 3 20% of the root weight. In experiments in 

which 14 CO 2 was supplied to the shoots of young 

cucumber plants infected by G. fasciculatum, as 

much as 20% of the radioactive carbon fixed by 

the plant was used by the fungus (Jakobsen & 

Rosendahl, 1990). 

In nutrient-deficient soils such as sand dunes, 

recently disturbed soil, spoil heaps, areas covered 

by volcanic ash, etc., successful colonization by 

plants appears to be correlated with root infection 

by Glomales (Allen, 1991). In closed vegetation 

such as mature grassland which contains a 

diversity of plants, spore extraction reveals a 

wide diversity of AM and VAM species. The roots 

of different plant species making up the community 

are in close contact and may also be 

connected by a hyphal network (Newman, 

1988). There is experimental evidence using 

isotopically labelled 15 N, 32 P, and 14 C that there 

may be an interchange of mineral nutrients and 

carbon between unrelated plant species 

mediated by VAM mycelia, but Newman (1988) 

has cautioned against the conclusion that any 

increases in labelled materials necessarily imply 

net gains to receiver plants at the expense of 

donors. There is also experimental evidence 

using soil microcosms seeded with a mixture of 

grassland grasses and dicotyledons and inoculated 

with Glomus constrictum that mycorrhizal 

infection may increase species diversity by 

selectively enhancing the performance of less 

dominant dicotyledons. This results largely 

from a reduction in relative abundance of 

canopy dominants such as Festuca ovina (Grime 

et al., 1987). 

7.7 Trichomycetes 

The Trichomycetes are a group of fungi which 

grow commensally in the guts of terrestrial, 

freshwater and marine arthropods such as 

insects, millipedes and crustaceans. In most 

cases there is little evidence that the host is 

harmed by their presence, although it has been 

shown that some species may extend parasitically 

into the ovarian tissue to form chlamydospores 

(cysts) in place of eggs. These are deposited 

amongst egg masses laid by uninfected females. 

McCreadie et al. (2005) have documented an 

element of plasticity in the association of a 

given trichomycete species, Smittium culisetae, 

with its blackfly host which may vary from 

commensalistic in well-fed larvae to mutualistic 

under starvation conditions to parasitic if the 

ovaries of adult females are infected. 

More than 50 genera and over 200 species 

have been described but doubtless many more 

await discovery (Lichtwardt, 1986, 1996; Misra, 

1998; Misra & Lichtwardt, 2000). Members of the

TRICHOMYCETES 

223 

group have a worldwide distribution and are 

especially common in the guts of larvae of 

aquatic insects. A few species belonging to one 

order (Harpellales) have been grown in culture 

and appear to have no unusual nutritional 

requirements. The term trichomycete (Gr. ‘hairy 

fungus’) refers to the fuzzy appearance of heavily 

infested gut linings. Branched or unbranched 

thalli are attached by a holdfast to the 

hindgut cuticle or to the peritrophic membrane, 

a transparent membranous sleeve which 

surrounds digested food material in the mid-gut 

of certain insects. Asexual reproduction is by 

various types of spore, including trichospores, 

chlamydospores, arthrospores or sporangiospores. 

Sexual reproduction by the formation 

of zygospores is known in the Harpellales. 

The occurrence of zygospores, the presence of 

chitin in the walls of Smittium culisetae (Sangar & 

Dugan, 1973) and molecular studies (O’Donnell 

et al., 1998; Gottlieb & Lichtwardt, 2001) all 

provide evidence linking Trichomycetes with 

the Zygomycota. It is possible that the class 

Trichomycetes is polyphyletic, and it is therefore 

preferable to refer to the gut fungi as a biological 

group, trichomycetes with a lower-case ‘t’ 

(Lichtwardt, 1986). 

Three orders have been distinguished, namely 

the Harpellales, Asellariales and Eccrinales, of 

which we shall consider only the first. The 

Amoebidiales, previously included, are now 

classified with the protozoa. 

7.7.1 Harpellales 

Harpella melusinae is one of the most common and 

abundant trichomycetes with a worldwide distribution 

in temperate regions. It is found in larval 

blackflies (Simulium spp.) which live attached to 

stones, twigs and aquatic vegetation submerged 

in rapidly flowing streams. The dissection of 

larval guts reveals the peritrophic membrane, to 

the inner wall of which unbranched cylindrical 

thalli are attached. Developing thalli receive 

nutrients from the material passing through 

the gut. The peritrophic membrane is continuously 

secreted by endothelial cells lining the 

upper part of the mid-gut, i.e. new membrane 

material is added at the upper end. Young thalli 

are present here and progressively older thalli 

further down. Attachment is by a simple holdfast 

(Fig. 7.47a). The holdfast consists of a chamber at 

the base of the thallus from which numerous 

finger-like projections protrude, cemented to but 

not penetrating the peritrophic membrane 

(Reichle & Lichtwardt, 1972). The cylindrical 

part of the thallus is divided by septa into 2 12 

or more uninucleate segments called generative 

cells. The septal ultrastructure consists of a 

flared pore associated with a plug, somewhat 

resembling the bordered pit of a conifer xylem 

tracheid. This feature is characteristic of trichomycetes 

(Moss, 1975). 


The entire contents of the thallus are converted 

to reproductive cells. Reproduction begins at the 

terminal generative cell and progresses basipetally 

(towards the holdfast) by production of 

trichospores (Figs. 7.47a c). Trichospores are 

really monosporous sporangia. They have been 

defined as ‘exogenous, deciduous sporangia 

containing a single uninucleate sporangiospore 

and normally having one to several basally 

attached filamentous appendages’ (Lichtwardt, 

1986). The trichospores, which are usually coiled 

but sometimes straight, develop at the upper end 

of a generative cell (Fig. 7.47a). The nucleus of the 

generative cell divides mitotically, one daughter 

nucleus remaining in the generative cell, the 

other entering the developing trichospore. In 

H. melusinae there are four basal appendages 

which, before trichospore release, are spirally 

coiled inside the upper part of the generative cell 

(Figs. 7.47b,c; Reichle & Lichtwardt, 1972). At the 

distal end of the trichospore within the cytoplasm 

is an elongated apical spore body 

(Fig. 7.47a). This contains holdfast material 

which is released after extrusion of the sporangiospore 

on its germination within the insect 

gut, cementing the holdfast to the gut wall (Moss 

& Lichtwardt, 1976; Horn, 1989a). Trichospores 

are separated from the generative cell by a 

septum and are released by breakdown of the 

wall beneath it. After release, the appendages 

uncoil and extend up to 10 times their original 

length. The released trichospores are passed out 

from the larval gut with faecal material and the


Fig 7.47 Harpella melusinae. (a) Thallus 

attached by a holdfast to the peritrophic 

membrane from the mid-gut of a larva of a 

blackfly, Simulium sp.The thallus is divided by 

septa into three generative cells, each of which 

is producing a curved trichospore at its upper 

end.The apical spore body at the upper end of 

the trichospore contains material extruded to 

cement the holdfast to the peritrophic 

membrane. (b) Detached trichospore bearing 

four filamentous appendages at its base. 

(c) Developing trichospore showing the coiled 

filamentous appendages wrapped around inside 

the wall of the generative cell. 

(d) Chlamydospore which has germinated to 

form two generative cells, each of which is 

developing a trichospore. (e) Zygospore 

development.Two adjacent thalli have 

conjugated and from one of the conjugating 

cells a zygosporophore has been produced, 

terminating in a biconical zygospore. Bars: (a,b) 

¼ 10 mm, (c,e) ¼ 5 mm, (d) ¼ 15 mm. (d) after 

Moss and Descals (1986); (e) after Lichtwardt 

(1967). 

appendages cause the trichospores to be 

entangled with faeces and other particulate 

material. Further development of trichospores, 

i.e. the extrusion of a sporangiospore from its 

sporangium and the formation of a holdfast, 

only occurs after ingestion and is stimulated by 

conditions in the larval gut. 

Smittium culisetae (Harpellales) inhabits the 

midgut and hindgut of larval mosquitoes and 

can be grown in culture. Horn (1989a,b, 1990) has 

investigated in vitro the conditions which trigger 

sporangiospore extrusion in this and related 

species of Smittium. The trigger for extrusion in 

S. culisetae is a two-stage process. Phase 1, which 

simulates mid-gut conditions, involves exposure 

to 20 mM KCl at pH 10 followed by phase 2, in 

which the pH is reduced to 7, simulating hindgut 

conditions. Following this sequence of treatments 

sporangiospores (¼ trichospores sensu 

stricto) are rapidly extruded, a process in which 

they increase in size by the uptake of water 

and by vacuolation, generating turgor pressure 

which aids extrusion. Spore germination quickly 

follows with the secretion of holdfast material 

from the apical spore body through canals in the 

distal wall of the sporangiospore (Horn, 1989a). 

A second asexual, free-living stage in the 

life cycle of H. melusinae is the chlamydospore 

(sometimes termed ovarian cyst or cystospore), 

masses of which are deposited by adult female

TRICHOMYCETES 

225 

Simulium in the place of eggs (Moss & Descals, 

1986; Lichtwardt, 1996). A similar stage has 

been reported from Simulium infected with 

Genistellospora homothallica (Labeyrie et al., 1996). 

Ovarian tissue is invaded by the fungus, growing 

in a parasitic mode. Cysts of H. melusinae dissected 

from ovaries are surrounded by a membranous 

sheath. They are ellipsoidal and, on germination, 

form two germ tubes, one at each pole, ending as 

a spherical knob, the generative cell initial. A 

single generative cell develops from each initial 

and forms a terminal trichospore (Fig. 7.47d). The 

chlamydospores are deposited among egg masses 

and infection of young larvae results from 

ingestion of trichospores produced by them. The 

ovarian chlamydospores therefore represent 

a ‘missing link’ in the life cycle of Harpellales. 

Adult blackflies do not contain trichomycete 

thalli because at the final ecdysis (moult) 

before pupation, the cuticular lining of the 

larval gut is shed. 


This occurs by the production of zygospores and 

has so far been reported only in Harpellales. In 

H. melusinae zygospores are rarely detected, 

possibly because they are associated with the 

last stage of development of the Simulium larval 

host before pupation and are shed at ecdysis. 

Zygospore formation is preceded by conjugation 

between swollen cells on adjacent thalli (see 

Fig. 7.47e; Lichtwardt, 1967). From one of the 

conjugating cells a zygosporophore grows out, 

and from this a biconical zygospore develops. 

The biconical shape, which is characteristic of 

the Harpellales, is possibly adapted to passage 

through the insect gut. In some members of the 

group zygospores bear polar filamentous appendages, 

but these are absent in Harpella (Moss & 

Lichtwardt, 1977). The cytological details of 

zygospore formation have not been fully worked 

out but in H. melusinae the zygospore, zygosporophore 

and the two conjugant cells each contain 

a single nucleus. Moss and Lichtwardt (1977) have 

speculated that the four nuclei might have been 

derived from meiotic division of a diploid zygote 

nucleus within the fused conjugants. On this 

hypothesis the conjugant cells would be interpreted 

as gametangia, a situation markedly 

different from that found in other zygomycetes. 

Relationships 

On the basis of similarities in serological reactions, 

septal pore structure and in sporangial 

morphology, it has been suggested that the 

Harpellales are related to the Kickxellales, an 

order of mostly dung- and soil-inhabiting saprotrophic 

zygomycetes (Moss & Young, 1978). 

However, the evidence for a phylogenetic relationship 

between these two groups is conflicting. 

K.L. O’Donnell et al. (1998) and Gottlieb and 

Lichtwardt (2001) have attempted to correlate 

morphological criteria with molecular data (18S 

rDNA) but found only poor support, whereas 

Tanabe et al. (2004), comparing a range of DNA 

sequences, found a strong link between 

Harpellales and Kickxellales (see Fig. 7.1).

8 

Ascomycota (ascomycetes) 


The phylum Ascomycota (colloquially called 

ascomycetes) is by far the largest group of 

fungi, estimated to include more than 32 000 

described species in 3400 genera (Kirk et al., 

2001). It is assumed that the majority of 

ascomycetes has yet to be discovered, and the 

total number of species may well be higher by 

a factor of 10 20 or even more (see Hawksworth, 

2001). The name is derived from the Greek words 

askos (a leather bottle, bag or bladder) and mykes 

(a fungus), so ascomycetes are sac fungi. The 

characteristic feature of the group is that the 

sexually produced spores, the ascospores 

(see p. 25), are contained within a sac, the 

ascus. In most ascomycetes the ascus contains 

eight ascospores and is turgid, ejecting its spores 

by a squirt mechanism. 

There is a very wide range of lifestyles. 

Some ascomycetes are saprotrophs, others 

necrotrophic or biotrophic parasites of plants 

and animals, including humans. Examples of 

biotrophic parasites are the Erysiphales, the 

cause of many powdery mildew diseases of 

plants (Chapter 13), the Taphrinales (p. 251) 

causing a range of plant diseases associated 

with growth abnormalities, and the 

Laboulbeniales, relatively harmless ectoparasites 

of beetles and some other insects (Blackwell, 

1994; Weir & Blackwell, 2001). Many ascomycetes 

grow as endophytes in symptomless associations 

with plants. Some are mutualistic symbionts, for 

example the lichens (Chapter 16) which make up 

about 40% of the described species of ascomycetes. 

Lichens are dual organisms consisting of 

a fungus (usually an ascomycete) and a photosynthetic 

alga or cyanobacterium living in close 

association. This type of association has evolved 

independently in several unrelated groups of 

ascomycetes and indeed it has been claimed that 

several major fungal lineages are derived from 

lichen-symbiotic ancestors (Lutzoni et al., 2001), 

although this hypothesis is under dispute (Liu & 

Hall, 2004; see Fig. 8.17). Symbiotic mycorrhizal 

relationships also exist between true truffles 

(e.g. Tuber spp.) or false truffles (e.g. Elaphomyces 

spp.) and trees such as oak and beech (see pp. 423 

and 313). The range of habitats is wide, as would 

be expected of such a large and diverse group of 

fungi. Ascomycetes grow in soil, are common on 

the above-ground parts of plants, and are also 

found in freshwater and in the sea. 

Most ascomycetes are recognized by their 

fruit bodies or ascocarps, i.e. the structures 

which surround the asci. These will be described 

more fully later (see Fig. 8.16). 

8.2 Vegetative structures 

Ascomycetes may grow either as yeasts, i.e. 

unicells multiplying by budding or fission, 

or as mycelia consisting of septate hyphae 

(Fig. 8.1a). Some fungi may switch from the 

yeast to the filamentous state or vice versa, 

i.e. they are dimorphic. A good example of a 

dimorphic fungus is Candida (see Fig. 8.1b).

VEGETATIVE STRUCTURES 

227 

Fig 8.1 (a) Hypha of Hormonema dematioides.The positions of 

the first septa are indicated by arrows. (b) Candida parapsilosis. 

Pseudohypha budding off cells which continue to bud in a 

yeast-like manner. 

Candida albicans is the cause of diseases such as 

thrush in mammals, including man. 

The mycelial septa of ascomycetes are usually 

incomplete, developing as transverse centripetal 

flange-like ingrowths from the cylindrical wall of 

a hypha, which fail to meet at the centre so that 

in most ascomycete septa there is one central 

pore permitting cytoplasmic continuity and 

streaming between adjacent segments of mycelium 

(Buller, 1933; Gull, 1978). This means that 

organelles such as mitochondria and nuclei 

are free to travel from cell to cell; the large 

nuclei are constricted as they pass through the 

pore (Fig. 8.2). Individual cells may be uni- or 

multinucleate and the cytoplasmic continuity 

between the cells means that the mycelium 

of an ascomycete is effectively coenocytic. 

Proteinaceous organelles termed Woronin 

bodies (Buller, 1933) may be closely grouped 

near the central pore (Fig. 8.3). Woronin bodies 

are globose structures or ‘hexagonal’ (polyhedral) 

crystals made up essentially of one protein 

(Tenney et al., 2000), and surrounded by a unit 

membrane. They measure 150 500 nm in width 

and are sufficiently large to block the septal 

pore. They rapidly do so near regions where 

a hypha is physically damaged. Usually one 

Woronin body blocks one pore. The blockage in 

the septal pore is consolidated by deposition of 

further material (for references see Markham & 

Collinge, 1987; Markham, 1994; Momany et al., 

2002). Woronin bodies are formed near the 

hyphal apex and are transported to more distal 

regions of the hypha as septa develop. Woronin 

bodies have been recorded from ascomycetes and 

their related conidial fungi, but there are no 

reliable reports from other fungal phyla. 

The mycelium of many ascomycetes is 

homokaryotic (Gr. homoios ¼ like, resembling; 

karyon ¼ a nut, meaning nucleus), i.e. all nuclei 

in a given mycelium are genetically identical. 

Heterokaryotic mycelia also occur and generally 

arise through anastomosis, i.e. the cytoplasmic 

fusion of vegetative hyphae. Following anastomosis 

between homokaryons of differing genotypes, 

nuclei, other organelles and plasmids may 

be transferred between one mycelium and 

another so that a given mycelium or even a 

single cell may contain nuclei of different kinds. 

However, the ability to form heterokaryons is 

under genetic control and a degree of genetic 

similarity between homokaryons is necessary 

for it to occur. Failure to establish a heterokaryon 

is a phenomenon known as heterokaryon 

incompatibility or vegetative incompatibility 

(Caten & Jinks, 1966; see pp. 320 and 594).

228 ASCOMYCOTA (ASCOMYCETES) 

Fig 8.2 Nucleus of Botrytiscinerea passing through a septal 

pore. (a) View of the entire hyphal diameter. (b) Close up.Note 

the constricted appearance of the nucleus. 

Fig 8.3 Transmission electron micrograph of a transverse 

septum in the hypha of Emericella nidulans showing 

five Woronin bodies near the central septal pore. 

Scale bar ¼ 0.25 mm. Reprinted from Momany et al. (2002), 

Mycologia,withpermission.ßThe Mycological Society of 

America. 

Some ascospores, e.g. those of Neurospora tetrasperma, 

are heterokaryotic, and multinucleate 

conidia can also be heterokaryotic. Following 

mycelial anastomosis between homokaryons, 

nuclear division succeeded by migration may 

result in the rapid spread of an introduced 

nucleus into a mycelium, thus transforming a 

homokaryon into a heterokaryon. An ascomycete 

mycelium may thus consist of a mosaic of cells, 

some of which are homokaryotic and others 

heterokaryotic. Because the different types of 

nuclei do not always divide at the same rate, 

the ratio of nuclear types in a heterokaryotic 

mycelium may change with time and respond to 

changes in external conditions such as nutrient 

availability. This gives the mycelium a degree of 

genetic flexibility which sometimes manifests 

itself as the formation of sectors in a mycelium 

in agar culture (Fig. 8.4). Another important 

source of genetic variability which may arise 

within a heterokaryon is the parasexual cycle, a 

process in which genetic recombination is 

brought about in the absence of meiosis. This is 

discussed more fully below. 

8.3 Life cycles of ascomycetes 

8.3.1 Sexual life cycles 

Sexual life cycles in the strict sense, i.e. involving 

nuclear fusion and meiosis, occur only in those 

ascomycetes which possess asci, because it is 

within the young ascus that these events occur.

LIFE CYCLES OF ASCOMYCETES 

229 

Fig 8.4 Sectoring of a mycelial colony of Pseudeurotium sp. 

The slow-growing wild-type mycelium appears dark due to the 

formation of melanized cleistothecia.Two non-fruiting sectors 

have formed which show faster vegetative growth but no 

sporulation on the rich agar medium. 

Ascospores of most ascomycetes contain one or 

more haploid nuclei, and therefore most (but by 

no means all) ascomycetes have a haploid 

vegetative mycelium. The mycelium is often 

capable of asexual reproduction, e.g. by fragmentation, 

budding or by the formation of conidia, 

chlamydospores, sclerotia, etc. The structure and 

formation of conidia is described below. Some 

yeasts, e.g. Saccharomyces cerevisiae, show an alternation 

of diploid and haploid yeast-like states 

and here the diploid state is the commonly 

encountered form (p. 265), in contrast to 

Schizosaccharomyces in which the vegetative cells 

are haploid (p. 253). 

The mating behaviour of ascomycetes may 

be homothallic or heterothallic. In homothallic 

ascomycetes the mycelium derived from a single 

ascospore is capable of reproducing sexually, 

i.e. by developing asci. Examples are Emericella 

nidulans, Pyronema domesticum and Sordaria fimicola. 

However, the homothallic condition does 

not preclude outcrossing as is shown by the 

formation of hybrid asci containing black 

(wild type) and white (mutant) ascospores in 

crosses between different strains of Sordaria 

fimicola (see Fig. 12.2). In heterothallic ascomycetes 

the ascus usually contains four ascospores 

of one mating type and four of the other. 

The two mating types differ at a single allele 

and the mating types may be designated A and a, 

a and a, or (þ) and ( ). Sexual reproduction 

occurs following plasmogamy between cells of 

the two mating types. Plasmogamy is of three 

main types: 

1. Gametangio-gametangiogamy. Fusion occurs 

between differentiated gametangia. An example 

is Pyronema domesticum where fusion 

is between the trichogyne, a filamentous 

extension of the large, swollen ‘female’ 

gametangium (the ascogonium) and a 

less swollen ‘male’ gametangium, the antheridium, 

which donates nuclei to the trichogyne 

and thereby to the ascogonium (see 

p. 416). 

2. Gameto-gametangiogamy. Fusion takes place 

between a small unicellular male gamete 

(spermatium) and a differentiated female 

gametangium (ascogonium). The spermatium 

is rarely capable of independent germination 

and growth and may only germinate to 

produce a short conjugation tube which 

fuses with the wall of the ascogonium. An 

example is Neurospora crassa in which the 

spermatium fuses with a trichogyne (see 

Fig. 12.7). 

3. Somatogamy. Fusion takes place between 

undifferentiated hyphae, i.e. there are no 

recognizable sexual organs. This type of 

sexual behaviour is shown by Coprobia granulata, 

whose orange ascocarps are common on 

cattle dung. 

8.3.2 Asexual life cycles 

Most fungi which were formerly classified in the 

artificial group Deuteromycotina or Fungi 

Imperfecti are conidial forms (anamorphs) of 

Ascomycota, although a few have affinities with 

Basidiomycota. Evidence for a relationship to 

Ascomycota comes from morphological similarity 

and from DNA sequence comparisons. 

Morphological similarities include the structure 

of the mycelium, the layering of the hyphal


wall as seen by electron microscopy, the finestructure 

of nuclear division, and also close 

resemblances of conidial structure and development. 

Some genera contain species which reproduce 

by asexual means only, whilst closely 

similar forms have sexual as well as asexual 

reproduction. Examples include Aspergillus and 

Penicillium, which are anamorphs of several 

genera of Ascomycota (Trichocomaceae; see 

pp. 308 313) and Fusarium which is the 

anamorph of Gibberella and Nectria (members of 

the Hypocreales; see p. 343). It is presumed that 

fungi which reproduce only by conidia have lost 

the capacity to form ascocarps in the course of 

evolution. 

8.3.3 Parasexual reproduction 

This is a process in which genetic recombination 

can occur through nuclear fusion and crossingover 

of chromosomes during mitosis. Meiosis 

does not occur, and instead haploidization takes 

place by the successive loss of chromosomes 

during mitotic divisions. It is believed that the 

necessary cytological steps take place in a regular 

sequence which Pontecorvo (1956) has termed 

the parasexual cycle. The essential steps include 

(i) nuclear fusion between genetically distinct 

haploid nuclei in a heterokaryon to form 

diploid nuclei; (ii) multiplication of the diploid 

nuclei along with the original haploid nuclei; 

(iii) the development of a diploid homokaryon; 

(iv) genetic recombination by crossing-over 

during mitosis in some of the diploid nuclei; 

and (v) haploidization of some of the diploid 

nuclei by progressive loss of chromosomes 

(aneuploidy) during mitosis. 

This process was discovered in Emericella 

(Aspergillus) nidulans, which can reproduce sexually 

by forming asci and asexually by forming 

conidia (see Fig. 11.17). By changing the nutrient 

content of the medium on which the fungus is 

grown, the development of asci and therefore of 

normal sexual reproduction can be prevented. 

Genetic mapping based on gene recombination 

following conventional sexual reproduction 

has been compared with mapping based on 

parasexual recombination and has yielded identical 

results. 

Parasexual recombination is known to occur 

not only in Ascomycota but also in Oomycota 

and Basidiomycota. It makes possible genetic 

recombination in organisms not known to reproduce 

by sexual means and helps us to understand 

why purely asexual fungi such as many 

species of Aspergillus and Penicillium have achieved 

success and have continued to flourish in the 

course of evolution. However, because parasexual 

reproduction is comparatively rare in nature, 

it is probably only a partial substitute for sexual 

reproduction, so that purely asexual species are 

more prone to accumulating deleterious mutations 

(Geiser et al., 1996). 

8.4 Conidia of ascomycetes 

The asexual spores or conidia of ascomycetes 

are remarkably diverse in form, structure and 

modes of dispersal, but their development or 

conidiogenesis occurs in a limited number of 

ways (see below). The cell from which a conidium 

develops is the conidiogenous cell and usually 

one or more such cells are borne on a stalk, the 

conidiophore. Conidiophores which are narrow 

and not differentiated from the vegetative mycelium 

are said to be micronematous (Gr. nema ¼ a 

thread) whilst those that are clearly differentiated 

are macronematous. Conidiophores 

frequently arise singly as in Eurotium repens 

(Fig. 11.16), Emericella nidulans (Fig. 11.17) and in 

many species of Penicillium (Fig. 11.18). 

However, in certain fungi the conidiophores 

may aggregate to form a conidioma. Descriptive 

terms have been given to different types 

of conidioma. Conidiophores aggregated into 

parallel bundles (fascicles) are termed coremia 

(Gr. korema ¼ a brush) or synnemata (Gr. prefix 

syn ¼ together). Examples are Penicillium 

claviforme (Fig. 11.19) and Cephalotrichum 

(Doratomyces) stemonitis (Fig. 12.39). Seifert (1985) 

has distinguished several types of synnema, some 

of which are simple, some compound, some 

made up of parallel conidiophores, and others

CONIDIUM PRODUCTION IN ASCOMYCETES 

231 

where the hyphae making up the synnema are 

intricately interwoven (see Kirk et al., 2001). 

In many ascomycetes the conidiophores develop 

on or in a stroma (Gr. stroma ¼ bed, cushion), 

an aggregation of pseudoparenchymatous cells. 

A good example of a conidial stroma is seen in 

the wood-rotting candle-snuff fungus, Xylaria 

hypoxylon (see Fig. 12.11a). Here, powdery white 

conidia develop at the tips of the branches of 

the conidial stroma and, later, asci develop in 

flask-shaped perithecia at the base of the old 

stroma. The term sporodochium (Gr. spora ¼ a 

seed; doche ¼ a receptacle) is used for the 

cushion-like conidiomata bearing a layer of 

short conidiophores. An example is the conidial 

(Tubercularia) state of Nectria cinnabarina (see 

Fig. 12.20c). 

Another type of conidioma is the acervulus 

(Lat. acervulus ¼ a little heap), a saucer-shaped 

fructification which may develop inside the 

tissues of a host plant or may be superficial. 

Subepidermal acervuli develop from a pseudoparenchymatous 

stroma, and as the acervulus 

matures the overlying epidermis of the host 

becomes ruptured to expose conidia formed 

from conidiogenous cells lining the base of the 

saucer. The conidia are held together in slime 

and are chiefly dispersed by rain splash. A good 

example of an acervular fungus is Colletotrichum 

(see Fig. 12.51). The teleomorphs of Colletotrichum, 

where known, are species of Glomerella, many of 

which are serious plant pathogens. In many 

ascomycetes and their allies, the conidia are 

borne inside flask-shaped conidiomata termed 

pycnidia (Gr. diminutive of pyknos ¼ dense, 

packed, concentrated). Traditionally, fungi with 

pycnidial and acervular states have been grouped 

together in the artificial taxon coelomycetes 

(Sutton, 1980), in contrast to hyphomycetes in 

which the conidiogenous cells are exposed on 

single conidiophores or in synnemata, coremia 

or sporodochia (see above). Pycnidia may be 

superficial or embedded in host tissue. The opening 

of the pycnidium is generally by means of 

a circular ostiole. Conidia formed from conidiogenous 

cells lining the inner wall of the 

pycnidium are held together in slimy masses 

which ooze out through the ostiole, sometimes 

as spore tendrils. They are generally dispersed 

by splash or in water films. In some cases the 

pycnidia, instead of producing conidia with an 

asexual function, produce spermatia which are 

involved in fertilization. Examples of fungi with 

pycnidial anamorphs are Leptosphaeria acuta with 

a Phoma anamorph (Fig. 17.3), and Phaeosphaeria 

nodorum (anamorph Stagonospora nodorum; see 

Fig. 17.4). 

8.5 Conidium production 

in ascomycetes 

There are several steps in the production and 

release of conidia, namely (1) conidiogenesis, 

i.e. conidial initiation; (2) maturation; (3) delimitation; 

(4) secession, i.e. separation from 

the conidiogenous cell; (5) proliferation of the 

conidiogenous cell or conidiophore to form 

further conidia. Many of the current ideas on 

conidiogenesis stem from a seminal paper by 

Hughes (1953) based on light microscopy 

studies of conidial development in a range of 

hyphomycetes. Hughes classified the development 

of conidia in a limited number of ways. 

His ideas were extended by other workers, and 

advances were also made possible by the use 

of electron microscopy and time-lapse cinephotomicrography 

(Cole & Samson, 1979). 

An excellent review of these aspects of 

conidiogenesis has been written by Cole (1986). 

The descriptions which follow are based on the 

account by de Hoog et al. (2000a). Conidiogenesis 

occurs in two ways which appear to be distinct 

at first glance: blastic and thallic (see Fig. 8.5). 

In reality, when surveying conidium formation 

and release in a range of fungi, there is a 

continuum of development of which these two 

concepts represent extremes (Minter et al., 1982, 

1983a,b; Minter, 1984). 

8.5.1 Blastic conidiogenesis 

The conidium develops by the blowing-out of 

the wall of a cell, usually from the tip of a hypha, 

sometimes laterally as in Aureobasidium (conidial


Fig 8.5 Two basic modes of development during 

conidiogenesis of a hyphal apex (a): blastic (b) and thallic (c). 

From de Hoog et al. (2000a), with kind permission of 

Centraalbureau voor Schimmelcultures. 

state of Discosphaerina; see Fig. 17.25). In certain 

yeasts including Saccharomyces, the blastic development 

of new daughter cells is known as 

budding (see Fig. 10.3). Two kinds of blastic 

development have been distinguished: 

1. Holoblastic. All the wall layers of the 

conidiogenous cell contribute to the wall of 

the newly formed conidium (see Fig. 8.6b). 

Aureobasidium pullulans (Fig. 17.25) and Tricladium 

splendens (conidial Hymenoscyphus; see Fig. 25.12) 

are examples. In some genera with dark (i.e. 

melanized), relatively thick-walled conidiophores 

such as Stemphylium and Alternaria (anamorphs 

of Pleospora), the conidia develop holoblastically, 

but a narrow channel persists in the wall of 

the conidiogenous cell through which cytoplasm 

had passed as the spore expanded. This type of 

development has been described as porogenous 

(Luttrell, 1963) or tretic (Ellis, 1971a) and the 

conidia are sometimes termed porospores or 

poroconidia (see Figs. 17.10 17.13; Carroll & 

Carroll, 1971; Ellis, 1971b). 

2. Enteroblastic. The wall of the conidiogenous 

cell is rigid and breaks open. The initial of 

the conidium is pushed through the opening 

and is surrounded by a newly formed wall 

(Fig. 8.6c). Two types of enteroblastic development 

have been distinguished, phialidic and 

annellidic (see Fig. 8.7). In phialidic development 

a basipetal succession of conidia (phialospores, 

phialoconidia) develops from a specialized conidiogenous 

cell, the phialide (Gr. diminutive of 

phialis ¼ flask), usually shaped like a bottle 

with a narrow neck. Phialides are formed singly 

Fig 8.6 Two alternative types of conidiogenesis starting from 

an undifferentiated hyphal apex (a). In holoblastic 

conidiogenesis (b), the entire wallbecomes inflated to form the 

conidium initial. In enteroblastic conidiogenesis (c), the 

conidium initial develops through a hole in the rigid outer wall. 

From de Hoog et al. (2000a), with kind permission of 


or in clusters at the tip of a conidiophore or, 

more rarely, laterally. There may be one or 

several nuclei in a phialide. As shown in Fig. 8.8 

for Thielaviopsis basicola, the initial of the firstformed 

phialoconidium is surrounded by the 

apical wall of the phialide and is, in reality, 

holoblastic. The phialide wall breaks transversely 

near its tip and the first conidium, surrounded 

by a newly formed wall and capped by the wall 

from the broken tip of the phialide, is pushed 

out (Hawes & Beckett, 1977; Ingold, 1981). The 

new wall material which encases the phialoconidium 

is secreted in the form of a cylinder from 

the surface of the cytoplasm deep within the 

phialide, a process known as ring wall building 

(Minter et al., 1983a). Before the conidium is 

extruded, a septum develops within the phialide 

below its neck, at the base of the conidium. 

The upper part of the wall of the now open-ended 

phialide persists as a small collar, the collarette. 

The nucleus or nuclei within the phialide 

continue to divide mitotically. A second conidium 

develops below the first, and is surrounded 

by newly secreted wall material. This conidium is 

also cut off by a septum and pushed out. Part of 

the newly secreted wall material may persist 

around the inside of the neck of the phialide as 

periclinal thickening. The process is repeated 

so that many phialoconidia may develop from 

a single phialide. In phialides which have 

developed several conidia, the periclinal


233 

Fig 8.7 Enteroblastic phialidic (left) and enteroblastic (right) annellidic conidiogenesis. From de Hoog et al.(2000a),withkind 

permission of Centraalbureau voor Schimmelcultures. 

Phialidic conidiogenesis 

Annellidic conidiogenesis 

a. Apex of conidiophore expands to form a phialide a. Apex of conidiophore differentiates to form a conidiogenous 

with a blown-out holoblastic conidium initial (o). 

cell (annellide) and the initial of a holoblastic first conidium (1). 

b. The first-formed conidium (1), surrounded by a new wall b. The first conidium is cut off by a septum. 

secreted inside the phialide, is pushed out and breaks 

the outer wall of the phialide whose tip persists as a cap. 

c. The first conidium is cut off by a septum. c. A second conidium (2) develops beneath the first. 

d. A second conidium develops below the first, also d. The septum cutting off the second conidium is formed beyond 

surrounded by new wall secreted inside the phialide. the point at which the original annellide wall was ruptured 

and persists as an annellation. 

e. A third conidium develops in basipetal succession 

adding to the length of the conidial chain.The lower 

part of the broken original wall of the phialide has 

persisted as a collarette, the extent of which is shown 

by vertical dashed lines. Successive layers of wall 

material may accrete in the neck of the phialide to 

form a periclinal thickening. 

e. The development of further conidia results in the addition 

of more annellations so that an annellated zone, marked by 

vertical dashed lines, increases in length. 

thickening may be seen even with the light 

microscope, but in others it is less obvious. 

During maturation of the phialoconidium, 

the spore may increase in size, its wall may 

become thickened and ornamented by spines 

and may become pigmented by melanin and 

other materials. In some genera of ascomycetes 

and their conidial derivatives, the phialospores 

are dry and appear in chains. Dry-spored conidial 

chains are often persistent and are typical of 

Aspergillus and Penicillium (see Figs. 11.16 11.18). 

The hydrophobic nature of the spore wall is due 

to incorporation of hydrophobin rodlets. The 

adherence of the conidia in chains depends on 

the strength of the septum between adjacent 

spores. Secession of the conidia into separate 

spores occurs by breakage of the septum. Where 

the spore wall is wet, the succession of conidia 

may briefly persist in the form of a short chain 

(false chain) or may collapse into slimy balls at 

the tips of the phialides (no-chain phialides). 

An example of the latter is Trichoderma (conidial


Fig 8.8 Conidiogenesis inThielaviopsis basicola. 

(a) Phialides and phialoconidia.To the left is a 

branched conidiophore with a short phialide 

which has not yet formed conidia and a longer 

phialide in which the tip has broken 

transversely and the first phialoconidium is 

being extruded.This spore is capped by the 

remnants of the phialide tip. Developing 

phialoconidia can be seen in the necks of the 

phialides. (b) Three end spores from a spore 

chain.The capped terminal spore is more 

bulbous than the cylindrical spores which 

succeedit. (c) A branched conidiophore bearing 

two phialides with chains of hyaline thin-walled 

phialoconidia and a dark, thick-walled 

transversely septate chlamydospore.These 

two distinct conidial states are synanamorphs. 

Scale bar: (a) ¼ 10 mm, (b) ¼ 20 mm. 

Hypocrea; see Fig. 12.16). Phialoconidia are, in 

general, unicellular but multicellular conidia 

are found in certain genera such as in the transversely 

septate conidium of Sporoschisma (conidial 

Melanochaeta; for references see Sivichai et al., 

2000). 

Annellidic conidiogenesis (Fig. 8.7) in many 

ways resembles phialidic, and indeed the term 

annellidic phialide is sometimes used for this 

type of conidiogenous cell. These are also termed 

annellides (Lat. annulus ¼ little ring) or annellophores, 

and the spores which develop from them 

are annelloconidia. As in phialidic development, 

the first-formed annelloconidium is holoblastic. 

The difference between the two modes of 

development is that new wall material which is 

secreted within the annellide protrudes beyond 

its neck and the septum which cuts off the newly 

formed conidium also forms beyond the neck. 

As each new conidium develops in basipetal 

fashion, a small ring of wall material (annellation) 

is left at the neck of the annellide, which 

thus grows in length as successive conidia 

develop. This accumulation of short collars of 

wall material is the annellated zone (see Fig. 8.7). 

With normal light microscopy annellation may 

be difficult to see, but detection is improved by 

interference contrast or phase contrast optics. 

Examples of fungi reproducing by annelloconidia 

are Scopulariopsis brevicaulis (see Fig. 12.38; 

Cole & Kendrick, 1969a) and Cephalotrichum 

(Doratomyces) stemonitis (Fig. 12.39). Both genera 

contain species which are conidial forms of 

Microascus.


235 

Secession of conidia, irrespective of their 

mode of development, is in most cases by 

dissolution of the septum or septa which 

separate them from the conidiogenous cell or 

from adjacent spores. This process is termed 

schizolytic secession (Gr. schizo ¼ to split, divide; 

lyticos ¼ able to loosen). In some other cases 

secession is brought about by the collapse of a 

special separating cell beneath the terminal 

conidium. This is termed rhexolytic secession 

(Gr. rhexis ¼ a rupture, breaking). 

8.5.2 Thallic conidiogenesis 

Thallic conidiogenesis (Gr. thallos ¼ a branch) 

occurs by conversion of a pre-existing hyphal 

element in which terminal or intercalary cells of 

a hypha become cut off by septa (see Fig. 8.9). Two 

kinds of thallic development have been distinguished: 

holothallic (Gr. holos ¼ whole, entire) 

and thallic-arthric (Gr. arthron ¼ a joint). 

In holothallic development a hyphal element, 

e.g. a terminal segment of a hypha, is converted 

as a whole into a single conidium (see Fig. 8.9). 

Secession of such conidia may be schizolytic 

or rhexolytic. Microsporum spp. (anamorphic 

Arthroderma), which are skin pathogens (dermatophytes) 

of mammals, provide examples of this 

holothallic development (see Fig. 11.6). During 

thallic-arthric conidiogenesis, septa develop in 

a hypha and divide it up into segments which 

separate into individual cells by dissolution of 

the septa (see Fig. 8.9). Geotrichum candidum 

(anamorphic Galactomyces), a common soil 

fungus and frequent contaminant of milk and 

milk products, develops conidia in this way 

(see Fig. 10.10; Cole, 1975). 

The proliferation of the conidiogenous cell 

or the conidiophore may occur in various ways, 

for example by the formation of a new growing 

point in the region of the conidiophore beneath 

the point at which the first conidium was 

formed. The new apex extends beyond the 

point of origin of the first conidium and develops 

a new conidiogenous cell. These methods of 

conidiophore regeneration are discussed more 

fully in relation to some of the different genera. 

Fig 8.9 Holothallic and thallic arthric conidiogenesis.From de Hoog et al. (2000a), with kind permission of Centraalbureau voor 

Schimmelcultures. 

Holothallic conidiogenesis with rhexolytic secession Thallic arthric conidiogenesis with schizolytic secession 

a. The terminal portion of a hypha is cut off by a septum. a. A terminal segment of a hypha. 

b. A second septum laid down near the first cuts off a b. Septa develop, dividing the segment into several cells. 

subterminal segment, the separating cell. 

c. The terminal cell enlarges to form the conidium. c. The septa divide, each separating into two layers. 

d. Collapse of the separating cell causes conidium secession. d. The daughter cells separate.


8.6 Development of asci 

The morphogenesis of asci and ascospores has 

been reviewed by Read and Beckett (1996). In 

yeasts and related fungi, the ascus arises directly 

from a single cell, but in most other ascomycetes 

it develops from a specialized hypha, the ascogenous 

hypha, which in turn develops from an 

ascogonium (Fig. 8.10a). The ascogenous hypha of 

many ascomycetes is multinucleate, and its tip 

is recurved to form a crozier (shepherd’s crook). 

Within the ascogenous hypha, nuclear division 

occurs simultaneously. Two septa at the tip of 

the crozier cut off a terminal uninucleate cell 

and a penultimate binucleate cell (Fig. 8.10c) 

destined to become an ascus. The ante-penultimate 

cell beneath the penultimate cell is termed 

the stalk cell. The terminal cell of the crozier 

curves round and fuses with the stalk cell, and 

this region of the ascogenous hypha may grow 

on to form a new crozier in which the same 

sequence of events is repeated. Repeated proliferation 

of the tip of the crozier can result in 

a tight cluster of asci in many ascomycetes or 

a succession of well-separated asci as in Daldinia 

concentrica (see Fig. 12.10c). Specialized septal 

plugs, more elaborate than normal Woronin 

bodies, block the pores in the septa at the base 

of the ascus (Kimbrough, 1994). The septal pore 

plugs probably aid in retaining the high turgor 

pressure which develops in asci shortly before 

ascospore discharge. 

In the ascus initial the two nuclei fuse and 

the diploid fusion nucleus undergoes meiosis to 

form four haploid daughter nuclei (Figs. 8.10d,e). 

Fig 8.10 Diagrammatic representation of cytological features during ascus development. (a) Ascogenous hypha with a crozier at its 

tip developing from an ascogonium. (b) Conjugate nuclear division of the two nuclei in the crozier. (c) Two septa have cut off a 

binucleate penultimate cell.The two nuclei fuse to form a diploid nucleus.The uninucleate terminal segment of the ascogenous hypha 

has recurved and fused with the ascogenous hypha to form the stalk cell. (d) The penultimate cell enlarges to become an ascus initial 

within which the fusion nucleus begins to divide meiotically. A new crozier is developing from the stalk cell. (e) Second division of 

meiosis has occurred in the developing ascus.The behaviour of the new crozier repeats that of the first. (f) Mitotic division of the 

four haploid nuclei resulting from meiosis in the first ascus. (g) Ascospores formed.

DEVELOPMENT OF ASCI 

237 

These nuclei then undergo a mitotic division 

so that eight haploid nuclei result (Fig. 8.10f). 

The eight nuclei may divide further mitotically 

so that each ascospore is binucleate, or, 

if still more mitoses follow, the ascospore 

becomes multinucleate. For example, a single 

mitosis occurs in the immature ascospores of 

Neurospora crassa, and the spores remain binucleate 

for 2 3 days after they have been delimited. 

Later, a series of four or more synchronous 

mitoses occur after the spores have become 

pigmented so that they contain 32 or more 

nuclei when they are mature (Raju, 1992a). 

Where the ascospores are multicellular, there 

are repeated nuclear divisions accompanied by 

the formation of septa which divide up the spore. 

In some ascomycetes more than eight ascospores 

are formed, usually in numbers which are a 

multiple of eight, e.g. in the coprophilous genera 

Podospora and Thelebolus. In others the eight 

multicellular ascospores break up into partspores, 

e.g. in Hypocrea (Fig. 12.15c) and 

Cordyceps spp. (Fig. 12.33b). In Taphrina ascospores 

may bud mitotically within the ascus so that 

the mature ascus contains numerous yeast cells 

(Fig. 9.2c). Asci with fewer than eight spores 

are also known, e.g. in Neurospora tetrasperma 

where the four ascospores are binucleate, in 

Phyllactinia guttata where there are two ascospores 

(Fig. 13.14e), or in Monosporascus cannonballus 

which has a single ascospore. 

8.6.1 Cleavage of ascospores 

In many ascomycetes, studies of the fine structure 

of asci during cleavage of the ascospores 

have shown that a system of double membranes 

continuous with the endoplasmic reticulum 

extends from the envelope of the diploid fusion 

nucleus (Fig. 8.11). The double membrane develops 

to form a cylindrical envelope lining the 

young ascus. This peripheral membrane cylinder 

or lining layer is termed the ascus vesicle or 

ascospore-delimiting membrane. The ascospores 

are cut out from the cytoplasm within the 

ascus by infolding and fusion of the inner 

edges of the double membrane around a portion 

of cytoplasm and a nucleus (Fig. 8.11d). In some 

ascomycetes, e.g. Taphrina, a peripheral 

membrane cylinder has not been observed and 

the nuclei within the ascus become enveloped by 

ascospore-delimiting membranes formed by 

direct invagination of discrete parts of the 

ascus plasma membrane. 

Between the two layers of the ascosporedelimiting 

membrane enclosing the ascospores, 

the primary spore wall is secreted. The inner 

membrane forms the plasma membrane of the 

ascospore and the outer membrane becomes 

the spore-investing membrane. Secondary wall 

material is secreted within the primary wall. 

There may be several such layers. In Sordaria 

humana a total of four spore wall layers have 

been distinguished, a primary wall layer and 

three secondary layers (Read & Beckett, 1996). 

The secondary wall layers are often quite thick, 

and in dark-walled ascospores the pigment is 

usually laid down within the secondary wall 

layers. The spore wall may be smooth or 

extended to form a variety of ornamentations 

such as spines, ridges or reticulations. The ascus 

epiplasm, i.e. the residual cytoplasm remaining 

outside the spores after these have become 

cleaved out, may continue to play a part in the 

formation of the ascospore wall. For example, 

in Ascobolus immersus, the outer leaf of the sporedelimiting 

membrane may extend irregularly 

outwards into the surrounding epiplasm to form 

a perisporic sac within which secondary wall 

material is deposited, derived from the epiplasm, 

and passing as globular bodies through the 

membrane of the perisporic sac. This secondary 

wall material ornaments the ascospore wall but 

is not involved in the formation of the purple 

pigment characteristic of Ascobolus ascospores 

(Wu & Kimbrough, 1992). 

In many ascomycetes the outermost layer of 

the ascospore wall, the perispore, is mucilaginous, 

as seen for example in Ascobolus immersus 

(Fig. 14.5), Sordaria fimicola (Fig. 12.1c) and 

Pleospora herbarum (Fig. 17.10a). The properties 

of this outer wall layer may aid in the lubrication 

of the spore and also enable it to be compressed 

as it emerges from the ascus. Further, it may aid 

in the attachment of ascospores to substrata. 

It may also cause ascospores to stick together 

to form multisporous projectiles, an adaptation 

which results in an increased distance of


Fig 8.11 Ascus development in Ascobolus (after Oso,1969). (a) Young ascus showing the formation of membrane-bounded vesicles 

(V) from the nucleus (N).The ascus wall (AW) is lined by the plasmalemma (PM). (b) Appearance of the ascospore membrane (AM) 

at the tip of the ascus and the arrangement of vesicles along the periphery of the ascus. (c) Ascospore membrane now in the form of 

a peripheral tube open at the lower end.The diploid nucleus has divided. (d) Invagination of the ascospore membrane between the 

haploid nuclei. (e) Young ascospores (S) delimitedby the ascospore membrane from the epiplasm (E). (f) Separation of the two layers 

of the ascospore membrane due to the formation of the primary spore wall (PSW) between them. 

ascospore discharge as compared with singlespored 

projectiles (Ingold & Hadland, 1959). This 

adaptation is especially common in coprophilous 

fungi, i.e. those which grow and fruit on 

herbivore dung, such as Ascobolus (Fig. 14.5) and 

Sordaria. A special adaptation occurs in another 

coprophilous fungus, Podospora, in which the 

basal part of the spore proper develops as a 

primary appendage, whilst other parts of the 

perispore extend as mucilaginous secondary


239 

appendages (see Figs. 12.3, 12.4; Beckett et al., 

1968). The appendages of adjacent spores intertwine 

so that the spores are discharged strung 

together in the manner of a slingshot (Ingold, 

1971). In some aquatic ascomycetes the ascospores 

have extensions of the spore wall which aid 

in attachment. Pleospora scirpicola, which forms 

ascocarps on the submerged parts of culms 

of Schoenoplectus lacustris, an inhabitant of the 

shoreline of freshwater lakes, canals and slowmoving 

rivers, has long, mucilaginous, tapering 

extensions from each end of the ascospore 

(Fig. 17.1d). Appendaged ascospores are especially 

common in marine ascomycetes. The appendages 

develop in a variety of ways and unfurl in sea 

water, slowing down their rate of sedimentation 

and increasing the likelihood of their attachment 

to underwater substrata such as wood 

(Hyde & Jones, 1989; Hyde et al., 1989; Jones, 

1994). 

Germ pores or germ slits, through which 

germ tubes emerge on spore germination, are 

found in many ascomycetes, especially those 

with thick dark-pigmented walls. Germ pores, 

representing thin areas in the spore wall, occur 

at each end of the spore in Neurospora and 

germination may occur at either or at both 

ends. In Sordaria humana there is a single germ 

pore at the lower end of the ascospore plugged 

by a pore plug (Read & Beckett, 1996). The 

ascospores of Xylariaceae, e.g. Xylaria, Hypoxylon 

and Daldinia, have black walls with a hyaline 

germ slit running along the length of the spore 

(Figs. 12.10 and 12.14). 

Because the division which follows the fournucleate 

stage is mitotic and because the division 

plane is usually parallel to the length of the 

ascus, adjacent pairs of spores starting from the 

tip of an ascus are normally sister spores and 

are thus genetically identical. Rare exceptions to 

this situation are occasionally found where the 

division planes are oblique, or for other reasons 

(see Raju, 1992a). 

8.6.2 The ascus wall 

The wall of the ascus consists of several 

distinguishable layers. The outer layer is laid 

down first and inside it is a succession of laterformed 

layers so that the mature wall may 

consist of four or more layers (Bellemère, 1994; 

Read & Beckett, 1996). The wall material 

includes chitin, polysaccharides and proteins, 

but there is no evidence of lipid. The ascus 

wall is elastic. All or parts of it may stretch 

considerably during ascospore liberation, and 

contraction of the elastic wall provides the force 

for ascospore discharge. During discharge all 

the layers of the ascus wall may remain 

attached to each other, thus appearing as a 

single layer. Such asci are termed unitunicate 

(Lat. tunica ¼ a garment). Despite the term 

unitunicate which refers to the behaviour 

(i.e. function) of the ascus wall during ascus 

dehiscence, the wall of unitunicate asci is often 

composed of two superposed tunicae, a thin, 

single-layered or double-layered exoascus and 

a thicker endoascus. The endoascus may be 

fibrillar, or at first granular and then with 

parallel or reticulate fibrils (Parguey-Leduc 

& Janex-Favre, 1984). During ascospore discharge 

the two layers of the ascus wall 

remain attached, i.e. they do not glide over 

each other. 

A variant of the unitunicate type of ascus 

dehiscence is found in the lichenized ascomycetes 

Lecanora and Physcia (the Lecanora or rostrate 

type of dehiscence). In Physcia stellaris the ascus 

has a prominent amyloid dome. The ripening 

ascospores push against this dome and on 

ascospore discharge it is extruded to form 

a rostrum (Lat. rostrum ¼ beak) which extends 

upwards to the surface, whilst its base remains 

attached to the upper part of the wall of the 

ascus (see Figs. 8.12e,f; Honegger, 1978). 

In other ascomycetes, the ascus wall appears 

distinctly two-layered (bitunicate) when viewed 

with the light microscope (Luttrell, 1951; 

Reynolds, 1971, 1989). The layers of many (but 

not all) bitunicate asci separate at ascospore 

discharge into two functionally distinct layers 

(see Fig. 8.12), and such asci are termed fissitunicate 

(Dughi, 1956). Fissitunicate asci are particularly 

common in the Loculoascomycetes. 

Development of the wall of a bitunicate ascus 

takes place in two stages prior to ascospore 

formation. The first stage involves the growth 

of the ascus initial and the expansion of the


Fig 8.12 Types of ascus dehiscence. (a) Prototunicate ascus; the wall dissolves to release the ascospores passively. (b,c) Operculate 

asci before and after discharge; the ascus opens by means of a lid or operculum. (d) Discharged inoperculate ascus which has opened 

through a pore. (e,f) Rostrate ascus as seen in Physcia. In (e) a thickened part of the upper wall of the ascus is being extruded and 

is visible in a discharged ascus (f) as an extension of the inner part of the ascus wall, the rostrum. (g) Discharged bilabiate ascus 

showing the longitudinal slit by which the ascus opens. (h,i) Bitunicate ascus before and after the first stage of spore release. 

Rupture of the ectotunica has allowed the endotunica to expand. (e,f) after Honegger (1978). 

ascus mother cell. During this stage the outer 

layers of the wall making up the ectotunica 

(¼ ectoascus) are deposited. In the second stage, 

secondary wall layers making up the endotunica 

(¼ endoascus) are laid down within the primary 

wall. The development of bitunicate asci has 

been studied by Reynolds (1971) and by Parguey- 

Leduc and Janex-Favre (1982). At the beginning 

of development, asci are surrounded by a single 

homogeneous layer which is sometimes granular, 

bearing externally a loose network (a fuzzy 

coat) of interascal material. The ascus wall 

becomes divided into a densely granular external 

layer (the ectoascus) and a clearer, but equally 

granular, inner layer (the endoascus). A clear 

space then separates these two layers. The 

granular material of the endoascus rearranges 

itself into lines of fibrils at first following a wavy 

pattern as seen in transverse sections of developing 

asci. Later the fibrils become strongly 

folded into pointed zigzag shapes, a development 

which progresses from the inside towards the 

outside of the endoascus. The folds of the zigzags 

are closely pressed against the pointed teeth 

which mark out the plasmalemma. The density 

of the fibrils increases considerably throughout 

the thickness of the endoascus. Finally the two 

layers of the ascal wall, separated from each 

other by a clear space, appear as a double-layered 

ectoascus and a single-layered endoascus within 

which the fibrils are strongly pleated into 

accordion-like folds. The pointed crests of the 

pleats lie parallel to each other and perpendicular 

to the plasmalemma of the ascus. The 

folding of the layers of the endoascus and 

plasmalemma permit the rapid expansion of 

the ascus prior to spore discharge, i.e. by 

providing material which can unfold rapidly. 

Towards the tip of the non-discharged ascus 

the crests of the pleated folds of the endoascus


241 

may converge and appear as a kind of apical 

basket which has been termed by Chadefaud 

(1942) the nasse apicale (Fr. nasse ¼ keep net, 

eel trap). 

In some asci the ascus wall does not function 

in ascospore discharge, but dissolves or 

disintegrates at maturity, the spores being 

released passively. Such asci are termed prototunicate 

(see Fig. 8.12a). This type of ascus is 

characteristic of certain groups of ascomycetes 

such as the Eurotiales and Onygenales but they 

are also found in unrelated groups (Currah, 1994). 

Examples are Eurotium (Fig. 11.16) and Gymnoascus 

(Fig. 11.9). 

8.6.3 The apical apparatus of asci 

The apical dome of the ascus may be modified in 

various ways. In certain types of discomycete 

with an open saucer-like fruit body or apothecium, 

the ascus is capped by a wall which has 

an annulus of thinner wall material forming a 

lid or operculum (Lat. operculum ¼ a cover, lid) 

(van Brummelen, 1981). When the ascus explodes 

to discharge its ascospores, the operculum may 

be lifted off completely or may hinge to one side 

(see Figs. 14.5, 14.6). Such asci are operculate 

(Figs. 8.12b,c). However, the majority of ascomycetes 

have no ascus lid; they are inoperculate 

and when ascospore discharge occurs, the tip 

of the ascus opens by a pore (Fig. 8.12d). 

The presence or absence of an operculum is 

a character used in the classification of 

discomycetes. Operculate asci are characteristic 

of Pezizales including genera such as Aleuria, 

Ascobolus and Pyronema (see Chapter 14). 

Inoperculate discomycetes include Helotiales 

such as Sclerotinia (Figs. 15.1, 15.2) and many 

other orders. In a few cases, e.g the lichenized 

ascomycete Pertusaria and the coprophilous 

fungus Ascozonus, the ascus may burst by one 

or two longitudinal slits at the apex (see 

Fig. 8.12g). Such asci are described as bilabiate 

(i.e. two-lipped). 

Other kinds of specialized structures found in 

ascus tips are generally referred to as the apical 

apparatus. Their functions relate to the mechanism 

of discharge (see below). In many perithecial 

fungi the tip of the ascus contains an apical 

ring or annulus. This is a specially thickened 

inward extension of the apical wall of the ascus, 

arranged in the form of a cylindrical flange 

(Fig. 8.13). In some fungi (e.g. Xylaria) the annulus 

is amyloid, i.e. it stains blue with Melzer’s iodine, 

an aqueous solution of I 2 in KI (Beckett & 

Crawford, 1973). In other ascomycetes, reddishbrown 

(dextrinoid) staining may be observed, 

whereas in yet others (e.g. Sordaria) the annulus 

does not stain with iodine (Read & Beckett, 1996). 

When ascospores are discharged the annulus 

is everted, i.e. turned inside out like a sleeve 

(see Fig. 8.13b). The cylindrical opening of the 

annulus is considerably less than the diameter of 

the ascospores which pass through it as shown 

in Fig. 8.13a for Xylaria longipes and Fig. 12.1 for 

Sordaria fimicola, so that the annulus must be 

sufficiently elastic to expand and contract as an 

ascospore passes through it. The function of the 

annulus is to act as a sphincter, minimizing the 

decrease in hydrostatic pressure inside the ascus 

as spore discharge proceeds. It may also separate 

the spores from each other as they pass through, 

and by gripping the tapering rear portion of an 

ascospore impart some force which helps to 

expel it (Ingold, 1954a). Filiform (i.e. needleshaped) 

ascospores are discharged singly and 

not in groups. This is well shown in the ergot 

fungus Claviceps purpurea and its allies such as 

Cordyceps (Figs. 12.27, 12.33). Their ascus 

apices are capped by a swollen plug of wall 

material pierced by a narrow pore. Ascospores 

are squeezed out through the pore, sometimes 

with an interval of several seconds between 

successive discharge events (Ingold, 1971). 

Other elaborations of the upper part of the 

ascus have been reported (Beckett, 1981; 

Bellemère, 1994). 

The actual form of the mature ascus is very 

variable. In prototunicate forms, i.e. with nonexplosive 

ascospore release, the ascus is often 

a globose sac, but in the majority of ascomycetes 

the ascus is cylindrical, and the spores are 

expelled from the ascus explosively. 

8.6.4 Hamathecium 

In many cases the asci are surrounded by 

packing tissue in the form of paraphyses


Fig 8.13 Xylaria longipes. Fine structure of the ascus apex 

(after Beckett & Crawford,1973). (a) L.S. undischarged ascus 

showing the apical ring. (b) L.S. discharged ascus showing the 

eversion of the apical ring. 

(Gr. para- ¼ near, beside, parallel; physis ¼ 

growth), or pseudoparaphyses. The general 

term for such sterile inter-ascal tissue is the 

hamathecium (Gr. hama ¼ all together, at the 

same time) (Eriksson, 1981). Paraphyses are filaments 

which are attached to the ascocarp near 

the bases of the asci and are free at their upper 

ends as in Pyronema (Figs. 14.2a,c) and Ascobolus 

(Fig. 14.6). Pseudoparaphyses are hyphae which 

usually arise above the level of the asci and grow 

downwards between them. They may become 

attached at their lower ends as in Pleospora 

(Fig. 17.9). Because the paraphyses and pseudoparaphyses 

pack tightly around the asci, the 

latter cannot expand laterally but are forced to 

elongate. A hamathecium is lacking in certain 

groups of ascomycetes, e.g. the Eurotiales 

and Clavicipitales, and also in Mycosphaerella 

(Fig. 17.19). The sum of all contents of the 

ascoma (i.e. the hamathecium plus asci) but 

excluding the ascoma wall is called the centrum. 

8.6.5 The mechanism of 

ascospore discharge 

Explosive release of ascospores follows increased 

turgor pressure, caused by water uptake by the 

ascus. In the young ascus, after the spores have 

been cut out, the epiplasm remains lining the 

ascus wall, and this surrounds a large central 

vacuole containing ascus sap, within which 

the ascospores are suspended. The epiplasm is 

rich in the polysaccharide glycogen which can 

be visualized cytochemically by its reddishbrown 

staining with the I 2 /KI stain. As the ascus 

matures, the red stain diminishes in intensity 

due to the conversion of the polysaccharide to 

osmolytes of lower molecular weight. This brings 

about an increased osmotic concentration of 

the ascus sap, followed by increased water 

uptake. The resulting increase in turgor pressure 

causes the ascus to stretch and, eventually, 

to burst open, squirting out the ascospores. 

The osmotic pressure of the sap in mature asci 

extending from apothecia of Ascobolus immersus 

has been determined to be up to 3 bar (0.3 MPa), 

with glycerol being the main organic osmolyte 

(Fischer et al., 2004). In Gibberella zeae, the turgor 

pressure required for ascus discharge (1.54 MPa) 

seems to be caused mainly by a K þ and Cl influx 

across the plasma membrane, with the most 

abundant organic osmolyte (mannitol) making 

only a small contribution (Trail et al., 2005). 

Higher turgor pressures have been recorded 

when asci are mounted in water (Ingold, 1939, 

1966). 

In cup fungi (discomycetes), as the asci 

mature they elongate and project above the


243 

Fig 8.14 Ascospore puffing in 

Aleuria aurantia. Athickwhitecloud 

of ascospores has been released by 

a cluster of apothecia. Reprinted 

from Fuhrer (2005), with 

permission by Bloomings Books 

Pty Ltd.Original image kindly 

provided by B. Fuhrer. 

general surface of the hymenium. Their tips may 

be phototropic, as in the coprophilous fungus 

Ascobolus, and this ensures that the ascospores 

are directed upwards, towards the light. In some 

discomycetes, especially those with operculate 

asci (e.g. Ascobolus, Peziza), large numbers of 

ripe asci may discharge their spores simultaneously, 

a phenomenon known as puffing 

(Fig. 8.14). This may also occur, but less obviously, 

in forms with inoperculate asci, e.g. Sclerotinia 

and Rhytisma. Puffing results in a cloud of ascospores 

being discharged for greater distances than 

with spores discharged from a single ascus 

(Buller, 1934; Ingold, 1971). 

In the flask fungi (pyrenomycetes), such as 

Sordaria or Podospora, as an ascus ripens it 

elongates and takes up a position inside the 

ostiole, often gripped in position by a lining layer 

of hairs, periphyses (Gr. prefix peri ¼ near, 

around, roundabout). In this case the asci 

discharge their spores in turn. The necks of the 

perithecia in Sordaria and Podospora are phototropic 

so that the ascospores are shot towards the 

light. A variant of this method of discharge is 

found in fungi whose perithecia have necks very 

much longer than the length of the asci, such 

as Ceratostomella and Gnomonia. Here, before 

discharge, the asci break at their bases and 

detached asci move up a canal inside the 

perithecial neck and are held in place within 

the ostiole by periphyses as they discharge their 

spores (Ingold, 1971). 

The behaviour of the bitunicate type of ascus 

during discharge has been described as the 

Jack-in-the-box mechanism (Ingold, 1971). The 

outer wall is relatively rigid and inextensible. 

As the ascus expands, the outer wall ruptures 

laterally or apically (see Figs. 8.12h,i) and the 

inner wall then stretches before the ascus 

explodes. Ascus discharge is thus a two-stage 

process. This type of mechanism is found in 

Loculascomycetes such as Sporormiella (Fig. 17.18), 

Leptosphaeria (Fig. 17.3) and Pleospora (Figs. 17.1, 

17.9). 

In Cochliobolus the ascus is bitunicate but the 

endotunica is incomplete at its base, i.e. vestigially 

or partially bitunicate. In C. cymbopogonis the 

eight ascospores are spirally coiled around each 

other in the ascus and each has a recurved tip 

(Figs. 8.15a,b). The ectoascus bursts open near 

its tip and the sheaf of ascospores is expelled, 

the incomplete endoascus forming a thimblelike 

cap over the tips of the ascospores as they 

pass through the long pseudothecial neck. The 

spores are not explosively discharged but 

are extruded, en masse, from the neck of the 

pseudothecium in a long tendril from which 

they are dispersed by rain splash. In water the 

spores separate from each other and push away 

the endotunica which earlier capped their tips 

together (see Fig. 8.15d; El-Shafie & Webster, 

1980; Alcorn, 1981). 

It is likely that in most cases the spores are 

spatially separated from each other as they are


Fig 8.15 Ascospore liberation in Cochliobolus cymbopogonis. (a) Ascospore with a recurved tip. (b) Ascus containing a sheaf of 

eight spirally coiled ascospores.The ascus is bitunicate but the endoascus is not shown. (c) Ascus during the first stage of discharge. 

The ectoascus has broken (arrow), the endoascus has broken at its base and has extended, remaining as a thimble-like cap over 

the sheaf of ascospores. (d) An ascus after the release of the ascospores which have straightened out and pushed the broken 

endoascus aside. (e) Diagrammatic representation of a section through a pseudothecium showing stages in ascospore release. 

Scale bar, (a,b) ¼ 50 mm; (c,d) ¼ 200 mm. After El-Shafie and Webster (1980). 

constricted on passing through the ascus pore. 

This has been neatly demonstrated by spinning 

a transparent disc over the surface of a culture 

of Sordaria discharging spores (Ingold & 

Hadland, 1959). The ascus contents are laid out 

on the disc in the order in which they are 

released. Various patterns of spore clumping and 

separation are visible, and although in many asci 

the eight spores are well separated from each 

other, in others there is a tendency for spores to 

stick together. Calculations made from 

measurements of the length of the ascospore 

deposit and the speed of rotation of the disc, as 

well as by other methods, have revealed ascospores 

to be the fastest-accelerating biological 

objects (Trail et al., 2005; Vogel, 2005). The actual 

time taken for ascus discharge was estimated by 

the rotating disc method to be 0.000024 s (Ingold 

& Hadland, 1959). When ascospores stick 

together, they are discharged further than 

single-spored projectiles. In many coprophilous 

ascomycetes (e.g. Ascobolus, Saccobolus, Podospora)

TYPESOFFRUITBODY 

245 

the spores may be attached together by mucilaginous 

secretions and may be projected for 

distances of 30 cm in Ascobolus immersus and 

50 cm in Podospora fimicola. The distances to 

which individual ascospores are discharged 

vary, but are often in the range of 1 2 cm. 

In some ascomycetes the ascospores are 

not discharged violently, and in such cases the 

asci are often globose instead of cylindrical. 

The Hemiascomycetes (Chapter 10), 

Plectomycetes (Chapter 11) and several other 

groups have asci of this type. In Ophiostoma 

(Fig. 12.36) and Sphaeronaemella fimicola 

(Fig. 12.42) the ascus walls dissolve to release 

a mass of sticky spores which ooze out as a drop 

held in place by a ring of hairs surrounding the 

ostiole at the tip of a cylindrical neck which 

surmounts the perithecium. They are dispersed 

by insects. Breakdown of asci within the fruit 

body is also found in Chaetomium (Fig. 12.9). 

Ripe ascospores are extruded from the neck of 

the perithecium in a tendril. Possibly they are 

dispersed by jerking movements generated as 

the rough-walled perithecial hairs twist around 

each other. Tendrils of ascospores are sometimes 

found in ascomycetes which normally discharge 

their spores violently, e.g. Daldinia concentrica 

(Plate 5a), Hypocrea pulvinata (Plate 5c) and Nectria. 

In many marine ascomycetes the ascus walls 

are evanescent and dissolve to release the 

ascospores passively. In ascomycetes with subterranean 

fruit bodies, e.g. in the truffle Tuber 

and its relatives (Figs. 14.7, 14.8), the ascospores 

are not discharged violently, but are dispersed 

when the fruit bodies are eaten by rodents 

and other animals attracted by their characteristic 

odour. 

8.7 Types of fruit body 

The main types of ascomycete fruit body have 

been listed earlier (p. 21) and are drawn in 

Fig. 8.16). In yeasts and related fungi the asci are 

not enclosed by hyphae, but in most ascomycetes 

they are surrounded by hyphae to form an 

ascocarp (i.e. an ascus fruit body) or ascoma. 

An old term for ascus is theca (Gr. theca ¼ a case), 

and although this word is not now in general 

use, it is still found as a suffix in terms for 

different types of ascocarp. Byssochlamys forms 

clusters of naked asci (Fig. 11.15). In Gymnoascus 

there is a loose open network of peridial hyphae 

Fig 8.16 Different types of 

ascocarp, diagrammatic and not to 

scale. (a) Gymnothecium made up of 

branched hyphae which do not 

completely enclose the asci. 

(b) Cleistothecium completely 

enclosing the asci which are formed 

throughout the ascocarp.There is no 

opening. (c) Apothecium, an open cup 

lined by a layer of asci and associated 

structures forming the hymenium. 

(d) Perithecium with a layer of asci at 

the base. It opens by a pore or ostiole. 

Its wall or peridium is made up of 

flattened cells. (e) Pseudothecium. 

The asci are formed within locules in 

apseudoparenchymatousascostroma. 

There is no peridium. (d) after Ingold 

(1971), (e) after Luttrell (1981).


forming a gymnothecium (Gr. gymnos ¼ naked) 

and the asci can be seen through the network 

(Fig. 11.8). Gymnothecia are also seen in 

Myxotrichum (Fig. 11.10) and Ctenomyces (Fig. 11.5) 

where certain peridial hyphae extend as hooked 

hairs. In most species of Aspergillus and Penicillium 

which possess ascocarps, the asci are enclosed 

in a globose fructification with no special 

opening to the outside. Such ascocarps are 

termed cleistocarps or cleistothecia (Gr. 

kleistos ¼ enclosed). A modified cleistothecium 

capable of cracking open along a line of weakness 

is found in the Erysiphales (powdery 

mildews), and this is called a chasmothecium 

(Gr. chasma ¼ an open mouth). In the cup fungi 

(Pezizales and Helotiales) as well as in many 

lichenized ascomycetes the asci are borne in 

open saucer-shaped ascocarps, and at maturity 

the tips of the asci are freely exposed (see Plates 6 

and 7). Such fruit bodies are termed apothecia (Gr. 

apo- ¼ away from, separate). The Pyrenomycetes 

(e.g. Sphaeriales and Hypocreales) have perithecia 

(Gr. peri- ¼ around) which are flask-shaped 

fruit bodies opening by a pore or ostiole (see 

Fig. 12.1, Sordaria fimicola). The perithecial wall 

is formed from sterile cells derived from hyphae 

which surrounded the ascogonium during development. 

Perithecia are often single, as in Sordaria 

and Neurospora, but in some genera they are 

embedded in or seated on a mass of tissue 

forming a perithecial stroma (for examples, 

see Plate 5). The development of pseudothecia 

differs from that of perithecia in that the asci 

are contained in one or several cavities (locules) 

formed within a pre-existing ascostroma (Gr. 

stroma ¼ mattress, bed) (Luttrell, 1981). Examples 

are Leptosphaeria (Fig. 17.3) and Sporormiella 

(Fig. 17.18). Although the structure and development 

of perithecia and pseudothecia are essentially 

different, the term perithecium is often 

loosely applied to both. 

8.8 Fossil ascomycetes 

Ascomycetes are an ancient group of fungi, and 

fossilized structures possibly representing ascocarps 

made up of septate, anastomosing hyphae 

have been described from the Proterozoic period 

about 1 billion years ago (Butterfield, 2005). 

Lichen-like associations between fungi and 

cyanobacteria or algae may have existed some 

600 million years ago (Yuan et al., 2005). What are 

believed to be the remains of perithecia have 

been reported from beneath the epidermis of 

stems and rhizomes of one of the earliest known 

land plants, Asteroxylon, in the Rhynie chert of 

the Devonian period about 400 million years ago 

(Taylor et al., 1999, 2005). Fossil cleistothecia containing 

asci and ascospores resembling those 

of present-day Trichocomaceae have been 

found in coal balls of the Carboniferous age 

(Stubblefield & Taylor, 1983; Stubblefield et al., 

1983). Stalked ascocarps with well-preserved 

ascospores have been found in amber, the 

fossilized resin of a conifer. They have been 

assigned to an extant genus Chaenothecopsis 

(Mycocaliciaceae). Their close resemblance of 

present-day species which are also associated 

with resin indicate little evolutionary change 

during the past 20 million years (Rikkinen & 

Poinar, 2000). 

On morphological grounds, Barr (1983) 

suggested that the ancestors of Ascomycota 

should be sought among the Chytridiomycota. 

Confirmation of this view has since been 

obtained by comparison of DNA sequence 

data. Ascomycota are also closely related to 

Basidiomycota, each being a derived monophyletic 

group (Bruns et al., 1992; Berbee & Taylor, 

2001). Berbee and Taylor (2001) have estimated 

that these two groups evolved from a common 

ancestor about 600 million years ago, well 

before the development of vascular terrestrial 

plants. 

8.9 Scientific and economic 

significance of ascomycetes 

The study of ascomycetes is of considerable 

scientific importance. Neurospora crassa has been 

the subject of intensive genetical research 

related to its relatively simple nutrient requirements, 

rapid growth, its capacity to produce

CLASSIFICATION 

247 

mutants and the ease with which it can be grown 

and cross-mated in culture. The dissection of 

ascospores from its asci by micromanipulation 

has enabled tetrad analysis to be performed. 

Research on this fungus led to the important 

one-gene one-enzyme concept. Budding yeast 

(Saccharomyces cerevisiae) and a fission yeast 

(Schizosaccharomyces pombe) were amongst the 

first eukaryotes for which the entire genome 

was sequenced. Studies on S. cerevisiae were basic 

to the understanding of the biochemistry of 

anaerobic respiration whilst studies of S. pombe 

have provided key facts by which to interpret the 

fundamental process of cell division, which in 

turn has a bearing on the understanding of the 

apparently uncontrolled growth of cancerous 

cells. The economic significance of fermentation 

processes involving ascomycetes and their conidial 

relatives is immense. Examples include alcoholic 

fermentations by yeasts as the basis of the 

wine and brewing industries, antibacterial antibiotics 

such as penicillin from Penicillium chrysogenum 

and cephalosporin from Acremonium spp., 

and organic acids such as citric acid from 

Aspergillus niger. The immunosuppressant drug 

cyclosporin, which reduces the tissue rejection 

response and thus facilitates organ transplants, 

is a metabolite of Tolypocladium inflatum. Some 

ascomycetes are important in food production as 

in bread-making by yeast, cheese ripening by 

Penicillium roqueforti and P. camemberti and 

the fermentation of soybeans and wheat 

by Aspergillus, yeasts and bacteria to produce 

soy sauce. The mycoprotein Quorn is produced 

from mycelial biomass of Fusarium venenatum. 

Examples of the direct use of ascocarps as food or 

food flavourings are morels (Morchella spp.) and 

truffles (Tuber spp.). 

However, food spoilage may result from 

ascomycete contamination. A well-known example 

is contamination of cereal grains and grass 

by sclerotia of the ergot fungus Claviceps 

purpurea, which can cause severe, sometimes 

fatal, neurological, muscular and circulatory 

diseases such as gangrene or abortion in cattle 

and man. Studies on the alkaloid toxins 

contained in ergot sclerotia led to the discovery 

of drugs useful in obstetrics and the treatment 

of migraine, and in the identification of the 

hallucinogen lysergic acid. Another potentially 

serious mycotoxin is aflatoxin produced in 

groundnuts, cereals and other foodstuffs 

infected by Aspergillus flavus. Aflatoxins are 

highly carcinogenic in poultry and mammals, 

including man. Other mycotoxins include zearalenone 

from Gibberella zeae, which causes 

infertility in cattle and pigs, and trichothecenes 

from Trichothecium roseum and Fusarium spp., 

which cause aleukia in farm animals and 

man. A family of plant growth hormones, 

the gibberellins, now produced commercially, 

were discovered in an investigation of Bakanae 

(foolish seedling) disease of rice. 

It is not surprising that such a large group 

as the Ascomycota should contain numerous 

pathogens of plants and animals. Lifestyles 

are similarly varied, including biotrophic, hemibiotrophic 

and necrotrophic associations. Many 

ascomycote pathogens are of considerable economic 

importance. 

8.10 Classification 

It is impractical to attempt a detailed classification 

of ascomycetes which could include 

around 55 orders and 291 families (Kirk 

et al., 2001). We shall adopt the simplified 

classification outlined by M. E. Barr (2001) and 

Kurtzman and Sugiyama (2001). Based on a 

wealth of microscopic data, and especially the 

results of several phylogenetic analyses, five 

major groups (classes) of Ascomycota have 

been proposed, namely Archiascomycetes 

(Chapter 9), Hemiascomycetes (Chapter 10), 

Plectomycetes (Chapter 11), Hymenoascomycetes 

(Chapters 12 16) and Loculoascomycetes 

(Chapter 17). The latter three are sometimes 

called ‘higher ascomycetes’ or Euascomycetes. 

The class Hymenoascomycetes contains ascomycetes 

producing asci in a hymenium, i.e. in a 

fertile layer around which the ascocarp develops. 

This is in contrast to the Loculoascomycetes, 

where the asci develop in a pre-formed stroma. 

Since the Hymenoascomycetes are a very large 

and diverse group, we have subdivided them in 

this book.


Fig 8.17 Outline of a possible ascomycete phylogeny, 

presented as a consensus tree based on sequences of the RNA 

polymerase II gene. Lichenized fungi are printed in bold. 

Redrawn from Liu and Hall (2004), with permission. ß 2004 

National Academy of Sciences,U.S.A.


249 

An outline of current phylogenetic relationships 

among the Ascomycota has been given by 

Liu and Hall (2004) and is shown in Fig. 8.17. 

More detailed delimitations of the individual 

groups will be discussed in subsequent chapters. 

In our treatment of the ascomycetes, we have 

attempted to consider purely asexual forms in 

the taxonomic context of their ascomycete state 

wherever practical and where known with 

certainty.

9 

Archiascomycetes 


Several independent phylogenetic analyses of 

DNA sequence data (e.g. Berbee & Taylor, 1993; 

Sjamsuridzal et al., 1997; Liu & Hall, 2004) have 

grouped together a range of seemingly very 

diverse genera of ascomycetes. This group is considered 

to be the oldest of three broad evolutionary 

lineages of Ascomycota and has thus been 

named Archiascomycetes (Nishida & Sugiyama, 

1994). The core of the Archiascomycetes consists 

of the genera Taphrina and Protomyces, which 

are facultative biotrophic plant pathogens, and 

the saprotrophic fission yeast Schizosaccharomyces. 

Also now included are the yeast-like Pneumocystis, 

which causes pneumonia in immunocompromised 

patients (see p. 259); the filamentous 

fungus Neolecta, which parasitizes the roots 

of higher plants (Redhead, 1977; Landvik 

et al., 2003); and the anamorphic yeast Saitoella. 

Yet other genera are included as possible 

members because even though their appropriate 

DNA sequences have not yet been obtained, 

they are known to be related to confirmed 

members. In total, the class Archiascomycetes 

currently contains some 150 species in 

10 genera. 

Because of their diverse morphological 

appearances and modes of life, it is difficult 

to describe common characters typical of the 

Archiascomycetes. With the exception of Neolecta, 

which produces apothecia, ascocarps are lacking 

and asci are produced individually by yeast 

cells or by conversion of hyphal tips. There are 

no differentiated ascogenous hyphae. Asexual 

reproduction is usually by simple division of 

vegetative yeast cells by budding or fission. Even 

in Neolecta, the apothecia are highly unusual in 

that they lack ascogenous hyphae and paraphyses, 

and in that the ascospores are capable of 

producing yeast-like conidia by budding while 

still within the ascus or after discharge (Redhead, 

1977). This phenomenon is also found in Taphrina 

(see Fig. 9.2c). 

The presence of Neolecta in the most basal 

group of ascomycetes indicates that the capacity 

to produce fruit bodies is probably an ancient 

trait. The inclusion of both yeasts and mycelial 

forms among the Archiascomycetes makes it 

impossible to decide the chicken-and-egg question 

as to which of these states is ancestral and 

which is derived. It is significant that all recent 

molecular studies have placed Taphrina within 

the Archiascomycetes because this genus has 

long been suspected to be close to the 

origin of both the higher ascomycetes and the 

basidiomycetes (Savile, 1968; Alexopoulos et al., 

1996). Further, the position of Pneumocystis 

has been unclear until recently, oscillating 

between Basidiomycota (Wakefield et al., 1993) 

and Archiascomycetes (Sjamsuridzal et al., 1997; 

Kurtzman & Sugiyama, 2001), and thereby 

further supporting the suspected ancestral 

status of the organisms included among the 

Archiascomycetes. 

Two genera Taphrina and Schizosaccharomyces 

are of special significance to mycology 

and will be discussed more fully below, together 

with a brief account of Pneumocystis.

TAPHRINALES 

251 

9.2 Taphrinales 

The Taphrinales are ecologically biotrophic parasites 

mainly of flowering plants, causing a wide 

variety of disorders which often lead to strikingly 

abnormal development of the infected host 

tissue to form witches’ brooms, galls or leaf 

curls. About six genera are known of which 

Protomyces (10 species) and Taphrina (95 species) 

are the most important. Both Protomyces and 

Taphrina can be isolated from their hosts as 

ascospores, and these germinate in pure culture 

by budding to form saprotrophic haploid yeast 

cells. In the host plant, however, a mycelium 

of intercellular septate hyphae is produced. In 

Protomyces, hyphae are diploid, whereas they are 

dikaryotic in Taphrina. Dikaryotic hyphae are 

most unusual among ascomycetes but are typical 

of basidiomycetes. Biotrophic infection of the 

host plant culminates in individual hyphal tips 

undergoing meiosis (preceded by karyogamy 

in Taphrina), producing usually eight haploid 

ascospores which are discharged violently. We 

will discuss only Taphrina here; for Protomyces and 

related genera, species descriptions are given 

by Reddy and Kramer (1975). 

9.2.1 Taphrina 

Species of Taphrina are mostly parasitic on 

Fagaceae and Rosaceae (Mix, 1949), causing 

diseases of three main kinds. (1) Leaf curl or 

blister diseases, e.g. Taphrina deformans, the cause 

of peach leaf curl (Fig. 9.1; Plate 4a); T. tosquinetii, 

the cause of leaf blister of alder; and T. populina, 

the cause of yellow leaf blister of poplar. (2) 

Diseases of above-ground plant organs in which 

the infected twig undergoes repeated branching 

to form dense tufts of twigs called witches’ 

brooms. Examples are T. betulina, causing 

witches’ brooms of birch (Plate 4b), T. insititiae 

causes witches’ brooms of plum and damson, 

and T. wiesneri causes witches’ brooms and leaf 

curl of cherry. However, not all witches’ brooms 

are caused by Taphrina, and similar twig proliferation 

is also associated with infection by mites. 

(3) Diseases of fruits, e.g. T. pruni, which causes 

the condition known as pocket plums in which 

the fruit is wrinkled and shrivelled and has a 

cavity in the centre in place of the stone. Taphrina 

amentorum causes conspicuous tongue-like 

outgrowths on female catkins of alder, Alnus 

glutinosa (Plate 4c). 

Taphrina deformans 

Peach leaf curl is common on leaves and twigs 

on peach and almond, especially after a cool and 

moist spring. Towards the end of May, infected 

peach leaves show raised reddish puckered 

blisters which eventually acquire a waxy bloom 

(Fig. 9.1). Sections of leaves in this condition 

show an extensive septate mycelium growing 

between cells of the mesophyll and between the 

cuticle and epidermis, where the hyphae end in 

Fig 9.1 Taphrina deformans. Peach leaf 

showing leaf curl.

252 ARCHIASCOMYCETES 

swollen tips which have been termed chlamydospores 

by Martin (1940) but are, in fact, ascus 

initials or ascogenous cells (see Fig. 9.2). The 

interface between the parasitic fungus and the 

host takes the form of contact between their 

walls. No specialized haustoria have been found 

in T. deformans (Syrop, 1975), although they have 

been reported in some other species. Cytological 

studies (Martin, 1940; Kramer, 1961; Syrop & 

Beckett, 1976) have revealed that the segments of 

the mycelium and the young ascogenous cells 

are mostly binucleate. If the cells are multinucleate, 

then the nuclei are at least arranged in 

pairs (Syrop & Beckett, 1976). In the ascogenous 

cell, the two nuclei fuse and the diploid nucleus 

divides mitotically. The upper of the two daughter 

nuclei then undergoes meiosis followed by a 

mitosis so that eight nuclei result, which form 

the nuclei of the eight ascospores. The lower 

daughter nucleus remains in the lower part of 

the ascogenous cell and is often separated from 

the upper nucleus by a cross wall. During these 

nuclear divisions, the wall of the ascogenous 

cell has stretched to form an ascus. Delimitation 

of the ascospores occurs at the eight-nucleate 

stage. The individual nuclei become enclosed 

by double-delimiting membranes which do not 

arise from the nuclear envelope as in most 

ascomycetes, but by invagination of the plasmalemma 

of the developing ascus (Syrop & Beckett, 

1972). Within the ascus, the ascospores may 

bud so that ripe asci may contain numerous 

yeast cells (see Fig. 9.2c). These yeast cells can be 

regarded as the anamorphic state of Taphrina, 

and they have been named Lalaria (Moore, 1990; 

Inácio et al., 2004). The asci form a palisade-like 

layer above the epidermis, and it is their presence 

which gives the infected leaf its waxy 

bloom. 

The ascospores and yeast cells are projected 

from the ascus which often opens by a characteristic 

slit (Fig. 9.2c). Yarwood (1941) has 

shown that there is a diurnal cycle of ascus 

development and discharge in T. deformans. 

Nuclear fusion takes place during the afternoon 

or evening; nuclear divisions are complete by 

Fig 9.2 Taphrina deformans. (a) T.S. peach 

leaf showing intercellular mycelium and 

subcuticular ascogenous cells. (b) T.S. peach 

leaf showing ascogenous cells and asci, 

containing eight ascospores. (c) T.S. leaf 

showing a dehisced ascus, an eight-spored 

ascus and an ascus in which the ascospores 

are budding. Ascospores budding outside 

theascusarealsoshown.(d j) Cytology of 

ascus formation (after Martin,1940). (d,e). 

Fusion of nuclei in ascogenous cell. 

(f) Elongating ascogenous cell containing 

two nuclei formed by mitosis from the 

fusion nucleus.The upper nucleus has begun 

to divide meiotically. (g) Uninucleate ascus 

with uninucleate basal cell. (h,i) Four- and 

eight-nucleate asci. (j) Binucleate germ tube 

in germinating ascospore.

SCHIZOSACCHAROMYCETALES 

253 

about 5 a.m. and the spores appear mature by 

8 a.m. However, maximum spore discharge does 

not occur until about 8 p.m. Outside the ascus, 

ascospores or yeast cells may continue budding 

and the fungus can be grown saprotrophically 

as a yeast in agar or liquid culture. The yeast 

cells are often pigmented due to the presence of 

b-carotene and several other carotenoid pigments 

(van Eijik & Roeymans, 1982). Young 

leaves can be infected from such yeast cells and 

it has been shown that a culture derived from 

a single ascospore can cause infection resulting 

in the formation of a fresh crop of asci, so that 

T. deformans is homothallic. In this respect it differs 

from some other species, e.g. T. epiphylla, 

where the fusion of yeast cells, presumably of 

different mating types, is necessary before infection 

can occur (Kramer, 1987). In T. deformans the 

binucleate condition is established at the first 

nuclear division of a yeast cell placed on a peach 

leaf, and the two daughter nuclei remain associated 

in the germ tube which penetrates the 

cuticle (Fig. 9.2j). In other Taphrina species, the 

germ tube penetrates through stomata but is 

unable to breach the intact cuticle (Taylor & 

Birdwell, 2000). 

9.2.2 Growth hormones 

In infections of peach leaves with T. deformans, 

the distortions of the host tissue are associated 

with division and hypertrophy of the cells of the 

palisade mesophyll. In liquid cultures, especially 

on media containing tryptophane, considerable 

quantities of the auxin-type phytohormone 

indole acetic acid (IAA) have been demonstrated. 

A number of different cytokinins are also 

produced by several species of Taphrina in culture 

(Kern & Naef-Roth, 1975; Tudzynski, 1997). 

Together, these hormones promote processes of 

cell division, enlargement and differentiation in 

plants, and leaves infected with T. deformans 

show higher levels of auxins and cytokinins 

than uninfected leaves (Sziráki et al., 1975). It is 

therefore tempting to assume that the fungus 

produces these substances also in planta. 

However, this has not been formally proven 

yet, and the Taphrina peach system seems to 

have been less thoroughly examined than the 

interaction between Plasmodiophora brassicae and 

cabbage plants (see p. 63). 

9.2.3 Control of Taphrina deformans 

Taphrina deformans is by far the most serious 

pathogen among the Taphrinales, and it occurs 

wherever peach or almond trees grow. It is not 

yet entirely clear how T. deformans overwinters; 

Butler and Jones (1949) and Smith et al. (1988) 

considered it unlikely that the mycelial form is 

involved because leaves harbouring mycelium 

are shed in the autumn. It is more probable 

that yeast cells arising from discharged ascospores 

survive saprotrophically on the surface of 

twigs or in bud scales. Between November and 

March, the yeast cells develop thick walls and in 

spring, as the peach buds open, they produce 

germ tubes which penetrate the young leaves. 

The first symptoms of infection can be seen as 

soon as the buds break, but no further infection 

occurs from about early July onwards. This may 

be because T. deformans has a relatively low 

temperature maximum of 26 30°C (Butler & 

Jones, 1949). 

Good chemical control of T. deformans can 

be achieved by spraying with Bordeaux mixture 

in autumn after leaf fall, in order to reduce the 

population of yeast cells on the twigs. Another 

spray in early spring, at the time of bud swelling, 

will give improved control of infection because 

the time span in which Taphrina can infect 

is limited. Dithiocarbamates or other simple 

fungicides are commonly used in spring 

(Smith et al., 1988). Other diseases caused by 

Taphrina can be controlled in a similar way if 

necessary. 

9.3 Schizosaccharomycetales 

The classification of the Schizosaccharomycetales 

has been the subject of controversial 

discussions, but the emerging consensus is 

that there is only one genus with three species, 

S. japonicus, S. octosporus and S. pombe (Kurtzman 

& Robnett, 1998; Vaughan-Martini & Martini, 

1998a; Barnett et al., 2000). All three species grow


as saprotrophic yeasts which reproduce asexually 

by fission, i.e. by division of a vegetative cell 

into two daughter cells of equal size (Fig. 9.3a). 

Schizosaccharomyces is therefore called the fission 

yeast. Occasionally, especially in S. japonicus, true 

septate hyphae can be formed, and these may 

fragment into arthrospores. Sexual reproduction 

is by conjugation of two haploid vegetative 

yeast cells, followed by karyogamy and meiosis 

which gives rise to four or, more usually, eight 

ascospores (Figs. 9.3a,b). 

Schizosaccharomyces can be isolated from substrates 

rich in soluble carbon sources, e.g. tree 

exudates, fruits, honey and fruit juices. The bestknown 

species are S. octosporus and S. pombe. The 

latter is the fermenting agent of African millet 

beer (pombe) and arak in Java. It can tolerate 

ethanol levels up to 7% (v/v). Both species grow 

well in liquid culture or on solid media such as 

malt extract agar, developing ripe asci within 

3 days at 25°C. All stages of the life cycle can be 

readily seen if a preparation of cells from an agar 

culture of S. octosporus is made in water (Fig. 9.3). 

Individual cells are globose to cylindrical, 

uninucleate and haploid. Cell division is 

preceded by intranuclear mitosis, towards the 

end of which the nucleus constricts and becomes 

dumb-bell shaped (Tanaka & Kanbe, 1986). The 

division of the cell into two daughter cells is 

brought about by the centripetal development of 

a septum which cuts the cytoplasm into two. The 

two sister cells may remain attached to each 

other for a while, or may separate by breakdown 

of a layer of material in the middle of the septum 

(Sipiczki & Bozsik, 2000). 

Ascus formation in S. pombe is preceded by 

copulation. Schizosaccharomyces octosporus is homothallic, 

and quite often adjacent sister cells 

may fuse together. In the case of S. pombe, both 

homothallic and heterothallic strains are known, 

the latter with a bipolar mating system (hþ and 

h mating types). When cells of opposite mating 

type of S. pombe are grown together in liquid 

culture, especially under conditions of nitrogen 

starvation, a strong sexual agglutination 

occurs. This clumping together of the cells 

becomes visible as a flocculation of the culture. 

Changes in cell surface properties are 

Fig 9.3 Schizosaccharomyces octosporus. 

(a) Vegetative cells, three of which showing 

transverse division.Two cells to the right of 

the picture are conjugating. (b) Four- and 

eight-spored asci.


255 

important in agglutination, and fimbriae have 

been observed at the surface of cells stimulated 

by the appropriate pheromone (Johnson et al., 

1989). Using stable heterothallic haploid strains, 

the purification of the pheromones of S. pombe 

has been achieved; both are linear oligopeptide 

hormones (Davey, 1992; Imai & Yamamoto, 1994). 

The binding of a hormone released by cells of one 

mating type to receptors in the membranes of 

cells of opposite mating type initiates a signalling 

chain which in turn triggers the cellular 

response leading to agglutination and conjugation 

(Davey, 1998). The principle of mating 

factors will be discussed in more detail for 

Saccharomyces cerevisiae (p. 266). 

During agglutination, two cells come into 

contact by a portion of their cell wall. In homothallic 

strains, the fusing cells are often sister 

cells formed by preceding mitotic division. 

A pore is formed in the centre of the attachment 

area and this widens and elongates to form a 

conjugation canal (Fig. 9.3a). During this process 

the nuclei, one from each cell, migrate towards 

each other and fuse. Vacuoles may appear in the 

young ascus following nuclear fusion. The fused 

nucleus elongates and may reach half the length 

of the ascus, and then divides by constriction, 

the nuclear membrane remaining intact during 

division. The two daughter nuclei migrate to 

opposite ends of the ascus and divide further. 

These two divisions constitute meiosis. A single 

mitotic division usually follows so that eight 

haploid nuclei result, and eight ascospores are 

finally differentiated (Tanaka & Hirata, 1982). 

Four-spored asci are also common. The ascospores 

are released passively following disintegration 

of the ascus wall. 

The life cycle of Schizosaccharomyces (Fig. 9.4) is 

thus interpreted as being based on haploid 

vegetative cells which fuse to form asci, the 

only diploid cells. Meiosis in the ascus restores 

the haploid condition. Some variation in this 

pattern may occur. For example, in S. japonicus 

and S. pombe, limited division of the zygote in the 

diploid state before ascospore formation may 

take place, and it is possible to select diploid 

strains (Tange & Niwa, 1995). 

Physical and chemical analyses of the 

cell walls of Schizosaccharomyces show that they 

are principally composed of a b-(1,3)-glucan 

with b-(1,6)-branches making up 50 54% of 

the total cell wall carbohydrates, and of an 

a-(1,3)-glucan with a-(1,4)-branches contributing 

28 32%. There are also trace amounts of a 

branched b-(1,6)-glucan (Manners & Meyer, 1977; 

Kopecka et al., 1995). The b-(1,3)-glucan synthase is 

involved in all aspects of wall synthesis, including 

polarized growth, septum formation, and the 

formation and germination of ascospores (Cortés 

et al., 2002). A galactomannan linked to wall 

matrix glycoprotein makes up about 9 14% of 

the cell wall polysaccharides (Manners & Meyer, 

1977). As in other Archiascomycetes, chitin is 

present only in traces (Sietsma & Wessels, 1990), 

but it seems to play an important role in 

ascospore formation (Arellano et al., 2000). The 

walls of ascospores contain amylose and give a 

blue reaction with iodine. 

Fig 9.4 The life cycle of the 

homothallic yeast 

Schizosaccharomyces octosporus. 

Small open circles represent 

haploid nuclei; diploid nuclei are 

larger and split. Key events in the 

life cycle are plasmogamy (P), 

karyogamy (K) and meiosis (M).


In the following sections we give brief summaries 

of areas in which research on S. pombe is 

of outstanding significance for the discipline 

of biology as a whole. We anticipate that the 

relevance of this yeast for fundamental research 

will further increase in the future. Whilst we do 

not believe in the concept of a ‘model organism’ 

or even a ‘model fungus’, it is becoming 

clear that S. pombe, based on its more ancestral 

position in the phylogenetic system, is in many 

ways more relevant to the study of eukaryotic 

biology than its great rival, the more derived 

Saccharomyces cerevisiae (see p. 270). The entire 

genomes of both yeasts have been sequenced, 

and research is under way with S. pombe to find 

out the minimum number of genes (approximately 

17.5% of all genes) required for the 

basic functioning of this organism (Decottignies 

et al., 2003). 

9.3.1 Schizosaccharomyces pombe and 

the cell cycle 

The term ‘cell cycle’ denotes a carefully controlled 

sequence of regulatory and biosynthetic 

processes which guide a cell arising from mitosis 

towards its division into two daughter cells. 

Research on S. pombe has given us a fundamental 

understanding of the cell cycle. The literature 

on this topic is vast, and it is beyond the scope 

of this book to give more than the briefest of 

summaries. Our account borrows heavily from 

the textbook by Lewin (2000), which also provided 

the basis of the diagrammatic summary 

(Fig. 9.5). 

A young cell arising from mitotic division 

starts its life in the G1 phase (G ¼ gap) and may 

synthesize RNA, protein and other cellular constituents. 

It may grow in size but it does not 

duplicate its DNA at this point. The first crucial 

control point of the cell cycle is the 

START point, located in G1. At this point, the 

cell becomes committed to mitosis, and other 

options notably sexual reproduction are no 

longer available, i.e. beyond the START point the 

cell becomes insensitive to mating pheromones. 

When DNA duplication is actually initiated, 

the cell moves from the G1 to the S (synthesis 

of DNA) phase. After DNA replication has been 

completed, the G2 phase follows, during 

which the S. pombe cell further enlarges in size 

and produces all organelles and macromolecules 

which are required to support two daughter 

cells. A second control point is the boundary 

between G2 and the M (mitotic) phase; when 

this has been passed, the cell stops elongating. 

Condensation and separation of the chromosomes 

occur, followed by septation and physical 

separation of the two daughter cells. The identification 

of genes whose products are involved 

in the regulation of the cell cycle was possible 

by analysing temperature-sensitive mutants, 

i.e. mutants which grow normally at reduced 

(permissive) temperature (e.g. 25°C) but are 

blocked at some stage of the cell cycle at a 

higher (restrictive) temperature (e.g. 37°C). 

The most fundamental gene involved in the 

cell cycle is cdc2 because its product a protein 

kinase is involved at both the START and G2/M 

control points, and it is now known to fulfil 

the same universal role in all eukaryotes, including 

humans (Lee & Nurse, 1987; Nurse, 1990). 

In order to act in such a way, the cdc2 protein 

(written as Cdc2) combines with different 

proteins at specific stages of the cell cycle. 

These proteins are termed cyclins because their 

levels in the yeast cell show one peak in each cell 

cycle, followed by their degradation or inactivity. 

There are G1 cyclins and G2 cyclins which have 

different properties in combination with Cdc2. 

However, the activity of Cdc2 is modulated not 

only by the binding of cyclins, but also by kinases 

or phosphatases which, respectively, phosphorylate 

or dephosphorylate the Cdc2 protein. These 

respond to environmental stimuli and often 

antagonize each other in their effects on Cdc2. 

This allows a fine-tuning of the cell cycle in 

response to environmental factors such as the 

presence of pheromones which would prevent 

progression through START, or nutrient availability. 

Whilst the regulation of Cdc2 is relatively 

well understood, few of its substrates have 

been identified as yet, and this is an area of 

ongoing research. 

An understanding of the cell cycle of 

S. pombe is of significance far beyond mycology 

because the principles are conserved across all 

eukaryotes. In mammals, one regulatory factor


257 

Fig 9.5 ThecentralroleofCdc2inthecellcycleofS. pombe.The START checkpoint is passed only if Cdc2 is combined with a 

G1 cyclin (cig2) and is phosphorylated at a threonine residue at position161 (Thr) but dephosphorylated at a tyrosine residue at 

position15 (Tyr).The second major checkpoint is between the G2 and M phases; here Cdc2 needs to be coupled with a G2 cyclin 

(Cdc13) and must be phosphorylated at Thr but dephosphorylated at Tyr.The cell cycle is therefore controlled by the type of cyclin 

available for coupling with Cdc2, and by the action of kinases such as wee1or mik1and phosphatases (e.g.Cdc25). Adapted from 

Lewin (2000). 

which stops the cell cycle at the G2/M control 

point and commits the cell to apoptosis (selfdestruction) 

is DNA damage. This recognition 

mechanism is a most important protection 

against uncontrolled cell growth (cancer). These 

and other implications of the work on the cell 

cycle of S. pombe have resulted in the award of 

the Nobel Prize for Medicine and Physiology, 

among others, to Sir Paul Nurse in 2001. His 

Nobel lecture (Nurse, 2002) is a stimulating and 

readable account of the unravelling of the cell 

cycle in S. pombe.


Fig 9.6 The cytoskeleton and the cell cycle in 

Schizosaccharomyces pombe. A new cell initially grows only at 

the old end (a) before bipolar growth is assumed (b). In 

growing cells, microtubules (dark lines) are orientated 

longitudinally, forming a basket around the nucleus (large 

sphere) and projecting into the poles. Actin patches (white 

dots) are located in the growing tips, as they are in 

filamentous fungi. At mitosis (c), microtubules form the 

intranuclear spindle while actin aggregates to form a cortical 

ring in the vicinity of the dividing nucleus (d,e).The ring 

constricts as the wall of the septum is laid down; upon 

completion of nuclear migration into the poles, the nuclear 

spindlebreaksdownandthebasketofcytoplasmic 

microtubules reforms (f). After cell fission has been 

completed (g), actin relocates into the old end (h) at which 

growth is resumed. Redrawn from Brunner and Nurse (2000), 

Philosophical Transactions ofthe Royal Society,bycopyright 

permission of The Royal Society. 

9.3.2 Morphogenesis in S. pombe 

Many aspects of the cell biology and ultrastructure 

of S. pombe have been studied extensively, 

and the results pertaining to the cytoskeleton 

are of particular relevance to filamentous fungi. 

Freshly divided cells of S. pombe grow only 

at one end (the ‘old end’ opposite the septum), 

i.e. growth is initially monopolar (Fig. 9.6a) 

before bipolar growth starts in early G2 phase 

(Fig. 9.6b). In growing cells, microtubules are 

located in the cytoplasm and are orientated 

longitudinally, enclosing the nucleus like a 

basket. Mutant and inhibitor studies have 

revealed a crucial role for microtubules in 

co-ordinating polarized growth, i.e. in focusing 

cell wall extension to either or both of the 

two opposite poles (Brunner & Nurse, 2000; 

Hayles & Nurse, 2001). Microtubules seem to be 

involved in transporting the Tea1 protein to the 

poles. This protein acts as a termination signal 

for microtubule elongation, and by 

attracting microtubules it effectively controls 

its own transport (Mata & Nurse, 1998; Sawin 

& Nurse, 1998). Interactions between Tea1p 

and other proteins mark the cell end, i.e. the 

site of Tea1p accumulation, thereby fixing the 

growth direction in S. pombe (Niccoli et al., 2003; 

Sawin & Snaith, 2004). Actin is also located in the 

growing poles of S. pombe. We can speculate 

that actin filaments and microtubules fulfil 

a similar role in S. pombe as in the apices of 

filamentous fungi, with microtubules mediating 

long-distance transport and actin fine-tuning 

the fusion of secretory vesicles with the plasma 

membrane. 

When mitosis starts, there is a complete 

remodelling of the cytoskeleton, with the disappearance 

of cytoplasmic microtubules and the

PNEUMOCYSTIS 

259 

formation of the intranuclear spindle (Hagan, 

1998). No further cell wall extension takes 

place during mitosis, presumably because no 

cytoplasmic microtubules are available to drive 

it. By contrast, actin relocates from the poles to 

the centre of the cell, forming a ring around 

the equator in close proximity to the nucleus 

(Figs. 9.6c,d). Actin aggregation is co-ordinated 

by a protein (Mid1p) emitted from the nucleus 

to form a broad cortical band, which in turn 

is controlled by the activity of the nuclear protein 

kinases Plo1p and Pdk1p (Bähler et al., 1998; 

Brunner & Nurse, 2000; Bimbó et al., 2005). 

Since the positioning of the nucleus in the 

cell is determined by microtubules, these are 

ultimately responsible for morphogenesis in 

S. pombe. Microtubules pull apart the two 

daughter nuclei (Figs. 9.6d,e), and when these 

have reached the two opposite poles (Fig. 9.6e), 

the spindle breaks down and the basket of 

cytoplasmic microtubules is re-established (Fig. 

9.6f). Meanwhile, the actin ring co-ordinates the 

inward growth of the septum wall. When the 

septum has been completed, actin relocates to 

the two old ends, one in each daughter 

cell, which resume growth (Figs. 9.6g,h). It is 

remarkable that the septum is laid down 

precisely in the middle of a cell which was 

itself synthesized by asymmetric elongation of 

its two ends. 

If a cell of S. pombe comes into close proximity 

to a cell of opposite mating type and is in the G1 

phase prior to the START point, it will conjugate. 

The formation of a projection tip during conjugation 

requires the presence of actin for localized 

cell wall synthesis and lysis, and microtubules 

to localize actin towards this new if transient 

growing point (Petersen et al., 1998). Cell-to-cell 

fusion also requires the accumulation of actin 

(Kurahashi et al., 2002). 

9.4 Pneumocystis 

This is an unusual but appropriately named 

group of organisms living as cyst-like cells in 

the lungs of mammalian hosts, where they 

cause pneumonia in immunocompromised 

individuals. The identity of these organisms as 

fungi was established beyond doubt only relatively 

recently, following DNA sequence comparisons. 

Recently, these techniques have also 

permitted the distinction between different 

taxonomic entities within Pneumocystis which 

correlate with the taxonomy of their hosts. 

Thus, the original name P. carinii is now applied 

by most workers only to a species infecting rats, 

with the human pathogen called P. jirovecii 

(Stringer et al., 2002). 

Little is known about the life cycle of 

Pneumocystis because this organism cannot 

be grown satisfactorily outside its host. Cushion 

(2004) summarized evidence indicating that 

there is probably a haploid trophic phase in 

which cells divide by binary fission in an amoebalike 

way, i.e. by constriction. Trophic cells of 

Pneumocystis are firmly attached to mammalian 

pneumocyte I cells in the alveolar regions of 

lung tissue. The cell wall of the trophic stage 

is unusually thin and flexible. If two compatible 

trophic cells fuse, a diploid zygote is formed 

and undergoes meiosis, producing a thick-walled 

cyst containing eight ascospores which are 

presumed to develop into a fresh crop of trophic 

cells upon germination. Pneumocystis can 

cause lethal pneumonia in immunocompromised 

hosts and the pneumonia it causes is 

regarded as an AIDS-defining illness. Infections 

have also been linked with the sudden infant 

death syndrome, reflecting contact of children 

with Pneumocystis very soon after birth. Exposure 

to inoculum seems to have little effect on 

immunocompetent individuals, although there 

is evidence that they may carry latent Pneumocystis 

infections of limited duration. Considerable 

uncertainty exists about the epidemiology 

of Pneumocystis. Although there have been occasional 

reports of the detection of P. jirovecii 

DNA in nature, there is no convincing evidence 

of any external reservoir of inoculum which 

could represent a source of human infections. 

The fungus therefore seems to be spread mainly 

or exclusively between humans. One way by 

which Pneumocystis may avoid the mammalian 

immune response is its ability to alter the 

properties of surface glycoproteins acting as 

antigens.


There are many oddities about Pneumocystis 

(Stringer, 1996, 2002). One is that this fungus 

lacks ergosterol, utilizing cholesterol instead 

as its major membrane sterol. This explains 

the insensitivity of Pneumocystis to amphotericin 

B, the most important drug against fungal 

infections of humans (see Fig. 10.9). In contrast, 

although the cell wall of trophic cells of 

Pneumocystis is unusually thin, this fungus is susceptible 

to inhibitors of b-(1,3)-glucan synthesis 

such as echinocandins (Schmatz et al., 1990). 

Thirdly, there are only two rRNA gene repeat 

units, in contrast to other fungi which contain 

some 50 250 copies of it (see Fig. 1.24).

10 

Hemiascomycetes 


The class Hemiascomycetes contains the classical 

ascomycete yeasts, exclusive of those which 

belong to the Archiascomycetes (see the preceding 

chapter) and the ‘black yeasts’ such as 

Aureobasidium (see p. 486). Detailed descriptions 

of the individual yeast genera and species are 

given in Kurtzman and Fell (1998) and Barnett 

et al. (2000). A useful taxonomic overview is that 

by Kurtzman and Sugiyama (2001). There is only 

one order, the Saccharomycetales, which has 

been divided into 11 families and 276 species 

(Kirk et al., 2001; Kurtzman & Sugiyama, 2001). 

However, detailed phylogenetic analyses of the 

Hemiascomycetes (Kurtzman & Robnett, 1998, 

2003) indicate that this family arrangement is 

likely to be modified in the future, and for this 

reason we shall focus on selected genera. 

The key feature that distinguishes the Hemiand 

Archiascomycetes from the higher ascomycetes 

(Euascomycetes) is that ascogenous 

hyphae and an ascocarp, i.e. an investment of 

sterile hyphae surrounding the asci, are lacking 

in the first two groups. Instead, the asci are 

formed freely and singly, either directly following 

karyogamy or more rarely after a prolonged 

diploid phase. Another distinguishing feature 

is the composition of the cell wall, which 

contains very little chitin in the Hemi- and 

Archiascomycetes. Chitin is often confined to a 

small ring around the site where the daughter 

cell is produced (the bud scar). An ultrastructural 

feature of distinction concerns the septal pore 

of any hypha that may be produced. One or 

several pores may be present, and these are 

usually very small or plugged. They lack Woronin 

bodies, in contrast to Euascomycete septa 

which usually have only one large pore with 

associated Woronin bodies (Alexopoulos et al., 

1996; M. E. Barr, 2001; see Fig. 8.3). Hence, the 

Euascomycete septal pore permits passage of 

organelles including nuclei (see Fig. 8.2), whereas 

the micropore of the Hemiascomycete septum 

does not. Cytoplasmic communication between 

adjacent hyphal cells therefore does not seem 

to be possible. 

It is impossible to give a watertight set of 

criteria by which Hemiascomycetes can be distinguished 

from Archiascomycetes. The predominant 

growth form of Hemiascomycetes in culture 

as well as in nature is the yeast state, although 

a limited mycelium or pseudomycelium may 

also be present. Archiascomycetes may grow as 

a mycelium in nature but as yeasts in the laboratory 

(Taphrina, Protomyces). In Archiascomycetes, 

asci may (Taphrina, Protomyces) or may not 

(Pneumocystis, Schizosaccharomyces) forcibly discharge 

their spores, whereas asci of Hemiascomycetes 

generally have evanescent walls, i.e. 

they release their ascospores passively. 

In the absence of asci and ascospores, the 

microscopic identification of yeasts is difficult 

or impossible, and other methods have to 

be employed, e.g. physiological tests based on 

the ability of test species to grow on any of 

a standard set of carbon or nitrogen sources

262 HEMIASCOMYCETES 

(Yarrow, 1998; Barnett et al., 2000). The analysis of 

DNA sequences (e.g. 18S rDNA) is now performed 

routinely in many laboratories, and a comparison 

with the extensive databases of appropriate 

sequences should afford identification at least to 

genus level. In this way, hemiascomycete yeasts 

can be distinguished from Archiascomycetes 

and also from basidiomycete yeasts. Such a distinction 

should be unequivocal since it utilizes 

the very same characters by which the classes 

Hemi- and Archiascomycetes were established. 

10.1.1 Occurrence and isolation of 


Hemiascomycete yeasts are prominent as epiphytic 

saprotrophic colonizers of plant organs, 

especially where sugars are present, e.g. in the 

nectar of flowers, on fruits, and on wounded 

or exposed surfaces of plants. Between 10 5 and 

10 7 yeast cells g 1 plant material (fresh weight) 

may be present (Phaff & Starmer, 1987). Yeasts 

also occur in the soil, although only a few exclusively 

soil-borne species have been described. 

Most yeasts are probably introduced into the soil 

with the plant material with which they were 

originally associated (Phaff & Starmer, 1987). 

Yeasts also occur in freshwater and marine 

situations. Some species are associated with 

insects and other animals, including the guts of 

vertebrates which have a thriving yeast mycota. 

Yeasts may grow on skin surfaces and one 

species Candida albicans can, under certain 

circumstances, turn into a mild or severe 

pathogen of humans, especially of immunocompromised 

patients (see p. 276). Hemiascomycetes 

are of little importance as plant pathogens with 

the exception of Eremothecium spp. which cause 

lesions on citrus fruits, cotton and other 

crop plants, and are spread by sucking insects 

(see p. 284). 

Many species of Hemiascomycetes can grow 

under conditions of reduced water availability 

corresponding to about 50% glucose or a nearsaturated 

NaCl solution. Consequently, they can 

colonize most types of preserved foods, whereby 

the type of preservative determines the species 

composition (Pitt & Hocking, 1985; Fleet, 1990). 

Fortunately, food spoilage by yeasts does not 

normally result in the production of toxins, 

in contrast to bacteria or certain filamentous 

fungi. However, the economic losses of food 

spoilage due to yeasts are still considerable. 

Hemiascomycete yeasts are easily isolated 

onto most standard agar media augmented 

with a suitable antibiotic to suppress bacteria, 

e.g. a mixture of penicillin G and streptomycin 

sulphate (100 200 mg l 1 each), added to the 

cooling agar after autoclaving. Plant or soil samples 

can be plated either directly, or the yeasts 

can be suspended by shaking the sample in 

sterile distilled water containing a detergent 

such as 0.01% (v/v) Triton X-100 or Tween 80. 

The undiluted sample or a dilution series in 

water can be plated out, and the density of 

colony-forming units (CFU) g 1 soil or leaves 

can be calculated. Yeasts are just large enough 

to be resolved as individual cells when a Petri 

dish is inverted and viewed with a 10 objective, 

whereas bacterial cells are not resolved at that 

magnification. 

10.1.2 The importance of 


A very small number of species is of immense 

importance to biotechnology, and an adequate 

discussion is beyond the scope of this book. 

Below is a mention of the most important 

aspects; some further applications and the 

yeast species involved have been summarized 

by J. F. T. Spencer et al. (2002). 

1. Alcoholic fermentation mainly by 

Saccharomyces cerevisiae. This is the oldest and yet 

still the most important area of biotechnology, 

with about 10 11 l of beer and 3 10 10 l of wine 

produced worldwide each year (Oliver, 1991; 

Kurtzman & Sugiyama, 2001). The discovery of 

alcoholic fermentations has been made several 

times independently in the history of mankind. 

Details of fermentation processes are given in 

on pp. 274 276. Industrial alcohol (ethanol) is 

often obtained from fermentations of corn 

starch hydrolysate by S. cerevisiae, but there is 

an ongoing interest in using other yeasts 

(Pachysolen tamophilus, Pichia stipitis) for the

SACCHAROMYCES (SACCHAROMYCETACEAE) 

263 

production of ethanol from pentose sugars 

in wastes of industrial processes (Jeffries & 

Kurtzman, 1994). 

2. Bread-making. About 1.5 10 6 tons of 

fresh cells of S. cerevisiae are produced worldwide 

per annum for use in the production of bread 

dough (see p. 274). 

3. Single-cell protein (SCP). This term describes 

the conversion of low-cost substrates into proteinrich 

biomass of unicellular organisms. Yeasts 

have a high nutritional value to animals and 

man because they are rich in vitamins and 

protein, and because they do not generally 

produce mycotoxins. Since they also have very 

simple growth requirements, yeasts can be used 

to convert low-cost substrates such as wastes from 

industrial processes into high-value products for 

human or animal consumption. While the use of 

mineral oil as a substrate was a somewhat 

predictable failure, other substrates such as 

whey wastes from cheese production, molasses 

from sugar cane or pentose-containing wastes 

from paper production are promising (Tuse, 1984; 

Scrimshaw & Murray, 1995; Paul et al., 2002). 

Currently, about 800 000 tons of fodder yeasts are 

produced per annum (Kurtzman & Sugiyama, 

2001), but an extended application of single-cell 

protein technology is hampered by the low 

current cost of alternative protein sources such 

as soy meal or fish meal (Harrison, 1993; 

Scrimshaw & Murray, 1995). 

4. Vitamin production. Riboflavin (vitamin 

B2) is produced industrially by Eremothecium 

spp. (see p. 284). 

5. Production of recombinant proteins, 

e.g. enzymes, or clinically relevant molecules 

such as antigens, insulin and epidermal growth 

factor. Expression systems for heterologous 

proteins, i.e. proteins of interest whose gene 

has been linked to the promoter sequence of 

the producing organism, include S. cerevisiae 

and Pichia pastoris. The latter holds advantages 

because proteins of interest are secreted more 

efficiently. Further, the glycosylation (sugar) 

chains which are added to the polypeptide 

during and after its translation in the rough 

endoplasmic reticulum are more similar between 

Pichia and mammals than either is to S. cerevisiae. 

Therefore, Pichia proteins cause fewer immunological 

problems in clinical use (see p. 281). 

6. Biological control. Because yeasts do not 

produce mycotoxins and because of their ability 

to colonize the skin of fruits, they are being 

developed as biological control agents against 

postharvest losses in fruit crops. Pichia guilliermondii 

sprayed onto fruits selectively reduces 

development of moulds caused by Penicillium 

spp. (Chalutz & Wilson, 1990; McLaughlin et al., 

1990). 

10.2 Saccharomyces 

(Saccharomycetaceae) 

About 10 16 species of Saccharomyces are 

currently recognized (Vaughan-Martini & 

Martini, 1998b; Barnett et al., 2000; Kirk et al., 

2001). We will focus on S. cerevisiae, which in many 

ways is the most important fungus yet discovered. 

About 25 strains of S. cerevisiae exist, and these 

have different physiological properties which are 

relevant to their biotechnological applications. 

Many were formerly regarded as different species 

(Vaughan-Martini & Martini, 1998b; Rainieri 

et al., 2003). Saccharomyces cerevisiae is the brewer’s 

and baker’s yeast (see below), although some of 

the best brewing yeasts in current use belong 

to S. pastorianus (¼ S. carlsbergensis). In nature, 

S. cerevisiae is found on ripe fruits, like many 

other yeasts. Grape and fruit wines are still often 

made by relying on spontaneous fermentations 

by yeasts which happen to be growing on the 

skin of the fruits used. 

The relatively small size of yeast cells 

(about 6 8 5 6 mm) has limited their investigation 

by light microscopy, but great progress 

has been made recently by the use of fluorescent 

dyes. Further, by fusing the green fluorescent 

protein (GFP) gene to the promoters of diverse 

yeast proteins, it has become possible to locate 

the site of a defined gene product within the 

yeast cell (Kohlwein, 2000). The availability 

of freeze-substitution fixation for transmission 

electron microscopy has led to the production 

of highly resolved ‘natural’ images of


organelles and cellular processes (Baba & Osumi, 

1987), although many issues of yeast cytology 

have remained controversial. A vegetative yeast 

cell (Fig. 10.1) is densely packed with organelles, 

including one nucleus, a large central 

vacuole, and mitochondria. Mitochondria are 

very dynamic in shape, showing a pronounced 

tendency to fuse into one or a few large reticulate 

organelles when the energy demand is 

high, or to fragment into numerous small 

promitochondria during anaerobic fermentation 

or metabolic inactivity (Jensen et al., 2000; 

Okamoto & Shaw, 2005). 

An immense amount of literature exists on 

S. cerevisiae, covering aspects of genetics and 

molecular biology (Pringle et al., 1997), physiology 

(see Jennings, 1995), cytology (Baba & Osumi, 

1987) and biotechnology (Spencer & Spencer, 

1990; Walker, 1998). We can only broach a few 

selected topics here to give an impression of 

Fig10.1 Saccharomyces cerevisiae. Sketch of a budding yeast cell as seen by transmission electron microscopy using material fixed by 

freeze-substitution.The presence of a morphologically recognizable Golgi stack is unusual among Eumycota. Modified and redrawn 

from Baba and Osumi (1987).


265 

the enormous importance of S. cerevisiae for 

fundamental cell biology. This fungus was the 

first eukaryote (in 1996) to have its complete 

genome sequenced, and this together with the 

ease of genetic manipulation has further 

enhanced the status of S. cerevisiae as a workhorse, 

if not ‘model organism’, for eukaryote 

research. 

10.2.1 The life cycle of S. cerevisiae 

Vegetative cells of S. cerevisiae are generally 

diploid in nature, although tetraploid or aneuploid 

strains also occur. Strains may be homoor 

heterothallic. The chromosome number is 16 

(Cherry et al., 1997). The life cycle of S. cerevisiae 

is presented in Figs. 10.2 and 10.3. The haploid 

ascospores often fuse within the ascus where 

they were formed (Fig. 10.3d), or shortly after 

release. However, if individual ascospores 

become isolated, they can germinate and reproduce 

as haploid cells by budding. Where two 

haploid cells of opposite mating type are in close 

contact, they secrete peptide hormones and produce 

plasma membrane-bound receptors which 

recognize the hormone of opposite mating type. 

The binding of a hormone molecule to the 

matching receptor sets a signalling chain in 

motion (reviewed by Bardwell, 2004) which 

arrests the mitotic cell cycle at G1, stimulates 

transcription of mating-specific genes and 

causes polarized growth of the two cells towards 

each other (Leberer et al., 1997). Mating initially 

involves an increased ability of the surfaces of 

two cells to adhere to each other. This so-called 

sexual agglutination is mediated by glycoproteins. 

It seems that these are components of 

fimbriae, i.e. long filaments radiating outwards 

from the cell wall (see Fig. 23.15). Agglutination 

is followed by co-ordinated digestion of the 

walls separating the two cells. Plasmogamy and 

karyogamy follow swiftly (Gammie et al., 1998). 

The resulting diploid cell (Fig. 10.3e) can carry on 

reproducing asexually by budding. In contrast 

to Schizosaccharomyces pombe, there are therefore 

two mitotic cycles in the life cycle of S. cerevisiae. 

Under optimum conditions, the culture doubling 

time by mitosis is about 100 min. 

Diploid strains of S. cerevisiae can be induced 

to form ascospores by suitable treatment, and 

this yeast is therefore termed an ascosporogenous 

yeast, in contrast to asporogenous yeasts 

in which ascospores have not been observed. 

Meiosis can be induced by growing the yeast on 

a nutrient-rich presporulation medium containing 

an assimilable sugar, a suitable nitrogen 

source for good growth (nitrate is not utilized), 

Fig10.2 The life cycle of S. cerevisiae. Both haploid and diploid cells can reproduce by budding.Open and closed circles represent 

haploid nuclei of opposite mating type; diploid nuclei are larger and half-filled. Key events in the life cycle are plasmogamy (P), 



Fig10.3 Saccharomyces cerevisiae. (a) Vegetative yeast cells 

reproducing by budding. (b) Yeast asci containing mostly four 

spores, sometimes with only three spores in focus. (c) Ascus 

showing a budding ascospore (arrow). (d) Ascus in which two 

spores have fused together and are budding. (e) Two ascospores 

fusing (top left), and two fused ascospores forming a 

diploid bud (right). 

and vitamins of the B group. Such a medium 

results in well-grown cells which will sporulate 

on transfer to a sporulation medium. Sporulation 

occurs best on media in which budding 

is inhibited. Low concentrations of an assimilable 

carbon source are necessary to provide 

energy for the sporulation process. Acetate agar 

(1 g glucose, 8:2 g Na acetate3H 2 O and 2.5 g yeast 

extract l 1 ) is a good sporulation medium 

(Yarrow, 1998). 

Diploid yeast cells convert directly into 

asci within 12 24 h of incubation in a suitable 

sporulation medium. The frequency of ascus 

formation in most isolates is quite low, usually 

less than 10% (Vaughan-Martini & Martini, 

1998b). The cytoplasm differentiates into four 

thick-walled spherical spores, although the 

number of spores may be fewer (see Fig. 10.3d). 

The nuclear divisions which precede ascus 

formation are meiotic. As is also the case in 

mitosis, the nuclear envelope remains intact 

during meiosis, taking up a lobed shape as the 

nuclear spindles draw the chromosomes into two 

and then four corners of the envelope (Fig. 10.4). 

The mechanism of ascospore formation has been 

extensively reviewed by Neiman (2005). It is very 

similar to that of higher ascomycetes, the main 

difference being that there is no common vesicle 

enclosing all nuclei prior to ascospore delimitation. 

Instead, a cup-shaped double-membrane, 

the prospore membrane, associates with each of 

the four spindle-pole bodies, and this gradually 

encapsulates its nuclear lobe until the four 

nuclei separate (Figs. 10.4g,h). As in other ascomycetes, 

the ascospore wall is then laid down 

in the lumen between the two membranes 

surrounding the developing ascospore.


267 

Fig10.4 Saccharomyces cerevisiae. 

Diagrammatic summary of the processes of 

meiosis and ascospore delimitation (from 

Beckett et al.,1974). (a d) The spindle pole 

body replicates and the two new spindle pole 

bodies move to opposite poles of the nucleus. 

The nuclear membrane remains intact. (e,f) 

Further replication of the spindle pole bodies 

and rearrangement.The nuclear envelope is 

still intact. New membranes, the ascosporedelimiting 

membranes, form outside the spindle 

pole bodies. (g,h) Envelopment of the 

lobes of the dividing nucleus by the ascospore-delimiting 

membranes results in the 

formation of four haploid uninucleate 

ascospores. 

10.2.2 Mating in S. cerevisiae 

Many strains of S. cerevisiae are heterothallic, 

and the ascospores are of two mating types. 

Mating type specificity is controlled by a single 

genetic locus which exists in two allelic states, 

a and a, and segregation at the meiosis preceding 

ascospore formation results in two a and two a 

ascospores. Fusion normally occurs only between 

cells of opposite mating type, and this has 

been termed legitimate copulation. Such fusions 

result in diploid cells which can, under appropriate 

conditions, form asci with viable 

ascospores. 

The mating type (MAT) alleles are rather small 

and structurally similar to each other, but differ 

in their central region which comprises about 

650 base pairs (bp) in MATa and 750 bp in MATa 

(Fig. 10.5). Because of this difference, mating type 

alleles are often called idiomorphs. In haploid 

a-cells, the MATa locus expresses two genes, both 

of which encode regulatory proteins. The a1 gene 

product interacts with a constitutively expressed 

protein not encoded by the MAT locus, Mcm1p, 

to activate several a-specific genes outside 

the MAT locus, notably those encoding the 

a-pheromone which is secreted by a-cells, and


Fig10.5 The structure of the mating type idiomorphs a (top) and a (bottom) of Saccharomyces cerevisiae.The two alleles differ only 

in their central (Y) regions which contain parts of two genes a1anda2ora1anda2.The entire lengths of these genes and their 

directions of transcription are indicated by arrows.The function of a2 is unknown. In diploid cells, the lack of expression of a1andthe 

formation of a dimeric a2/a1protein suppresses the expression of mating type-specific proteins including hormones and their 

receptors. nt ¼ nucleotides.Redrawn from Haber (1998) Annual Reviews of Genetics 32,withpermission.ß1998 Annual Reviews, 

www.annualreviews.org. 

the plasma membrane receptor Ste2p, which 

can bind a-pheromone from the environment. 

In diploid cells, expression of a1 and thus of 

a-specific proteins is repressed. The a2 gene 

encodes a repressor protein which interacts 

with several other regulatory proteins, 

including Mcm1p, to repress the expression of 

a-specific genes, including those encoding the 

a-pheromone and the a-factor receptor Ste3p. In 

the absence of the a1 and a2 gene products, 

haploid cells have an a-phenotype with respect to 

mating behaviour because a-genes are constitutively 

expressed. The function of a2 is unknown, 

and the a1 gene product is active only in diploid 

cells, combining with the a2 protein to repress 

haploid-specific genes including those encoding 

the two pheromones and their receptors. 

Another gene repressed by the a2/a1 dimer 

is RME1, which encodes a repressor of meiosis. 

Meiosis can therefore only take place if a diploid 

a/a nucleus exists in which Rme1p is repressed 

by the a2/a1 dimer, and if nutrient conditions 

are limiting. The signal for nutrient limitation 

is sensed and transmitted by a cyclic AMPdependent 

signalling chain (Klein et al., 1994). 

Therefore, the most important difference 

between a/a diploids and homozygous diploids 

or haploids is that only the a/a diploids can initiate 

meiosis under nutrient-limiting conditions, 

leading to the production of ascospores which 

are more resistant to adverse conditions than 

vegetative cells. It is likely that this enhanced 

survival of ascospores is the reason why haploid 

or homozygous populations of S. cerevisiae and 

some other ascomycetes (e.g. Schizosaccharomyces 

pombe) possess the intriguing ability to switch 

their mating type, thereby acquiring the ability 

to undergo meiosis. An excellent account of the 

experiments and ideas leading to the unravelling 

of the mating factor switch in S. cerevisiae has 

been given by Haber (1998), and we borrow 

heavily from it in the following summary. 

Strathern and Herskowitz (1979) observed 

that the ability to switch their mating type is 

acquired only by cells which have previously 

divided at least once. The pattern established by 

a single germinating a-type haploid ascospore is 

shown in Fig. 10.6: the first daughter cell has the 

mating type a, but then the mother cell switches 

its mating type prior to its second division, 

so that two a-cells result. Meanwhile, the first 

daughter (a-type) cell undergoes its first division 

so that a cluster of two a- and two a-type cells 

is produced. Conjugation can occur, and the 

two zygotes can carry on dividing as diploid 

yeast cells with the additional option to 

undergo meiosis and produce asci if required. 

The mating type switch is brought about by the


269 

Fig10.6 Mating type switch in Saccharomyces 

cerevisiae. A germinating a-type ascospore 

denoted by its white nucleus produces a bud 

which has the same mating type. Ash1mRNA is 

selectively translocatedinto the bud (a), and its 

protein Ash1p is expressed in the daughter 

nucleus (b), preventing it from switching its 

mating type. However, the mother cell is now 

competent to switch its mating type to a 

because it has divided once before (c); when it 

undergoes its second division (d,e), it produces 

an a-type daughter cell.The 

first-formed daughter cell cannot switch its 

mating type because it has no previous history 

of cell division.Consequently it produces a 

daughter of a-type. Mating (f) occurs between 

one a-andonea-type cell apiece, and conjugation 

results in two diploid cells which can 

reproduce by further budding (g) or by meiosis 

and ascus formation. Based on Haber (1998). 

HO endonuclease, the gene of which is only 

expressed in mother cells which have divided 

at least once (Nasmyth, 1983). Expression of the 

HO endonuclease gene is controlled by a series of 

repressor proteins, and one of them Ash1p is 

confined to the daughter cell upon division. This 

is due to the selective transport of its mRNA 

molecule into the bud prior to cytokinesis (Long 

et al., 1997). 

Hicks et al. (1977) proposed the cassette model 

to account for the mating type switch, and this 

has been confirmed by subsequent experimentation. 

In addition to the mating type locus which 

is active in a given haploid cell, each haploid 

genome possesses two further complete copies, 

one to the left of the active locus which usually 

contains the a allele (i.e. HMLa) and the other to 

the right, encoding a (i.e. HMRa). These genes are 

silenced, i.e. they are not transcribed because 

their DNA is coated by histones and other proteins 

encoded and regulated by numerous other 

genes. Silencing is determined by the location 

of these gene copies in the proximity of silencing 

sequences (Haber, 1998). The mating type switch 

is perfomed when the HO endonuclease cleaves 

the currently active locus at the Y/Z boundary 

(see Fig. 10.5), followed by the digestion of one 

of the two DNA strands of the Z region by an 

exonuclease. A new sequence is then copied 

into that gap from either of the two silent genes, 

using the one-stranded Z region as a template. 

The integrity of the silent gene which acts as


template is unaffected during that process 

(for details, see Haber, 1998). Hence, yeast cells 

can repeatedly switch their mating type. There is 

an element of selectivity in the mating type 

switch because, for example, a-cells choose the 

silent a-locus 85 90% of the time (Weiler & 

Broach, 1992). In the case of a-cells, preference 

for the switch to the a mating type is brought 

about by the a2 protein (for details, see Haber, 

1998). 

10.2.3 The cell wall of S. cerevisiae 

The wall of S. cerevisiae represents a considerable 

biochemical investment, making up 15 30% of 

the dry weight of vegetative cells. Up to three 

wall layers can be distinguished by electron 

microscopy. They differ in their chemical composition, 

and the relatively simple architecture of 

the wall of S. cerevisiae is considered a model for 

other fungi (Molina et al., 2000; de Nobel et al., 

2001). The middle layer is electron-translucent 

and consists of the main structural scaffold 

of branched b-(1,3)-glucan molecules which bind 

b-(1,6)-glucans and chitin. The latter, however, is 

present only in low quantities (1 2% of the total 

wall material) and it is unevenly distributed, 

being concentrated in a ring around the region 

where the bud emerges. The outer wall layer of 

S. cerevisiae is electron-dense because it consists 

mainly of proteins. These determine the 

cell surface properties, including the porosity 

(pore size) of the cell wall (Zlotnik et al., 1984) 

and adhesiveness to other cells (flocculation; see 

p. 274). The outer wall proteins may be highly 

glycosylated in S. cerevisiae by the addition of 

large mannose chains. In pathogenic yeasts such 

as Candida albicans, this outer layer is also 

important because of its involvement in attachment 

of the fungus to its host, and because it 

conveys antigenic properties. There are two main 

groups of outer cell wall proteins (CWPs) in 

S. cerevisiae. The members of one are modified 

by a glycosylphosphatidylinositol (GPI) chain 

which is indirectly linked to the b-(1,3)-glucans 

of the central wall layer via the b-(1,6)-glucans. 

These proteins are called GPI CWPs. The second 

type of outer cell wall protein is called Pir CWP 

(Pir ¼ protein with internal repeats) and is 

linked directly to the b-(1,3)-glucan component 

(Kapteyn et al., 1999; de Nobel et al., 2001). Both 

GPI CWPs and Pir CWPs are structural 

proteins. The innermost layer (periplasmic 

space) is also electron-dense and consists of 

proteins, but these are mostly enzymes which 

are too large to pass through the central layer. 

They are therefore restrained by the glucan layer 

(de Nobel & Barnett, 1991). 

The polarity of wall synthesis in S. cerevisiae 

is controlled by the localization of the plasma 

membrane-bound enzymes (glucan synthetases, 

chitin synthetases) which produce the elements 

of the middle layer, and by the secretion of the 

structural outer wall proteins as well as enzymes 

which cross-link the various elements of the 

cell wall. Cell wall synthesis is thus regulated 

spatially by the polarity of the yeast cell, and 

temporally by the cell cycle; the transcription 

of many genes involved in cell wall synthesis 

is cell cycle-dependent (Molina et al., 2000; 

Rodríguez-Peña et al., 2000). 

10.2.4 Morphogenesis and the cell cycle 

of S. cerevisiae 

One oddity about S. cerevisiae is that it does 

not require microtubules for the maintenance 

of its cellular polarity, as shown by mutant 

and inhibitor studies. In other eukaryotes, 

including filamentous fungi and also the fission 

yeast Schizosaccharomyces pombe, microtubules 

are employed for long-distance transport processes. 

It is possible that they are dispensible in 

S. cerevisiae simply because of the small distance 

between the mother cell and the growing 

bud. Of course, microtubules are required in 

S. cerevisiae as in all other eukaryotes for nuclear 

division. Actin, in contrast, is crucial for cell 

polarity and cell viability in S. cerevisiae (Pruyne 

& Bretscher, 2000b; Pruyne et al., 2004). 

The cell cycle of S. cerevisiae is similar to that 

of Schizosaccharomyces pombe (see p. 256) and other 

eukaryotes in its regulatory mechanisms (Lewin, 

2000; Alberts et al., 2002), except that the G2 

phase is lacking, and that cell division (cytokinesis) 

is initiated early in the cycle, the bud being 

already present during the S phase. A summary 

of the budding process is given in Fig. 10.7.


271 

Fig10.7 The mitotic cell cycle of Saccharomyces cerevisiae. 

Actin patches and cables are drawn in white; the septin ring is 

black. Secretory vesicles are not drawn, but their distribution 

follows essentially that of actin patches. (a) Initiation of the 

bud site occurs during the S phase by the assembly of actin 

patches around a septin ring. (b) Bud extension during late S 

phase.The cap co-ordinates apical bud growth by establishing 

actin cables which mediate the transport of secretory vesicles 

into the bud, and their fusion in the region of the cap. (c) A 

later stage of bud growth; the cap components become 

distributed more evenly over the bud membrane surface, and 

growth is non-polarized (isodiametric). Meanwhile, the dividing 

nucleus is drawn, via cytoplasmic microtubules (not 

shown), to an actin/myosin ring superimposed onto the septin 

ring.The nucleus divides so that each cell receives one daughter 

nucleus. (d) Re-establishment of polarized growth by the 

formation of two septin rings, one on either side of the bud 

site.Growth leads to closure of the pore between the mother 

and daughter cell. Redrawn from Sheu and Snyder (2001), with 

kind permission of Springer Science and Business Media. 

Useful and comprehensive reviews are those by 

Pruyne and Bretscher (2000a,b) and Sheu and 

Snyder (2001). The bud site is determined by the 

assembly of a protein cap at the inner surface 

of the plasma membrane. This cap contains an 

essential regulatory protein, Cdc42p, which is 

controlled directly by the cell cycle and in turn 

determines the sequestration of numerous other 

scaffold and regulatory proteins by the cap. 

Budding differs between haploid and diploid 

cells, the former initiating new buds adjacent 

to the previous one, and the latter budding in 

a bipolar fashion (Pruyne et al., 2004). 

One important group of proteins are the 

septins, which form a ring around the bud site 

(Fig. 10.7a). Actin filaments are initiated from 

the centre of the cap. As the bud extends in a 

polarized fashion, the septin ring remains at the 

site of bud emergence whereas the cap which 

governs bud extension migrates with the bud, 

staying at the apex and controlling bud extension 

(Fig. 10.7b). Later, the cap components and 

actin filament attachment points become distributed 

diffusely over the bud surface. This 

leads to the fusion of secretory vesicles over 

the entire bud surface, and to a change in the 

growth pattern from polarized to isodiametric 

(Fig. 10.7c). 

The septin ring binds numerous proteins, 

including important regulatory ones (Versele & 

Thorner, 2005). Actin and myosin are attracted 

early during bud emergence, and a contractile 

actin ring is superimposed on the septin ring. 

Later, during nuclear division, cytoplasmic 

microtubules are also captured; these, in turn, 

are in contact with the microtubules of the 

intranuclear mitotic spindle, and thus the dividing 

nucleus is drawn towards the ring, with one 

daughter nucleus apiece ending up in each of 

the two cells (Fig. 10.7c; Kusch et al., 2002). 

Cytokinesis is brought about as the actin ring 

contracts (Lippincott & Li, 1998). At this point, 

septins appear as a double ring, sandwiching 

the constricting actin ring. The septin double 

ring assembles two caps, and these serve as a 

nucleation centre for actin filaments which 

direct secretory vesicles to the bud site, closing 

the wall between mother and daughter cell 

(Fig. 10.7d). The regulatory mechanisms are 

immensely complex but are beginning to be 

unravelled (Pruyne & Bretscher, 2000a,b; 

Pruyne et al., 2004; Versele & Thorner, 2005) 

and are likely to be of fundamental significance 

because the division of cells by a constricting 

actin ring is found also in other fungi and 

in animal systems, although apparently not in 

plants.


Following separation of the daughter cell, 

a circular, crater-like bud scar is left as a 

permanent mark on the surface of the mother 

cell (see Fig. 10.12). The maximum number of 

scars that could be accommodated on the surface 

of a yeast cell is about 100, suggesting that 

individual yeast cells are not capable of unlimited 

budding. Individual yeast cells age just like 

other organisms, although the timing of death 

is determined by complicated genetic factors 

and the sum of metabolic energy expended 

throughout the life of the yeast cell, rather 

than the number of the bud scars per se 

(Jazwinski, 2002). 

Under certain environmental conditions 

(notably nutrient deficiency) diploid and, to a 

lesser extent, haploid cells of S. cerevisiae can 

change their growth pattern from budding, 

which produces heaps of cells only on the agar 

surface, to the formation of pseudohyphae which 

can grow into the agar. Pseudohyphae may be 

of significance in the ecology of S. cerevisiae 

because they allow the organism to spread over 

and penetrate into substrates, and to assimilate 

nutrients more readily (Gimeno et al., 

1992). Formation of pseudohyphae requires an 

enhanced adhesion of the cells to each other and 

an enhanced polarity of daughter cell growth. 

Not surprisingly, the signalling events leading 

to pseudohyphal growth are rather complex 

(Palecek et al., 2002; Ceccato-Antonini & 

Sudbery, 2004). 

10.2.5 Membrane cycling in S. cerevisiae 

An enormous amount of work has been done 

to elucidate the secretory route in S. cerevisiae, 

and a sizeable collection of temperature-sensitive 

mutants with defects at different points of the 

secretory route has been assembled (Schekman, 

1992). Further, individual stepwise modifications 

to proteins travelling the secretory route can be 

identified, especially with respect to their 

glycosylation pattern and proteolytic cleavage 

of parts of the original polypeptide chain 

(Graham & Emr, 1991). The export of proteins 

starts with their synthesis in the rough endoplasmic 

reticulum and continues with their 

processing in a Golgi system. Along this route, 

the proteins are modified by the addition of 

glycosylation chains, and by the proteolytic 

cleavage of signal sequences. Transport has 

long been thought to occur by means of vesiclelike 

carriers, and the biochemical events leading 

to the budding of a vesicle from its source 

and its fusion with the destination membrane 

(e.g. ER ! Golgi) have been extensively characterized 

(Rothman & Orci, 1992). However, it is 

still unclear whether discrete vesicular carriers 

are an obligate transport system in vegetative 

yeast cells. An alternative is the dynamic maturation 

model in which sheets of ER become 

transformed into Golgi compartments which 

gradually dilate and fragment into secretory 

vesicles (Rambourg et al., 2001). Whatever their 

initial history, secretory vesicles emerge from 

the Golgi system (Baba & Osumi, 1987) and 

migrate to the growing bud along actin cables 

(Finger & Novick, 1998). 

The cell membrane shows a high capacity 

for endocytosis, i.e. the removal of excess membrane 

material and the uptake of specific molecules 

by membrane-bound receptors from the 

liquid medium of the environment. The occurrence 

of endocytosis has been controversial 

in filamentous fungi, but it has been obvious 

for some time that this must take place in 

S. cerevisiae as it is the route through which 

mating hormones are internalized and transported 

to the vacuole for degradation. While 

actin is certainly involved in endocytosis, it is 

still unclear whether the actin patches long 

known to exist inside the plasma membrane of 

S. cerevisiae cells are the scaffold around which 

the inward-budding of the plasma membrane is 

moulded (Shaw et al., 2001). Endocytosis occurs 

when pits are formed at the plasma membrane 

and bud inwards to form small vesicles (endocytotic 

vesicles) which fuse to form a tubular 

early endosome. From there, material is transported 

via a late endosome to the vacuole in 

which it is degraded (Munn, 2000; Shaw et al., 

2001). The protein ubiquitin plays a vital role as 

a tag for endocytosis at the plasma membrane 

and for transport of endosomes to the vacuole 

(Horák, 2003). The purposes of endocytosis could 

include the removal of excess membrane material, 

the removal of nutrient uptake systems


273 

no longer required, and the removal of mating 

type receptors, e.g. after the fusion of two 

haploid cells. 

10.2.6 The yeast vacuole 

The vacuole is the central destination of membrane 

trafficking in S. cerevisiae. It receives input 

directly from the secretory route in the form 

of most vacuolar proteins which are separated 

at the Golgi stage from those bound for secretion. 

Material also reaches the vacuole from 

the endocytotic route (see above), and from 

the cytoplasm, especially during starvation. 

Cytoplasmic material may be engulfed directly 

by the tonoplast (microautophagy) or redundant 

material may first be surrounded by a double 

membrane to form an autophagosome whose 

outer membrane then fuses with the tonoplast 

(macroautophagy). Details of these processes 

have been described by Klionsky (1997) and 

Thumm (2000). Degradation of protein is a 

major function of the vacuole in starvation 

situations, and about 40% of the total protein 

content of a yeast cell can be degraded 

within 24 h (Teichert et al., 1989). Not surprisingly, 

the vacuole contains a large set of powerful 

hydrolytic enzymes, especially proteases 

(Klionsky et al., 1990). 

When nitrogen is abundant, it is stored in 

the vacuole as arginine at concentrations of 

up to 400 mM, and this can be re-released into 

the cytoplasm if nitrogen becomes limiting 

(Kitamoto et al., 1988). Likewise, phosphate can 

be stored and released (Castro et al., 1999), as 

can many other ionic nutrients (Jennings, 1995). 

Toxic ions and metabolites may be stored in 

the vacuole (e.g. Ramsay & Gadd, 1997). Vacuoles 

thus fulfil a crucial function in maintaining 

the homeostasis of the yeast cytoplasm against 

changing external conditions. In order to fulfil 

such functions, the vacuolar morphology 

can change dramatically, e.g. by fragmentation 

of one large central vacuole into numerous small 

ones (Çakar et al., 2000). 

10.2.7 Killer yeasts and killer toxins 

Killer yeasts are strains which produce toxins 

capable of killing other strains belonging to the 

same or to closely related species. Toxin producers 

are resistant against their own toxin, but may 

be susceptible to toxins produced by other 

strains. Three important virus-encoded killer 

toxins (K1, K2, K28) are known to exist in 

S. cerevisiae; all three are polypeptides and are 

encoded by double-stranded RNA encapsulated 

in virus-like particles (VLPs). Another group of 

double-stranded viruses (the L-A viruses) belonging 

to the genus Totivirus is necessary for the 

replication of the killer toxin VLPs. The subject 

of killer yeasts has been reviewed by Magliani 

et al. (1997) and Marquina et al. (2002). 

The best-researched killer toxin is K1. It is 

encoded by a single open reading frame and 

is synthesized as a single polypeptide which is 

initially localized in the ER membrane. As the 

membrane-bound polypeptide travels the secretory 

route, it is modified by glycosylation and 

proteolytic cleavage, much like other secretory 

proteins. In the Golgi system, the polypeptide is 

cleaved into two parts which are held together 

by disulphide bonds, and a third part, the glycosylated 

region, which is not part of the active 

toxin. The active toxin is secreted and diffuses 

into the growth medium. The two parts of the 

active molecule fulfil two different functions; 

the b-chain binds the molecule to its receptor 

site which is the b-(1,6)-glucan component of 

the cell wall. Following binding to the wall, the 

toxin is thought to be transferred to the 

plasma membrane where the a-chain forms 

a trans-membrane pore. Death of the target cell 

occurs because the trans-plasma membrane 

proton and ionic gradients are disrupted. The 

toxin can bind to the wall of the producing 

cell but not to its plasma membrane; presumably 

a membrane receptor is altered, masked 

or destroyed. Self-immunity is conveyed by a 

precursor molecule of the mature toxin (Boone 

et al., 1986). 

The K1 toxin has been an important instrument 

in elucidating the processing of proteins 

along the secretory route, and the mechanism 

of cell wall synthesis in S. cerevisiae. Additionally, 

there are biotechnological implications. The 

possession of a killer toxin conveys a selective 

advantage upon a yeast strain, and killer yeasts 

are particularly common (25% of all isolates)


in habitats which contain abundant nutrients, 

such as the surface of ripe fruits (Starmer 

et al., 1987). Not surprisingly, contaminations 

by killer yeasts can be a problem in long-term 

fermentation processes, e.g. wine production 

(van Vuuren & Jacobs, 1992), and attempts have 

been made to incorporate the killer virus into 

yeast strains used for biotechnological purposes 

(Javadekar et al., 1995). Killer toxins 

cannot themselves be used against clinically 

relevant yeasts because the molecules are so 

large that they would elicit an immune response 

in the patient. However, it is possible to create 

antibodies which mimic the membrane-disrupting 

action of killer toxins (Polonelli et al., 1991). 

Whether these will become useful in medicine, 

e.g. against Candida infections, remains to be 

seen, but the existence of natural human 

antibodies with a killer toxin effect on Candida 

points to potential applications of this strategy 

(Magliani et al., 1997, 2005). 

10.2.8 Bread-making 

The principle behind the leavening of bread 

dough by baker’s yeast is the same as in brewing, 

i.e. the anaerobic metabolism of glucose and 

other reducing sugars via pyruvic acid into 

ethanol and CO 2 . The difference is that the 

released CO 2 is the important product in breadmaking 

because it is responsible for the texture 

of the bread. Ethanol may, however, contribute 

to the flavour of fresh bread. Originally, a portion 

of the risen dough medium was retained as 

a starter for the next baking session, or surplus 

yeast from brewing processes was used (Jenson, 

1998). Specific yeasts for baking were first 

produced in Vienna in 1846, and baker’s yeast 

is now produced commercially under aerobic 

conditions because the yield of biomass can be 

maximized (Caron, 1995). In the bread dough the 

yeast cells are subjected to anoxic or anaerobic 

conditions and must be able to release CO 2 

quickly. The carbon sources available to yeast 

cells in bread dough are hexoses, especially glucose, 

and the disaccharides maltose and sucrose, 

all of which are present at fairly low concentrations. 

Starch is not utilized by S. cerevisiae but can 

be hydrolysed by amylases present in the flour, 

and the glucose thereby released may be 

available to the yeast (Oliver, 1991; Jakobsen et 

al., 2002). A very thorough account of the 

microbiology and processes of baking is that 

by Spicher and Brümmer (1995). 

10.2.9 Beer brewing 

Several good accounts of the process of beer 

brewing have been given (e.g. Oliver, 1991; 

Russell & Stewart, 1995; Hartmeier & Reiss, 

2002), and there are numerous popular books 

exploring the diversity of beers worldwide. 

In his masterful history of beer, Hornsey (2003) 

has summarized evidence of the first known 

records and recipes of beer which date back 

6000 years or more and originate from Mesopotamia 

and ancient Egypt, where beer was more 

widely consumed than wine. The art of brewing 

may be almost as ancient as the cultivation 

of cereals, and indeed some historians believe 

that brewing was a major incentive for the 

development of agriculture around 6000 BC 

(Hornsey, 2003). Brewing has remained the 

most important area of biotechnology to this 

day. Astonishing quantities of beer are being 

consumed, with several sources agreeing on the 

Czech Republic as the top beer-drinking nation 

at around 160 l per person per annum, followed 

by the Republic of Ireland (155 l) and Germany 

(128 l). These values appear frugal when put 

into the historical context, e.g. of one gallon 

(3.8 l) as the daily personal allowance of ale for 

monks in medieval England (Hornsey, 2003). 

Two fundamentally different types of fermentation 

exist, and these differ in the strains of 

yeast used. In bottom-fermenting beers, especially 

lager beers, the yeast settles as a sludge at 

the bottom of the brewing vessel at the end 

of the fermentation, whereas it floats at the top 

in top-fermenting beers, especially the English 

ales, porters, stouts, and the German Altbier. In 

Germany, a purity law was passed in 1516 which 

banned the use of ingredients other than water, 

yeast, malted barley and hops. Although now 

formally abolished by the European Union, most 

brewers still abide by it. In contrast, ale and 

lager brewers outside Germany often add other 

ingredients to their beer, e.g. cereals other than 

barley, other fermentable sugar sources such


275 

as syrups or enzymatic starch digests, fruits or 

interesting spices. 

Since S. cerevisiae cannot utilize starch, this 

has to be hydrolysed into fermentable sugars 

first. The starch reserves in the endosperm of 

barley are hydrolysed naturally by endogenous 

amylases when the grains germinate. At a 

suitable time, the germination process is terminated 

by drying and heating (kilning), and the 

degree to which the malt is roasted determines 

the colour of the beer. For instance, heavily 

roasted malts are used for the dark milds, porter 

ales and stouts. During mashing, the ground 

malt is heated in water to about 65°C; surviving 

endogenous enzymes or added enzymes continue 

with starch hydrolysis, and with the 

degradation of proteins to amino acids. Hops 

are added to the liquid (wort) which is then 

boiled, traditionally in a copper vessel, and after 

filtration and cooling the yeast is added. Top 

fermentation of ales takes a few days at 15 22°C 

whereas lager beers are fermented for up to 

2 weeks at 8 15°C. In addition to ethanol, yeast 

metabolites which impart flavour to the beer are 

esters of higher alcohols (e.g. isobutanol), diketones, 

diacetyl, isobutyraldehyde and methylglyoxal. 

Sulphur-containing metabolites may also 

be important. There are several ways in which 

the flavour profile can be modified to give a 

desirable taste. For example, a yeast strain 

with the appropriate ester profile can be used, 

or new strains expressing the required enzymes 

can be engineered. A re-fermentation, often 

with Brettanomyces spp., may be performed in 

order to alter the flavour profile (Vanderhaegen 

et al., 2003). 

Towards the end of the fermentation, the 

yeast cells should flocculate, i.e. form aggregates. 

Flocculation is dependent on the expression of 

a number of surface proteins (flocculins) which 

recognize and bind to the mannose residues on 

mannoproteins located in the outermost wall 

layer of other yeast cells (Verstrepen et al., 2003). 

These flocculins are probably located in fimbriae, 

short hairs (0.5 mm long) on the cell surface 

which have been observed by ultrastructural 

studies (Day et al., 1975). Numerous environmental 

factors such as carbon and nitrogen deficiency, 

ethanol levels and cell age contribute to 

efficient flocculation, the control of which is one 

of the most difficult tasks in brewing. Whether 

flocculated yeast accumulates at the top or 

bottom of the vessel seems to depend on the 

flocculins as well as other wall surface properties 

(Dengis & Rouxhet, 1997). Attempts are being 

made to engineer improved brewer’s yeast 

strains with respect to their flocculation behaviour 

(Verstrepen et al., 2003) and also their ability 

to utilize other carbon sources, including starch 

(Hammond, 1995). 

Most beer in Europe is brewed in batch fermentations, 

but in other countries continuous 

cultures following the chemostat principle are 

performed. Either way, the ale or lager must be 

stored for a while before it is sterilized and 

filled into barrels or bottles. In the case of 

cask-conditioned Real Ales, the beer is filled 

directly into the casks and stored until it is ready 

to be sold to public houses; cask-conditioned ale 

is therefore in direct contact with the yeast until 

it is served to the customer. It requires skilled 

brewers and publicans to keep cask-conditioned 

Real Ale, but it does, in the opinion of many, 

result in a superior pint. 

10.2.10 Wine production 

Wine is the fermentation product of starting 

materials which already contain high levels of 

monosaccharides, i.e. typically fruit juices and 

especially the must of grapes. Wine is at least 

as ancient as beer and seems to have originated 

in Transcaucasia and the Near East in the early 

Neolithic, around or before 6000 BC (McGovern, 

2003). One of the pre-requisites for wine-making 

was the invention of pottery, since the fermentation 

process requires anaerobic conditions. Wine 

has been given a special place in many civilizations 

by its association with religious ceremonies, 

e.g. in ancient Egypt, Greece, Rome and in 

Christianity. In France, Portugal, Luxemburg 

and Italy, more than 50 l wine are consumed 

per person per annum. 

Red wine takes its colour (and high tannin 

content) from the skin of the grapes which 

are macerated, and the juice (‘must’) is left in 

contact with the solid parts for some time. In 

contrast, in white wine and rosé wine, the must


is extracted rapidly from the white or red grapes, 

respectively. Once the must has been obtained 

and filtered, subsequent treatment is similar 

for red, rosé and white wines. The must is either 

fermented directly, relying on the natural yeast 

flora of the grapes (‘spontaneous fermentation’), 

or a pure yeast starter culture is added at such 

high concentrations that this strain suppresses 

the wild yeasts. Spontaneous fermentations still 

account for 80% of the worldwide wine production, 

and up to 100 000 wild yeast cells mostly 

not belonging to S. cerevisiae may be found on 

the surface of one berry or in 1 ml must (Dittrich, 

1995). The diversity of yeasts changes rapidly 

during the initial stages of the wine fermentation, 

with S. cerevisiae displacing the obligately 

aerobic species as oxygen becomes depleted. The 

total fructose and glucose content of musts may 

be as high as 150 g l 1 . In principle, fermentation 

is completed when no further release of CO 2 

occurs, either due to exhaustion of sugars or due 

to ethanol poisoning of the yeast, but in practice 

fermentations are often terminated artificially 

by addition of sulphite, especially if a sweet wine 

is desired. 

Fermentation may carry on for up to 1 year 

with white wine; red wine develops faster but 

is often stored in barrels for prolonged periods to 

permit maturation. If red wine is stored in oak 

wood, it is called ‘barrique’ wine and it acquires 

a characteristic additional flavour. Good concise 

accounts of the processes and microbiology of 

wine making are those of Dittrich (1995) 

and Hartmeier and Reiss (2002). 

10.2.11 Production of sake¤ 

Saké production (for a review, see Oliver, 1991) 

involves the conversion of rice starch into monosaccharides 

which are then fermented into 

ethanol. Saké is thus technically a beer rather 

than a wine. It has been produced for several 

thousand years in China, but its current production 

principles based on the synergistic action 

of two fungi date back to the fifth century AD. 

Saké production relies on the degradation of 

starch in cleaned and boiled rice by a filamentous 

fungus, Aspergillus oryzae, which produces 

several different amylases as well as proteases 

and other enzymes (see p. 302). Koji, a solid 

culture of A. oryzae on steamed rice, is used as 

a starter for starch hydrolysis. 

Fermentation (moromi) is carried out in 

a large volume of water to which successive 

quantities of boiled rice, koji and the S. cerevisiae 

starter culture (moto) are added. Stepwise addition 

and a highly ethanol-tolerant yeast strain 

ensure that saké is the most strongly alcoholic 

beverage produced by fermentation without 

distillation, containing up to 20% (v/v) ethanol. 

Fermentation takes about 25 days and is followed 

by storage, maturation and filtration. In order 

to avoid contamination by lactic acid bacteria, 

saké is pasteurized. It is interesting to note that 

this practice was introduced in the sixteenth 

century, 300 years before Pasteur. 

10.3 Candida (anamorphic 

Saccharomycetales) 

Candida is a very large genus of anamorphic 

Saccharomycetales, currently comprising some 

165 accepted species (Meyer et al., 1998; Kirk et al., 

2001), with new ones being described at a high 

frequency. The genus is polyphyletic (Kurtzman 

& Robnett, 1998). By far the best-known species 

is C. albicans, which is associated with human 

disease, and on which we will focus here. A very 

similar species, and possibly one which has 

been misdiagnosed as C. albicans in the past, is 

C. dubliniensis (Martinez et al., 2002). Other species 

(C. glabrata, C. inconspicua, C. krusei) may also cause 

opportunistic infections of man. In contrast, 

Candida utilis (now called Pichia jadinii; see 

p. 281) has been used for food and fodder 

production for over 80 years, and other Candida 

spp. are also suitable for this purpose (Boze et al., 

1995; Scrimshaw & Murray, 1995). 

Candida spp. are cosmopolitan and can be 

found in many ecological situations (Meyer et al., 

1998), e.g. the surface of fruits and other plant 

organs, rotting wood, the soil, sea water, or 

associations with mammals and insects (especially 

bees). Candida spp. can contaminate grape 

musts during the early stages of wine making

CANDIDA (ANAMORPHIC SACCHAROMYCETALES) 

277 

but are usually displaced by S. cerevisiae later. 

Candida albicans is slightly atypical of the genus 

in that it does not appear to be distributed 

widely in the environment and can be considered 

a commensal of humans and other warmblooded 

animals. 

10.3.1 Dimorphism in Candida albicans 

Candida albicans can grow as yeast cells, true 

septate hyphae, or pseudohyphae which are an 

intermediate form between these two extremes 

(see Fig. 1.1d). Thick-walled chlamydospores 

may be formed by hyphae or pseudohyphae. 

This dimorphism or polymorphism has long 

been thought to represent an important pathogenicity 

determinant, pathogenicity commonly 

being associated with hyphal growth whereas 

yeasts are indicative of saprotrophic commensal 

growth. The switch between yeast and hyphal 

states is reversible and is determined by an interplay 

of several factors, e.g. temperature (hyphae 

at 37°C, yeasts below), pH (hyphae at neutral 

pH, yeasts at acid pH), nutrient abundance 

(yeast growth) or deficiency (hyphal growth), 

and presence (hyphal growth) or absence 

(yeast growth) of blood serum. Thus, conditions 

which mimic the bloodstream encourage hyphal 

growth, whereas conditions as found on the skin 

or in mucosal linings tend to promote yeast 

growth. Candida albicans is a commensal colonist 

of most humans, occasionally causing skin 

lesions, but under exceptional circumstances it 

turns into a serious pathogen causing deepseated 

or systemic mycoses, especially when the 

host’s immune system is weakened, e.g. in 

AIDS sufferers or patients who have undergone 

an organ transplantation. From such infections, 

C. albicans is usually recovered in the 

hyphal form. 

The yeast and hyphal forms differ in many 

features which have a bearing on their ability 

to cause disease (Odds, 1994). For instance, 

hyphae are coated with mannoproteins which 

adhere strongly to mammalian proteins found 

in the membranes of cell surfaces. Such adhesive 

proteins (adhesins) take the shape of fimbriae 

projecting beyond the cell wall (Yu et al., 1994; 

Vitkov et al., 2002; see Fig 23.15). Enhanced 

adhesion may play a role in pathogenesis, 

especially when coupled with the invasive 

mode of growth displayed by hyphae (Gow 

et al., 1999). Further, hyphae secrete aspartyl proteases 

and lipases capable of degrading host 

tissue (Hube & Naglik, 2001). Mannoproteins as 

well as proteases are potential targets for new 

anti-Candida drugs. 

Yeast-hyphal dimorphism in C. albicans has 

been investigated in some detail. The signalling 

chains leading to the formation of a hypha are 

extremely complex, involving cyclic AMP as well 

as mitogen-activated protein kinase (MAP kinase) 

pathways. Both are also involved in the switch 

from yeast cells to pseudohyphal growth in 

S. cerevisiae (Brown & Gow, 2002). An extensive 

cross-talk between different signalling pathways 

is not surprising, since the switch from yeast to 

hypha responds to many different environmental 

signals which need to be integrated. The 

control mechanisms determining the switch 

from yeast to (pseudo)hyphal growth may also 

be similar between S. cerevisiae (see Section 10.2.4) 

and C. albicans. 

10.3.2 Mating and switching in 

Candida albicans 

Whereas C. albicans is permanently diploid, other 

Candida species such as C. glabrata are haploid. 

An exclusively diploid vegetative phase is very 

unusual among true fungi, although it is found 

in Protomyces (Archiascomycetes; see p. 251) 

or Xanthophyllomyces (Heterobasidiomycetes; see 

Fig. 24.3) and, of course, in the Oomycota 

(see Chapter 5). Until recently, C. albicans was 

thought to reproduce strictly asexually. However, 

when the genome sequence of C. albicans became 

available and was examined closely, a complete 

set of genes relevant to mating, homologous 

with those known for S. cerevisiae, was detected, 

and it was found that the fungus is heterozygous 

for the two mating type idiomorphs a and 

a, similar to the diploid cells of S. cerevisiae but 

unable to sporulate. The signalling processes 

involved in mating are likely to be similar 

between S. cerevisiae and C. albicans (Bennett & 

Johnson, 2005), and conjugation in C. albicans has 

now been observed between diploid strains each


Fig10.8 Examples of 

white opaque switching in 

Candida albicans.(a)Cellsfroma 

white colony plated at low density. 

A switch has occurred from white 

(wh) to opaque (op). (b) A white 

colony which has been aged on a 

plate with limited gas exchange. 

This has caused increased rates of 

switching from white (wh) to 

opaque (op) at the colony edge. 

Original images kindly provided by 

D.R. Soll and K. Daniels. 

containing only either mating type, although 

karyogamy was doubtful and meiosis was not 

observed (Magee & Magee, 2000; Lockhart et al., 

2003). If tetraploid strains result from karyogamy 

in nature, these may undergo meiosis or random 

loss of chromosomes by a parasexual cycle, 

i.e. C. albicans may have a cryptic sexual phase 

in its life cycle which has eluded mycologists 

for over a century (Gow, 2002). Wong et al. (2003) 

have suggested that Candida glabrata has a 

similarly cryptic sexual cycle. 

In contrast to S. cerevisiae, there are no silent 

additional copies of mating type idiomorphs 

in the genome of C. albicans. Before a diploid 

strain of C. albicans heterozygous for mating 

type idiomorph (i.e. a/a) can mate, it will therefore 

have to convert to a/a or a/a by a mechanism 

different from the mating type switch based 

on a cassette system as found in S. cerevisiae 

(see p. 266). 

A remarkable phenomenon that has been 

known for some time is the spontaneous and 

reversible switching of yeast colony phenotypes 

in C. albicans. A given strain can switch its colony 

morphology between smooth, wrinkled or starlike, 

and white or opaque (Fig. 10.8). The 

latter switch is particularly well-characterized 

(Slutsky et al., 1987; Soll, 2002) and occurs at 

an unusually high frequency (about one colony 

in 1000 10 000). The different morphological 

appearances of white and opaque colonies are 

due to differences in size, shape and surface 

properties of the yeast cells. Genetically, the 

switch is accompanied by the co-ordinated upor 

down-regulation of numerous genes, some of 

them potentially involved in pathogenesis 

(Soll, 2003). Examples are secretory proteases 

or an ABC transporter involved in drug resistance 

(see p. 278). Not surprisingly, these two 

different colony types have widely differing 

pathogenic properties, the white-phase cells 

appearing to be better adapted to colonization 

of internal organs and opaque-phase cells superior 

in colonizing external skin regions. 

An interesting link between mating and 

switching is that the latter is suppressed in 

strains heterozygous for the mating type idiomorphs 

a and a. This may be mediated by the 

regulatory heterodimer presumably formed by 

protein products of the a and a idiomorphs. 

Another noteworthy observation involves sexual 

reproduction: opaque cells mate about 10 6 

times more efficiently than white cells (Miller & 

Johnson, 2002). Mating competence in C. albicans 

is therefore regulated at two levels, namely the 

requirement for a given cell to be homozygous 

for mating type (either a or a) and to be in the 

opaque state (Soll et al., 2003). It is furthermore 

possible that some of the phenotypes characteristic 

of opaque cells are required for mating, in 

addition to or instead of being pathogenicity 

factors. In this context, it is of interest that 

there is a mass switch from opaque to white 

at 37°C, and that mating between opaque cells 

of opposite mating type is strongly stimulated 

on skin surfaces which have a lower temperature 

(Lachke et al., 2003). Clearly, the ability of 

C. albicans to adapt to different situations by 

changing between several pre-programmed cell 

types, e.g. the mating-competent opaque and the 

invasive white cells, contributes to the success

CANDIDA (ANAMORPHIC SACCHAROMYCETALES) 

279 

of this organism as a pathogen (Staib et al., 2001; 

Bennett & Johnson, 2005). 

10.3.3 Treatment of candidiasis and 

resistance mechanisms 

Candida infections often occur following treatment 

with antibacterial antibiotics which also 

kill the benign bacteria which compete against 

Candida. Such superficial infections are especially 

common in mucosal linings of the mouth cavity, 

vagina or on the skin. They are collectively called 

‘thrush’. Infections of the oesophagus occur in 

patients with weakened immune system and are 

considered an AIDS-defining illness. The mucous 

membranes and skin are usually effective as 

primary barriers against infection, and Candida 

cells within the human body are vigorously 

attacked by the immune system (Murphy, 1996; 

Magliani et al., 2005). If all these barriers are 

broken or weakened, deep invasive candidiasis 

can occur. Yeast cells (conidia) can be disseminated 

in the blood stream, and individual organs 

can become colonized by hyphae. Contaminated 

catheters are also an important entry point 

for Candida. An extended account of candidiasis 

in all its forms has been given by Kwon-Chung 

and Bennett (1992). 

Generally, treatment of Candida infections 

is difficult because of the relative genetic similarity 

between Candida and humans, which 

greatly reduces the range of available targets 

as compared to the treatment of bacterial 

infections. Consequently, certain anti-Candida 

drugs have severe side effects. None the less, 

drugs belonging to several different classes 

are in current clinical use, as reviewed by 

Georgopapadakou (1998), Cowen et al. (2002) 

and Sanglard and Bille (2002). Lucid accounts of 

the fascinating array of mechanisms by which 

Candida achieves resistance against the various 

drugs are those by Ghannoum and Rice (1999), 

Sanglard (2002) and Akins (2005). 

Many drugs target ergosterol, a fungal 

membrane sterol which is not found in animals. 

Amphotericin B (Fig. 10.9a) or nystatin are 

polyene antibiotics which associate with ergosterol 

in the membranes of Candida, forming 

pores in the plasma membrane and thereby rendering 

it leaky. Amphotericin B has severe 

side effects but has to be used especially against 

deep-seated infections (Lemke et al., 2005). 

Resistance is usually based on the replacement 

of ergosterol by a precursor molecule, or a general 

reduction of the sterol content in the plasma 

membrane. 

Fig10.9 The most important anti-Candida drugs in current use. (a) The polyene compound amphotericin B. (b) The triazole 

compound fluconazole. (c) The allylamine terbinafine. (d) The fluoropyrimidine compound 5-fluorocytosine. (e) The echinocandin 

caspofungin.


The azole-type fungicides inhibit the enzyme 

lanosterol demethylase which is involved in 

ergosterol biosynthesis (see Fig. 13.16). A muchused 

example is fluconazole (Fig. 10.9b) which is 

free from severe side effects. There are several 

resistance mechanisms in C. albicans. The most 

common, found in 85% of all resistant isolates 

(Perea et al., 2001), is based on active exclusion of 

the drug by means of ABC (ATP binding cassette) 

transporters or similar mechanisms. These are 

plasma membrane proteins with numerous 

(usually 12) transmembrane domains and two 

cytoplasmic ATP-binding domains. Alternating 

binding and hydrolysis of ATP changes the conformation 

of these proteins, enabling them to 

open and close membrane pores. ABC transporters 

are often capable of transporting a group 

of different metabolites, thereby producing 

cross-resistance. The natural role of ABC transporters 

probably lies in the exclusion of endogenous 

antibiotics, toxins or other substances, e.g. 

mating factors in S. cerevisiae. The second most 

important type of resistance against azole-type 

drugs (65% of all isolates) is a mutation of the 

cellular target, i.e. the azole binding site on the 

enzyme lanosterol demethylase. The fact that 

the occurrences of these two types of resistance 

add up to more than 100% indicates that many 

clinical C. albicans isolates (about 75%) possess 

both resistance mechanisms. A third resistance 

mechanism against azoles is the overexpression 

of the gene ERG11 encoding lanosterol demethylase, 

which occurs in about 35% of resistant 

isolates (Perea et al., 2001). 

A third group of compounds, the allylamines 

(e.g. terbinafine; Fig. 10.9c) act against a different 

enzyme involved in ergosterol biosynthesis, squalene 

epoxidase (see Fig. 13.16). Terbinafine is 

not used extensively on its own, but it is useful 

in combination with other drugs in order to 

treat infections by resistant Candida strains. 

Another target, nucleic acid biosynthesis, 

is attacked by 5-fluorocytosine (Fig. 10.9d). 

Following uptake, it is deaminated to 5-fluorouracil 

and converted to 5-fluoro-UTP or a corresponding 

deoxynucleotide, which inhibit RNA 

and DNA biosynthesis, respectively. Resistance is 

associated with a reduced capacity of the fungus 

to metabolize 5-fluorocytosine. Mammalian cells 

do not efficiently metabolize this drug but intestinal 

bacteria can, which precludes the oral use 

of this antibiotic. 

A recently described group are the echinocandins 

which inhibit b-(1,3)-glucan synthesis. 

There is preliminary evidence that echinocandins 

such as caspofungin (Fig. 10.9e) do not 

act directly on b-(1,3)-synthase but in an indirect 

manner by interfering with upstream regulatory 

proteins (Edlind & Katiyar, 2004). No drugs 

against mannoproteins or aspartic proteases are 

as yet commercially available, although treatment 

against HIV uses protease inhibitors which 

also affect C. albicans (Dupont et al., 2000). 

Research efforts into new anti-Candida drugs are 

intensive, given that the incidence of Candida 

infections is strongly on the increase, few substances 

are currently available, and resistance of 

Candida against them is becoming a problem. 

10.3.4 Ecology and drug resistance of 

Candida albicans 

Numerous investigations of the distribution of 

Candida spp. on their hosts have been carried out. 

Generally, C. albicans is by far the most frequent 

species, followed by C. parapsilosis. Other species 

such as C. glabrata, C. krusei and C. tropicalis 

are very much less frequent. Within the species 

C. albicans, many different strains exist, and their 

colonization pattern has been followed on the 

same human host over time (Xu et al., 1999; 

Kam & Xu, 2002). Each human being can be 

colonized by a diversity of strains. Displacement 

of one strain by another is possible, as is the 

transfer of strains between humans. Appropriate 

analyses of allelic distributions have shown that 

the mode of genetic inheritance is predominantly 

clonal, i.e. sexual reproduction and 

the exchange of genetic material between different 

Candida strains do not seem to play an 

important role (Lott et al., 1999). There are no 

significant differences in the Candida populations 

between healthy individuals and AIDS 

patients unless, of course, the population 

dynamics are shaken up by anti-Candida drug 

treatments. In the course of a prolonged treatment 

of patients against oral candidiasis, 

Martinez et al. (2002) reported the displacement

GALACTOMYCES (DIPODASCACEAE) 

281 

of the initially predominant, fluconazolesensitive 

C. albicans flora by fluconazoleresistant 

C. dubliniensis strains especially in 

those patients where C. albicans had failed to 

develop resistance. Resistance may arise spontaneously 

after prolonged treatment, and the 

spread of resistant clones in hospitals may not 

be as important with Candida as, for example, 

with multiple drug-resistant bacteria (Taylor 

et al., 2003). 

processes of proteins of pharmacological interest 

(Daly & Hearn, 2005). 

10.5 Galactomyces (Dipodascaceae) 

The genus Galactomyces (formerly called Endomyces) 

is characterized by true hyphae which 

10.4 Pichia (Saccharomycetaceae) 

The genus Pichia contains 94 species (Kurtzman, 

1998; Kirk et al., 2001) and is characterized by 

budding cells, with only a few species also 

producing arthroconidia, pseudohyphae and 

hyphae. Sexual reproduction is by ascospores 

(1 4 per ascus) which are often hat-shaped 

(galeate). Molecular characterization of the 

genus is still in progress (Suzuki & Nakase, 1999) 

and will undoubtedly lead to rearrangements 

in future. 

Pichia is cosmopolitan and ubiquitous. A 

surprising number of species has been isolated 

from the frass of wood-attacking beetles 

(Kurtzman, 1998); others grow on the exudates 

(slime fluxes) of trees or on decaying cacti, or 

they occur as contaminants of industrial fermentations. 

Two species are of particular biotechnological 

interest: Pichia jadinii (anamorph Candida 

utilis), formerly called Torula yeast, has been 

developed since World War I as a food yeast 

for single-cell protein. It can utilize the pentoses 

of pulping-waste liquors from the paper industry 

and is also grown on other biological wastes 

(Boze et al., 1995). 

Pichia pastoris is interesting for a different 

reason; it can utilize methanol by expressing 

and secreting large quantities of alcohol oxidase. 

Since the protein glycosylation chains of 

P. pastoris are similar to those of humans, and 

because the products of heterologous genes are 

secreted efficiently, P. pastoris has advantages 

over S. cerevisiae in the industrial production 

Fig10.10 Galactomyces candidus. (a) Vegetative hyphal apex. 

The two lateral branches near the base are developing 

conidiophores. (b) Conidiophore showing the development 

and separation of arthroconidia. (c) Gametangia developing as 

lateral bulges of the hyphae on either side of a septum. 

(d) Fusion of gametangia to form asci. In one ascus, a single 

ascospore is differentiated. (e) Mature asci, each containing 

a single ascospore.


form septa and quickly fragment into arthrospores 

(Fig. 10.10), giving the colonies a creamy 

appearance. The septa have micropores, like 

those of true hyphae of C. albicans. Six species 

are now known; by far the most important is 

G. candidus (anamorph Geotrichum candidum), 

formerly known as Galactomyces geotrichum (de 

Hoog & Smith, 2004). It is a ubiquitous mould 

which is common in soil, dairy products, sewage 

and other substrata. It is also thought to be a 

common constituent of the skin and gut flora 

of humans and animals, although reports of 

it being a human pathogen have generally 

remained unsubstantiated (Kwon-Chung & 

Bennett, 1992). In addition, G. candidus is a wellknown 

cause of post-harvest rot in ripe fruits 

and vegetables especially when these are kept 

in plastic bags. Infected plant organs become 

soft and eventually, upon puncturing, exude 

a creamy mass of decaying tissue which has 

a sour smell; hence the name ‘sour rot’ (Agrios, 

2005). 

The fungus grows readily in culture, forming 

broad hyphae with finer lateral branches. The 

vegetative cells contain 1 4 nuclei. Branching 

is of two kinds, pseudodichotomous near the 

apex, and lateral immediately behind a septum. 

It is from such lateral branches that conidia 

develop (Figs. 10.10a,b). Conidiophores are difficult 

to differentiate from vegetative hyphae. 

Prior to conidium formation, apical growth of 

a hypha ceases, then septa are laid down in the 

tip region. The septa are two-ply, and separation 

of the two layers making up the septum 

leads to the disarticulation of the terminal part 

of a hypha into cylindrical segments termed 

arthrospores or arthroconidia (Cole & Kendrick, 

1969b). Conidia of other Galactomyces spp. are 

virtually indistinguishable from those of 

G. candidus. 

Galactomyces candidus may be homo- or heterothallic, 

but the sexual state is not frequently 

seen. After mating, fertile hyphae are produced 

and gametangia arise in pairs on either side of 

a septum, in the broad main hyphae or short 

side branches (Figs. 10.10c e). Fusion of the 

gametangia gives rise to a globose fusion cell 

which becomes transformed directly into an 

ascus. The ascus contains only a single ascospore 

which has two wall layers, a smooth inner layer 

and a furrowed outer layer. Each ascospore 

contains 1 2 nuclei. Whether and when meiosis 

occurs is not yet known. 

The Geotrichum arthroconidial state is found 

also in the only other genus of the Dipodascaceae, 

Dipodascus, which produces multispored 

asci with 4 128 spores. A superficially similar 

state, Saprochaete, is formed by a genus of phylogenetically 

unrelated fungi now called Magnusiomyces. 

Species descriptions and a key of 

Galactomyces, Dipodascus and Magnusiomyces have 

been provided by de Hoog and Smith (2004). 

10.6 Saccharomycopsis 

(Saccharomycopsidaceae) 

Saccharomycopsis (formerly Endomycopsis) is a mycelial 

yeast which reproduces by buds (blastospores 

or yeast cells) and also forms asci parthenogenetically 

or following isogamous fusion. About 

10 species are known (Kurtzman & Smith, 1998; 

Barnett et al., 2000). Saccharomycopsis fibuligera 

grows in flour, bread, macaroni and other 

starchy substrates, and produces a complex of 

numerous active extracellular amylases, an 

unusual property in yeasts (Hostinová, 2002). 

This has been used to develop S. fibuligera as 

a food yeast for cattle feed which can be grown 

on potato starch processing wastes (Jarl, 1969). 

This species is also used extensively for starch 

hydrolysis by starter cultures in Far Eastern 

fermented food (Beuchat, 1995). 

In culture, S. fibuligera may form budding 

yeast cells and branched septate hyphae which 

produce blastospores laterally and terminally 

(Fig. 10.11). Arthrospore formation has also 

been demonstrated. Ascus formation in this 

homothallic species can be induced by growing 

the yeast for a few days on malt extract agar 

and transferring it to distilled water. The asci 

are mostly four-spored, and the spores are 

hat-shaped (Fig. 10.11d), having a flange-like 

extension of the wall.

SACCHAROMYCOPSIS (SACCHAROMYCOPSIDACEAE) 

283 

Fig10.11 Saccharomycopsis fibuligera. (a,b) Mycelium from three-day-old culture showing blastospore formation. (c) Blastospores 

germinating by germ tube, or budding to form a further blastospore. (d) Ayoung ascus and two mature asci containing four 

hat-shaped ascospores. (e) Germinating ascospore. (a,c e) to same scale. 

Fig10.12 Scanning electron micrographs of Saccharomycopsis javanensis preying upon Saccharomyces cerevisiae. (a) Points of 

penetration (arrowheads) at an early stage. Also note the bud-scars on an older S. cerevisiae cell in the centre of the picture. 

(b) Collapsed cells of penetrated prey (arrows) at a later stage.Original images kindly provided by M.-A. Lachance. Reprinted 

from Lachance et al. (2000) by copyright permission of the National Research Council of Canada.


Fig10.13 Eremothecium coryli.(a)Vegetative 

growth as a mass of hyphae and yeast cells. (b) 

Ascus containing eight ascospores. Both 

images to same scale. 

Most members of the genus Saccharomycopsis 

have been observed to behave as predacious 

yeasts on leaf surfaces, i.e. they attack, penetrate 

and digest the cells of other yeasts (Fig. 10.12). 

This phenomenon is different from that of killer 

yeasts because no toxins appear to be involved. 

Instead, penetration and killing is brought 

about mainly by cell wall-degrading enzymes, 

notably b-(1,3)-glucanase (Lachance et al., 2000). 

It is interesting to note that all those yeasts 

capable of preying on others are incapable 

of utilizing sulphate as a source of sulphur, 

although not all yeasts deficient in sulphate 

transport are predacious. Predation can be cannibalistic, 

but many other yeasts belonging to 

the Asco- and Basidiomycota are also attacked. 

Clearly, the phylloplane is a highly competitive 

environment. 

10.7 Eremothecium 

(Eremotheciaceae) 

This genus contains five species which were 

formerly classified in different genera but have 

now been shown to be closely related by DNA 

sequence analyses (Kurtzman, 1995; de Hoog 

et al., 1998). Pseudohyphae and true hyphae are 

present in culture, and vegetative reproduction 

is often by budding yeast cells. Asci are formed 

terminally or in intercalary positions, and 

they contain 8 32 needle-shaped ascospores 

(Fig. 10.13). 

Eremothecium spp. are the only important 

plant pathogens among the Hemiascomycetes 

and can infect numerous plant species, causing 

damage especially on cotton (Gossypium spp.). 

They are transmitted by hemipteran insects 

which may harbour inoculum in their stylet 

pouches. The route of entry into the plant 

is often via the stigma of the flower (Batra, 

1973). Eremothecium (formerly Nematospora) coryli 

(Fig. 10.13) causes a disease called stigmatomycosis 

on a wide range of plants, including hazel 

(Corylus). 

In biotechnology, E. ashbyi and E. (Ashbya) 

gossypii are used in fermentations for the

11 

Plectomycetes 


The class Plectomycetes originally contained all 

ascomycetes which produce their asci within a 

cleistothecium, i.e. a ‘closed case’. DNA sequence 

comparisons have revealed that this character 

was a fairly good one because, with the major 

exception of the powdery mildews (Erysiphales; 

see Chapter 13) and few scattered examples in 

the Pyrenomycetes (Chapter 12) and Helotiales 

(Chapter 15), most cleistothecium-forming fungi 

and the anamorphs associated with them have 

been found to be monophyletic (Berbee & Taylor, 

1992a; Geiser & LoBuglio, 2001). As they stand 

now, the Plectomycetes can be defined by the 

following set of characters (Alexopoulos et al., 

1996; Geiser & LoBuglio, 2001). 

(1) A cleistothecium or gymnothecium is 

usually present; a cleistothecium proper has a 

thick and continuous (pseudoparenchymatous) 

wall, whereas in the gymnothecium the wall 

consists of an open cage-like construction 

of hyphae, the reticuloperidium (Greif & 

Currah, 2003). Naked asci are produced only in 

rare cases. 

(2) Ascogenous hyphae are usually not 

conspicuous. 

(3) Asci are scattered throughout the cleistothecium, 

not produced by a fertile layer 

(hymenium). 

(4) Asci are mostly globose and thin-walled, 

and the ascospores are released passively after 

disintegration of the ascus wall, not by active 

discharge. 

(5) Ascospores are small, unicellular and 

usually spherical or ovoid. 

(6) Conidia are commonly produced from 

phialides (in Eurotiales) or as arthroconidia, 

which are typically formed as chains of conidia 

alternating with sterile cells. An arthroconidium 

becomes released when the neighbouring cells 

disintegrate. This rhexolytic secession is typical 

of the microconidia of Onygenales and 

Ascosphaerales. The alternative is schizolytic 

secession in which adjacent cells separate when 

the septum joining them splits into two (see 

Figs. 8.9, 10.10), but this is not found in the 

Plectomycetes. However, terminal thick-walled 

chlamydospores and multicellular blastic macroconidia 

may be produced by some Plectomycetes. 

Plectomycetes are predominantly saprotrophic 

fungi associated with the soil. Many have 

a capacity to degrade complex biopolymers, e.g. 

starch and cellulose, while others degrade 

proteins such as keratin which makes up hair, 

horn and feathers. If proteolytic fungi can grow 

at 37°C, they are potentially pathogenic to 

mammals, and some of them are indeed among 

the most dangerous fungal pathogens of man. 

Many other Plectomycetes produce important 

secondary metabolites, e.g. antibiotics and 

mycotoxins. 

Several taxonomic arrangements have been 

proposed for the Plectomycetes (e.g. Kirk et al., 

2001; Eriksson et al., 2003), but we have chosen 

that of Geiser and LoBuglio (2001) because of its 

clarity. This divides the Plectomycetes into three 

orders, the Ascosphaerales, Onygenales, and 

Eurotiales (Table 11.1). We will consider

286 PLECTOMYCETES 

Table 11.1. Classification of Plectomycetes following Geiser and LoBuglio (2001) and Kirk et al. (2001). 

Order Family No. oftaxa Examples of 

teleomorphs 

Examples of 

anamorphs 

Ascosphaerales 

(see Section11.2) 

Onygenales 


Eurotiales 


Ascosphaeraceae 3 gen.,13 spp. Ascosphaera (mostly unknown) 

Eremascaceae 1gen., 2 spp. Eremascus (unknown) 

Onygenaceae 

(see p. 290) 

Arthrodermataceae 

(see p. 293) 

Gymnoascaceae 

(see p. 295) 

Myxotrichaceae 

(see p. 295) 

Trichocomaceae 

(see p. 297) 

22 gen.,57 spp. Ajellomyces, 

Auxarthron, 

Amauroascus, 

Onygena 

Malbranchea, 

Chrysosporium, 

Coccidioides, 

Histoplasma, 

Paracoccidioides, 

Blastomyces 

2gen.,48spp. 

Ctenomyces, Chrysosporium, 

Arthroderma Microsporum, 

Epidermophyton, 

Trichophyton 

10 gen., 23 spp. Gymnoascus (mostly unknown) 

4gen.,12spp. Myxotrichum Geomyces, 

Malbranchea, 

Oidiodendron 

20 gen., 4500 spp. Byssochlamys, 

Emericella, 

Eupenicillium, 

Eurotium, 

Talaromyces 

Aspergillus, 

Paecilomyces, 

Penicillium 

Monascaceae 2 gen.,7 spp. Monascus Basipetospora 

Elaphomycetaceae 1gen.,20 spp. Elaphomyces (unknown) 

(see p. 313) 

representatives from all three orders, with a 

particular emphasis on the Eurotiales which 

contain the important anamorphic genera 

Aspergillus and Penicillium. 

11.2 Ascosphaerales 

This small order currently comprises the 4 

teleomorphic genera Arrhenosphaera (1 species), 

Ascosphaera (11 species), Bettsia (1 species) and 

Eremascus (2 species). The first three genera are 

associated with beehives whereas Eremascus is 

a food-spoilage fungus. All genera can grow on, 

and sometimes require, substrates rich in sugar 

or salt. Some species are truly xerophilic, i.e. they 

can grow at water activities (a W ) lower than 0.85, 

which is equivalent to a solution containing 

60% glucose. Ascosphaerales are atypical of 

the Plectomycetes because they do not produce 

true cleistothecia, but DNA-based phylogenetic 

studies have shown that they belong here (Berbee 

et al., 1995). 

11.2.1 Eremascus 

In mycology as in many other areas of biology, 

it is virtually impossible to establish a rule without 

having to qualify it almost immediately 

by giving exceptions and modifications to it. 

Eremascus is a member of the Euascomycete clade 

with free asci which are not organized into

ASCOSPHAERALES 

287 

ascocarps, and it is thus an exception to the 

generalization which places such fungi in the 

Archiascomycetes (Chapter 9) or Hemiascomycetes 

(see Eremothecium, Galactomyces, Saccharomycopsis; 

Chapter 10). Support for the inclusion of 

Eremascus in the Euascomycetes comes not only 

from molecular data (Berbee & Taylor, 1992a; 

Anderson et al., 1998) but also from the presence 

of typical Euascomycete septa with one central 

pore and associated Woronin bodies (Kreger-van 

Rij et al., 1974). Further, the arthroconidia are 

delimited by a double-septum (Harrold, 1950) 

and are released by rhexolytic secession, which is 

typical of certain Plectomycetes (see Fig. 11.3f). 

Two species are known, E. albus and E. fertilis 

(Fig. 11.1). Both are associated with sugary substrates 

such as mouldy jam, but several collections 

of E. albus have been made from powdered 

mustard. Harrold (1950) has shown that both 

fungi grow best on media with a high sugar 

content (e.g. 40% sucrose), but do not grow well 

in a water-saturated atmosphere. The mature 

mycelium consists of uninucleate segments. 

Both species are homothallic. On either side of 

a septum, short gametangial branches arise 

which are swollen at their tips and, in the case 

of E. albus, coil around each other. The gametangial 

tips of E. albus are usually uninucleate and, 

following breakdown of the wall separating the 

tips of adjacent gametangia, nuclear fusion 

occurs. This is followed by meiosis and mitosis 

so that eight nuclei result, each one being 

surrounded by cytoplasm to form a uninucleate 

ascospore (Fig. 11.1m). The ascospores are 

dispersed passively following breakdown of the 

ascus wall. On germination a multinucleate germ 

tube emerges, but the uninucleate condition is 

soon established by the formation of septa. 

11.2.2 Ascosphaera 

Ascosphaera spp. are associated with bees and 

related insects, growing saprotrophically in their 

nests on the gathered pollen and nectar. They can 

be maintained in pure culture but commonly 

Fig11.1 Eremascus.(a d) Eremascus fertilis, stages in the development of asci. (e g) Eremascus albus, stages in the development 

of asci. Note the coiling of the gametangia and the globose ascospores of E. albus.(h m) Eremascus albus, nuclear behaviour 

during ascus formation (after Harrold,1950). (h) Uninucleate gametangia. (i) Plasmogamy and karyogamy. (k m) Nuclear divisions 

preceding ascospore formation.


Fig11.2 Ascosphaera apis. (a) Dead infected bee larvae. (b) Young sporocyst. (c) Several intact mature sporocysts. (d) Ruptured 

sporocyst with released ascospore balls. 

require up to 40% glucose in the medium. On 

lower-strength agar media they may still grow but 

often fail to produce ascospores. Ascosphaera apis is 

a pathogenic species causing ‘chalk brood’ disease 

of honey bees (Apis mellifera). Dead infected larvae 

appear white and hard like chalk (Fig. 11.2a), and 

black spore balls may break through the integuments 

(Skou, 1972, 1975, 1988). The disease occurs 

as an epidemic in some years and can seriously 

weaken bee colonies, especially if accompanied by 

pests such as Varroa mite infestations. 

Some species are homothallic but A. apis is 

heterothallic. Ascospores are produced in a 

unique structure termed a sporocyst (Skou, 

1982). The ‘female’ colony produces an ascogonium 

terminating in a trichogyne, and plasmogamy 

occurs between the trichogyne and an 

undifferentiated hypha of the opposite mating 

type. Following plasmogamy, the trichogyne 

grows backwards into the ascogonium, the wall 

of which swells greatly to form the sporocyst 

(Fig. 11.2b; Spiltoir, 1955). When it is mature, 

the sporocyst acquires a brown pigmentation 

(Figs. 11.2c,d). Within the sporocyst, a system of 

binucleate cells with croziers forms eight-spored 

asci in clusters. The ascus walls are evanescent, 

and the ascospores from the asci of any one 

cluster stick together as spore balls which are 

released when the sporocyst wall breaks 

(Figs. 11.2c,d). The sporocyst is not homologous 

with a cleistothecium because it arises 

from a single cell which enlarges prior to formation 

of the asci, whereas a cleistothecium is 

multicellular and grows around the developing 

asci. 

In order to produce ascospores on infected 

bee larvae, A. apis requires a slight reduction of 

temperature (normally around 33 36°C in intact 

hives) to about 30°C. Infections by A. apis are 

usually most severe in cool weather, especially 

in spring. Interestingly, bee colonies have been 

found to respond to A. apis infections by 

elevating their temperature, and this so-called 

‘behavioural fever’ may retard the outbreak of 

the disease (Starks et al., 2000). A further way for 

bees to control the disease is hygiene, i.e. they 

uncap brood cells and remove dead larvae before 

A. apis can sporulate on them. Bees can be bred 

for hygiene, and the basis of this is thought 

to be an enhanced sensitivity to the odour of

ONYGENALES 

289 

infected larvae rather than hygienic behaviour 

per se which is instinctive (Masterman 

et al., 2001). Larvae become infected by A. apis 

by ingestion. Many types of commercially available 

honey contain viable spores of A. apis 

(Anderson et al., 1997). 

11.3 Onygenales 

This order of the Plectomycetes is of utmost 

significance to medical mycologists because it 

contains most of the true human pathogens, i.e. 

fungi able to cause disease in otherwise healthy 

and immunocompetent individuals. Some taxonomic 

confusion has arisen because many of the 

serious pathogens have been known for a long 

time only in their anamorphic form and continue 

to be called by their anamorphic names. The 

current Dictionary of the Fungi (Kirk et al., 2001) 

recognizes three families Arthrodermataceae, 

Gymnoascaceae and Onygenaceae but it 

excludes the family Myxotrichaceae which is of 

uncertain placement (incertae sedis), possibly 

belonging to the Helotiales (Tsuneda & Currah, 

2004). Since members of this last family have 

many features in common with the other three, 

we will consider them briefly here. Including the 

Myxotrichaceae, there are some 120 species in the 

Onygenales. 

Defining features of the Onygenales are that 

their ascoma consists of loosely interwoven and 

often thick-walled hyphae which sometimes bear 

complex and species-characteristic appendages 

(Figs. 11.3a, 11.5, 11.8, 11.9). Such a cage-like 

ascoma is termed gymnothecium, and the 

meshwork of hyphae making up the basket 

(peridium) is called reticuloperidium. Greif 

and Currah (2003) have shown that the reticuloperidium 

can be pierced by the stiff hairs of 

arthropods such as flies, and gymnothecial 

appendages may also be caught by the limbs 

of flies during grooming. Movements by the 

animals shake the ascospores out of the 

Fig11.3 Onygenaceae. (a) Quarter-segment of a gymnothecium of Ajellomyces capsulatus showing coiled appendages. (b) Ascospore 

of A. capsulatus. (c) Tuberculate macroconidia of Histoplasma capsulatum. (d) Microconidia of H. capsulatum. (e) The‘pilot wheel’ stage 

of Paracoccidioides brasiliensis. One giant yeast cell is producing several buds. (f) Malbranchea-type arthroconidia.The conidia are 

released by rhexolytic secession, i.e. conidia are spaced apart by sterile cells which eventually disintegrate. (a,c e) to same scale. 

Redrawn and modified from de Hoog et al. (2000a), with kind permission of Centraalbureau voor Schimmelcultures.


Fig11.4 Onygena. (a) Stalked gymnothecial stromata of 

O. equina on a cast sheep’s horn. (b) Ascogenous hyphae and 

asci of O. corvina. 

gymnothecium and distribute them. Thus, the 

gymnothecium may be an adaptation to dispersal 

by arthropods. 

The asci are formed loosely throughout the 

gymnothecium. Asci are eight-spored and evanescent, 

releasing their ascospores passively. Ascus 

development is similar to that in other higher 

ascomycetes, with the cytoplasm being delimited 

by two membranes between which the ascospore 

wall is laid down. The inner membrane 

eventually becomes the ascospore plasma membrane 

(Ito et al., 1998). The anamorphic states are 

usually more readily seen than the teleomorph 

and typically consist of rhexolytic arthrospores, 

although thick-walled chlamydospores are also 

sometimes present. 

Members of the Onygenales are cosmopolitan, 

although many individual species have a very 

limited distribution. Thankfully, this is true especially 

of many of the human pathogens. Most 

species, including the pathogenic ones, are soilborne 

and associated with keratin-containing 

substrates such as hair, hooves, feathers and 

the dung of carnivores (Hubalek, 2000). An 

excellent review of the order has been compiled 

by Currah (1985); Geiser and LoBuglio (2001) and 

Sugiyama et al. (2002) have discussed phylogenetic 

aspects. 

11.3.1 Onygenaceae 

This family contains 22 genera and 57 species 

and includes the most important human pathogens. 

The anamorphic states are arthrosporic 

with rhexolytic secession (e.g. Malbranchea; 

Fig. 11.3f), or solitary terminal spores are produced 

which may be unicellular (Chrysosporiumlike) 

or multicellular. The ascospores carry 

ornamentations (spines, pits or reticulations). 

The gymnothecia often have a few conspicuously 

large coiled hyphae (see Fig. 11.3a). Kwon-Chung 

and Bennett (1992), de Hoog et al. (2000a) and 

Sigler (2003) have given accounts of the most 

important pathogens; these are associated 

with the teleomorph genus Ajellomyces (Guého 

et al., 1997), although gymnothecia are seldom 

formed and the species are better known by 

their anamorphic names. Histoplasma capsulatum, 

Blastomyces dermatitidis and Paracoccidioides 

brasiliensis are particularly closely related to 

each other, and this grouping has been given 

family status by Untereiner et al. (2004), with 

Coccidioides immitis being less closely related and 

retained in the Onygenaceae. We shall consider 

these four pathogenic species together because 

of their medical importance. It is not permitted 

to work with them in standard laboratories 

because they are among the handful of fungi 

currently listed in hazard category 3 (Kirk et al., 

2001). Teleomorph genera other than Ajellomyces 

are Auxarthron, Amauroascus and Onygena; the 

latter, being the type of the family, is also briefly 

considered (p. 293).

ONYGENALES 

291 

Onygenaceae as human pathogens 

The salient features of the four important 

human pathogens are listed below. The points 

at which C. immitis differs from the other three 

are indicated. 

1. All four species are probably mainly 

saprotrophic in the soil, having become serious 

pathogens mainly because of their ability to 

grow at 37°C, evade the human immune system, 

bind to human tissue, and produce proteases. 

Pathogenicity is probably coincidental and 

represents a dead end in the life cycle of these 

fungi because the transmission of inoculum 

from infected humans to the environment or 

to other humans is negligible (Berbee, 2001). 

Infection of humans occurs by inhalation of 

microconidia produced in the soil. These are 

sufficiently small to penetrate into the alveoli of 

the lung. There, yeast-like stages are formed 

which are the agents of disease. This is in contrast 

to Candida albicans where hyphae rather 

than yeast cells represent the invasive stage. 

2. All species are dimorphic, with a 

temperature-dependent switch from hyphae 

(27°C) to yeast (37°C). In C. immitis, instead of 

producing yeast cells at 37°C, the conidium 

swells to produce an endospore-forming cyst or 

spherule. In all four species, however, the switch 

is relatively simple because the temperature shift 

is sufficient to trigger it. This differs from C. 

albicans in which the switch from yeast-like to 

hyphal growth is influenced by a complexity of 

environmental factors (see p. 277). 

3. Pulmonary infections may take the form 

of influenza-like symptoms in the majority of 

immunocompetent patients but sometimes 

develop into more severe tuberculosis-like 

illnesses. Following initial infection, yeast cells 

(or endospores) can be disseminated, causing 

systemic mycoses in other organs. In the case of 

mild infections, patients may make a complete 

recovery and may then possess lifelong immunity. 

This observation raises the possibility that 

vaccines may be developed against these pathogens 

(Cox & Magee, 2004; Nosanchuk, 2005) and 

also against Candida albicans and other fungi 

(Magliani et al., 2005). 

4. The yeast cells of P. brasiliensis, 

H. capsulatum and B. dermatitidis are internalized 

by macrophages of their human hosts, but they 

have a remarkable ability to survive and even 

reproduce inside the lytic vacuoles by raising the 

intravacuolar pH and withstanding the attack 

of the lytic enzymes and the ‘oxidative burst’ 

created by the macrophages. Yeast cells inside 

macrophages represent latent inoculum which 

can cause relapses many years after the initial 

infection, especially when the host’s immune 

system becomes weakened by other causes. Thus, 

these three species have been likened, in terms of 

their pathology, to the bacterium Mycobacterium 

tuberculosis (Borges-Walmsley et al., 2002; Woods, 

2002). 

5. Even prolonged chemotherapy may not 

altogether eliminate the pathogens. The drugs in 

common current use are similar to those applied 

against C. albicans (p. 278) and include amphotericin 

B and azole-type compounds (Harrison & 

Levitz, 1996). Since long treatment periods are 

required to control these diseases effectively, 

the side effects of the drugs in current use are 

problematic. The anti-Candida drug caspofungin 

(see Fig. 10.9e) also shows promise against 

onygenalean pathogens (Letscher-Bru & 

Herbrecht, 2003). 

6. Diseases caused by all four pathogens are 

much more prevalent in men than in women, 

often by a ratio of 10 : 1 or higher. This is due to 

the inhibitory effects of oestrogen and other 

female steroid hormones on the conidium yeast 

transition (Hogan et al., 1996; Aristizabal et al., 

1998). 

Ajellomyces capsulatus (anamorph Histoplasma 

capsulatum) 

Gymnothecia of this species (Fig. 11.3a) are easily 

recognized, with a few conspicuous coiled 

appendages and very small ascospores (


Histoplasma capsulatum grows as a mycelium 

at room temperature, but at 37°C it develops 

small budding yeast cells (3 5 mm) which can 

spread throughout the patient under favourable 

conditions. The normal route of infection is by 

inhalation, especially of the small microconidia. 

One common way to become infected is by 

cleaning buildings of bird or bat excreta, or by 

exploring caves in which these animals dwell; 

histoplasmosis is therefore also called the 

‘spelunker’s disease’ (Woods, 2002). Three strains 

of H. capsulatum are distinguished, and they are 

present in soil, especially when contaminated 

with bird or bat guano. Endemic areas are North 

America (var. capsulatum) or equatorial Africa 

(var. duboisii). Histoplasma capsulatum var. farciminosum 

infects horses sporadically in Africa, Asia 

and Eastern Europe (Weeks et al., 1985). 

Ajellomyces dermatitidis (anamorph 

Blastomyces dermatitidis) 

The gymnothecia of A. dermatitidis are similar to 

those of A. capsulatus, but asexual reproduction is 

by means of stalked or sessile conidia which are 

smooth or spiny, but not tuberculate. Yeast cells 

are formed at 37°C, and these are much larger 

(10 12 mm in diameter) and have a thicker wall 

than those of H. capsulatum. The disease (blastomycosis) 

starts as an infection of the lung 

which can spread systemically to other sites, 

especially skin and bones. As in H. capsulatum, 

considerable efforts are currently being made to 

characterize the cell surface properties in 

B. dermatitidis (Hogan et al., 1996; Brandhorst 

et al., 2002). Crucial roles are probably played by 

the presence or absence of a-(1,3)-glucan in the 

cell wall, and by surface adhesins which are 

proteins that mediate the recognition of yeast 

cells by the host’s immune system. 

The fungus is soil-borne, especially in moist 

soil such as the banks of rivers. It is of North 

American origin, being particularly prevalent in 

the Mississippi and Ohio river valleys. Isolates 

from Africa represent a genetically different 

subpopulation (Guého et al., 1997). 

Paracoccidioides brasiliensis 

No teleomorph has been described as yet, but 

DNA sequence data predict that it will be an 

Ajellomyces if it is found (Guého et al., 1997). 

Conidia (arthroconidia) are seldom formed in 

culture, but the fungus is readily recognizable 

in the yeast state at 37°C because it produces a 

large, thick-walled central cell (30 mm in diameter) 

from which several smaller daughter cells 

bud off, often several at the same time. This type 

of budding is therefore called the ‘pilot-wheel 

stage’ (Fig. 11.3e). The first organ affected by 

paracoccidioidomycosis is the lung, but the 

infection may spread, causing grossly deforming 

lesions on mouth, nose and in gastrointestinal 

regions. The fungus is thought to occur in forest 

soils in areas with heavy rainfall in Central and 

South America. As with the other serious pathogens 

described in this section, the precise 

ecological niche of P. brasiliensis is still obscure, 

but it is possibly spread by the nine-banded 

armadillo, Dasypus novemcinctus (Restrepo et al., 

2001). 

Coccidioides immitis 

In culture, C. immitis reproduces by Malbrancheatype 

arthroconidia (Fig. 11.3f). In infected tissues, 

arthrospores swell and give rise to large, thickwalled 

spherical cysts or spherules (50 100 mmin 

diameter) which produce endospores. Endospores 

are very small (3 4 mm) and are readily disseminated 

in the bloodstream. Each endospore can 

develop into a new spherule. The disease (coccidioidomycosis) 

can be benign with influenza-like 

symptoms, but infections of the lung may spread 

to other organs such as the skin, brain and bones. 

Coccidioidomycosis can be fatal even to immunocompetent 

humans (Dixon, 2001). 

DNA sequence comparisons indicate a relationship 

with the teleomorphic genus Uncinocarpus 

(Sigler et al., 1998). Further, detailed studies of 

the distribution of specific DNA sequences in the 

genomes of isolates from various patients have 

revealed that sexual recombination must occur 

in nature, even though no teleomorph is known 

(Burt et al., 1996). Coccidioides immitis is a soil-borne 

fungus present as arthrospores, especially in arid 

regions of the south-western United States and 

in localized places in South America. It can infect 

wild mammals, but outbreaks occur especially 

among farmers and building workers, and after 

dust storms, earthquakes and other events that

ONYGENALES 

293 

disturb the soil. One hot spot of infection is the 

San Joaquín Valley in Southern California, where 

coccidioidomycosis is known as ‘valley fever’. The 

Californian population of C. immitis is reproductively 

isolated from populations elsewhere and 

has recently been given the status of a separate 

species, C. posadasii (Fisher et al., 2002). A readable 

account of the history of C. immitis has been given 

by Odds (2003), and Cox and Magee (2004) have 

covered general aspects of its interactions with 

the mammalian host. 

Onygena 

This is perhaps the most unusual yet least 

researched member of the Onygenaceae. Its 

fructification (Fig. 11.4a) is interpreted as a 

stalked ascostroma, i.e. an aggregate of several 

gymnothecia at the tip of a sterile stalk which 

may be 1 cm or more in length. The stalks are 

phototropic during growth. At maturity, the 

peridium of the stroma ruptures, thereby exposing 

the ascospores. There are two species, 

O. corvina which is associated with animal hair 

and bird feathers, and O. equina growing on the 

hooves and horns of herbivorous mammals 

(Currah, 1985). Both species are strongly keratinolytic, 

and although little work has been 

published on their biological features, we can 

assume that keratinolysis proceeds as in other 

Onygenales. According to Kunert (2000), the key 

feature is the ability to use keratin as the sole 

source of both carbon and nitrogen. The vast 

surplus of nitrogen is released into the environment 

as ammonia, thereby generating an alkaline 

pH of 9.0 or higher. The cystein-rich keratin also 

contains sulphur in excess of the growth requirements 

of keratinolytic fungi. This is often released 

as sulphate, thereby buffering the pH increase 

caused by the release of ammonia. 

Like many protein-degrading fungi, Onygena 

produces a cadaverous smell in culture, and 

Currah (1985) has suggested that this might 

attract carrion flies if produced in nature. This 

would make Onygena an insect-dispersed fungus. 

11.3.2 Ar throdermataceae 

There are only two genera in this small family. 

Ctenomyces (Fig. 11.5), with only one species 

(C. serratus), has a Chrysosporium anamorph 

in which one-celled microconidia are formed as 

terminal or intercalary cells of hyphae. Species of 

Arthroderma also sometimes produce Chrysosporium-like 

microconidia (Fig. 11.6b) but are better 

known by their macroconidial synanamorphs 

Epidermophyton, Microsporum and Trichophyton. 

These are multicellular with transverse septa, 

and are spindle-shaped or cylindrical. They are 

typical and readily recognized (Fig. 11.6a). The 

perfect state has not been found for many 

of these anamorphs, but they are suspected to 

be phylogenetically close to Arthroderma (Gräser 

et al., 1999; Hirai et al., 2003). Howard et al. (2003) 

have given a useful summary of Arthroderma and 

its associated anamorphs, listing 47 species. The 

teleomorph of the Arthrodermataceae is a typical 

gymnothecium with a basket of branching and 

anastomosing hyphae enclosing spherical asci 

which release their spores passively. Characteristic 

appendages are often present, e.g. in 

Ctenomyces (Fig. 11.5), a keratinolytic species associated 

with feathers. The combed appendages 

may serve to attach the gymnothecium to bird 

feathers for dispersal (Currah, 1985). 

Members of the Arthrodermataceae are generally 

keratinolytic, i.e. they degrade skin and hair. 

Howard et al. (2003) distinguished between species 

primarily associated with man (anthropophilic), 

animals (zoophilic) or the soil (geophilic). Because 

of their ability to grow on the skin, hair and nails 

of animals, the Arthrodermataceae are collectively 

called dermatophytes. Diseases caused by 

dermatophytes are colloquially known as ‘ringworm’, 

whereas they are called tinea within the 

medical profession, with descriptive terms such 

as capitis, barbae, corporis and pedis added to 

describe mycoses of the scalp, beard, general 

body, or feet, respectively (Howard et al., 2003). 

These infections are usually confined to the outer 

(dead) skin regions and are relatively easily 

controlled either by the superficial (topical) 

application of creams containing a wide variety 

of drugs, or by oral treatment especially with 

triazoles or terbinafine (see p. 278; Weitzman & 

Summerbell, 1995; Gupta et al., 1998). Griseofulvin, 

produced by Penicillium griseofulvum (see 

p. 302), was one of the first oral and topical 

drugs and is still in use today, especially in


Fig11.5 Ctenomyces serratus. (a) Gymnothecia attached to a horse hair with which the fungus was baited. (b) Gymnothecial 

appendage. Note the thick walls. Micrographs taken from material kindly provided by R. Sharma. 

Fig11.6 Asexual states of 

Arthrodermaracemosum 

(Arthrodermataceae). 

(a) Microsporum-type macroconidia. 

The spores are multicellular and 

thick-walled, with granular 

external ornamentations. 

(b) Chrysosporium-like microconidial 

state. Redrawn from de Hoog et al. 

(2000a), with kind permission of 

Centraalbureau voor 


the treatment of dermatomycoses in children, 

although resistance has developed among some 

strains of dermatophytes. Transmission of tinea 

infections to humans is often from pets, especially 

dogs, but also herbivores such as cows 

and horses. One species particularly common on 

cows is T. verrucosum (Fig. 11.7). The main 

transmission route for athlete’s foot and infections 

of toenails, both caused mainly by T. 

mentagrophytes and T. rubrum, is the use of 

communal facilities such as swimming pools 

and dressing rooms. Extensive listings of the 

various skin mycoses and the species causing 

them have been compiled by Weitzman and 

Summerbell (1995) and Howard et al. (2003). 

Members of the Arthrodermataceae are of 

historical interest because they were among 

the first fungi recognized as causing disease. In 

1842, Robert Remak succeeded in experimentally 

infecting himself with a fungus now known 

as T. schoenleinii (Ainsworth, 1976). Another 

milestone was laid by Raymond Sabouraud 

who pioneered the identification of dermatophytes 

on the basis of their appearance on

ONYGENALES 

295 

Fig11.7 Friesian cattle showing 

typical symptoms of Trichophyton 

verrucosum infections. Lesions are 

indicated by arrows.The circular 

lesion around the eye is 

particularly large because the 

animal has spread the infection 

by rubbing. 

culture media, in addition to the clinical 

symptoms (see Weitzman & Summerbell, 1995). 

All Arthrodermataceae appear to be heterothallic. 

Different strains of A. simii can induce enhanced 

growth but not complete mating and 

gymnothecium formation in strains of opposite 

mating type of a range of other species 

(Stockdale, 1968). Using this feature as a test 

system, it has been found for most anthropophilic 

species that all known isolates are of only one 

mating type, e.g. ( ) for T. rubrum. Since the 

Arthroderma state of dermatophytes is found only 

on substrates in contact with soil (Summerbell, 

2000), the lack of sexual reproduction in most 

anthropophilic species may be the result of 

adaptation to a highly patchy and specialized 

habitat (Howard et al., 2003). 

Geophilic members of the Arthrodermataceae 

are best isolated from soil or other substrata 

enriched in hair, skin or feathers (e.g. rodent 

burrows or birds’ nests) using horse hair or 

human hair as bait. Gymnothecia can be picked 

up with the aid of a dissection microscope, 

and transferred to a suitable medium such as 

Sabouraud agar (Sharma et al., 2002). 

11.3.3 Gymnoascaceae 

The Gymnoascaceae are a small family (10 genera, 

23 species; Kirk et al., 2001). A recent phylogenetic 

study is that by Sugiyama et al. (2002). Members 

of the Gymnoascaceae are isolated mainly from 

soil and are saprotrophic, degrading keratin and 

also cellulose. The genus Gymnoascus has 

been described by von Arx (1986). Gymnoascus 

reessii is a species commonly encountered on 

herbivore dung, producing strikingly coloured 

gymnothecia which are at first yellow, then red 

and finally brown as the ascospores mature. The 

reticulo peridium consists of branched, recurved, 

thick-walled hyphae loosely enclosing a mass of 

asci (Fig. 11.8). Ascocarp development can be 

followed readily in culture and begins from 

paired gametangia which arise from the same or 

different hyphae. The antheridium is club-shaped 

and the ascogonium coils around it (Fig. 11.9a). 

The ascogonium then becomes septate and its 

cells give rise to ascogenous hyphae (see Fig. 

11.9b), whose tips develop into croziers. Asci 

develop from the penultimate cells of the croziers 

(Kuehn, 1956). The branched reticulo peridial 

hyphae arise from vegetative hyphae in the 

region of the gametangium (Figs. 11.9b,c). The 

asci do not discharge violently; the ascus wall 

disappears and the spores escape through the 

loose envelope. There is no conidial stage. 

11.3.4 Myxotrichaceae 

This family contains 4 genera (12 species). 

Anamorphs are Oidiodendron or Malbranchea. 

The genus Oidiodendron may have important


Fig11.8 Gymnoascus reessii. 

Ascocarp showing thick-walled 

branched reticulo peridial 

hyphae and asci. 

Fig11.9 Gymnoascus 

reessii, gymnothecium 

development. 

(a) Antheridium 

and ascogonium. 

(b) Ascogonium showing 

development of 

ascogenous hyphae. 

The peridial envelope 

is also developing. 

(c) Young 

gymnothecium showing 

asci at the tips of 

ascogenous hyphae. 

functions in soil ecosystems, and keys and 

species descriptions have been provided by 

Calduch et al. (2004) and Rice and Currah 

(2005). Myxotrichum chartarum is cellulolytic and 

has been known as a paper spoilage organism 

since the early nineteenth century. Gymnothecia 

form a thick chocolate-brown layer on paper 

or cardboard (Fig. 11.10a) and are also readily 

formed in culture. They are typical of the 

Onygenales, consisting of a reticuloperidium 

of anastomosing hyphae with beautiful curved 

appendages (Fig. 11.10b). Other Myxotrichum spp.

EUROTIALES 

297 

have gymnothecia with simpler appendages, or 

these lack appendages altogether (Currah, 1985). 

The taxonomic position of Myxotrichaceae is 

uncertain, recent phylogenetic studies suggesting 

an affinity with inoperculate discomycetes 

(Helotiales; Tsuneda & Currah, 2004). Support for 

this proposal comes from ecological surveys in 

which Oidiodendron spp. as well as members of 

the Helotiales have been isolated as mycorrhizal 

symbionts of ericaceous plants (Berch et al., 

2002; Peterson et al., 2004; see also p. 442). 

Since both the teleomorphs and anamorphs of 

Myxotrichaceae are clearly referable to the 

Onygenales, a connection with the Helotiales 

would be surprising, rendering the concept of a 

gymnothecium with evanescent asci one of the 

most striking examples of convergent evolution 

among the fungi (Greif & Currah, 2003). 

11.4 Eurotiales 

To the practical mycology student, the order 

Eurotiales is among the most important groups 

of fungi because it contains many ubiquitous and 

readily recognized species, notably in the anamorphic 

genera Aspergillus and Penicillium. Virtually 

any environmental sample soil, water, rhizosphere, 

air, and indoor or food contaminations 

will yield viable spores. One important feature of 

many species of Aspergillus and Penicillium is that 

Fig11.10 Myxotrichum chartarum. (a) Thick layer 

of gymnothecia on cardboard from a damp cellar. 

(b) Gymnothecium with dark curved appendages. 

Reprinted fromTribe and Weber (2002), with 

permission from Elsevier.


they are xerophilic, i.e. capable of growing at 

a water potential (a W ) at or below 0.85. Thus, they 

are major food spoilage organisms, growing on 

stored cereals, spices, nuts, bread, dried and cured 

ham, pickles, jams and preserves (Lacey, 1994; 

Filtenborg et al., 2002). Colonization of food and 

feedstuff can result in its contamination by 

serious mycotoxins (see pp. 304 306). 

Colonies typically spread slowly but quickly 

assume a greenish-blue pigmentation due to 

abundant conidium formation. The pigmentation 

of mature conidia is at least partly due to melanin 

(see Fig. 12.46; Plate 4d). The conidial state is more 

commonly observed than the teleomorph, and 

indeed many species have lost their capacity 

of sexual reproduction altogether (Geiser et al., 

1996). Loss of sexual reproduction seems to have 

occurred independently on several occasions 

within the Eurotiales. When present, the ascocarps 

range from gymnothecial structures with 

loose mesh-like reticuloperidia (e.g. Talaromyces) 

to the hard sclerotium-like fructifications of 

certain species of Eupenicillium. The conidial 

states are generally phialidic. Microscopically, 

the conidiophores of Aspergillus and Penicillium 

can be categorized according to the arrangement 

of phialides on the conidiophore (Fig. 11.11). The 

phylogenetic value of these structures may be 

limited, but they are very useful for species 

identification. In Aspergillus (Fig. 11.11a), the conidiophore 

tip is swollen into a hemispherical or 

club-shaped structure, the vesicle. Phialides may 

be formed directly at the vesicle surface in which 

case the conidiophore is said to be uniseriate 

(Figs. 11.11a, 11.16a; Raper & Fennell, 1965). 

Alternatively, a palisade of sterile cells (metulae) 

is formed by the vesicle, and the tips of the 

metulae give rise to the phialides (biseriate 

conidiophores; Fig. 11.17a). No vesicle is produced 

in Penicillium (Figs. 11.11b and 11.18), and instead 

the conidiophore tip either gives rise to phialides 

directly in the monoverticillate arrangement 

(Pitt, 1979), or it produces one series of metulae 

(biverticillate) or further branching layers. In 

terverticillate penicilli, the conidiophore tip 

produces one or several rami, each of which 

develops several metulae which in turn produce 

several phialides each. In quaterverticillate 

Fig11.11 Examples of conidiophores of three important anamorphic genera of theTrichocomaceae. (a) Aspergillus penicillioides. 

(b) Penicillium notatum (¼ P. chrysogenum), the original penicillin-producing strain isolated by Sir Alexander Fleming in1928. 

(c) Paecilomyces marquandii. All images to same scale.

EUROTIALES 

299 

penicilli, a further branch, the ramulus, is 

inserted between the ramus and the metula. 

Paecilomyces, another important anamorphic 

genus in the Eurotiales, has conidiophores similar 

to those of Penicillium, except that the phialides 

are more loosely arranged and have a different 

shape, being more elongated with a narrow 

drawn-out tip (Fig. 11.11c). Conidia of 

Paecilomyces are usually pale rather than pigmented 

green or blue. 

The order Eurotiales is thought by some to 

consist of only a single family, Trichocomaceae, 

and these two terms are often used interchangeably. 

However, Geiser and LoBuglio (2001) also 

included the Monascaceae (not discussed further 

here) and Elaphomycetaceae (see p. 313). Many 

species of the Trichocomaceae are much better 

known by their anamorphic names, and these will 

continue to be used by most mycologists, especially 

those working in applied fields. Correlations 

of anamorphic and teleomorphic taxa are 

given in Table 11.2 (Pitt et al., 2000). These data 

show that a teleomorph has been found only for 

about 40% of all Aspergillus species described 

to date, and 31% of Penicillium spp. The taxonomy 

of the Eurotiales is still in a considerable state of 

confusion because it is not possible unequivocally 

to correlate the various anamorphs with the 

appearance of cleistothecia and other features 

such as DNA sequence data and biochemical 

features (Ogawa et al., 1997; Ogawa & Sugiyama, 

2000). 

11.4.1 Aspec ts of morphogenesis 

in Aspergillus 

To recapitulate on our discussion of 

conidiogenesis on p. 235, a phialide, according 

to Kendrick (1971), is: 

a conidiogenous cell in which at least the first 

conidium initial is produced within an apical 

extension of the cell, but is liberated sooner or 

later by the rupture or dissolution of the upper 

wall of the parent cell. Thereafter, from a fixed 

conidiogenous locus, a basipetal succession of 

enteroblastic conidia is produced, each clad in 

a newly laid-down wall to which the wall of the 

conidiogenous cell does not contribute . . . The 

length of the phialide does not change during 

the production of a succession of conidia . . . 

The development of phialoconidia in Aspergillus 

niger is illustrated in Fig. 11.12. Young phialides 

are somewhat club-shaped in outline. In A. niger, 

A. nidulans and many other species of 

Aspergillus and Penicillium, the phialoconidia are 

uninucleate, but in some species they are multinucleate. 

The tip of the phialide expands to form 

a spherical knob which is the initial of the firstformed 

spore. Meanwhile, the single nucleus in 

the phialide divides, and a daughter nucleus 

passes into the spore which begins to be 

separated by the formation of a septum at the 

phialide tip. The expansion of the first conidium 

leads to the rupture of the phialide wall near its 

tip, and the remnants of the broken phialide wall 

persist as a cap around the first-formed conidium. 

Before the rupture of the phialide wall, 

a layer of cell wall material is laid down 

(Fig. 11.12d). This layer becomes the outer wall 

Table 11.2. A summary of some anamorphic 

states found in the Trichocomaceae, and their 

associated teleomorphs. 

Anamorphic name 

Teleomorphic name 

Aspergillus (218) Chaetosartorya (3) 

Emericella (33) 

Eurotium (24) 

Fennellia (3) 

Hemicarpenteles (2) 

Neosartorya (19) 

Petromyces (3) 

Sclerocleista (2) 

Geosmithia (10) Talaromyces (3) 

Paecilomyces (48) Byssochlamys (4) 

Talaromyces (3) 

Thermoascus (4) 

Penicillium (249) Eupenicillium (44) 

Talaromyces (33) 

For each taxon, the numbers of species are 

indicated in brackets. Numerically important 

genera are highlighted in bold.Note that only a 

few ofthe 48 Paecilomycesspecies arereferable 

to theTrichocomaceae, many others belong to 

Pyrenomycetes (see p. 360). Summarized from 

Pitt et al. (2000) and Samson (2000).


Fig11.12 Phialoconidium ontogeny in Aspergillus niger (modified from Subramanian,1971). (a) Young phialide. (b) Mitosis in phialide. 

(c) Conidium initial with daughter nucleus. (d) Breakage of phialide wall and formation of a new wall layer surrounding the conidial 

cytoplasm. (e,f) Mitosis in the phialide and extrusion of the second phialospore. Note that the phialide has not increased in length. 

(g,h) Further mitosis in the phialide and formation of the third spore. Note the formation of an inner conidial wall within the outer, 

and the isthmus connecting mature adjacent spores within the chain. 

layer of the conidium within which an inner wall 

develops later (Fig. 11.12h). Nuclear division 

continues within the phialide, and cytoplasm 

and a wall are laid down around a daughter 

nucleus to form a second conidium which is 

extruded from the broken tip of the phialide 

(Figs. 11.12e,f). The second and all subsequent 

conidia differ from the first in that they are not 

enveloped by remnants of the broken phialide 

wall. The cytoplasm of the second conidium is 

initially continuous with that of the first by 

means of a cylindrical isthmus. The formation of 

an inner wall layer by the conidia severs this 

cytoplasmic connection. The surviving empty 

isthmus is sometimes termed the connective. 

Each phialide can produce 100 spores or more, 

so that the total crop from one conidiophore 

may be more than 10 000 conidia (Adams et al., 

1998). The fine structural details of conidium 

production in A. nidulans have been described 

by Mims et al. (1988). 

In the phialide, a transition from the polarized 

growth pattern of the mycelial hypha, conidiophore 

and phialide to yeast-like (isodiametric) 

growth of the nascent conidium takes place. 

Results obtained from experiments with the

EUROTIALES 

301 

biseriate species Aspergillus (Emericella) nidulans 

can be compared with those summarized earlier 

for the two ‘model yeasts’, Schizosaccharomyces 

pombe (pp. 256 259) and Saccharomyces cerevisiae 

(p. 270). While the cell cycle (nuclear division) 

is always followed by cell division (cytokinesis) 

in these yeasts, this is not necessarily the case 

in A. nidulans. For instance, when a uninucleate 

conidium of A. nidulans germinates, several 

mitotic divisions take place prior to and during 

the emergence of the germ tube before the first 

septum is laid down near the base of the germ 

tube. Subsequent septa are formed at regular 

intervals along the hypha, and each hyphal 

segment contains about 3 4 nuclei (Fiddy & 

Trinci, 1976). Only the nuclei in the apical cell 

continue to divide whereas those in intercalary 

compartments are arrested at the G1 stage but 

become reactivated later if a lateral branch is 

formed (Kaminskyj & Hamer, 1998). As the mycelium 

develops and spreads horizontally on an 

agar surface, conidiophores begin to grow out 

vertically after about 16 h in optimal conditions, 

with the first conidia being produced about 8 h 

later. Thus the time span from the germination 

of a conidium to the production of the new crop 

of conidia is only 24 h. It is not surprising that 

Aspergillus and Penicillium-type moulds are omnipresent 

in our environment! 

The development of the conidiophore tip has 

been described in detail by Mims et al. (1988) and is 

shown in Fig. 11.13. After vertical growth for 

a limited distance (about 100 mm inA. nidulans), 

the tip of the conidiophore swells to form the 

vesicle (Fig. 11.13a). In the conidiophore, cytokinesis 

is suppressed whereas nuclear division 

continues, resulting in a multinucleate cell. In 

contrast, nuclear division and cytokinesis are 

tightly controlled beyond the vesicle stage 

because a single nucleus migrates into each of 

the 60 or so metulae which are formed by the 

vesicle of A. nidulans (Fig. 11.13b). Each metula 

then produces about two uninucleate phialides 

(Fig. 11.13c). At the phialide tip, conidia are 

formed (Fig. 11.13d), and here the transition 

from polarized to yeast-like growth takes place. 

The nucleus divides as the conidium enlarges, and 

one daughter nucleus migrates along microtubules 

into the spore whereas the other remains 

in the phialide, ready to divide again. The signalling 

events which co-ordinate the interactions 

between the nuclear division cycle and cytokinesis 

are beginning to be unravelled (Ye et al., 1999). 

As in the case of S. cerevisiae and S. pombe, 

septin-type proteins play a crucial role in organizing 

morphogenesis in A. nidulans and most probably 

other members of the Eurotiales, although 

detailed studies are lacking. In A. nidulans, septin 

rings with superimposed constricting actin rings 

are found at the sites of septum formation, the 

points of origin of metulae at the vesicle surface, 

the point of origin of phialides, and at 

the phialide tip where conidia are budded off 

(Momany & Hamer, 1997; Westfall & Momany, 

2002). All rings except for the last-mentioned are 

transient, disappearing as soon as the septum is 

complete. 

11.4.2 Morphogenesis in Penicillium 

Little work has been carried out on conidiogenesis 

in Penicillium, although it is reasonable to assume 

that the general principles will be similar to those 

described above for Aspergillus (Borneman et al., 

2000). One interesting case is P. marneffei, which is 

the only species displaying a switch from hyphae 

to yeast cells, growing as a mycelium at 25°C and 

as yeast cells at 37°C. Upon transfer of a mycelial 

colony to 37°C, nuclear division becomes tightly 

coupled with cytokinesis so that uninucleate 

hyphal segments are formed which fragment 

into arthrospores (Garrison & Boyd, 1973; 

Andrianopoulos, 2002). These form yeast cells 

which reproduce by fission at 37°C. Interestingly, 

the same regulatory mechanism is responsible 

for phialidic conidiogenesis at 25°C and for the 

switch from multinucleate hyphae to uninucleate 

yeast cells (Borneman et al., 2000), supporting the 

notion that conidiogenesis by phialides should be 

regarded as yeast-like growth. 

In Penicillium cyclopium, conidiophore formation 

is thought to be induced by a hormone called 

conidiogenone, which is permanently produced 

by growing colonies. When the concentration 

of conidiogenone exceeds a particular threshold 

(10 7 10 8 M), conidiogenesis, i.e. growth and 

differentiation of the conidiophore, is triggered 

(Roncal et al., 2002). For conidiogenesis to occur, 

hyphae must usually be exposed to air. This may


Fig11.13 Conidiophore development in Aspergillus nidulans. (a) Tip of a conidiophore which has swollen to produce a vesicle.The 

conidiophore is multinucleate (nuclei not visible). (b) Development of metulae. Each metula contains one nucleus. (c) Production of 

phialides, two from each metula.Each phialide contains one nucleus. (d) Production of uninucleate conidia. All images to same scale. 

be because the hormone is concentrated in the 

cell wall, rather than diffusing into the medium. 

In liquid cultures, conidiogenesis in P. cyclopium 

can be triggered by the addition of Ca 2þ ions 

which are thought to act merely by enhancing the 

sensitivity of the fungus to its own hormone 

(Roncal et al., 2002). It is not known whether 

a similar hormonal system exists in Aspergillus. 

11.4.3 The roles of Aspergillus and Penicillium 

in biotechnology 

Species of Aspergillus and Penicillium are among 

the most important organisms used in biotechnology, 

second only to S. cerevisiae. Their applications 

are diverse, including the production of 

enzymes or primary and secondary metabolites, 

and direct colonization and modification of foodstuff. 

We will briefly consider examples of each 

of these applications. 

Food production 

Species of Aspergillus have been used in the Far 

East for food production for many centuries, and 

we have already mentioned the role of A. oryzae 

in the degradation of rice starch as a first step in 

saké production (see p. 276). Similar two-stage 

fermentation processes were developed for soy 

sauces, although in this case the raw material 

consists of a mixture of soy beans and wheat, and 

proteolytic as well as amylolytic enzymes are relevant. 

The degradation of this substrate is called 

the koji process, and it is one of the best examples 

of a solid-substrate fermentation. As such, 

it requires great skill to find the optimum 

moisture level of the soybean cake because 

excessive moisture will limit aeration, whereas 

low moisture limits growth. The koji fermentation 

is completed within 72 h, and it utilizes 

mainly A. oryzae and A. sojae. Interestingly, on the 

basis of morphological as well as molecular data 

(Geiser et al., 2000), these appear to be domesticated 

forms of the potent mycotoxin producers 

A. flavus and A. parasiticus, respectively (see p. 304). 

The partially degraded substrate enriched in 

fungal extracellular enzymes is then suspended 

in brine, and the main fermentation (moromi) is 

carried out with a consortium of bacteria and 

yeasts. The Aspergillus enzymes continue to be 

active during the moromi fermentation, thus 

releasing a steady supply of degradation products. 

A readable account of soy sauce production is 

that by Aidoo et al. (1994). Other Far Eastern food 

types produced with the aid of Aspergillus spp. 

have been summarized by Nout and Aidoo (2002).

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Cheese production involves complex consortia 

of bacteria and numerous different yeast species, 

but two Penicillium spp. are important in specialized 

cheeses. These are P. roqueforti for blue-veined 

cheeses, and P. camemberti for white mould 

cheeses. The subject has been summarized by 

Jakobsen et al. (2002). The moulds are inoculated 

together with enzymes or bacterial starters after 

the cooling of the pasteurized milk, and gradually 

colonize the maturing cheese. They contribute 

significantly to the texture as well as the flavours, 

with the characteristic blue cheese or camembert 

flavours being due mainly to the activity of extracellular 

lipases which break down short-chain 

fatty acids. A substantial contribution is also 

made by protein and peptide degradation products 

resulting from the activities of fungal 

proteinases and peptidases (Jakobsen et al., 2002). 

Production of enzymes 

The prominent role of Aspergillus and Penicillium 

species in food production is, of course, due to 

their ability to produce large quantities of extracellular 

enzymes. This feature has also been 

harnessed for industrial purposes, with the 

majority of all commercial fungal enzymes produced 

by Aspergillus spp. (Oxenbøll, 1994). 

Proteases, amylases, lipases and pectinases are 

important in many industrial processes, including 

the manufacture of dairy, bakery, distillery 

and brewery products, juices and leather, and in 

the starch industry. 

Citric acid fermentation 

Citric acid is found in many fruits, and it is used 

for flavouring and pH control of food and beverages. 

In combination with carbonates and 

bicarbonates, it is also used to create the 

effervescent effect when medications such as 

vitamin preparations or aspirin are dissolved in 

water. Initially extracted from citrus fruits, citric 

acid has been produced commercially by Aspergillus 

niger since about 1923 and this fungus remains 

the world’s most important producer. The total 

current annual world production of citric acid 

is about 9 10 6 tons. Curiously, although production 

of citric acid by A. niger is one of the most 

efficient biotechnological fermentations with 

conversion of up to 95% (by weight) of the sugar 

substrate, the biochemistry of it is still only 

poorly understood. The uptake of sugar (as 

hexose) is followed by glycolysis in the cytosol, 

the tricarboxylic acid cycle in the mitochondrion, 

and export of citric acid into the cytosol and 

thence into the extracellular medium where it 

accumulates, creating a pH below 3. Citric acid 

production proceeds optimally when an excess of 

sugar and aeration is provided, whereas phosphate 

and trace elements, especially manganese, 

must be limiting. Excellent reviews of citric acid 

production have been published by Brooke (1994) 

and Karaffa and Kubicek (2003). 

Production of antibiotics 

The accidental discovery of penicillin by a contamination 

of Penicillium notatum growing on a 

bacterial agar culture (Fleming, 1929, 1944) 

followed by the re-discovery of penicillin by 

Florey and Chain and its development into an 

antibiotic against Gram-negative bacteria has 

been told many times, and the original 1945 

Nobel Lectures by Fleming, Florey and Chain can 

be found at http://www.nobel.se. In nature, 

penicillin (Fig. 11.14a) is produced by P. notatum, 

the closely related or identical P. chrysogenum, by 

A. nidulans and a few other conidial fungi, whereas 

the chemically related cephalosporins are produced 

by Acremonium chrysogenum (formerly 

Cephalosporium chrysogenum), which probably 

belongs to the Pyrenomycetes (p. 348). Together, 

penicillin- and cephalosporin-type antibiotics 

take a staggering 50% share (approximately 

11 billion US$) of the total worldwide sales of 

antibiotics (Schmidt, 2002). Aspergillus nidulans has 

been useful for studies of the genetics and 

biosynthesis of penicillin production because 

it is easily manipulated by molecular biological 

methods. However, for commercial production 

P. chrysogenum has been used traditionally. The 

first penicillins were produced commercially 

by purification of the final product from 

static liquid cultures. Over several decades, highproducing 

mutants were generated, resulting 

in a 50 000-fold enhanced penicillin yield relative 

to that of the original strain, and current yields 

are as high as 50 g penicillin l 1 of liquid culture 

(Schmidt, 2002). A wide range of penicillin (and 

cephalosporin) derivatives has been produced,


Fig11.14 Important metabolites produced byTrichocomaceae. (a) Penicillin G, an antibiotic against Gram-positive bacteria which is 

synthesized from three amino acids.The cleavage point of penicillin acylases is indicated by an arrow. (b) Griseofulvin, an antifungal 

antibiotic which is synthesized as a heptaketide, with three methyl groups (arrows) added subsequently by methylation. (c) The 

polyketide aflatoxin B 1 

. (d) Ochratoxin A.This is a pentaketide to which the amino acid phenylalanine is linked via a previously added 

one-carbon group (arrow). (e) The derived tetraketide patulin. 

partly to counter bacterial resistance and 

partly to broaden the range of applications or 

reduce allergic responses by patients. Current 

production seems to be mainly semi-synthetic; 

penicillin G is produced by P. chrysogenum, 

followed by the removal of the side-chain to give 

6-aminopenicillanic acid, which is then derivatized 

chemically. There are tendencies to use 

microbial enzymes (penicillin acylases) for the 

removal of the side chain (see Fig. 11.14a) and for 

subsequent synthetic steps (Arroyo et al., 2003; 

Bruggink et al., 2003). Good general reviews of 

the history of penicillin biotechnology have 

been written by Rolinson (1998) and Demain and 

Elander (1999). The biosynthesis of penicillins 

and cephalosporins in fungi has been described 

in detail by Martin et al. (1997). 

Another important secondary metabolite of 

the Trichocomaceae is griseofulvin (Fig. 11.14b), 

which is used as a systemic antifungal drug, 

especially against dermatophytes (see p. 293). 

Griseofulvin was first detected in P. griseofulvum 

(Oxford et al., 1939) and was then re-discovered in 

P. janczewskii (see Brian, 1960). It is now known to 

be produced by a wide range of Penicillium spp. 

as well as Aspergillus versicolor and by the Hemiascomycete 

Eremothecium coryli (Bérdy, 1986). 

Commercial production is still achieved by 

means of fungal fermentations. 

11.4.4 Mycotoxins 

Members of the genera Aspergillus and Penicillium 

are notorious for their production of secondary 

metabolites which are highly toxic against many 

different organisms and are therefore collectively 

called mycotoxins. Since these fungi are 

often found as food contaminants, their mycotoxins 

present a major health hazard and, consequently, 

have been thoroughly investigated. 

We summarize the major groups of substances 

here, i.e. aflatoxins, ochratoxin A and patulin 

(Figs. 11.14c e). These are derived at least in part 

from the polyketide pathway in which acetylcoenzyme 

A or malonyl-CoA units are fused 

head-to-tail in a stepwise fashion. The principle

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has similarities to the synthesis of fatty acids 

from acetyl-CoA. Synthesis proceeds in cycles, 

with one addition in each cycle which is followed 

by modification of the side chain (initially a keto 

group). Many other mycotoxins arising from 

diverse biochemical pathways are produced 

by Aspergillus and Penicillium, and an excellent 

introduction to the biochemical diversity of 

mycotoxins has been given by Moss (1994). 

Good reviews of ecological aspects and health 

implications of these mycotoxins have been 

written by Scudamore (1994), Bhatnagar et al. 

(2002) and Pitt (2002). The ability to produce 

mycotoxins such as aflatoxin, ochratoxin or 

patulin is found in diverse groups of Aspergillus 

and Penicillium. Since all or most of the genes 

involved in the biosynthesis of a given mycotoxin 

tend to be clustered in the genome, it is possible 

that sporadic horizontal gene transfer has 

occurred between different species, thus explaining 

the lack of correlation between mycotoxin 

production and phylogenetic placement (Varga 

et al., 2003). 

Aflatoxins 

These polyketide-type metabolites are produced 

by strains of Aspergillus flavus but not, apparently, 

by the closely related A. oryzae (Bayman & 

Cotty, 1993). The most common is aflatoxin B 1 

(Fig. 11.14c), which is so named because it 

fluoresces blue on a thin-layer chromatography 

plate under UV light (aflatoxins G fluoresce 

blue green). The fluorescence of aflatoxins is 

so strong that heavily contaminated food 

samples, e.g. the kernels of Brazil nuts, will 

fluoresce under UV light. Aflatoxin B 1 is one of 

the most potent carcinogens known, being 

capable of inducing liver cancer at concentrations 

below 1 mgkg 1 body weight (Cotty et al., 

1994). Consequently, stringent regulations 

concerning maximum permissible aflatoxin 

levels are in place in many countries. However, 

these toxins may still present a health hazard 

to consumers, and also to agricultural workers 

because spores of A. flavus contain such high 

toxin levels that their inhalation may pose a risk 

of liver cancer (Olsen et al., 1988). Although the 

crop may well become contaminated on the field, 

A. flavus infections become visible only during the 

storage of agricultural produce. Since the fungus 

is xerophilic, it can colonize even dry products 

(Lacey, 1994). Nuts, peanuts and spices are 

particularly susceptible, but almost any food 

can be contaminated. An infamous outbreak 

of aflatoxicosis, turkey-X disease, occurred in 

the UK in 1960 when about 100 000 turkeys 

were killed by contaminated groundnut meal. 

Further, cows eating contaminated feed will 

produce milk containing the slightly modified 

aflatoxins M (Scudamore, 1994). Because of their 

ubiquity and extreme toxicity, aflatoxins must 

be considered the most important food-borne 

mycotoxins worldwide. The biosynthetic pathways 

of aflatoxins are well characterized (Klich & 

Cleveland, 2000). The mycotoxin sterigmatocystin, 

produced by various Aspergillus spp., is a 

precursor of aflatoxin and is also carcinogenic, 

although it is comparatively rare in food and 

feed (Moss, 1994). The production of secondary 

metabolites usually occurs only when vegetative 

growth has ceased and when conidium formation 

ensues; the regulatory mechanisms coupling 

conidiation with secondary metabolism are 

beginning to be unravelled for A. nidulans 

(Adams & Yu, 1998). 

Ochratoxin A 

This is a pentaketide/amino acid hybrid molecule 

(Fig. 11.14d) which is produced by numerous 

species of Aspergillus and Penicillium, especially 

P. verrucosum, which is common on cereals in 

temperate climates, and A. ochraceus and 

A. carbonarius, which grow on the flesh of coffee 

berries during drying. Coffee can, therefore, be 

contaminated with ochratoxin A, but mercifully 

much of it is destroyed during roasting (Viani, 

2002). Ochratoxin A consumed with contaminated 

cereals or meat has a long residence 

time (half-life 35 days) in the human body. 

It is highly nephrotoxic and has been implicated 

in a degenerative human kidney disorder 

called ‘Balkan endemic nephropathy’; it is also 

strongly suspected to cause cancer of the gall 

bladder (Stoev, 1998; O’Brien & Dietrich, 2005). 

Further, ochratoxin A causes a renal degenerative 

disorder of farm animals, especially pigs. A 

chemically closely related mycotoxin is citrinin.


Patulin 

Although patulin is a small (tetraketide-derived) 

molecule (Fig. 11.14e), its biosynthesis is complex, 

involving the formation and subsequent 

cleavage of an aromatic ring (Moss, 1994). Patulin 

is produced by several species of Aspergillus and 

Penicillium as well as Byssochlamys nivea (see p. 307), 

but the most important producer by far is 

P. expansum, a cause of brown rot of apples. 

Patulin is often detected in apple juices, sometimes 

at concentrations greatly exceeding safety 

limits set at or below 50 mgl 1 . It is, however, 

destroyed during alcoholic fermentation to wine 

or cider (Moss & Long, 2002), or by adding 

sulphite. It is also formed by A. clavatus in spent 

barley from beer brewing which is often fed to 

cattle. Patulin may be carcinogenic; it also reacts 

with the sulphydryl groups of proteins, thereby 

inactivating enzymes (Mahfoud et al., 2002). 

A review of safety issues and methods for analysis 

and control of patulin levels in food has been 

written by Moake et al. (2005). 

11.4.5 Pathogenic species 

In principle, all species of Aspergillus and Penicillium 

and indeed many other types of fungi can 

cause health hazards because of the potential of 

their spores to act as allergens to those suffering 

from hay fever or asthma. Further, many species 

of Aspergillus and Penicillium produce mycotoxins 

(see above). In the present section we will consider 

only those species which cause mycoses, i.e. 

infections which require chemotherapy. Good 

general reviews have been written by Kwon- 

Chung and Bennett (1992) and Summerbell 

(2003). 

Aspergillus 

Two species cause most of the mycotic infections 

associated with Aspergillus. These are A. fumigatus 

(69% of all reports) and A. flavus (17% of reports) 

(Summerbell, 2003). Both produce similar 

diseases. Like many other fungal pathogens of 

humans, these species primarily cause infections 

of the respiratory tract and the lung, although 

wound infection can also occur occasionally. In 

immunocompetent patients, non-spreading 

‘fungus balls’ (aspergillomas) may be formed 

in the lung in cavities caused, for example, by 

previous tuberculosis. In immunocompromised 

patients, invasive aspergillosis may arise, i.e. the 

infection spreads throughout the lung and even 

to other organs. Aspergillosis is a major cause of 

death among cancer patients and is strongly on 

the increase among AIDS sufferers. One reason 

why A. fumigatus is a more frequent cause of 

infection than A. flavus may be that its conidia 

are smaller (3 mm diameter or less) and can 

penetrate more deeply into the lung. They are 

also more buoyant in the air, and Chazalet et al. 

(1998) have routinely measured concentrations 

above 1 conidium m 3 air even in protected 

hospital environments. This means that every 

human normally inhales several hundred 

conidia of A. fumigatus every day. One disease 

caused almost solely by A. fumigatus is allergic 

bronchopulmonary aspergillosis, in which infections 

occur in patients already suffering from 

chronic irritation of the lung, e.g. due to asthma 

or cystic fibrosis. The disease can lead to fatal 

destruction of the lung tissue. Treatment by 

chemotherapy is possible, with amphotericin B 

and the triazole itraconazole being the major 

current drugs. In-depth reviews on all aspects of 

diseases caused by A. fumigatus have been written 

by Latgé (1999, 2001). 

Aspergillus fumigatus is a particularly thermotolerant 

species with an upper growth limit at 

52°C (Dix & Webster, 1995), although it can survive 

80°C for up to 60 min (Jesenská et al., 1993). 

It is one of the most abundant moulds found in 

compost heaps and other situations in which the 

decay of vegetation generates heat. Workers at 

compost sites are therefore subjected to a massive 

spore inoculum, although the incidence of aspergillosis 

does not seem to be generally higher 

among them. This indicates the opportunistic 

nature of aspergillosis in man. In fact, the spores 

of thermophilic actinomycetes seem to cause 

most of the problems associated with ‘compost 

worker’s lung’ (van den Bogart et al., 1993). 

Penicillium 

In general, species of Penicillium are not as 

thermotolerant as Aspergillus, with only relatively 

few species capable of growing at 37°C. Consequently, 

clinical reports of Penicillium infections

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are uncommon, with the major exception of 

P. marneffei. As already noted, this species grows as 

a fission yeast at 37°C, and it causes systemic and 

disseminated infections in South East Asia which 

have increased dramatically with the spread of 

AIDS there. The disease symptoms are similar 

to those of Histoplasma capsulatum (see p. 290), 

including the predominance of the disease in 

male patients (Harrison & Levitz, 1996). Disseminated 

infections are most commonly found in 

lung, liver and skin and can be treated with 

amphotericin B and itraconazole (Harrison & 

Levitz, 1996). Penicillium marneffei can be isolated 

with high frequency from the internal organs of 

bamboo rats as well as their burrows in South East 

Asia. However, since contact between these 

rodents and humans is probably infrequent, 

there may be unknown sources of inoculum in 

the environment to which both rats and humans 

are exposed (Vanittanakom et al., 2006). 

11.4.6 Byssochlamys 

Byssochlamys is a small genus of soil fungi 

currently comprising four species (Pitt et al., 

2000) which are noteworthy because of their 

thermotolerance. The most tolerant structures 

are the ascospores which may survive heating to 

90°C for 25 min, especially in the presence of 

high sucrose concentrations (Beuchat & Toledo, 

1977; Bayne & Michener, 1979). Byssochlamys spp. 

are important contaminants of canned fruits or 

bottled fruit juices (Tournas, 1994) because of 

their heat tolerance, ability to produce pectolytic 

enzymes, and tolerance of conditions of low 

oxygen tension. Contamination can be dangerous 

because Byssochlamys spp. can produce several 

mycotoxins, including patulin (Rice et al., 1977). 

Another habitat associated with human activity 

is silage in which Byssochlamys is a common 

contaminant (Inglis et al., 1999). In nature, 

Byssochlamys is ubiquitous in the soil. In orchards, 

it may be splashed onto the fruit prior to or 

during harvesting. 

In culture, Byssochlamys spp. reproduce asexually 

by the formation of chains of hyaline conidia 

derived from tapering open-ended phialides 

(Fig. 11.15a) which have been assigned to the 

Paecilomyces type. Terminal, thick-walled 

Fig11.15 Byssochlamys nivea. 

(a) Phialospores and 

chlamydospores. (b) Coiled 

ascogonium surrounding an 

antheridium. (c) Ascogonium 

bearing ascogenous hyphae 

which in turn produce asci. 

Note the absence of sterile 

investing hyphae.


unicellular chlamydospores are also found. The 

asci of Byssochlamys develop best in cultures 

incubated around 30°C. In B. nivea, a clubshaped 

antheridium becomes encoiled by an 

ascogonium (Fig. 11.15b). Later, the coiled ascogonium 

develops short branches (ascogenous 

hyphae) which bear globose, eight-spored asci 

either terminally or laterally, so that eventually 

clusters of asci can be found. There is no sign of 

any sterile hyphae enclosing them (Fig. 11.15c). 

Like most if not all members of the Eurotiales, 

Byssochlamys spp. appear to be homothallic. 

11.4.7 Aspergillus and its teleomorphic 

states 

Keys to Aspergillus may be found in Raper and 

Fennell (1965), Domsch et al. (1980) and Klich 

(2002). There are about eight teleomorphic 

genera which have an Aspergillus conidial state 

(Table 11.2), although many Aspergillus species 

(about 60%) have no known sexual state. Among 

the purely asexual aspergilli are some of the 

most important species such as A. parasiticus, 

A. flavus, A. oryzae, A. niger and A. fumigatus. Geiser 

et al. (1996) proposed that the ability to reproduce 

sexually has been lost on many separate 

occasions, because many strictly mitotic Aspergillus 

species have teleomorphic species as their 

closest relatives. The loss of the teleomorph 

seems to have occurred very recently on an evolutionary 

timescale, which is also indicated by 

the fact that many Aspergillus species still produce 

sterile structures (e.g. sclerotia) or cells 

(e.g. Hülle cells; see below) which are similar to 

those found in cleistothecia. Such defects hint 

at the deletion of one or more of the many genes 

whose products are necessary for cleistothecium 

formation and meiosis. It is possible that purely 

asexual species are more likely to become extinct 

because they accumulate mutations without the 

possibility of meiotic recombination. Whilst the 

parasexual cycle can certainly be used to bring 

about efficient genetic recombination in the 

laboratory (Bradshaw et al., 1983; see Plate 4d), 

it is doubtful whether it occurs sufficiently 

frequently in nature to present a viable alternative 

to meiosis (Geiser et al., 1996). 

It is a contentious question as to how to name 

purely mitotic species. To bring current efforts at 

unifying anamorphic and teleomorphic taxonomy 

to an extreme, these Aspergillus species 

would have to be given the name of a teleomorph 

which does not exist. An additional problem is 

that the anamorphic features by which the 

genus Aspergillus is divided into sections do not 

correspond to the groupings obtainable with 

phylogenetic analyses (Peterson, 2000b). The 

nomenclature and taxonomy of Aspergillus are 

thus in a horrible state of flux, and for the time 

being we have a clean conscience in continuing 

to use the name Aspergillus, especially for those 

species with no teleomorph. One desirable consequence 

of this approach is that it considerably 

reduces the degree of confusion in mycology 

courses. The same approach, of course, applies to 

Penicillium. For both taxa, we will now introduce 

examples of the most common teleomorph 

forms. 

Eurotium 

Members of this genus are widely distributed in 

nature, especially in soil. They are responsible for 

the spoilage of foodstuffs, especially those with 

high osmotic concentrations. A typical example 

is E. repens (Fig. 11.16), which is common on 

mouldy jam. In culture, conidia are formed on 

agar media low in sugar content (e.g. 2% malt 

extract). The hyphal segment from which the 

conidiophore arises persists as a swollen foot cell 

(Fig. 11.16a). The tip of the conidiophore swells to 

form a club-shaped vesicle bearing directly on its 

surface a cluster of bottle-shaped phialides which 

give rise to chains of green conidia in basipetal 

succession. On agar media with a high sugar 

content (e.g. 2% malt extract with 20% sucrose), 

yellow spherical ascocarps also develop and 

conidia are sparse, so that the entire Petri 

dish may look bright yellow instead of olive 

green. Aerial hyphae develop coiled ascogonia 

(Fig. 11.16b), and although there are reports of 

associated antheridia, these are not always seen. 

The ascogonium becomes invested by sterile 

hyphae which grow up from the stalk of the 

ascogonium. The ascogonium becomes septate, 

and from its segments ascogenous hyphae 

develop which penetrate and dissolve the

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309 

Fig11.16 Eurotium repens. (a) Conidiophore. 

(b)Ascogonium.(c)Ascogoniumsurroundedbysterile 

hyphae. (d) Cleistothecium showing mature and 

immature asci. 

surrounding pseudoparenchyma derived from 

the investing hyphae. Globose asci develop from 

croziers at the tips of the ascogenous hyphae 

and, when ripe, the ascocarp consists of clusters 

of asci surrounded by a single-layered, yellowcoloured 

peridium. The peridium breaks open 

irregularly. The asci do not discharge violently, 

but the ascospores escape as the ascus wall 

breaks down. The ascospores are broadly lenticular, 

and are without obvious surface ornamentation 

in E. repens, although they may bear an 

equatorial furrow in other species. 

Eurotium repens, like nearly all Eurotium spp., 

is homothallic, and cultures can be transferred 

by means of conidia, ascospores or hyphal tips. 

If successive conidial transfers are made, the 

ability to form ascospores declines with each 

transfer. Ascospore production can be restored to 

the initial level by making one subculture from 

an ascospore (Mather & Jinks, 1958). This suggests 

that the formation of cleistothecia and conidiophores 

is partially controlled by cytoplasmic 

determinants, and it also indicates a way 

in which purely anamorphic forms may have 

evolved from Eurotium. Little recent work seems 

to have been carried out on sexual reproduction 

in Eurotium. 

Emericella 

Emericella differs from Eurotium in a number of 

features. Whilst in Eurotium the ascocarp is eventually 

surrounded by a single-layered peridial 

envelope, that of Emericella is enclosed by chains 

of very thick-walled cells termed Hülle cells


of the nest-like arrangement of cleistothecia surrounded 

by Hülle cells. This species has been used 

widely in genetic studies on sexual and parasexual 

recombination (Roper, 1966; Bos & Swart, 

1995) and, more recently, for experiments on 

morphogenetic aspects (see p. 299) as well as 

the biosynthetic pathways of penicillin and 

mycotoxins (pp. 302 and 304). 

Fig11.17 Emericella nidulans. (a) Conidiophore. Note that the 

phialides are not borne directly on the vesicle. (b) Hu«lle cells, 

thick-walled cells surrounding the ascocarp. (c) Ascus and 

ascospores. Note that the ascospores bear a double flange. 

(a) and (c) to same scale. 

(Fig. 11.17b). Whereas the ascospores of Eurotium 

are colourless and without conspicuous ornamentations, 

those of Emericella are red and bear 

a prominent double equatorial flange, so that 

the spores resemble pulley wheels (Fig. 11.17c). 

The conidiophores also differ in that the phialides 

are not borne directly on the vesicle but on 

a series of cylindrical cells termed metulae. 

The best-known species is the soil fungus 

Emericella (Aspergillus) nidulans, so called because 

11.4.8 Penicillium and its teleomorphic 

states 

Keys to Penicillium have been provided by Pitt 

(1979, 2000) and Ramírez (1982). The anamorphic 

genus Penicillium presents the same kind of taxonomic 

and nomenclatural problems as Aspergillus. 

The classical conidial apparatus is a branched 

conidiophore, bearing successive whorls of 

branches which terminate in clusters of phialides 

(Figs. 11.11, 11.18). Members of the subgenus 

Aspergilloides produce phialides directly on 

the conidiophore and are thus superficially similar 

to Aspergillus. An example is P. spinulosum 

(Fig. 11.18a). More commonly, the phialides are 

borne on a further whorl of branches, the 

metulae, and such species are grouped by their 

phialide shape and depending on whether the 

penicilli are symmetrical (subgenus Biverticillium) 

or more irregular (subgenus Furcatum). Examples 

are given in Figs. 11.18b,c. A third possibility 

is that the metulae may in turn arise from a 

further verticil of branches, the rami (subgenus 

Penicillium; e.g. P. expansum, Fig. 11.18d). In some 

species, e.g. P. claviforme, the individual conidiophores 

may be aggregated together into clubshaped 

fructifications or coremia (Fig. 11.19). 

As in the case of Aspergillus, the morphology 

of the conidiophore unfortunately does not 

correlate with DNA sequencing data (Peterson, 

2000a), and it is possible that Penicillium will 

eventually be broken up into several new genera. 

However, whilst of only limited taxonomic value, 

the conidiophore architecture will continue 

to be used for identification purposes. Some 

species of Penicillium have teleomorphs which 

can be assigned to Talaromyces or Eupenicillium. 

The different kinds of ascocarp represented by 

these generic names can be correlated weakly 

with conidiophore branching (see below). As for

EUROTIALES 

311 

Fig11.18 Conidiophores of the four anamorphic subgenera of Penicillium.(a)Penicillium spinulosum (subgenus Aspergilloides). 

(b) Penicillium verruculosum (subgenus Biverticillium). (c) Penicillium citrinum (subgenus Furcatum), possibly ‘one of the most common 

eukaryotic life forms on earth’ (Pitt,1979). (d) Penicillium expansum (subgenus Penicillium). 

Aspergillus, there is evidence that the ability to 

reproduce sexually has been lost on several independent 

occasions in Penicillium (LoBuglio et al., 

1993). 

Penicillium is one of the most ubiquitous 

groups of fungi, occurring on all kinds of decaying 

materials. The conidia are universally present 

in air, so that Penicillium colonies are frequent 

contaminants of cultures. It was such a chance 

contaminant which led to the discovery of penicillin 

(see p. 302). Penicillium italicum and 

P. digitatum cause rotting of citrus fruits 

(Plate 4e) whilst P. expansum causes a brown rot 

of apples (see p. 304). 

Fig11.19 

plate. 

Penicillium claviforme producing coremia on an agar 

Eupenicillium 

Members of the genus Eupenicillium produce 

conidiophores which may be mono-, bi- or terverticillate. 

The terverticillate species (subgenus 

Penicillium) have been particularly well studied 

because many of them are relevant to man as 

producers of antibiotics (P. griseofulvum), in food 

production (e.g. P. camemberti and P. roqueforti) or


food spoilage (e.g. P. aurantiogriseum, P. digitatum, 

P. italicum, P. expansum), or as mycotoxin producers 

(P. expansum). A superbly illustrated key to 

terverticillate Penicillium spp. has been produced 

by Frisvad and Samson (2004), accompanied by 

phylogenetic analyses in which the grouping of 

these species into sections has been correlated 

with morphological features and the production 

of mycotoxins and other metabolites (Samson et 

al., 2004). An overview of secondary metabolites 

within Penicillium subgenus Penicillum has been 

compiled by Frisvad et al. (2004). 

In phylogenetic analyses, species of Penicillium 

subgenus Penicillium aggregate in a well-resolved 

Fig11.20 Talaromyces.(a)Talaromyces stipitatus, conidiophore. (b) Ascus and ascospores. Note the equatorial frill. (c) Talaromyces 

vermiculatus, ascocarp. (d) Conidiophore. Note the long tapering phialides characteristic of the subgenus Biverticillium. 

(e) Ascogenous hyphae and asci. Note that some asci arise in chains.

EUROTIALES 

313 

Fig11.21 Elaphomycesgranulatus.Two 

ascocarps, one cut open to show 

contents. 

Fig11.22 Elaphomyces 

granulatus. (a) Asci showing 

seven and two ascospores. 

(b) Mature ascospore. 

cluster around E. crustosum (Peterson, 2000a). 

Eupenicillium spp. produce cleistothecia with 

very tough peridia. The ascospores have pulley 

wheel-like flanges. Penicillium spp. associated with 

Eupenicillium often produce thick-walled sclerotia, 

and it is likely that these sclerotial forms are 

cleistothecial forms which have lost their ability 

to complete meiosis. 

Talaromyces 

The ascocarp of Talaromyces is rather different 

from that of Eupenicillium in having a peridium 

with soft cottony hyphae. It is thus a 

gymnothecium rather than a cleistothecium. 

Penicillium anamorphs of Talaromyces all belong 

to the subgenus Biverticillium (LoBuglio et al., 

1993), with long tapering phialides which are 

closely appressed to each other, rather than 

divergent (Fig. 11.20). In this they resemble 

Paecilomyces (Fig. 11.11c), some species of which 

are also associated with Talaromyces (see 

Table 11.2). 

11.4.9 Elaphomycetaceae 

Like so many other apparently diagnostic structures 

of fungi, the hypogeous (¼ subterranean) 

habit of the truffle has evolved independently 

several times. Whereas the best-known edible 

truffles belong to the Pezizales (see p. 423), the 

Elaphomycetaceae are firmly included among 

the Eurotiales (Geiser & LoBuglio, 2001). The 

genus Elaphomyces contains the most common 

hypogeous fungi of temperate climates, and 

E. granulatus (Figs. 11.21, 11.22) and E. muricatus 

can be collected throughout the year beneath the


litter layer under various trees, but especially 

beech with which they form ectomycorrhizal 

associations. Elaphomyces muricatus is often parasitized 

by Cordyceps ophioglossoides forming yellow 

mycelium around the subterranean fruit bodies, 

and a club-shaped perithecial stroma above 

ground (Plate 4f). There are 5 British species 

(Pegler et al., 1993) and about 20 species worldwide. 

Elaphomyces spp., along with other truffles 

and epigeous fungi, form an important part 

of the winter diet of squirrels (Currah et al., 

2000). The common name, hart’s truffle, indicates 

that the fruit bodies of Elaphomyces spp. 

are dug up and consumed by deer. 

The fruit bodies of Elaphomyces vary in size 

(about 1 4 cm in diameter) and are regarded as 

cleistothecia. When cut open, a two-layered rind 

(peridium) can be distinguished from a central 

mass containing the globose asci, traversed by 

lighter sterile ‘veins’. The asci in E. granulatus 

usually contain six spores and in E. muricatus two 

to four. The spores are dark brown and thickwalled 

when mature, and the conditions necessary 

for their germination are not known. There 

are no anamorphic states. 

Further evidence of the remarkable plasticity 

of fruit body morphology in the fungi comes in 

the shape of an unusual member of the 

Elaphomycetaceae from tropical South America. 

In Pseudotulostoma, a subterranean initial produces 

a sizeable stalk (up to 7 cm high) with 

a head which looks much like the gleba of 

a puffball but is, in fact, a cleistothecium. 

At maturity, the peridial layers disintegrate, 

leaving the ascospores to be distributed by the 

wind (Miller et al., 2001).

12 

Hymenoascomycetes: Pyrenomycetes 


The Pyrenomycetes are defined here according 

to Samuels and Blackwell (2001) as fungi which 

produce non-fissitunicate or occasionally prototunicate 

asci usually in flask-shaped ascomata 

(perithecia), less frequently in cleistothecia. The 

sub-class Pyrenomycetes is one of several groups 

belonging to the huge and heterogeneous class 

Hymenoascomycetes. The characteristic feature 

of this class is that the asci develop in an 

ascohymenial way, i.e. the ascoma is formed after 

plasmogamy and the pairing of nuclei have 

occurred, and the asci therefore arise from a 

hymenium. This is in contrast to asci being 

formed singly (Archiascomycetes, Hemiascomycetes), 

scattered throughout the fruit body (Plectomycetes), 

or formed in a locule within a preformed 

fruit body (Loculoascomycetes). Although 

the term ‘Pyrenomycetes’ is not generally understood 

in a taxonomic sense at the present, 

Samuels and Blackwell (2001) pointed out the 

monophyly of a core group of orders, including all 

those which we shall describe in this chapter 

(summarized in Table 12.1). 

The development of the perithecium follows 

several different schemes defined by Luttrell 

(1951), which are described in more detail for 

the different orders. Following fertilization and 

plasmogamy, the ascogonium gives rise to 

ascogenous hyphae while the perithecial wall is 

formed by hyphae arising from the ascogonial 

stalk or elsewhere. Sterile hyphae growing up 

from the basal fertile region (paraphyses) and 

periphyses which line the inner surface of the 

ostiole, may be present. The development of the 

opening of the perithecium is typically schizogenous, 

i.e. it is formed by the pushing apart 

of tissue by the periphyses at the apex of the 

perithecium. This is in contrast to lysigenous 

development, e.g. in the pseudothecial neck of 

Loculoascomycetes (see p. 459). Perithecia may be 

formed singly or in a perithecial stroma. 

Ascospore discharge is by active turgor-driven 

liberation or occurs passively, with the ascospores 

oozing out of the perithecial ostiole as 

a tendril (cirrhus). 

Although the core orders belonging to the 

Pyrenomycetes appear to be monophyletic, the 

fungi considered here follow numerous different 

lifestyles. Many species grow saprotrophically 

in terrestrial habitats, while others are associated 

with plants, covering a wide range from 

mutualistic or commensalistic endophytes over 

biotrophic pathogens through to hemibiotrophic 

and necrotrophic pathogens. Animals, especially 

insects, are also parasitized. Numerous biologically 

active metabolites are produced, including 

alkaloids, antibiotics and phytotoxins. 

12.2 Sordariales 

The order Sordariales is a substantial group of 

ascomycetes containing some 7 families, 115 

genera and over 500 species. We shall study 

representatives of only 2 families, the 

Sordariaceae (6 genera, 37 spp.) and 

Chaetomiaceae (15 genera, 150 spp.).

316 HYMENOASCOMYCETES: PYRENOMYCETES 

Table 12.1. Core groups of Pyrenomycetes as treated in this chapter. Species numbers (in brackets) are based 

mostly on Kirk et al. (2001). 

Taxon Examples ofteleomorphs Examples of anamorph 

Sordariales (see p. 315) Sordaria (14) 

Podospora and Schizothecium (80) 

Neurospora (12) 

Chrysonilia 

Chaetomium (80) 

Xylariales (see p. 332) Daldinia (13) Nodulisporium 

Xylaria (100) 

Nodulisporium 

Biscogniauxia (25) 

Nodulisporium 

Hypoxylon (120) 

Nodulisporium,Geniculosporium 

Kretzschmaria (5) 

Nodulisporium 

Hypocopra (30) 

Podosordaria (17) 

Lindquistia 

Poronia (2) 

Rosellinia (100) 

Dematophora 

Hypocreales (see p. 337) Hypocrea (100) Trichoderma 

Hypomyces (30) 

Cladobotryum,Verticillium 

Nectria (28) 

Acremonium,Cylindrocarpon, 

Fusarium 

Gibberella (10) 

Fusarium 

Sphaerostilbella (4) 

Gliocladium 

Clavicipitales (see p. 348) Claviceps (36) Sphacelia 

Cordyceps (100) 

Beauveria, Metarhizium, 

Tolypocladium 

Epichloe (8) 

Neotyphodium 

Balansia (20) 

Ephelis 

Ophiostomatales (see p. 364) Ophiostoma (100) Graphium, Leptographium, 

Sporothrix, Pesotum 

Microascales (see p. 368) Microascus (13) Cephalotrichum, Scopulariopsis, 

Wardomyces 

Ceratocystis (14) 

Thielaviopsis 

Sphaeronaemella (5) 

Gabarnaudia 

Diaporthales (see p. 373) Diaporthe (75) Phomopsis 

Cryphonectria (6) 

Endothiella 

Apiognomonia,Gnomoniella (18) Discula 

Magnaporthaceae (see p. 377) Magnaporthe (4) Pyricularia 

Gaeumannomyces (5) 

Phialophora 

Glomerellaceae (see p. 386) Glomerella (5) Colletotrichum 

The best-known genera of Sordariaceae are 

Sordaria, Podospora and Neurospora. Many Sordaria 

and Podospora spp. are coprophilous, fruiting on 

the dung of herbivores, but species growing on 

wood or in soil are also known. Neurospora occurs 

in nature on burnt soil and vegetation, especially 

in warmer countries. All three genera have 

been extensively used in genetic studies.

SORDARIALES 

317 

The dark-coloured perithecia usually have an 

ostiole lined by periphyses, but some genera are 

astomous, i.e. they have fruit bodies lacking 

ostioles, thus forming cleistothecia. Stromata are 

not produced. The asci are unitunicate and thinwalled, 

and the apical apparatus of the ascus is 

in the form of a thickened annulus or apical 

plate which does not stain blue with iodine. Freeended 

paraphyses are often present but may 

dissolve at ascus maturity. The ascospores are 

black and sometimes surrounded by a mucilaginous 

epispore, or they have mucilaginous 

appendages. The spores are mostly unicellular 

and germinate through a germ pore. 

In the Chaetomiaceae, the ascomata (perithecia 

or sometimes cleistothecia) are generally 

clothed with thick-walled ornamented hairs. The 

club-shaped asci are thin-walled and without 

apical apparatus. If a hamathecium is formed, it 

does not persist. The ascus wall dissolves and, in 

perithecial forms, the ascospores are extruded as 

a cirrhus. The ascospores are grey to brown in 

colour, mostly unicellular and with a single 

germ pore. Molecular data indicate a close 

relationship between the Chaetomiaceae and 

Sordariaceae (Huhndorf et al., 2004). 

12.2.1 Sordaria (Sordariaceae) 

Most species of Sordaria are cellulolytic. 

Perithecia are common on the dung of herbivores 

and occasionally on other substrata such as 

seeds and plant remains, while a few species are 

reported from soil. Guarro and von Arx (1987) 

have given a key to 14 species, 5 of which are 

coprophilous. Lundqvist (1972) has described and 

illustrated Nordic species. Sordaria fimicola is 

especially common on horse dung and has been 

widely used in experiments on nutrition, the 

physiology of fruiting, spore liberation and 

genetics. It is homothallic, and perithecial development 

occurs within 10 days on a wide range of 

media. A longitudinal section of a perithecium 

(Fig. 12.1) shows a basal tuft of asci at different 

stages of development. The asci elongate in turn 

so that only one ascus can occupy the ostiole at 

a time. Because each spore is about 13 mm wide 

and the diameter of the apical apparatus of the 

Fig12.1 Sordaria fimicola. (a) L.S. perithecium. 

(b) Ascus apex. (c) Ascospore showing mucilaginous 

epispore. After Ingold (1971).


ascus is only about 4 mm, the latter acts as a 

sphincter, gripping the spores as they leave the 

ascus. Projectiles which vary in size from one to 

eight spores may be formed. The larger the 

number of spores in the projectile, the greater 

the distance of discharge due to the fact that the 

surface-to-volume ratio of single spores is greater 

than that of multiple-spored projectiles, so that 

the effects of wind resistance are disproportionately 

high (Ingold & Hadland, 1959). Thus, 

single-spored projectiles have a mean discharge 

distance of about 1.5 cm whilst for eight-spored 

projectiles the distance is about 6 cm. The necks 

of the perithecia are phototropic and, as in 

many other coprophilous fungi, this adaptation 

ensures that the spores are projected away 

from the dung substratum. The ascospores of 

S. fimicola have a distinct mucilage envelope 

which enables them to adhere to herbage, but in 

S. humana the sheath is much reduced or absent. 

The ascospores of S. fimicola can survive for long 

periods. On drying, gas vacuoles (de Bary bubbles) 

may appear in the spore cytoplasm, but despite 

this the spores remain viable, and the bubbles 

disappear upon rehydration (Ingold, 1956; 

Milburn, 1970). Ascospore germination is 

enhanced by digestive treatment in the herbivore 

gut and this effect can be simulated in the 

laboratory by treatment with pancreatin or 

sodium acetate. 

Perithecium development 

There have been numerous studies on perithecial 

development and structure in Sordaria, e.g. in 

S. fimicola (Mai, 1977), S. humana (Uecker, 1976; 

Read & Beckett, 1985) and S. macrospora (Hock 

et al., 1978). Intercalary multinucleate cells of 

vegetative hyphae give rise to multinucleate, 

spirally coiled, septate ascogonia which are not 

associated with antheridia. In these species, 

there is no trichogyne and there are no microconidia 

(spermatia). The ascogonium is enveloped 

by branched investing hyphae which 

originate from the ascogonial stalk or from 

adjacent vegetative hyphae to form a spherical 

protoperithecium, i.e. an immature ascoma 

which does not, at this stage, show differentiation 

into a neck or ostiole. The outer region of 

the protoperithecium is made up of about five 

layers of rounded cells which have thick, 

pigmented (melanized) walls. Lying inside them 

are several layers of flattened, thinner, nonpigmented 

cells (see Fig. 12.1). Differentiation of 

the innermost cells of the protoperithecium 

gives rise to the centrum consisting of elongate, 

free-ended, thin-walled, septate paraphyses and 

ascogenous cells. As the ascoma matures, it 

changes in outline from spherical to pearshaped 

with an elongate neck, thus developing 

into a perithecium. Neck development is associated 

with meristematic activity of the cells at 

the base of the neck and by the appearance of 

short, tapering periphyses which line it. By 

pushing against each other the periphyses 

create the ostiole, the opening to the outside 

through which the asci will discharge their 

spores. Thus, the cells are pushed apart rather 

than lysed, and this process of ostiole development 

is called schizogenous. Phototropism of the 

perithecial neck is associated with differential 

enlargement of the periphyses. 

The ascogenous hyphae arise on a placentalike 

mound at the base of the centrum and 

elongate upwards. They show the usual type of 

crozier found in many ascomycetes with a 

binucleate penultimate cell (the mother cell of 

an ascus), a terminal cell and a stalk cell (see 

Fig. 8.10). Proliferation of the ascogenous hypha 

occurs by fusion of the recurved terminal cell 

with the stalk cell. Nuclear fusion in the ascus 

mother cell is followed by meiosis, yielding four 

haploid nuclei. Two further mitotic divisions 

produce 16 nuclei. Cleavage of the cytoplasm 

accompanied by wall formation results in eight 

binucleate ascospores. The fine structure of 

ascospore development has been studied by 

Mainwaring (1972). 

Perithecium development is affected by environmental 

factors such as temperature and 

nutrient supply. For S. macrospora, Hock et al. 

(1978) have shown that in pure culture on a 

defined nutrient medium, perithecium development 

requires a simultaneous supply of biotin 

and arginine. In the presence of certain other 

fungi such as Armillaria spp. and Mortierella spp., 

S. fimicola is stimulated to increased production 

of perithecia and ascospores and it is likely that 

this effect is related to the production of

SORDARIALES 

319 

vitamins by the stimulating fungi (Watanabe, 

1997). 

Mating systems of Sordaria 

Although S. fimicola is homothallic, it has the 

ability to hybridize. Wild-type strains have black 

ascospores, but mutants are known with pale or 

colourless spores. If a wild-type strain and a 

white-spored mutant strain are inoculated on 

opposite sides of a Petri dish, hybrid perithecia 

develop from heterokaryotic parts of the mycelium. 

The asci from hybrid perithecia usually 

have four black and four white ascospores. Six 

different arrangements of the ascospores are 

found in such hybrid asci (Fig. 12.2). Asci with 

four black or four white ascospores at the tip of 

the ascus are those in which the gene for spore 

colour segregated at the first meiotic nuclear 

division separating the paired chromosomes. In 

those with two black or two white ascospores at 

the tip of the ascus, segregation of the gene for 

spore colour occurred at the second meiotic 

division separating the two sister chromatids of 

each chromosome. First-division segregation 

results from the absence of a cross-over between 

the gene for spore colour and the centromere of 

the chromosome, whilst second-division segregation 

results from a single cross-over between 

gene and centromere. Since the likelihood of 

crossing-over depends on the distance between 

gene and centromere, the frequency of the two 

kinds of segregation pattern can be used for 

determining the distance of the gene for spore 

colour relative to the centromere. 

A low proportion of hybrid asci shows 5 : 3, 

6 : 2 or (very rarely) 7 : 1 colour segregation 

patterns. These findings are explained in terms 

of gene conversion, a non-reciprocal process 

where one allele of a gene converts another 

allele at the same locus to its own type (Lamb, 

1996). Similar patterns have been reported 

in other ascomycetes, e.g. Ascobolus immersus 

(p. 423). A model to account for the molecular 

basis of gene conversion was developed with the 

smut fungus Ustilago maydis (see p. 652). In this 

so-called ‘Holliday model’ DNA strands are 

exchanged at ‘Holliday junctions’ between two 

paired DNA double helices, which can result in 

the generation of hybrid or heteroduplex DNA. 

Following separation of the two double helices 

from each other, non-matching DNA will be 

excised and the undamaged strand will be used 

as template to synthesize the second, damaged 

strand (Holliday, 1964; Lewin, 2000). This can 

then give rise to the phenomenon of gene 

conversion which, if it happens in the ascus, 

is manifested as deviations from the 4 : 4 gene 

segregation patterns. 

Fig12.2 Sordaria fimicola.Squash 

preparation from a hybrid perithecium. 

Most ripe asci contain four black and 

four white ascospores.


Sordaria brevicollis and S. heterothallis are 

heterothallic. Both species form minute spermatia 

which are involved in the fertilization of 

mycelia of the opposite mating type. Sordaria 

brevicollis is a heterothallic relative of S. fimicola 

according to Guarro and von Arx (1987). In 

S. brevicollis it has been discovered that perithecium 

development can occur in unmated 

cultures of mating type A. In about 30% of such 

perithecia one or two asci with viable ascospores 

may form, with all spores being mating type A 

(Robertson et al., 1998). 

The molecular basis of homothallism has 

been elucidated in S. macrospora by Pöggeler 

et al. (1997). The molecular configuration of the 

genes conferring the ability to mate is similar 

to that in two heterothallic members of the 

Sordariaceae, Podospora anserina and Neurospora 

crassa. In Neurospora crassa (see Fig. 12.7) the 

haploid mating types are designated A and a. The 

‘alleles’ which confer mating competence in 

P. anserina and N. crassa consist of dissimilar 

DNA sequences termed idiomorphs which are 

present at the homologous loci in the mating 

partners. This term has been introduced to 

denote sequences like those of mating types A 

and a, which occupy the same locus in different 

strains but are related neither in sequence nor 

(probably) by common descent (Metzenberg & 

Glass, 1990). In S. macrospora, the two idiomorphs 

are contiguous (i.e. adjoin each other), and they 

have been used in experiments to transform (þ) 

and ( ) strains of P. anserina in order to induce 

them to form perithecia. 

12.2.2 Podospora and Schizothecium 

(Sordariaceae) 

The perithecia of Podospora and Schizothecium 

develop on herbivore dung. In Podospora, the 

upper part of the perithecium wall is often 

ornamented by various kinds of ‘vestiture’ 

(Lundqvist, 1972) such as short or long single 

hairs or long, pointed setae which may be 

aggregated into a tuft to one side of the 

perithecial neck as seen in P. anserina and 

P. curvicolla. In Schizothecium, the hairs are 

composed of swollen cells and agglutinate 

together to form short scale-like tufts (Bell & 

Mahoney, 1995). The separation between these 

two genera has been confirmed by phylogenetic 

analyses (Cai et al., 2005). Taking Schizothecium 

and Podospora together, about 80 species are 

known (Mirza & Cain, 1969; Lundqvist, 1972). 

Different species show a degree of substrate 

specificity. For instance, perithecia of P. curvicolla, 

P. pleiospora and S. vesticola are especially common 

on the dung of lagomorphs (rabbits and hares) 

whilst P. curvula fruits commonly on horse dung 

(Lundqvist, 1972; M. Richardson, 1972, 2001). The 

reasons for these preferences are not known. 

Some species have semi-transparent perithecia 

within which the outline of the club-shaped asci 

can be seen and the sequential development 

and discharge of individual asci can be followed 

(Fig. 12.3a). The number of spores in the ascus 

varies from 4 to 512. Spore number has been 

used as a taxonomic criterion in the past, 

although the species concept has been widened 

to include forms with a range of spore numbers. 

For example, 8-, 16-, 32- and 64-spored forms of 

Podospora decipiens are recognized. The name 

Podospora (Gr. podos ¼ foot, spora ¼ seed) refers 

to the mucilaginous appendage attached to one 

or both ends of the black ascospore (Fig. 12.3b). 

This character is also found in Schizothecium. In 

some of the commonest species, P. curvula and 

S. tetrasporum, the upper spore appendages are 

attached to the cap of the ascus, and when the 

ascus explodes, the spores, roped together by 

their appendages, are propelled as a single slingshot 

projectile (Fig. 12.3c). As in Sordaria, it has 

been shown that multi-spored projectiles are 

discharged further than single spores (Walkey & 

Harvey, 1966a). The ascus wall breaks across, just 

beneath the cap, and in contrast to Sordaria there 

is usually no distinctive apical apparatus. 

Developmental aspects 

Many morphological and experimental studies 

have been made on P. anserina, which Lundqvist 

(1972) treated as a synonym of P. pauciseta. This 

fungus was originally described from goose dung 

but also fruits on the dung of sheep, horse, 

cattle, mice, grouse and zoo animals. 

Perithecium development has been described 

for P. anserina (Beckett & Wilson, 1968; Mai, 

1976) and Schizothecium spp. (Bell & Mahoney,

SORDARIALES 

321 

Fig12.3 Schizothecium tetrasporum. (a) Perithecium 

showing asci through the semi-transparent wall. 

(b) Ascus. (c) Projectile consisting of four spores 

attached to the ascus cap and to each other by means of 

mucilaginous appendages. 

1996). It is similar to that described above for 

Sordaria. 

The development of the ascospores of 

P. anserina has been studied by Beckett et al. 

(1968). The ascospores (four in P. anserina, but see 

below) are delimited by a double membrane 

system as in other ascomycetes (Fig. 12.4). The 

primary spore wall develops between the two 

membranes and gradually pushes them apart. 

The inner membrane continues to function as 

the plasma membrane of the spore, whilst the 

outer functions as the spore-investing membrane. 

As the primary spore wall widens, 

secondary wall material is laid down towards 

the inside of the primary wall. These primary and 

secondary walls enclose the whole of the spore, 

including the spore head and the tail. A tertiary 

wall representing the pigmented layer of the 

spore head is laid down to the inside of the 

secondary layer (Figs. 12.4e g). The elongated 

tail of the spore is cut off from the spore head by 

a septum. The tertiary wall layer does not extend 

into the spore tail, which therefore remains colourless. 

Its contents degenerate. This part of the 

spore persists as the primary appendage, sometimes 

termed the pedicel. Secondary appendages 

develop at the apex of the spore head 

and at the primary appendage. They arise 

by localized evaginations of the spore-investing 

membrane. A thinner area in the tertiary wall at


Fig12.4 Podospora anserina, ascospore development (based on Beckett et al.,1968). (a) Binucleate ascospore initial enclosed by two 

membranes, between which the primary spore wall develops. (b d) The secondary spore wall develops within the primary wall, 

and the secondary appendages develop towards each end of the spore by outpushing of the spore membrane. (e g) Development of 

tertiary, pigmented wall layer. A further mitotic nuclear division occurs.The uninucleate tail of the spore is cut off from the body of 

the spore, and its cytoplasm degenerates, but the tail persists as the primary appendage. Note that the tertiary wall layer does not 

extend into the primary appendage. At the opposite pole, a thinner area in the tertiary wall marks the position of the germ pore. 

the end of the spore opposite the primary 

appendage marks the position of the germ pore 

(Fig. 12.4f). The secondary appendages of many 

species of Podospora are very elaborate branched 

structures. 

Mating systems of Podospora 

Anamorphs of Podospora species, where known, 

consist of dark-celled phialides which produce 

small, sticky, unicellular, uninucleate, hyaline 

phialoconidia assigned to the anamorph genera 

Phialophora and Cladorrhinum. These do not 

germinate and are presumed to function as 

spermatia (Bell & Mahoney, 1997; Lundqvist 

et al., 1999). 

The sexual compatibility within the genus 

varies. Most species for which information is 

available are homothallic, including species with 

eight-spored asci such as P. decipiens, and species 

with more than eight spores in the ascus, e.g. 

P. pleiospora (Lundqvist et al., 1999). Podospora 

anserina and S. tetrasporum are pseudohomothallic 

(Esser, 1974; Raju & Perkins, 1994). Podospora 

anserina normally has four-spored asci, each 

ascospore eventually becoming quadrinucleate 

following two post-meiotic mitotic nuclear divisions 

(see Fig. 12.6). During the final stages of 

development three nuclei remain in the main 

body of the spore and one nucleus passes into 

the primary spore appendage, where it

SORDARIALES 

323 

degenerates. Cultures derived from single ascospores 

form perithecia readily. Occasionally, 

however, smaller uninucleate ascospores may 

occur in some asci and when such spores are 

germinated, the resulting mycelium does not 

fruit. Instead, perithecia only develop when 

certain strains derived from uninucleate ascospore 

cultures are paired together. On each such 

strain, spermatia and ascogonia bearing trichogynes 

are formed, but these are self-incompatible; 

perithecia only develop if trichogynes of 

one strain are spermatized by spermatia of 

a genetically distinct strain. Thus, although the 

behaviour of the large ascospores suggests that 

P. anserina is homothallic, it is clear that the 

underlying mechanism controlling perithecial 

development is a heterothallic one of the usual 

bipolar type (i.e. with (þ) and ( ) strains). Most 

of the large ascospores (about 97%) contain 

nuclei of the two distinct mating types (Esser, 

1974). 

The fact that such a high proportion of the 

binucleate ascospores in four-spored asci contain 

nuclei of two distinct mating types implies some 

regulated process of nuclear movement and 

arrangement. The normal sequence of nuclear 

divisions occurs during ascus development, 

including the two nuclear divisions of meiosis 

and a post-meiotic mitosis (PMM). The plane of 

the two meiotic nuclear divisions lies parallel to 

the long axis of the developing ascus, but the 

spindles formed during PMM lie at a right angle 

to it (Fig. 12.5). Delimitation of the ascospores 

(closure) caused by invagination of the ascosporedelimiting 

membrane is associated with a ‘cage’ 

of microfilaments surrounding each spore 

initial. At the same time a ‘rope’ of microfilaments 

running along the whole length of the 

ascus develops, and the cage of each ascospore 

initial becomes attached to it (Figs. 12.5a,b). 

Pairing between nuclei of differing mating 

types occurs during the cleavage of the ascospores 

and this appears to be mediated by astral 

microtubules radiating from their closely associated 

spindle pole bodies (SPBs) and pulling the 

two nuclei together (Thompson-Coffe & Zickler, 

1994). This pairing between genetically different 

nuclei during ascospore formation is similar 

to the recognition mechanism leading to 

Fig12.5 Nuclear alignment in the pseudohomothallic 

four-spored fungi Podospora anserina and Neurospora 

tetrasperma. Fine continuous lines represent the spore cell 

membrane (omitted in c for clarity); dotted lines represent 

microfibrils; thicker continuous lines represent microtubules. 

Spindle pole bodies (SPBs) are shown as black bars and nuclei 

as open circles or ovals. (a) Following post-meiotic mitosis 

(PMM) the eight nuclei are seen in pairs linked to each other 

by microtubules which radiate from the SPBs. A rope of 

actin myosin is forming along the centre line of the ascus. 

(b) The nuclei become rearranged and move to a staggered 

formation along the microfibrillar rope as microfibrillar cages 

form and microfibrils extend upwards towards the SPBs.The 

spore membranes begin to invaginate. (c) Nuclei are re-aligned 

in a row, presumably by the actin myosin rope and cage 

assembly. Redrawn fromThompson-Coffe and Zickler (1994), 

with permission from Elsevier. 

karyogamy in the crozier prior to meiosis. 

Where the SPBs are not closely associated, 

uninucleate spores develop. 

It is interesting to compare nuclear behaviour 

within the asci of the two pseudohomothallic 

four-spored ascomycetes Podospora anserina and 

Neurospora tetrasperma (see Fig. 12.6). In N. tetrasperma, 

the mating type idiomorphs A and a lie 

close to the centromere so that A and a almost 

invariably go with the centromeres to opposite 

poles of the first meiotic division spindle (M I ), 

i.e. there is first-division segregation of the 

alleles for mating type. The second division 

spindles (M II ) then overlap. The third nuclear


Fig12.6 Schematic diagram of ascus development in the two pseudohomothallic ascomycetes Neurosporatetrasperma and Podospora 

anserina (based on Raju & Perkins,1994). Neurospora tetrasperma: (a,b) First meiotic nuclear division M I 

.The mating type alleles A and 

a are closely linked to the centromere and segregate at the first division. (c) During the second meiotic nuclear division M II 

the 

spindles of the dividing nuclei lie in tandem parallel to the long axis of the ascus. (d) Interphase of M II 

; the nuclei are aligned in pairs. 

(e) Telophase of a post-meiotic mitosis PMM I 

; the spindles are paired and lie transversely to the long axis of the ascus. (f) Interphase 

of PMM I 

; the four pairs of nuclei are realigned more or less regularly to one side of the ascus prior to ascospore delimitation. 

(g) Young ascospores are binucleate and heterokaryotic, containing both kinds of mating type allele. (h) Following a second 

post-meiotic mitosis PMM II 

, the ascospores contain four nuclei, two of each mating type. Podospora anserina: the alleles for mating 

type are not tightly linked to the centromere and do not segregate at M I 

(b) but at M II 

(c). (d f) as for N. tetrasperma.(g)Following 

ascospore delimitation, four binucleate, heterokaryotic ascospores are formed. (h) A second post-meiotic division has occurred. 

Three of the four resulting nuclei, two of one mating type and one of the other, remain in the body of the ascospore whilst the 

fourth nucleus migrates to the basal appendage and degenerates. 

division (PMM) brings A and a nuclei close 

together in four pairs, and walls develop 

around the nuclei and cytoplasm so that the 

binucleate ascospores each contain one A and 

one a nucleus. In P. anserina, the same result is 

achieved by different means. The mating type 

idiomorphs (þ) and ( ) are sufficiently distant 

from the centromere for a single cross-over to 

occur between the centromere and the locus of 

the idiomorphs. Second-division spindles do not 

overlap and, by the mechanism outlined above, 

nuclei of opposite mating types are brought close 

together at the PMM stage and become enclosed 

in walls as binucleate ascospores. A further 

mitosis brings the number of nuclei in each 

ascospore to four, and three nuclei remain in the 

body of the ascospore whilst one migrates to the 

tail (Raju & Perkins, 1994).

SORDARIALES 

325 

Mating type factors in Podospora anserina 

As explained above, wild-type P. anserina is 

pseudohomothallic, each binucleate ascospore 

normally containing both distinct mating type 

idiomorphs matþ and mat , whilst uninucleate 

ascospores contain either matþ or mat . The 

genes which control mating type specificity have 

been labelled FPR1 and FPR2 (fertilization plus 

and minus regulators). The molecular structure 

of both genes has been determined (Debuchy & 

Coppin, 1992; Coppin et al., 1997). The matþ locus 

contains 3800 + 200 base pairs (bp) with the FPR1 

gene within it, whilst the mat locus is larger 

and contains 4700 + 200 bp, enclosing FPR2 and 

three regulatory genes SMR2, SMR2 and FMR1. 

There is a close similarity between the structure 

of the mating type genes in P. anserina and 

Neurospora crassa. 

Studies on incompatibility in 

Podospora anserina 

Incompatibility is usually defined as the genetic 

control of mating competence, but this concept 

extends beyond the sexual phase to the vegetative 

phase. Two different systems provide genetic 

control, namely homogenic and heterogenic 

incompatibility (Esser & Blaich, 1994). 

Homogenic incompatibility is caused by the 

sexual incompatibility of nuclei carrying identical 

idiomorphs, and it thus favours outbreeding. 

In contrast, in heterogenic incompatibility (also 

known as heterokaryon, somatic or vegetative 

incompatibility), the coexistence of nuclei in a 

common cytoplasm is inhibited by the genetic 

difference in one or more genes. Thus heterogenic 

incompatibility restricts outbreeding. It 

may also play a role in speciation. Another 

consequence is the reduced risk of transmission, 

following hyphal anastomosis, of the spread of 

infectious cytoplasmic elements such as mycoviruses 

or transposons (e.g. in Cryphonectria, 

p. 375). 

Heterogenic incompatibility was discovered 

when attempts were made to cross strains of 

P. anserina of different geographic origin. When 

two mycelia grow towards each other and intermingle, 

hyphal anastomosis occurs. Nuclear 

exchange is not inhibited but is followed by an 

antagonistic reaction, sometimes accompanied 

by death of the fusing cells and by profuse 

branching of adjacent cells. This barrage 

phenomenon, observed as a white or colourless 

zone between two mycelia, occurs irrespective of 

mating type. Perithecium formation may occur 

in inter-racial crosses of differing mating types 

but the number of perithecia is much reduced. In 

some pairings, one or both of the reciprocal 

crosses between the different mating partners 

are unsuccessful. 

Nine unlinked loci are now known to be 

involved in the control of heterokaryon incompatibility, 

and these are termed het loci. A het 

locus can be defined as a locus in which 

heteroallelism cannot be tolerated in a heterokaryon. 

The nine het loci comprise five allelic 

systems (in which different alleles of the same 

gene provoke vegetative incompatibility) and 

three non-allelic systems (involving the interactions 

of two specific alleles from different loci). 

One locus (het-V) is simultaneously involved in an 

allelic and a non-allelic interaction (Saupe, 2000). 

The molecular structures of the genes at some of 

these loci have been characterized. The different 

genes encode very different products in the form 

of HET polypeptides. Complexes between the 

different HET polypeptides may function in the 

recognition process between self and non-self 

and may act as the trigger to mediate biochemical 

events causing vegetative incompatibility. 

Alternatively, HET heterocomplexes may function 

to poison the cell and thus may directly 

mediate growth inhibition and death (Glass et al., 

2000). 

The het-s/het-S allelic system of P. anserina is of 

particular interest. Both alleles encode polypeptides 

differing only in a few amino acids, 

and incompatibility results if a heterodimer is 

formed. However, whilst the HET-S protein is 

immediately active, HET-s is initially translated 

as an inactive form, HET-s , which is present in 

a soluble form in the cytoplasm. Biologically 

active HET-s molecules may arise by a rare 

spontaneous rearrangement to another tertiary 

conformation, and HET-s molecules have the 

ability to convert HET-s to their own state by 

catalysing this conformational change. This 

interaction may lead to the formation of aggregates. 

Once initiated, the conversion of HET-s to


HET-s spreads like an infection throughout a 

mycelium at a rate of several mm h 1 . Further, 

transmission can occur from a HET-s containing 

hypha to a HET-s mycelium by anastomosis. 

The ability of a protein to convert others to 

its own state in an infectious transcriptionindependent 

manner, accompanied by the 

formation of cytoplasmic aggregates, has the 

hallmarks of a prion disease (Coustou et al., 1997; 

Coustou-Linares et al., 2001). 

Senescence in Podospora anserina 

Podospora anserina has been the subject of 

research into senescence and has been treated 

as a model of the ageing phenomenon in more 

complex organisms (Griffiths, 1992; Bertrand, 

2000; Silar et al., 2001). In P. anserina senescence is 

defined as a diminution in the ability of cells to 

proliferate and/or differentiate. This may or may 

not culminate in cell death. In pure cultures of 

P. anserina, senescence is marked by a progressive 

reduction in growth rate and loss of ability to 

form perithecia. Eventually it proves impossible 

to transfer viable sub-cultures so that a given 

isolate has a limited lifespan. Different isolates of 

P. anserina have characteristic lengths of growth 

before growth ceases, and the mean lengths of 

growth can be used as a convenient indicator of 

lifespan. For example, two races A and S grown 

on cornmeal agar in glass tubes (20 150 mm) at 

26°C in the dark had mean lengths of 15 and 

170 cm, respectively (Smith & Rubenstein, 1973). 

A hypothesis to explain the phenomenon of 

senescence in P. anserina is that, after a period of 

growth characteristic of a given race of the 

fungus, a senescence factor appears in a culture 

and is presumed to be produced, or to reproduce 

itself, more rapidly than other cellular components. 

The factor is transmissible through hyphal 

anastomosis, i.e. fusion between a senescent 

hypha and a non-senescent hypha results in the 

non-senescent hypha acquiring the factor 

controlling senescence. Senescence is inherited 

maternally; it can be transmitted to 90% of the 

progeny of a senescent protoperithecial strain 

but to none of the progeny of a spermatial 

parent. No nuclear mixing is involved. 

A large number of genes (between 600 and 

3000) can modulate lifespan; 50% increase it 

and 50% diminish it (Rossignol & Silar, 1996). 

Senescence is a complex process affected by 

environmental factors and is also controlled 

by the interactions between nuclear and mitochondrial 

DNA (Osiewacz & Kimpel, 1999; 

Osiewacz, 2002). The onset of senescence is 

marked by the appearance of dysfunctional 

mitochondria and of circular plasmid-like senility 

DNAs derived from the mitochondria. 

During the respiratory activities of mitochondria, 

reactive oxygen species (ROS) are generated 

as by-products and these molecules are able to 

damage all cellular components, leading to 

cellular dysfunctions such as the cytochrome 

oxidase pathway (Osiewacz, 2002). To compensate 

for these dysfunctions, ROS scavengers can 

be produced which reduce the level of ROS. 

Alternative oxidative pathways may also be 

induced which may help in reducing the adverse 

effects of ROS (Dufour et al., 2000; Lorin et al., 

2001). It is interesting that different mutants 

with defective mitochondrial DNA associated 

with growth arrest can be restored to wild-type 

mitochondrial DNA by crossing, indicating 

an important role of sexual reproduction in 

this pseudohomothallic fungus (Silliker et al., 

1997). 

12.2.3 Neurospora (Sordariaceae) 

There are about 12 species of Neurospora, mostly 

growing on soil. A key has been provided by 

Frederick et al. (1969). Many species grow in 

humid tropical and subtropical countries but 

others have been reported from temperate areas 

(Perkins & Turner, 1988; Turner et al., 2001). In 

nature, the most conspicuous species colonize 

burnt ground and charred vegetation following 

fire caused by volcanic eruptions or deliberate 

burning to clear vegetation (slash and burn) or 

crop residues such as sugar cane. Within a few 

days the burnt areas are covered by an orange or 

pink powdery mass of macroconidia. The 

commonest species here is N. intermedia (Perkins 

& Turner, 1988). The association with burnt 

ground is related to the fact that dormant 

ascospores in the soil are stimulated to germinate 

by heat. Neurospora species also grow in 

warm humid environments such as wood-drying

SORDARIALES 

327 

kilns and bakeries where they cause serious 

trouble because of their rapid growth and 

sporulation. For this reason N. sitophila is sometimes 

called the red bread mould. Strains of 

N. intermedia are used in the preparation of the 

fermented food ‘omchom’ (ontjom) in which 

conidia are used to inoculate soybean or 

peanut solids from which oil and protein have 

been extracted by pressing. 

Neurospora as a genetic tool 

Neurospora has been widely used in genetic and 

biochemical studies (Perkins, 1992; Davis, 1995). 

The development of auxotrophic mutants 

deficient in successive steps of arginine 

biosynthesis led to the proposition of the ‘onegene 

one-enzyme’ hypothesis by Beadle and 

Tatum (1941) who were awarded the Nobel 

Prize in 1958. There is a very extensive literature 

relating to the genus. The loci of over 1000 genes 

have been mapped (Perkins et al., 2000), and the 

complete genome of N. crassa has now been 

sequenced. It is haploid and has seven chromosomes. 

The best-known species are N. crassa and 

N. sitophila, both of which are eight-spored and 

heterothallic. Neurospora tetrasperma is fourspored 

and pseudohomothallic. Some other 

species, e.g. N. africana, N. dodgei and N. terricola, 

are homothallic (Coppin et al., 1997). The homothallic 

species do not form conidia. 

The reasons why Neurospora has proven so 

useful as a tool in biochemical and genetic 

research are: (1) that it is haploid; (2) that wildtype 

strains have simple nutritional requirements, 

namely a carbon source, simple mineral 

salts and one vitamin, biotin; (3) that mutations 

can be induced readily by the use of chemical 

mutagens or UV irradiation of conidia; (4) that 

growth and sexual reproduction is rapid; and 

(5) that tetrad analysis by dissecting asci is 

straightforward. By the use of marked strains it 

is now not even necessary to dissect asci because 

tetrad analysis can be performed on octets of 

projected ascospores. Another advantage of 

Neurospora is that cultures can be preserved for 

long periods in suspended animation as spores 

stored over silica gel, or following lyophilization 

or freezing. 

The life cycle of Neurospora 

The life cycle of N. crassa is illustrated diagrammatically 

in Fig. 12.7. The name Neurospora is 

derived from the characteristically ribbed ascospores. 

The ascospore walls bear dark, raised, 

thicker ribs separated by thinner, paler, 

branched or unbranched inter-costal veins 

(Figs. 1.19 and 12.8). The spores are multinucleate 

and have reserves of lipids and the carbohydrate 

trehalose. The dark ascospores of N. crassa are 

viable for many years and do not germinate 

readily unless treated chemically (e.g. by furfural) 

or by heat shock (e.g. 60°C for 20 40 min). 

In contrast, the conidia are killed by such heat 

treatment. Following treatment, the ascospores 

germinate through a germ pore at either or both 

ends, forming at first a globose, inflated vesicle 

and then a coarse, incompletely septate, rapidly 

growing mycelium, each segment of which is 

multinucleate. Cytoplasm and organelles including 

nuclei pass freely through the septa. 

Within 24 h, the mycelium can begin asexual 

reproduction. The cues inducing conidial development 

include light, desiccation, and nutrient 

deprivation. Upright branches develop which, 

instead of continuing to grow by hyphal tip 

elongation, undergo repeated apical budding. 

The resulting cells are separated from each other 

by incomplete septa with a wide central pore. 

These cells have been termed proconidia 

(Springer & Yanofsky, 1989). The proconidia 

continue to bud apically, forming multinucleate 

macroconidia (blastoconidia) separated from 

each other by septa with narrower pores. The 

septa thicken and develop a centripetal furrow 

which widens, leaving a central strand of 

material, the connective, by which the spores 

remain attached to each other. Further conidia 

develop by budding of the terminal conidium 

on a chain and, when the terminal conidium 

gives rise to two buds, the chain branches 

(Figs. 12.8d,e; Hashmi et al., 1972). Conidia of 

this type belong to the form genus Chrysonilia 

(formerly Monilia). The individual segments of the 

spore chain break apart and are readily dispersed 

by wind. The surface of macroconidia in wildtype 

strains is made up of hydrophobin rodlets 

which impregnate it, but the conidia of the 

easily wettable mutant eas are devoid of rodlets


Fig12.7 The life cycle of Neurospora crassa, diagrammatic and not to scale (based on Fincham & Day,1971).The fungus is 

heterothallic and a mature ascus (left of diagram) contains four haploidmultinucleate ascospores of mating type a and four of mating 

type A. Ascospores germinate to form a branched, incompletely septate mycelium with multinucleate segments. Multinucleate 

macroconidia and uninucleate microconidia develop, and both types of conidium can germinate to form a new mycelium. 

Protoperithecia, consisting of a coiled ascogonium and a trichogyne, and surrounded by sterile hyphae, also develop on the haploid 

mycelium (right of diagram).When microconidia or macroconidia of opposite mating type are transferred to a trichogyne, 

plasmogamy (P) occurs and the protoperithecium develops into a perithecium. Ascogenous hyphae containing paired A and a nuclei 

grow out from the ascogonium. At the tip of the ascogenous hypha a crozier develops (bottom of diagram) and, within the 

penultimate cell, karyogamy (K) occurs between nuclei of the two mating types.Within this diploid cell, which is the ascus initial, 

meiosis (M) takes place, followed by mitoses (not shown). Ascospores are cleaved around the nuclei (not shown) and the mature 

asci discharge their ascospores through the neck of the perithecium.

SORDARIALES 

329 

Fig12.8 Neurospora crassa. (a) Ascus. 

(b) Ascospores showing ribbed surface. 

(c) Protoperithecium showing projecting 

trichogyne. (d) Macroconidia from one-day-old 

culture. (e) Enlarged view of developing 

macroconidia. (f) Microconidia forming sticky 

clusters. (g) Enlarged view showing origin of 

microconidia. (a d,f) to same scale; 

(e,g) to same scale. 

and cohere in sticky masses (Beever et al., 1978). 

The pink colour of the conidia is due to the 

presence of a carotenoid pigment, neurosporoxanthin, 

which is stimulated to develop by 

light. The spores are formed in vast numbers. 

In laboratories they can cause serious contamination 

of other cultures, partly because of the 

rapid growth of the mycelium (up to 5 mm h 1 ), 

and partly because macroconidia can develop 

in profusion beyond the rims of closed Petri 

dishes. In humid environments, the mycelium 

may grow through the cotton wool plugs of testtube 

cultures and sporulate on the plugs. Shaw 

(1993) has reported that macroconidia formed on 

steamed pine logs in Queensland, Australia, are 

collected by honeybees in their pollen baskets. 

Cultures derived from a single ascospore also 

develop two other types of reproductive structure. 

In contrast to the large, dry, wind-dispersed 

macroconidia which are formed within 1 2 days, 

clumps of smaller, oval, uninucleate, sticky 

microconidia develop after about 12 15 days 

(Figs. 12.8f,g; Maheshwari, 1999). The conidiogenous 

cells from which the microconidia develop 

have been interpreted as reduced phialides. The 

microconidia are capable of slow and variable 

germination but function primarily as spermatia. 

Coiled ascogonia, terminated by long tapering 

trichogynes and surrounded at the base by 

hyphae, also develop (Fig. 12.8c). Such structures 

are termed protoperithecia or bulbils and each 

often forms several trichogynes. In N. crassa and 

N. sitophila, no further development occurs in 

single ascospore cultures, i.e. each strain is selfincompatible. 

Incompatibility is controlled by a 

pair of mating type idiomorphs, A and a, and 

if two compatible strains are grown together in 

a Petri dish for a few days, microconidia of one


strain can be transferred to trichogynes of the 

opposite strain by flooding with sterile water. In 

nature it is possible that mites or insects are 

involved in transfer. There is evidence that a 

microconidium produces a pheromone which 

induces directional growth (positive chemotropism) 

of a trichogyne of opposite mating type 

towards it before plasmogamy occurs (Bistis, 

1983). The transfer of macroconidia or hyphae 

of the opposite strain to a trichogyne can also 

effect fertilization. Fusion between the trichogyne 

and the fertilizing cell is followed by 

the migration of one or more nuclei from the 

fertilizing cell down the trichogyne into the 

ascogonium. The development of ripe perithecia 

occurs within 7 10 days and follows the typical 

general ascomycete pattern. This has been 

described by Nelson and Backus (1968) in two 

homothallic species. Much is now known of the 

genetic control of sexual development in 

Neurospora and several genes have been identified 

which control steps in the process. The cytological 

details of ascus development have also 

been worked out. After the eight-nucleate 

stage in the developing ascus of N. crassa, several 

mitoses ensue so that a fully developed 

ascospore may contain as many as 32 nuclei 

(Raju, 1992a). 

Mating type genes in Neurospora 

In N. crassa, heterokaryons are not normally 

formed between mycelia of opposite mating 

types, and this implies that plasmogamy usually 

occurs only between a trichogyne of one strain 

and a fertilizing agent (e.g. a microconidium, 

macroconidium or hypha) of the opposite strain. 

This condition is termed restricted heterokaryosis. 

Even within one mating type, the ability 

to form heterokaryons is under genetic control, 

i.e. there is heterokaryon incompatibility as in 

Podospora anserina and heterokaryons generally 

develop only if the het genes which control 

compatibility are homoallelic (see p. 325). 

Several het genes have been identified (Mylyk, 

1976; Perkins, 1992), and Micali and Smith (2003) 

have provided evidence of a yet more complex 

regulation of heterokaryon incompatibility in 

the shape of suppressor genes which modify the 

effect of het and mating type genes. When the 

mycelia of unlike genotype anastomose, cytoplasmic 

incompatibility results in vacuolation 

and disorganization of cell contents in the 

region of the anastomosis. Similar cytoplasmic 

reactions are visible when anastomosis occurs 

between the hyphae of wild-type strains differing 

in mating types. In contrast to N. crassa, heterokaryons 

are readily formed between different 

mating type strains of N. tetrasperma, which thus 

exhibits unrestricted heterokaryosis. 

The molecular structure of the A and a 

idiomorphs has been elucidated in N. crassa. 

They are strikingly dissimilar (Glass et al., 1988). 

The A idiomorph is composed of a region of 

5301 bp bearing little similarity to the a idiomorph 

comprising 3235 bp (Glass et al., 1990; 

Staben & Yanofsky, 1990). The A idiomorph of 

N. crassa is also involved in heterokaryon incompatibility. 

There are similarities in the structure 

and functions of the mating type idiomorphs 

between N. crassa, Podospora anserina and the 

yeasts Saccharomyces cerevisiae and 

Schizosaccharomyces pombe, but there are also 

differences (p. 266; Glass & Lorimer, 1991). The 

idiomorphs of N. crassa are larger than those of 

the yeasts. Mating type idiomorphs are present 

in several homothallic species of Neurospora 

which hybridize with the A DNA probe of N. 

crassa (Coppin et al., 1997). This and other lines of 

evidence suggest that the heterothallic condition 

was primitive and that the homothallic condition 

has probably arisen several times in the 

course of evolution and may have a selective 

advantage (Metzenberg & Glass, 1990). 

The pseudohomothallic condition, represented 

by N. tetrasperma, is of interest. This 

species is functionally homothallic in that the 

mycelium from a single heterokaryotic ascospore 

containing nuclei of two distinct mating types 

can develop perithecia directly. However, homokaryotic 

mycelia can develop from uninucleate 

ascospores and also from about 20% of macroconidia. 

Such mycelia are capable of outcrossing. 

Raju (1992b) has summarized, 

Thus N. tetrasperma appears to have the best of 

both worlds. On one hand the single-mating-type 

homokaryotic cultures offer N. tetrasperma the 

advantages of outbreeding. On the other hand the

SORDARIALES 

331 

heterokaryotic (A þ a) cultures have the potential 

advantage of hybrid vigour. They can also enter the 

sexual cycle and produce ascospores without waiting 

for a sexual partner. This is very useful in situations 

where rapid completion of the life cycle is 

advantageous. 

Neurospora and the biological clock 

Many organisms show a daily (circadian) rhythm 

in their activities, entrained by a combination 

of light and temperature (Dunlap, 1999). When 

transferred to a uniform environment, they may 

continue to display the same rhythm, suggesting 

that it is controlled by some internal clock. 

Important research helping to interpret the 

molecular basis of circadian rhythmicity in 

fungi as well as other eukaryotes is being 

performed on N. crassa (Davis, 1995; Liu, 2003; 

Dunlap & Loros, 2004). A band mutant (bd) was 

discovered which, when grown in culture in long 

tubes, formed alternating bands of macroconidia 

interspersed by non-sporulating bands. In continuous 

darkness, bands continued to form, with a 

periodicity of 21.5 h, little affected by temperature. 

From the bd mutant, further mutants were 

developed by mutagenesis in which the frequency 

of the circadian rhythm was affected. The frq 

locus was identified as a key control element 

of the frequency of sporulation, with partial 

loss-of-function mutations capable of shortening 

the frequency to as little as 16 h or extending 

it to 29 h. The effect of temperature on the 

circadian rhythm seems to be controlled by the 

temperature-dependent alternative splicing of 

the frq mRNA, giving either of two major FRQ 

proteins (Colot et al., 2005). Several other loci are 

also involved in the integration of the rhythm 

with temperature and light. The white collar wc-1 

and wc-2 gene products are especially important, 

forming a heterodimer (WCC ¼ white collar 

complex) which stimulates frq transcription. The 

FRQ dimer, in turn, inhibits existing WCC and 

lowers the continued expression of WC-1, thus 

introducing a circadian pattern into the cycle 

such that the levels of FRQ proteins hit their 

lowest point late at night, and WC-1 (and WCC 

activity) late in the day (Dunlap & Loros, 2004). 

It should be noted that regulation is partly at 

the level of gene expression, partly by 

translation of existing mRNA molecules, and 

partly by protein phosphorylation/dephosphorylation. 

Entrainment of the rhythm, i.e. the 

switching on of the clock, is sensitive to blue 

light and the photo-receptor has been identified 

as the WC-1 component of WCC coupled with the 

chromophore FAD (flavin-adenine dinucleotide). 

12.2.4 Chaetomium (Chaetomiaceae) 

There are over 80 species of Chaetomium (von Arx 

et al., 1986), many of which are cosmopolitan, 

growing in soil and fruiting on cellulose-rich 

substrata such as seeds, textiles in contact with 

soil, straw, sacking and dung. Wood infected by 

Chaetomium spp. may undergo a superficial decay 

known as soft rot. Wood inside buildings 

damaged by flooding or water used in fire 

control is particularly susceptible. Most species 

are saprotrophic and cellulolytic, but some have 

been isolated from human lesions. Some produce 

mycotoxins (Ugadawa, 1984) and others have 

been used in biological control because of their 

competitive ability to colonize cereal stubble, 

thus displacing plant-pathogenic fungi (Dhingra 

et al., 2003). Many potentially valuable chemical 

compounds such as enzymes (cellulases, xylanases), 

pharmaceutical products and antifungal 

substances have been extracted from Chaetomium 

in culture. Chaetomium thermophile is thermophilic 

and has potential for use in composting palm 

oil fibre for recycling biomass (Suyanto et al., 

2003). 

The perithecia of Chaetomium are superficial, 

barrel-shaped, thin-walled and, in most species, 

clothed with projecting, dark, stiff hairs. In 

C. elatum, one of the commonest species, the 

hairs are dichotomously branched. In others, 

e.g. C. cochliodes, the body of the perithecium 

bears straight or slightly wavy, unbranched 

hairs, whilst the apex bears a group of spirally 

coiled hairs. The hairs are roughened or ornamented, 

and the type of ornamentation is an aid 

to identification (Guarro & Figueras, 1989). It is 

likely that the perithecial hairs have special 

functions. Jerking caused by the movement of 

the hairs over each other on drying may help in 

ascospore dispersal. Another possible function is 

to deter grazing of the perithecia by insects and


Fig12.9 Chaetomium globosum. (a) Perithecium showing 

cirrhus of ascospores. (b) Asci. (c) Ascospores. 

other arthropods (Wicklow, 1979). When the 

perithecia are ripe, a column-like mass (cirrhus) 

of dark ascospores is extruded through the 

ostiole, supported by the perithecial hairs 

which surround it (Fig. 12.9a). The spore 

column results from the breakdown of the asci 

within the body of the perithecium, i.e. the asci 

do not discharge their spores violently. The 

young asci are cylindrical to club-shaped, but 

this stage is very evanescent and is only found 

in young perithecia (Fig. 12.9b), often before 

the spores have become pigmented and sometimes 

before the perithecium has developed an 

ostiole. Spores of most species are pale brown to 

grey and lemon-shaped, with a single terminal 

germ pore. 

The development of perithecia in 

Chaetomium shows some variation between 

species (Whiteside, 1957, 1961). The ascogonia 

are coiled and lack antheridia. Investing hyphae 

arise from the ascogonial stalk or from vegetative 

cells surrounding the ascogonium. 

Perithecial hairs develop early from the external 

cell layer. The centrum is at first filled with 

hyaline pseudoparenchyma. At the apex of the 

perithecium, certain of these cells become 

meristematic and give rise to the elongate 

periphyses which line the inside of the ostiole. 

Ascogenous hyphae develop from the ascogonium 

at the base of the centrum and, at about 

this time, the surrounding pseudoparenchyma 

cells of the centrum deliquesce to form a cavity. 

In some species croziers develop, but in others 

they are absent. Paraphyses of two types have 

been described. In C. brasiliense, lateral paraphyses 

arise from the pseudoparenchyma cells 

outside the hymenium, whilst hymenial paraphyses 

have been illustrated in C. globosum 

(Whiteside, 1961). The paraphyses are evanescent 

and disappear as the asci mature. 

Most species of Chaetomium are homothallic, 

but a few, e.g. C. cochliodes, are heterothallic. 

Both homo- and heterothallic strains of C. elatum 

have been reported. Conidial states are rare in 

Chaetomium, but simple phialides and phialospores 

occur in C. elatum and C. globosum, whilst 

C. piluliferum forms both phialospores and 

globose thalloconidia of the Botryotrichum type 

(Daniels, 1961). 

12.3 Xylariales 

The order Xylariales is probably polyphyletic and 

comprises about 800 species in 8 families (Kirk 

et al., 2001). Members of this group produce dark 

perithecial stromata with asci which have an 

iodine-positive apical apparatus. Ascospores are 

typically melanized. Xylariales are saprotrophs 

or plant pathogens and are associated especially 

with the bark and wood of trees. 

We shall only consider one family, the 

Xylariaceae, which is by far the most important. 

The dark-coloured ascospores are generally 

smooth-walled and inaequilateral (one face 

being more strongly curved than the other), 

with a hyaline germ slit. Anamorphs are sometimes 

also stromatic, producing hyaline or 

lightly pigmented conidia holoblastically from 

a sympodially proliferating conidiogenous 

region, the sympodula (Fig. 12.13). They have

XYLARIALES 

333 

been placed in several anamorph genera, including 

Geniculosporium and Nodulisporium (Rogers, 

1979, 2000; Whalley, 1996). Some develop as a 

thin covering of the perithecial stroma. The 

conidia are dry and are dispersed by air currents, 

rain splash or insects. 

There are about 40 genera in the Xylariales. 

Most species (e.g. Xylaria, Hypoxylon, Daldinia) are 

hemi-saprotrophic or saprotrophic, fruiting on 

wood. These forms are ligninolytic and cause 

white-rot of their substrate (Rayner & Boddy, 

1988; Eaton & Hale, 1993). The limits of the 

mycelial colonies in decaying wood are demarcated 

by black zone lines (pseudosclerotial 

plates) made up of brown bladder-like fungal 

cells which fill the wood tissue (Campbell, 1933). 

Other genera fruit on herbivore dung, e.g. 

Hypocopra, Poronia, Podosordaria and Wawelia. 

Some are serious plant pathogens; for example, 

Hypoxylon mammatum (H. pruinatum) causes 

canker of aspen (Populus tremuloides and other 

Populus species) in North America (Manion & 

Griffin, 1986), Biscogniauxia mediterranea causes 

canker of cork oak (Quercus suber), and B. 

nummularia causes strip canker of beech (Fagus 

sylvatica). Kretzschmaria (Ustulina) deusta causes a 

fatal butt rot of beech, elm (Ulmus) and horse 

chestnut (Aesculus hippocastanum), whereas 

Rosellinia necatrix is a plurivorous root pathogen 

known to attack over 130 plant species. Members 

of the Xylariaceae have been isolated as endophytes 

(symptomless symbionts or commensals) 

from a range of plants on which they do not fruit 

so that their host range and distribution may 

extend far beyond that which would have been 

inferred from the occurrence of their ascocarps 

(Petrini & Petrini, 1985; Petrini et al., 1995). 

Although some species are plurivorous, others 

have a restricted host range, e.g. H. fragiforme 

which generally fruits on dead beech twigs 

(Fagus) and Xylaria carpophila which fruits only 

on fallen beech cupules. 

The development of perithecia in the family 

conforms to what Luttrell (1951) has termed the 

‘XyIaria’ type: 

The ascogonia are produced free upon the mycelium 

or more commonly within a stroma. Branches 

from the stalk cells of the ascogonium or from 

neighbouring vegetative hyphae surround the 

ascogonium and form the perithecial wall. Hyphal 

branches with free tips (paraphyses) grow upward 

and inward from the inner surface of the wall over 

the base and sides of the perithecium. Pressure 

exerted by the growth of opposed paraphyses 

expands the perithecium and creates a central 

cavity. The perithecium becomes pyriform as a result 

of growth of hyphae in the apical region of the wall 

to form a neck. The layer of inward-growing hyphae 

is continuous up the sides and into the perithecial 

neck. Growth of these hyphae within the neck 

produces a schizogenous ostiole lined with free 

hyphal tips (periphyses). The ascogonium produces 

ascogenous hyphae which typically grow out along 

the inner wall over the base and sides of the 

perithecium. Asci derived from the ascogenous 

hyphae grow among the paraphyses to form a 

continuous hymenium of asci and more or less 

persistent paraphyses lining the perithecial cavity. In 

some forms the paraphyses are evanescent, and the 

ascogenous hyphae form a plexus in the base of the 

perithecium. The asci then arise in a single 

aparaphysate cluster. 

The cytology of ascus development in Xylaria 

(Beckett & Crawford, 1973; Rogers, 1975a) and in 

the related genus Hypoxylon (Rogers, 1965, 1975b) 

follows the usual pattern in most cases. The 

ascospores may be uninucleate, binucleate, 

or occasionally multinucleate (Rogers, 1979). 

In X. polymorpha and H. serpens, immature 

ascospores are divided by a septum near the 

base which cuts off a small appendage. The 

appendage disappears in the mature ascospore, 

leaving a truncate base. The ascospore wall of 

Daldinia concentrica, as seen with the transmission 

electron microscope, consists of five 

recognizable layers numbered progressively 

from the outside inwards as wall layers 

W1 W5 (Beckett, 1976a). The thin, non-pigmented 

outer layer W1 acts as a sheath which 

completely encloses the spore. Before germination 

this layer is sloughed off (see below). The 

wall of the mature ascospore is dark, probably 

due to the pigment melanin located in an inner 

wall layer (W4). There is a hyaline germ slit 

in W4 running the length of the ascospore 

(Fig. 12.10a). Germ slits are microfibrillar in 

construction but their structure varies within 

the family (Beckett, 1979a,b). The germ slits


create a weak point in the ascospore wall, 

causing the spore to gape wide open as it swells 

and permitting the germ tubes to emerge 

(Beckett, 1976b; Chapela et al., 1990; Read & 

Beckett, 1996). The ascus tip contains a cylindrical 

apical apparatus which is amyloid (i.e. it 

stains bright blue with iodine). The apical 

apparatus is pierced by a narrow pore and is 

everted as the ascus explodes (Greenhalgh & 

Evans, 1967; Beckett & Crawford, 1973). 

12.3.1 Daldinia 

There are about 13 species of Daldinia worldwide 

(Ju et al., 1997), 5 of which grow in Northern 

Europe (Johannesson et al., 2000). They form 

concentrically zoned perithecial stromata on 

wood. The best known is D. concentrica, with 

stromata mostly on ash (Fraxinus excelsior) but 

occasionally on other hosts. Daldinia loculata 

(D. vernicosa) and D. fissa form stromata on 

charred branches of birch (Betula), gorse (Ulex) 

and some other hosts following fire. 

Daldinia concentrica colonizes the living 

branches of ash as a symptomless endophyte 

but can continue to grow saprotrophically, 

fruiting on dead branches and trunks. Recently 

infected wood (calico wood) has a dark speckled 

appearance caused by the presence of a darkcoloured 

mycelium in the vessels of the spring 

wood. Boddy et al. (1985) isolated D. concentrica 

from attached branches of ash and regarded it as 

a primary colonizer. Only a small number of 

individual mycelia were isolated from any one 

branch, but often these occupied extensive 

volumes of wood. Individual mycelia are 

detected by their reactions in culture to other 

individuals of the same species. Identical mycelia 

intermingle freely, showing no obvious reaction, 

but mycelia of different genotype show vegetative 

incompatibility when confronted. Such 

observations have led to the suggestion that 

the colonization of attached branches is by a 

process of latent invasion (Boddy & Rayner, 1983) 

whereby the fungus might be distributed in the 

sap stream of the living tree host as mycelial 

fragments or spores. It is likely that D. concentrica 

is heterothallic (Sharland & Rayner, 1986) like 

D. loculata which grows on fire-scorched birch 

branches (Johannesson et al., 2001). In this 

fungus, the Nodulisporium conidial stroma develops 

in spring beneath the birch bark before the 

perithecial stroma emerges. Pyrophilous (fireloving) 

insects feed on the conidia and also 

disperse them. Conidia of different mating types 

and different genotypes may be spread in this 

way, and since some perithecial stromata are 

known to contain several genetically distinct 

perithecia, multiple mating events are possibly 

involved. 

Fig12.10 (a,b) Xylaria hypoxylon. (a) Ascus.The ascus tip to the 

right has been stained with iodine to reveal the apical 

apparatus. (b) Conidiophores. (c,d) Daldinia concentrica. 

(c) Ascogenous hypha (after Ingold,1954b).The numbers 

represent successive asci working backwards from the apex. 

(d) Nodulisporium-type conidiophore.

XYLARIALES 

335 

Daldinia concentrica forms large (5 10 cm 

diameter) hemispherical purplish-brown annual 

stromata called ‘cramp balls’ or ‘King Alfred’s 

cakes’. They contain ripe asci between May and 

October. In cross section (Plate 5a), the stromata 

show a concentric zonation of alternating light 

and dark bands. The surface of young stromata 

may be covered with a pale fawn powdery mass 

of conidia. The conidia are dry and ovoid in 

shape, developing successively at the tips of 

branched conidiophores by the outgrowth of 

the wall and, when detached, leave a small scar 

(Fig. 12.10d). Conidia of this type have been 

named Nodulisporium tulasnei. Perithecia develop 

in the outer layers of the stroma. The perithecial 

wall is lined by ascogenous hyphae which are 

unusual in that there is often a considerable 

distance separating successive asci (Ingold, 

1954b) (Fig. 12.10c). The stroma of Daldinia 

apparently functions as a water reservoir and 

detached stromata will continue to discharge 

ascospores for about 3 weeks even if placed in a 

desiccator (Ingold, 1946). Spore discharge is 

nocturnal and the rhythm of spore discharge is 

maintained for several days if detached stromata 

are kept in continuous dark. In continuous light, 

periodic spore discharge ceases after about three 

days but is restored on return to alternating light 

and dark (Ingold & Cox, 1955). The output 

of spores from a single stroma of average size 

is about 10 million a night. The ability of 

perithecial stromata to store water enables the 

fungus to continue sporulating on dry branches. 

Mycelial growth is also possible at lower water 

potentials ( 10 MPa) than by competing fungi 

(Boddy et al., 1985). 

12.3.2 Xylaria 

There are over 100 species of Xylaria, most of 

which are lignicolous, but some are endophytic 

and others grow on fallen fruits (Whalley, 1985, 

1987). One of the best known is Xylaria hypoxylon, 

the candle-snuff fungus. Stromata are common 

on stumps and fallen branches of deciduous 

trees. As in most Xylariaceae growing on wood, 

the boundaries of individual mycelia within 

infected tissues are visible as conspicuous black 

demarcation lines. The stromata are branched 

and cylindrical or flattened. At the upper end, 

the stroma is covered by a white powdery mass 

of conidia (Figs. 12.10b, 12.11a). Perithecia 

develop later at the base of the stroma and are 

visible externally as swellings at the surface 

(Fig. 12.11b). The apical apparatus of the ascus is 

visible even in immature asci after staining in 

iodine as a bright blue cylindrical collar pierced 

by a narrow pore (Fig. 12.10a). Xylaria polymorpha 

(‘dead men’s fingers’) fruits in late summer and 

autumn at the base of old tree stumps. The 

stromata are swollen, finger-like and clustered 

(Plate 5b). The surface is at first covered by an 

inconspicuous conidial layer, but eventually 

perithecia develop beneath the surface of the 

whole stroma, and are not restricted to the basal 

region as in X. hypoxylon. Both species are active 

wood-rotting fungi causing decay of the whiterot 

type. Other common species with a more 

restricted host range are X. longipes on fallen 

branches of sycamore (Acer pseudoplatanus) and 

X. carpophila on fallen cupules of beech (Fagus 

sylvatica). 

12.3.3 Hypoxylon 

This is a large genus of over 120 species (Whalley 

& Greenhalgh, 1973; Ju & Rogers, 1996) forming 

stromata which are often hemispherical or 

sometimes flattened on the surface of wood 

and bark. Some show a preference for a particular 

host. Common species are H. fragiforme 

almost confined to branches and trunks of 

Fagus (Fig. 12.12a), H. multiforme on Betula 

(Fig. 12.12b), and H. rubiginosum which forms 

flat stromata on decorticated wood of Fraxinus. 

The young stromata of all these species 

bear a conidial felt of the Nodulisporium or 

Geniculosporium type (Fig. 12.13; Chesters & 

Greenhalgh, 1964). Most species show nocturnal 

spore discharge (Walkey & Harvey, 1966b). 

Freshly cut lengths of healthy beech branches 

incubated under water-saturated conditions 

show no evidence of the presence of H. fragiforme, 

but if similar sections are incubated under 

conditions in which the branches are allowed 

to dry, characteristic patches of stained or 

discoloured wood become apparent within 

21 days (Chapela & Boddy, 1988a,b). Isolations 

from such areas produce several genetically


Fig12.11 Xylaria hypoxylon. (a) Conidial 

stroma.Conidia are borne on the white 

tips of the branches. (b) Perithecial 

stromata which have developed at the 

base of the old conidial stroma.The 

knobbly swellings are the perithecia. 

distinct mycelia of H. fragiforme, indicating that 

the infections are derived from a number of 

separate ascospores. The fungus is present in 

apparently healthy sapwood as a number of 

inconspicuous pockets of ‘inoculum units’ from 

which mycelial growth is held in check by the 

high water content of the wood. On drying, 

these infections can spread rapidly. This phenomenon 

is another example of latent invasion 

(Boddy & Rayner, 1983). Chapela (1989) used the 

term ‘xylotropic endophyte’ for fungi such as 

H. fragiforme which occur within living trees and 

have the capacity to extend into secondary xylem 

upon drying of the wood. 

Ascospore eclosion 

The results of experimental studies on ascospore 

germination in H. fragiforme provide a partial 

explanation of its host specificity. Although 

known to fruit on several other woody hosts, 

perithecial stromata are most regularly associated 

with drying branches and trunks of 

European beech (Fagus sylvatica) and American 

beech (F. grandiflora). Ascospores suspended in 

extracts from living F. sylvatica twigs react by a 

dramatic germination process termed eclosion, 

an entomological term for the emergence of 

a pupa from its case or a larva from an egg 

(Chapela et al., 1990, 1993). In H. fragiforme this 

appears to be a host-specific recognition system. 

Exposure to aqueous extracts of beech twigs for 

a period of about 10 min activates the eclosion 

mechanism, which is a two-stage process. In the 

first stage the spore swells slightly and its germ 

slit widens until the pigmented spore wall opens 

abruptly along the germ slit, forcing the outer 

transparent sheath (corresponding to the W1 

layer of D. concentrica) to crack open transversely. 

This stage is a millisecond event. The second 

stage, lasting about 10 s, involves the widening 

of the germ slit up to about 7 mm, and expansion 

of the coloured wall of the ascospore. This 

forces the transparent outer sheath away from 

the rest of the spore, which then escapes and is 

free to germinate by the formation of a germ 

tube. Eclosion is readily observed with the light 

microscope, as summarized in Fig. 12.14 (see 

Webster & Weber, 2004). 

The triggers which stimulate eclosion have 

been identified as two monolignol glucosides, 

Z-syringin and Z-isoconiferin, which are mobile 

transport intermediates of lignin biosynthesis. 

Both induce eclosion at micromolar concentrations. 

However, the presence of these germination 

activators in beech extracts cannot fully 

explain the host specificity of H. fragiforme 

because eclosion is induced by extracts from a 

range of trees which do not normally support 

fruiting of this fungus, such as Abies, Corylus and 

Populus (Chapela et al., 1991).

HYPOCREALES 

337 

Fig12.13 

serpens. 

The conidial (Geniculosporium)stateofHypoxylon 

Fig12.12 Hypoxylon. (a) Perithecial stromata of H. fragiforme 

on beech (Fagus sylvatica).One stroma has been broken open 

to show the perithecia embedded in the outer layer. 

(b) Perithecial stromata of H. multiforme on birch (Betula 

pendula). 

12.4 Hypocreales 

The Hypocreales are a large group of fungi, 

although estimates vary as to the number of taxa 

contained in it. Kirk et al. (2001) included 117 

genera and 654 species, whilst Rossman (1996) 

stated that there may be 2000 5000 holomorphic 

taxa. Some are known only as anamorphs. 

Hypocreales are characterized by pale or brightly 

coloured perithecia (or rarely cleistothecia) 

which may be single or borne on or embedded 

in a fleshy stroma. The asci are unitunicate, with 

or without a well-defined apical apparatus. 

Perithecial development conforms to the 

‘Nectria’ type of Luttrell (1951). The ascogonia, 

which are formed within a stroma, become 

surrounded by concentric layers of vegetative 

hyphae which form a true perithecial wall. The 

cells of the inner wall layer in the apical region 

of the young perithecium produce a palisade of 

inward-growing hyphal branches. These hyphal 

branches grow downward to form a vertically 

arranged mass of hyphae with free ends termed 

apical paraphyses (Luttrell, 1965). Pressure 

exerted by the elongation of the apical paraphyses, 

accompanied by expansion of the wall, 

creates a central cavity within the perithecium. 

The free tips of the apical paraphyses ultimately 

push into the lower portion of the wall so that 

they become attached at both the top and 

bottom of the perithecial cavity. Ascogenous 

hyphae arising from the ascogonium spread out 

across the floor and sides of the cavity and 

produce asci by means of croziers. The asci grow 

upward among the apical paraphyses and form


Fig12.14 The course of events during eclosion of Hypoxylon fragiforme ascospores. (a,b) Dormant spores as seen in median (a) and 

surface view (b), the latter showing the germ slits (arrowheads). (c e) Rupture of wall layer W1along a longitudinal seam, gaping of 

germ fissure of ascospore, and escape of the spore from the perispore shell formed by wall layer W1.The sequence (c e) can be 

observed some10 min after exposure of ascospores to the beech extract. It occurs abruptly, taking about 3 s. (f) Further distension 

of valves composed of wall layers W2 W4, 30 min after addition of beech twig extract.The perispores are still visible as ghosts. 

(g) Formation of a germ tube some 8 h after addition of beech twig extract. All images to same scale. Reprinted from Webster 

and Weber (2004), with permission from Elsevier. 

a concave layer lining the inner surface of the 

wall in the basal region of the perithecium. 

At the upper end of the perithecium a schizogenous 

ostiole develops in the wall. It is lined 

with periphyses, i.e. hyphae with free apices 

which are attached at their bases to the inner 

wall of the neck. At maturity, the perithecia may 

protrude from the stroma and appear to be 

seated on its surface. Perithecial development 

of this type has been described for Nectria 

(Strickmann & Chadefaud, 1961; Hanlin, 1971), 

and for Hypocrea (Canham, 1969). 

There is an exceptionally wide range of 

anamorphs (Rossman, 2000; Seifert & Gams, 

2001). In most cases conidiogenous cells are 

phialides, and these may be terminal or lateral, 

single or grouped in synnemata, sporodochia or, 

more rarely, pycnidia. However, other 

developmental types of conidia may occur and 

in many species there are synanamorphs. The 

conidia are generally light-coloured and 

produced in slimy masses. The names of some 

anamorph genera related to Hypocreales are 

listed in Table 12.2. There is a tendency in 

modern classification, with support of molecular 

evidence, to link anamorph states with teleomorph 

genera even if they have, as yet, no 

proven connection from pure culture studies 

(Rossman, 2000). 

Many Hypocreales are saprotrophs active in 

the decay of plant substrata above ground, in soil 

or fresh water. Others are serious plant pathogens 

(e.g. Nectria and Fusarium spp.) or mycoparasites, 

especially of agaric, bolete or polypore 

basidiocarps (e.g. Hypomyces, Apiocrea and 

Hypocrea; Põldmaa, 2000) but also of cultivated

HYPOCREALES 

339 

mushroom mycelium. Some are lichenicolous. 

The ability to parasitize other fungi has been 

employed for the biological control of fungal 

pathogens of plants, using species of Trichoderma, 

Gliocladium and Clonostachys (see below). 

Several antifungal compounds, e.g. gliotoxin 

or viridin, are produced as secondary metabolites 

by anamorphs of Hypocrea spp. (Trichoderma and 

Gliocladium; see below). Other pharmacologically 

important secondary metabolites synthesized 

by anamorphic Hypocreales include the antibacterial 

antibiotic cephalosporin from Acremonium 

spp. The gibberellins are growth hormones 

ubiquitous in all higher plants, but they were 

first detected as a secondary metabolite 

produced by Gibberella fujikuroi (anamorph 

Fusarium moniliforme). This species causes the 

‘foolish seedling disease’ in rice, in which 

seedlings show excessive stem elongation and 

eventually keel over due to the production of 

gibberellic acid by the infecting fungus 

(Tudzynski, 1997). Mycotoxins poisonous to 

farm animals and humans are produced by 

some species of Fusarium (see below) and other 

species have been reported as human pathogens. 

The edible fungus food ‘Quorn’ is 

Table12.2. Some teleomorph anamorph 

connections in the Hypocreales. 

Teleomorph genus 

Nectria sensu lato 

Bionectria 

Calonectria 

Gibberella 

Hypocrea 

Sphaerostilbella 

Hypomyces 

Apiocrea 

Melanopsamma 

Anamorph genus 

Tubercularia, Fusarium, 

Cylindrocarpon, 

Verticillium, Heliscus, 

Flagellospora 

Clonostachys 

Cylindrocladium 

Fusarium 

Trichoderma,Gliocladium, 

Acremonium-like 

Gliocladium 

Mycogone,Cladobotryum 

Sepedonium 

Stachybotrys 

manufactured by large-scale fermentation of 

F. venenatum (previously identified as F. graminearum) 

(Trinci, 1991; Moore & Chiu, 2001). 

Cellulase production by Trichoderma reesei is 

exploited commercially. 

General accounts of the Hypocreales have 

been given by Rogerson (1970) with keys to 

genera, and by Rossman (1996). The taxonomic 

treatment, i.e. the division into orders and 

families, varies between different authors, some 

placing Claviceps and its allies as a family 

(Clavicipitaceae) of the Hypocreales, whilst 

others, e.g. M. Barr (2001), placed them in a 

separate order (Clavicipitales), a disposition 

followed in this book. However, all are agreed 

that the two groups are closely related, a view 

based on morphological and molecular evidence 

(Spatafora & Blackwell, 1993). Samuels and 

Blackwell (2001) included four families in the 

Hypocreales, i.e. Hypocreaceae, Nectriaceae, 

Bionectriaceae and Niessliaceae, but we shall 

consider representatives only of the first two. 

12.4.1 Hypocrea (Hypocreaceae) 

Species of Hypocrea, of which about 100 are 

known, usually fruit on decaying wood or 

occasionally on herbaceous plant material, forming 

brightly coloured fleshy perithecial stromata, 

with perithecia embedded in the outer 

layers. The thin-walled asci contain 8 two-celled 

ascospores, and in many species the spores 

separate into 2 part-spores before ascus 

discharge, so that 16 part-ascospores are released 

(Fig. 12.15c). The ascospores may be colourless 

(hyaline) or green in colour. Hypocrea pulvinata 

forms bright yellow stromata on the underside 

of dead overwintered basidiocarps of Piptoporus 

betulinus, the birch polypore. It is possible that 

this fungus grows parasitically on the basidiocarp. 

The ascospores are often visible as white 

tendrils issuing from the ostioles of the perithecia 

(Plate 5c). In culture, conidia are formed in 

sticky masses at the tip of single phialides 

(Fig. 12.15b; Rifai & Webster, 1966). Conidia of 

this type are described as Acremonium-like. 

Some species of Hypocrea have conidia of the 

Trichoderma type, in which whorls of phialides 

give rise to separate, sticky green or white


Fig12.15 Hypocrea pulvinata.(a)L.S. 

lower part of fruit body of Piptoporus 

betulinus showing perithecial stromata 

of Hypocrea in section (see also 

Plate 5c). (b) Acremonium-like conidia 

produced from upright phialides. 

(c) Asci and ascospores. Note how 

the two-celled ascospores may 

break up into unicellular part-spores. 

spore masses. Detailed descriptions of Hypocrea 

Trichoderma connections have been given by 

Chaverri and Samuels (2003). Hypocrea rufa 

forms conidia referable to T. viride (Fig. 12.16d), 

a species with globose, warty conidia. Conidia of 

the Gliocladium type, in which conidia derived 

from individual phialides coalesce in a single 

slimy mass, are found in cultures of H. gelatinosa 

(Figs. 12.16a,b; Webster, 1964). The distinction 

between Trichoderma and Gliocladium anamorphic 

states can be difficult and some species, e.g. G. 

virens, have been transferred to Trichoderma as T. 

virens (Fig. 12.17a), the anamorph of H. virens 

(Chaverri et al., 2001). 

The biology and taxonomy of Trichoderma 

have been reviewed by Samuels (1996, 2006), 

ecological aspects by Klein and Eveleigh (1998), 

and keys to identification have been given by 

Gams and Bissett (1998). It is a large genus and 

species identification is difficult using morphological 

criteria. DNA-based and biochemical 

techniques are now widely used to support 

identification. Such studies indicate that 

genus is a monophyletic group within the 

Hypocreaceae which evolved about 110 million 

years ago (Kullnig-Gradinger et al., 2002). 

Trichoderma spp. are cosmopolitan in soil and 

on decaying woody substrata. On soil isolation 

plates, Trichoderma spp. are often the most 

rapidly growing and dominant fungi, smothering 

the plates and forming clusters of sticky 

green phialoconidia within a few days. Certain 

species, especially T. harzianum and T. virens, have 

been used in the biological control of soil-borne 

fungal plant pathogens such as Rhizoctonia solani 

and Pythium ultimum (Papavizas, 1985; Chet, 1987; 

Lumsden, 1992; Tang et al., 2001). Antagonism to 

the fungal pathogen may be associated with 

coiling of Trichoderma around the host hypha, 

followed by penetration and parasitism 

(Figs. 12.17b d). Volatile and non-volatile 

antifungal antibiotics may also be produced. 

Several species of Trichoderma are troublesome 

contaminants and parasites of mycelia and 

basidiocarps of cultivated mushrooms in 

Europe and North America (Castle et al., 1998; 

Samuels et al., 2002). 

Trichoderma reesei is used commercially for 

cellulase production, secreting 20 g or more of 

cellulase l 1 culture fluid (Durand et al., 1988; 

Kubicek et al., 1990). Until recently, this interesting 

species had been isolated only once, during 

the Second World War on the Solomon Islands 

from canvas in contact with soil. Molecular 

studies have revealed that T. reesei is the 

anamorph of Hypocrea jecorina, an uncommon 

tropical species (Kuhls et al., 1996; Lieckfeldt 

et al., 2000).

HYPOCREALES 

341 

Fig12.16 Conidiophores of 

Hypocrea spp. (a) Gliocladium-type 

conidiophores of H. gelatinosa. 

(b) Details of phialides of 

H. gelatinosa.(c)Trichoderma viride 

conidial state of H. rufa. (d) Detail 

of phialides of H. rufa. (a,c) to same 

scale; (b,d) to same scale. 

The mating behaviour of Hypocrea spp. is 

poorly understood because perithecial development 

in culture occurs only rarely, except for the 

tropical species H. jecorina. This species shows 

bipolar heterothallism, half of its ascospores 

being of one and half of the opposite mating 

type (Lieckfeldt et al., 2000). Another tropical 

species, H. poronioidea, also forms perithecia in 

culture but the genetic basis of sexual reproduction 

is not clear. Cultures from eight partascospores 

in each of several asci were self-fertile 

(i.e. homothallic), whilst the other eight partascospores 

produced only conidia and were selfsterile. 

Another unusual feature of this fungus 

is that, in addition to having a Trichoderma 

anamorph, it has an Acremonium-like synanamorph. 

The Acremonium-like conidia can germinate, 

i.e. they have an asexual function, but it is 

possible that they also have a spermatial role 

(Samuels & Lodge, 1996). 

12.4.2 Nectria (Nectriaceae) 

The concept of the genus Nectria has changed in 

recent years. Previously considered to include 

about 200 species, the genus has now been 

narrowed to about 30, centred around 

N. cinnabarina (Rossman, 1983; Rossman et al., 

1999). Perithecia of Nectria are common on twigs 

and branches of woody hosts. Many are saprotrophic 

or weakly parasitic but some cause 

economically important diseases, e.g. N. coccinea 

causes bark disease of beech (Fagus sylvatica), 

whereas N. galligena infects apple and pear trees. 

Although there are some reports that N. galligena 

may have a prolonged latent (endophytic) phase, 

the fungus acts as a wound pathogen in most


Fig12.17 Mycoparasitism byTrichoderma spp. (a) Tip of conidiophore of T. virens with phialides. (b) Contact of a hypha of T. harzianum 

with one of Rhizoctonia cerealis. (c) Coiling of T. harzianum around a hypha of R. cerealis. (d) Intrahyphal growth of T. virens in a hypha 

of Fusarium sp. 

situations, entering through pruning wounds, 

cracks, leaf scars and sites of branch breakage. 

The colonization of the bark and cambium 

tissues results in a necrotic lesion, often with 

the dead heartwood visible in the centre, and 

surrounded by raised callus-like bark tissue 

where the tree launches a defence response. 

This type of symptom is called a canker 

(Fig. 12.18). Conidia and, later, perithecia are 

produced in the bark of cankers. Girdling 

results if a canker surrounds an entire branch, 

and this leads to the death of all shoot tissue 

distal to the lesion. 

The conidial states of Nectria include some 

terrestrial species of Fusarium, Cylindrocarpon and 

Tubercularia, whilst in freshwater streams they 

include the aquatic hyphomycetes Cylindrocarpon, 

Flagellospora and Heliscus (Section 25.2; Webster, 

1992). Some species have synanamorphic states 

with conidia of distinctive size and shape, e.g. 

macro- and micro-conidia (e.g. N. haematococca; 

Fig. 12.19). 

Nectria cinnabarina, the cause of coral spot, is 

common on freshly cut twigs of hardwood trees 

and shrubs, but may occasionally be a wound 

parasite on these hosts. The name coral spot 

refers to the pale pink conidial pustules, about 

1 2 mm in diameter, which burst through the 

bark (Plate 5d). Before the connection with 

Nectria was understood, these conidial pustules 

had been named Tubercularia vulgaris. They 

consist of a column of pseudoparenchyma bearing 

a dense tuft of conidiophores. These are long 

slender hyphae producing intercalary phialides 

at intervals along their length (Figs. 12.20b,d). 

Conidial pustules of this type are termed 

sporodochia. The conidia are sticky and form a 

slimy mass at the surface of the sporodochium. 

They are dispersed very effectively by rain splash. 

Around the base of the old conidial pustule 

perithecia arise (Plate 5d), and eventually the 

pustule may bear perithecia over its entire 

surface. Perithecial pustules develop in damp 

conditions in late summer and autumn and are

HYPOCREALES 

343 

Fig12.18 Canker caused by Nectria galligena 

on the twig of an old apple tree. 

readily distinguished from conidial pustules by 

their bright red colour and their granular 

appearance. The pustules are regarded as perithecial 

stromata, bearing as many as 30 perithecia. 

Ripe perithecia contain numerous 

club-shaped asci, each with eight two-celled 

hyaline ascospores (Fig. 12.20c). These are somewhat 

unusual in being multinucleate (El-Ani, 

1971). There is no obvious apical apparatus to the 

ascus (Strickmann & Chadefaud, 1961). 

Perithecial development begins by the formation 

of ascogonial primordia beneath the surface 

of the conidial pustule. The details of development 

are as described on p. 337. An important 

feature is the development of apical paraphyses 

which grow downwards from the upper part of 

the perithecial cavity. As the asci develop from 

ascogenous hyphae lining the base of the 

perithecial cavity, they grow upwards through 

the mass of apical paraphyses, which are difficult 

to find in mature perithecia (Strickmann & 

Chadefaud, 1961). 

Other species of Nectria differ from N. cinnabarina 

in a number of ways. In many, the perithecia 

are not grouped together on a stroma, but 

occur singly (e.g. in N. galligena). The asci of some 

species, e.g. N. mammoidea, have a well-defined 

apical apparatus (Fig. 12.21a). 

12.4.3 Fusarium (Nectriaceae) 

Fusarium-type conidia are known in several 

species of Nectria and also in the related genus 

Gibberella (Samuels et al., 2001). For many 

Fusarium species a teleomorph has not yet been 

found. The number of species recognized by 

morphological characters in pure culture varies 

from one authority to another. Booth (1971) 

included 44 species and 7 varieties; Gerlach and 

Nirenberg (1982) included 73 species and 26 

varieties, while Nelson et al. (1983) distinguished 

30 species. However, using molecular techniques 

a large number of species which cannot be 

distinguished by morphological characters are 

now being defined (O’Donnell, 1996), and a 

publically accessible database of diagnostic DNA 

sequences has been established as an aid to identification 

(Geiser et al., 2004). Species of Fusarium 

are cosmopolitan in soils from the permafrost of 

the Arctic to sand in the Sahara desert (Booth, 

1971). They are particularly common in cultivated 

soil and are associated with a wide range of 

plant diseases as indicated in Table 12.3 (Nelson 

et al., 1981). Some species are also known to 

cause diseases of humans such as onychomycosis 

(nail infections), keratomycosis of the cornea, 

ulcers, necroses, skin infections and fatal infections 

of internal organs, especially in immunocompromised 

patients (Joffe, 1986; de Hoog et al., 

2000a). 

A characteristic feature in the asexual reproduction 

of Fusarium is the development from 

phialides of fusoid, transversely septate macroconidia 

with a basal contracted foot cell 

(Fig. 12.22b). Microconidia, also formed from 

phialides, develop in some species. On plant 

hosts macroconidia often accumulate in 

orange pink sporodochia (Plate 5e, Fig. 12.22a). 

Macroconidia may be dispersed by rain splash


Fig12.19 Nectria haematococca. 

(a) Ascospores. (b) Phialides bearing 

macroconidia. (c) Macroconidia of the 

Fusarium type. (d) Phialides producing 

microconidia which accumulate in a drop 

of mucilage. (e) Microconidia. 

Fig12.20 Nectria cinnabarina.(a)V.S. 

perithecial stroma. (b) V.S. conidial 

stroma (sporodochium). (c) Asci. 

(d) Conidiophore, phialides and conidia.

HYPOCREALES 

345 

Fig12.21 Nectria mammoidea. (a) Ascus; 

note the apical apparatus. 

(b) Cylindrocarpon-type conidiophore with 

phialides and conidia. 

from such pustules (see Jenkinson & Parry, 

1994). In culture, greasy accumulations of macroconidia 

are termed pionnotes. Survival in soil is 

probably in the form of dormant chlamydospores 

which may be formed as a result of energy 

deprivation or in response to bacterial secretions. 

They are thick-walled and develop 

by modification of segments of the vegetative 

mycelium or by enlargement and modification 

of a segment of a macroconidium (Schippers & 

van Eck, 1981) (Figs. 12.22c,d). Chlamydospores 

are induced to germinate in the presence of root 

secretions (for references see Griffiths, 1974). 

One of the most commonly isolated species 

from soil is F. oxysporum, which often grows in 

association with roots. Many isolates are nonpathogenic 

but this fungus may also be a serious 

plant pathogen, reported from a very wide range 

of plant hosts. Although no sexual state is 

known, molecular studies show that it is monophyletic 

with the Gibberella Fusarium complex 

and can be regarded as an asexual Gibberella 

(Samuels et al., 2001). In this species over 80 

formae speciales characteristic of different host 

genera have been recognized, in addition to a 

large number of vegetative compatibility types 

and races (Gordon, 1993; Gordon & Martyn, 

1997). The large amount of genetic variation in 

F. oxysporum in the absence of conventional 

sexual reproduction is possibly explained by 

the demonstration of parasexual recombination 

even between members of different vegetative 

compatibility groups (Molnár et al., 1990). 

Fusarium wilts 

As can be seen from Table 12.3, formae speciales of 

F. oxysporum cause wilt diseases of numerous crop 

plants. The range of affected hosts is so wide that 

it is easier to mention those plants unaffected by 

Fusarium wilts, i.e. grasses and many tree species. 

Although F. oxysporum has no known sexual state, 

strains of this species complex show huge 

genetic variation which may come about by the 

presence of transposable elements (Daboussi & 

Capy, 2003) and the parasexual cycle (Teunissen 

et al., 2002). The variability of F. oxysporum is 

such that a given disease, e.g. Panama wilt of 

banana, is caused by several unrelated strains 

(K. O’Donnell et al., 1998), and that strains with 

different host specificities may be closely related 

(Hua-Van et al., 2001). 

Wilting is associated with the presence of 

fungal hyphae in the xylem vessels. Fusarium 

oxysporum can persist in the soil as chlamydospore 

inoculum for many years and infects the 

roots of hosts by direct penetration and


Table 12.3. Some species of Fusarium causing plant diseases of economic importance. From Holliday (1998). 

Anamorph Teleomorph Disease caused and name of host 

F. culmorum not known cortical rot, foot rot and pre-emergence blight of 

temperate cereals; head blight of barley, 

wheat and rye 

F. oxysporum not known a wide range of wilts, yellows and foot rots 

F. oxysporum f. sp. apii not known celery yellows 

F. oxysporum f. sp. cepae not known basalrot and storage rot of onion 

F. oxysporum f. sp. cubense not known Panama wilt of banana 

F. oxysporum f. sp. dianthi not known wilt of carnation and pinks 

F. oxysporum f. sp. elaeidis not known oil palm wilt 

F. oxysporum f. sp. lycopersici not known tomato wilt 

F. oxysporum f. sp. pisi not known pea wilt 

F. oxysporum f. sp. vasinfectum not known cotton wilt 

F. solani Nectria 

haematococca 

root and collar rot of many plants; canker of 

woody crops 

F. solani f. sp. cucurbitae not known foot rot of cucumber and melon 

F. solani f. sp. coeruleum not known storage rot and dry rot of potato 

F. avenaceum Gibberella 

avenacea 

damping off and rootdamage to cereals, conifers 

andlegumes 

F. sulphureum G. cyanogena storage rot and dry rot of potato tubers 

F. moniliforme G. fujikuroi diseases of many plants, e.g. banana black heart, 

cotton bollrot, maize and sorghum stalk rots, 

rice seedling bakanae disease 

F. sambucinum G. pulicaris hop canker, potato storage rot, root rot of 

many crops 

F. graminearum G. zeae numerous diseases of temperate and tropical cereals, 

e.g. pre- and post-emergence blights, root and 

foot rot, culm decay, head or kernel blight, 

ear scab and stalk rot. 

intercellular growth through the root tip into 

the xylem vessels (Bishop & Cooper, 1983). In 

planta, F. oxysporum exists mainly as microconidia 

which can spread in the xylem vessels. Sieve 

plates are overcome by germination and penetration, 

followed by the production of further 

microconidia. Wilting is caused by blockage of 

the xylem by fungal biomass and also by the 

accumulation of gums of plant origin, some of 

them released by fungal pectinase activity (Pegg, 

1985; Beckman, 1987). In cross section, infected 

stem bases show a browning of the vascular 

bundles. The host plant eventually dies because 

of water shortage (wilting), and after host death 

extensive colonization of host tissue and sporulation 

of F. oxysporum ensues. Extensive work 

is being carried out especially on molecular 

biological aspects of wilt diseases caused by

HYPOCREALES 

347 

Fig12.22 Fusarium culmorum. (a) Part of a sporodochium with clusters of phialides producing macroconidia. (b) Mature 

macroconidium from a two-week-old culture.The foot cell is indicated by an arrowhead. (c) Older macroconidia (eight-week-old) 

in which some cells have collapsed and the others have turned into chlamydospores. (d) Chlamydospores formed by a hypha 

submerged in agar. (b d) to same scale. 

F. oxysporum, and this has been summarized by Di 

Pietro et al. (2003). 

The control of diseases caused by Fusarium is 

mainly through the use of resistant host plant 

cultivars (Beckman, 1987). The disastrous economic 

consequences of the outbreak and spread 

of Panama wilt of banana caused by F. oxysporum 

f. sp. cubense which attacked the popular banana 

variety ‘Gros Michel’ were overcome by switching 

production to clones of the resistant variety 

‘Cavendish’ which could be planted into soils 

heavily contaminated with F. oxysporum f. sp. 

cubense (Moore et al., 2001). Another wellcharacterized 

example is tomato wilt caused by 

F. oxysporum f. sp. lycopersici. Resistance seems to 

be based mainly on major-gene resistance, and 

numerous resistance genes have been crossed 

into the cultivated tomato plant from wild 

relatives. These occur in several discrete gene 

clusters (Sela-Buurlage et al., 2001). A range of 

tomato cultivars with resistance against one or 

more of the three races of F. oxysporum f. sp. 

lycopersici is available for planting. 

Another approach actively pursued at present 

is the biological control of F. oxysporum. An 

interesting strategy is the use of apathogenic 

strains of F. oxysporum which colonize the root 

cortex but not the vascular system, and therefore 

have an endophytic lifestyle. They inhibit infections 

by pathogenic strains. Various explanations 

have been offered, including competition for 

nutrients, the induction of systemic acquired 

resistance in plants pre-infected with the apathogenic 

strains, and direct competition between 

apathogenic and pathogenic strains in the root 

cortex (Larkin & Fravel, 1999; Bao & Lasarovits, 

2001). Other soil micro-organisms such as 

Pseudomonas spp. are also being developed as 

biocontrol agents. 

Mycotoxins 

Some species of Fusarium (e.g. F. graminearum and 

F. moniliforme) are seed-borne, with mycelium 

being present inside the grain and often producing 

macroconidia on the surface. Infected seed 

not only ensures carry-over of the disease to 

following seasons but can be a source of 

mycotoxins if fed to livestock or consumed by 

humans. Mycotoxins such as zearalenone, fumonisin, 

trichothecenes and vomitoxin (Fig. 12.23)


are produced by Fusarium spp. present on animal 

and human feedstock (Creppy, 2002; Moss, 2002). 

Zearalenone, an oestrogenic hormone from 

F. graminearum, causes vulvovaginitis and infertility 

in cattle and pigs, and trichothecenes such as 

T-2 toxin from several other Fusarium species 

cause toxic aleukia (reduction in white blood cell 

count) in farm animals and humans (Joffe, 1986; 

Moss, 2002). 

12.4.4 Cylindrocarpon (Nectriaceae) 

Fungi with Cylindrocarpon-type conidia are anamorphic 

states of species of Nectria sensu lato, now 

placed in a distinct genus Neonectria (Rossman 

et al., 1999; Mantiri et al., 2001). The macroconidia 

of Cylindrocarpon are hyaline, curved, transversely 

septate phialoconidia which resemble those of 

Fusarium but do not have the constricted basal 

foot cell characteristic of the latter (compare 

Figs. 12.21b and 12.20c). Some species also have 

microconidia and some have chlamydospores. 

About 120 taxa (species and varieties) have been 

described and about 50 have been linked to 

Nectria sensu lato. Most species of Cylindrocarpon 

grow in soil and are saprotrophic or weakly 

parasitic. Cylindrocarpon destructans (formerly 

known as C. radicicola), whose teleomorph is 

Nectria radicicola (Samuels & Brayford, 1990), 

causes seedling blights and basal rots of bulbs, 

as well as root rots of various plants. 

Cylindrocarpon heteronema is the anamorph of 

Nectria galligena, the cause of apple and pear 

canker. 

12.5 Clavicipitales 

Fungi in this group have been and still are 

assigned to various groups (Spatafora & 

Blackwell, 1993; Rossman, 1996; Stensrud et al., 

2005), notably a family (Clavicipitaceae) of the 

Hypocreales or a separate order (Clavicipitales). 

Whatever its taxonomic rank, this group 

contains fungi with several distinguishing 

characteristics. Perithecia develop on a fleshy 

stroma. The perithecial centrum contains a 

central basal mound from which the asci arise. 

Any paraphyses which develop are obliterated 

by crushing as the asci enlarge (White, 1997; 

Rossman et al., 1999). The asci have a well-defined 

Fig12.23 Common mycotoxins produced by Fusarium spp. (a) The nonaketide zearalenone, a suspected carcinogen and 

oestrogen analogue produced by F. graminearum in maize and cattle feed. (b) Fumonisin B 1 

, a suspected cause of oesophageal 

cancer, produced by F. moniliforme infecting maize. (c) T-2 toxin, a highly cytotoxic trichothecene (sesquiterpene derivative) 

produced by F. graminearum in various cereals. (d) Vomitoxin (desoxynivalenol), a trichothecene produced by F. culmorum and 

F. graminearum in maize and wheat.

CLAVICIPITALES 

349 

thick apical cap perforated by a narrow pore 

through which the ascospores are discharged, 

singly and successively. The ascospores are 

long, narrow and often multi-septate, breaking 

up into part-spores. Most members (e.g. Claviceps, 

Balansia, Epichloe) are pathogens or endophytes 

of grasses, whereas Cordyceps parasitizes insects 

or fruit bodies of the hypogeous ascomycete 

Elaphomyces. Claviceps sclerotia are the source of 

toxic alkaloids, and grasses infected with endophytic 

Balansia may also be toxic to herbivorous 

insects and mammals. The grass host may thus 

be at least partially protected against insect 

herbivory, and the effects of alkaloids on 

grazing mammals can also be severe. The 

conidia of certain species of Cordyceps show 

promise as agents of biological control of insect 

pests (Evans, 2003). Some members of the 

Clavicipitales attack nematodes (Gams & Zare, 

2003). For example, Atricordyceps (now called 

Podocrella) is the teleomorph of Harposporium 

anguillulae (Samuels, 1983) (see Fig. 25.8), and 

phylogenetic analyses of nuclear ribosomal 

DNA have also placed the nematophagous 

fungus Drechmeria coniospora (see Fig. 25.8) in 

the Clavicipitaceae (Gernandt & Stone, 1999). 

The immunosuppressant drug cyclosporin A 

(Fig. 12.24a) is produced by Tolypocladium 

inflatum, anamorph of Cordyceps subsessilis 

(Hodge et al., 1996). A group of b-lactam antibiotics, 

the cephalosporins (Fig. 12.24b; see 

p. 302), are derived from the anamorphic 

Acremonium chrysogenum and A. salmosynnematum. 

Many other valuable secondary metabolites have 

been isolated from members of the Clavicipitales 

(Isaka et al., 2003). 

12.5.1 Claviceps 

There are over 40 species of Claviceps, all of which 

are parasitic on grasses, rushes and, occasionally, 

sedges (Alderman, 2003). The best known species 

is C. purpurea, the cause of ergot of grasses and 

cereals. Other economically important species 

are C. sorghi and C. africana which cause ergot 

of sorghum (Frederickson et al., 1991), C. paspali 

on Paspalum and C. fusiformis on pearl millet 

(Pennisetum typhoides). Claviceps purpurea occurs in 

temperate regions and has an exceptionally wide 

host range for a biotrophic pathogen, infecting 

over 400 grass species. The course of infection 

has been described by Luttrell (1980), Tenberge 

(1999) and Oeser et al. (2002). 

Life cycle 

The life cycle of C. purpurea is summarized in 

Fig. 12.25. The primary inoculum is an ascospore 

shot away from a perithecium which has developed 

from an overwintered sclerotium. The time 

of ascospore release coincides with anthesis in 

a susceptible host. Ascospores germinate on 

a grass stigma to form an intercellular mycelium 

which grows down to the base of the ovary 

towards the vascular bundle of the floret stalk 

(rachilla), thus gaining access to the photosynthetic 

products of the host. Subsequent growth is 

upwards and within a few days a conidial stroma 

develops beneath the ovary. A palisade of phialides 

lining labyrinthine chambers is formed 

from which a succession of unicellular, uninucleate 

conidia develops in a sugary syrup. This 

becomes visible on the grass florets as beads of 

liquid termed honeydew (Fig. 12.26b). The conidial 

stage was given the separate name Sphacelia 

segetum before its connection with ergot was 

understood. Honeydew contains glucose, fructose, 

sucrose and other sugars (Mower & 

Hancock, 1975a), and is attractive to insects, 

which feed on it and in so doing disperse conidia 

to healthy grass flowers, thus causing secondary 

infection. Infection of a grass flower by Claviceps 

results in increased translocation of water 

and sucrose towards the diseased flower, and 

infected flowers are more effective at acquiring 

photosynthetic products from the host than 

uninfected flowers (Parbery, 1996b). Within the 

infected host tissue, conversion of host-derived 

sucrose to mono-, di- and oligo-saccharides by the 

fungus creates a continuing sink for sucrose 

translocation, and evaporation at the surface of 

the diseased grain results in increased osmotic 

concentration of the sugars, possibly accelerating 

the rate of translocation (Mower & Hancock, 

1975b). The high osmotic concentration prevents 

conidial germination until the honeydew has 

been diluted. 

As infection proceeds, the entire ovary is 

pushed upwards by the developing fungal tissue


Fig12.24 Important metabolites from 

Clavicipitales. (a) Cyclosporin A, produced by 

Tolypocladium inflatum.This is used extensively as 

an immunosuppressive drug, e.g. after organ 

transplantations. (b) Cephalosporin C, 

a b-lactam antibiotic with activity against 

Gram-positive and Gram-negative bacteria. 

and sits like a cap over it. The ovary, which would 

normally develop into a caryopsis filled with 

grain, becomes replaced by fungal tissue. For this 

reason the disease caused by C. purpurea has been 

termed a replacement disease (Luttrell, 1980). 

The fungal structure which develops is considerably 

longer than the ovary which it replaces and 

it differentiates into a sclerotium up to 3 cm in 

length, the foot of which continues to obtain 

nutrients via the vascular connection in the host 

rachilla. The sclerotium is made up of three 

distinct layers: a thin purplish-brown rind, a 

discontinuous layer of mealy white tissue, and 

a central layer of translucent gelatinous tissue 

(Luttrell, 1980). 

Ergot is the French name for a cock’s spur, 

referring to the curved, banana-shaped sclerotia 

which project from the inflorescence of infected 

grasses and cereals in late summer (Fig. 12.26a). 

The sclerotia fall to the ground and overwinter 

near the surface of the soil. They need a period of 

low temperature before they can develop further. 

A chilling period of 0°C for at least 25 days 

is optimal for further development. The main 

reserve substance of the sclerotium is lipid, 

which may account for 50% of the dry weight. 

It is likely that the chilling period is necessary 

before enzymes capable of mobilizing the lipid 

reserves develop (Cooke & Mitchell, 1970). 

Sclerotia do not remain viable in soil in the 

field for more than a few months, often being 

invaded by fungi, bacteria, mites and insects 

(Cunfer & Seckinger, 1977). The following 

summer, sclerotia develop one or more perithecial 

stromata (clavae) about 1 2 cm high, shaped 

like miniature drumsticks (Fig. 12.26c). The 

perithecial stromata are positively phototropic 

(Hadley, 1968). 

The enlarged spherical head or capitulum 

contains a number of perithecia which are embedded 

in the stroma, each surrounded by a 

distinct perithecial wall (Fig. 12.27a). The cytological 

details of perithecial development have 

been studied in C. purpurea by Killian (1919) and 

in C. microcephala (regarded by some as a form of 

C. purpurea) by Kulkarni (1963). In the outer layers 

of the head of the perithecial stroma, clubshaped 

multinucleate antheridia and ascogonia 

undergo plasmogamy. Ascogenous hyphae made 

up of predominantly binucleate segments 

develop from the base of the ascogonium, and 

the tips of the ascogenous hyphae form croziers


351 

Fig12.25 The homothallic life cycle of 

Claviceps purpurea growing on rye (Secale 

cereale). A sclerotium fallen to the ground 

will produce a perithecial stroma after 

overwintering. In the perithecia, 

plasmogamy (P), karyogamy (K) and 

meiosis (M) give rise to filamentous 

ascospores, each with numerous haploid 

nuclei (small open circles). Ascospores 

germinate on the stigmata of the rye 

ovary, and mycelium penetrates to the 

ovary stalk (rachilla). Infections develop 

both as conidial regions and, lower down, 

as a sclerotium initial.The developing 

sclerotium pushes the ovary upwards, 

andthisremainsasacapabovethe 

conidial stroma.The stroma contains 

cavities lined by phialides which produce 

phialoconidia of the Sphacelia segetum 

type.These accumulate in beads of a 

sugary liquid (honeydew).Conidia are 

carried by insects to fresh rye stigmata 

and initiate secondary infections. Later in 

the season, the sclerotia enlarge and 

become visible as ergots. Some images 

redrawn from Luttrell (1980). 

with binucleate penultimate segments. The 

penultimate cell elongates to form the ascus, 

and fusion between the two nuclei occurs. There 

are numerous asci in each perithecium, each 

containing a bundle of eight filiform ascospores. 

The ascus bears a conspicuous perforated cap at 

its tip (Fig. 12.27c). 

Successful infection of rye (Secale cereale) from 

cultures derived from a single ascospore show 

that C. purpurea is homothallic. Despite this, 

genetic recombination is possible through 

heterokaryosis and parasexual reproduction 

(Tudzynski, 1999). Curiously, sclerotia are 

frequently formed from heterokaryotic mycelia, 

indicating multiple infection of the grass flower. 

Although common on rye and some other 

cereals in Europe and North America, C. purpurea 

is not usually troublesome on cereals in Britain. 

In the occasional years in which its incidence is 

high, there is a correlation with high relative 

humidity and low maximum temperature in 

June, which probably prolongs the period during


Fig12.26 Claviceps purpurea. (a) Head of rye (Secale cereale) bearing several sclerotia (ergots) of Claviceps purpurea. (b) Rye 

inflorescence at anthesis bearing two drops (arrowed) of the honeydew or Sphacelia conidial state of C. purpurea. A fly has landed 

near these drops. (c) Germinated sclerotium showing several stalked perithecial stromata. 

which the host grass flowers are open and 

therefore susceptible to infection. 

Ergotism 

The effect of infection on the host can result 

in yield reduction by as much as 80% of seeds. 

Severe though this reduction in crop yield 

is, the consequences of consumption of ergotcontaminated 

grain can be disastrous to herbivorous 

animals and humans alike. The purple 

sclerotia contain a number of toxic alkaloids 

(Buchta & Cvak, 1999) and if they are eaten they 

can cause severe illness and sometimes death. 

Even at relatively low concentration there may 

be severe effects on feed refusal, lack of weight 

gain in farm animals and on reduced fertility, 

resulting in part from agalactia, the inability to 

produce sufficient milk to nourish the young 

(Shelby, 1999). One effect of the toxins is to 

constrict the blood vessels, and the impaired 

circulation may result in gangrene or loss of 

limbs. Gruesome descriptions of the symptoms 

on humans have been related by several contemporary 

authors, e.g. Sidney (1846) who wrote: 

The medical effects of ergot, in small doses, have 

already been noticed as being extremely powerful, 

but if taken to any extent its results on the animal 

frame are truly awful. This has been proved by 

numerous experiments, of which Professor Henslow 

gives a most striking account in his most valuable 

notice of this disease; to which he adds a proper 

caution against their repetition now the question is 

settled. Animals which refused ergot mixed with 

their food have been compelled to swallow it, and it 

reduced them to a wretched condition. It was tried 

upon pigs, and also upon poultry, and the 

consequences were sickness, gangrene, and 

inflammatory action so intense, that the flesh 

actually sloughed away. In some cases, the limbs 

rotted off, and no description of animal suffering 

has ever exceeded the direful ills thus inflicted. 

These experiments were made with a view to 

determine whether the ergot of rye, constantly 

ground up with the flour in some parts of France, 

might not be the cause of the gangrenous disease 

so prevalent amongst the poor in certain districts. 

The symptoms of these epidemic diseases are


353 

and dumb, and, besides, lost a limb which actually 

rotted off, precisely in the same way as the limbs of 

the animals which were compelled to swallow the 

experimental ergot. 

Another effect is on the nervous system, 

resulting in convulsions, hallucinations and 

burning sensations. In the Middle Ages the 

symptoms of ergotism were called ‘St 

Anthony’s fire’ and there are numerous records 

of out-breaks of the disease (see Ramsbottom, 

1953; Fuller, 1969; Matossian, 1989). Matossian 

(1989) has outlined some of the social consequences 

of ergotism, e.g. in depressing population 

growth after the plague outbreaks in 

Europe, and in provoking witch trials in North 

America when women were accused of and 

executed for bewitching people who were probably 

suffering from ergot-induced food poisoning 

and hallucinations. 

With improved grain-cleaning techniques 

and a switch in carbohydrate consumption 

from rye to wheat, maize and potatoes, the 

disease is now rare in humans. Cattle and sheep 

which have eaten sclerotia from pasture grasses, 

or pigs and horses fed on ergot-contaminated 

grain, are still affected and if pregnant animals 

are involved there is a risk of abortion. However, 

these problems are now relatively rare. 

Fig12.27 Claviceps purpurea. (a) L.S. perithecial stroma. 

(b) T.S. young sclerotium showing the formation of 

phialoconidia on the surface. (c) Ascus and ascospores. 

Note the cap of the ascus. 

dreadful, and there seems to be very little doubt that 

the suspicions as to their originating from ergotted 

flour of rye are correct. Tessier, who has paid great 

attention to the subject, mentions a case which 

came under his own observation. A family were in 

a state of great destitution, and the father begged of 

a neighbouring farmer a quantity of ergotted rye to 

supply the urgent calls of his distressed family for 

food. The farmer gave it him, but added that he was 

afraid it was not wholesome. Still the calls of hunger 

prevailed, and in the face of this caution it was 

eaten. The result was the death of the father, 

mother, and five of the children out of seven. Two 

survived, but one of them became subsequently deaf 

Alkaloids of Claviceps purpurea 

Ergot alkaloids are used in human medicine. ‘No 

other class of compounds exhibits such a wide 

spectrum of structural diversity, biological activity 

and therapeutic uses as ergot derivatives’ 

(Křen & Cvak, 1999). This is because the tetracyclic 

ergoline ring structure (Fig. 12.28) mimics 

several neurotransmitter molecules such as 

noradrenaline, dopamine and serotonin 

(Mantegani et al., 1999). Two alkaloids, ergometrine 

and ergotamine, are of special importance 

and are produced by field strains of C. purpurea 

(Pažoutová et al., 2000). Ergometrine causes 

constriction of smooth muscle tissues. The 

name ergometrine is derived from endometrium, 

the lining of the uterus, because the 

drug is used to stimulate uterine contraction. 

Ergotamine can similarly accelerate uterine 

contraction and is used as a vasoconstrictor


Fig12.28 Biosynthesis of alkaloids in ergots of Claviceps purpurea. Starting from tryptophan and the mevalonic acid-derived metabolite 

dimethylallylpyrophosphate, dimethylallyltryptophan is synthesized. Ring closure, decarboxylation and addition of a methyl 

group from methionine (arrowhead) gives the simplest alkaloids, agroclavine and D-lysergic acid.The latter is then derivatized at its 

C-8 position to give more complex alkaloids such as ergometrine and ergotamine. LSD (D-lysergic acid diethylamide) is a semisynthetic 

derivative of D-lysergic acid. 

and a haemostatic drug. It was also the first 

medication available against migraine (Eadie, 

2004). A third ergot-derived drug is lysergic acid 

diethylamide (LSD), a synthetic derivative of 

lysergic acid. As is well known, this drug has 

hallucinogenic properties and is associated with 

euphoria (Minghetti & Crespi-Perellino, 1999). 

Numerous chemical derivatives have been 

synthesized, and ergot alkaloids are lead structures 

for drugs against a range of illnesses, 

including Parkinson’s disease and Alzheimer’s 

disease. 

The biosynthesis of ergot alkaloids in 

C. purpurea from tryptophan, mevalonic acid 

and methyl groups donated by methionine 

leads to the ergoline ring structure (Fig. 12.28). 

The simplest alkaloids are the clavine alkaloids 

such as agroclavine, but most of the pharmaceutically 

important ones are based on D-lysergic 

acid because it is the carboxylic acid group at C-8 

in D-lysergic acid which is further substituted. 

Simple substituted D-lysergic acid derivatives 

are ergometrine and the semi-synthetic LSD 

(Fig. 12.28). In the most complex ergot alkaloids, 

the ergopeptines, three amino acids are added 

to D-lysergic acid by a non-ribosomal peptide 

synthase, followed by ring closure. Ergotamine 

is a commonly found example of this type of 

alkaloid in C. purpurea (Fig. 12.28). Reviews of 

alkaloid biosynthesis have been written by 

Flieger et al. (1997) and Tudzynski et al. (2001). 

A concise general treatment is that by Lohmeyer 

and Tudzynski (1997). 

The ergot of commerce is produced by cultivating 

the fungus on rye, and profitable crops 

of ergot sclerotia are obtained, often on specially 

bred strains of male-sterile rye in Eastern Europe, 

Spain and Portugal (Németh, 1999). Rye flowers 

are infected with a suspension of conidia from 

strains of C. purpurea selected for high yield of 

certain alkaloids. Alkaloids are extracted from 

harvested sclerotia. Alkaloids are also extracted 

from special strains of C. purpurea grown saprotrophically 

in deep fermentation. About 60% of


355 

alkaloid production is currently derived from 

fermentations, the rest from harvested sclerotia. 

The advantages of saprotrophic fermentation 

are that the process can be closely controlled 

and the alkaloids produced are less variable than 

those from harvested ergots. A disadvantage is 

that the ability to produce alkaloids in economically 

significant amounts is variable and may be 

lost on prolonged cultivation. Nevertheless, 

the market share of alkaloids produced by 

fermentation is currently increasing (Tudzynski 

et al., 2001). 

Control of Claviceps 

The control of ergot in cereals is difficult. 

Although several techniques are available, none 

is completely effective. Use of ergot-free seed 

would reduce infection, but inoculum may 

survive from a previous crop. It can also be 

provided by wild grasses bordering the field 

because C. purpurea strains have wide host 

ranges. Deep ploughing, which buries the sclerotia, 

and crop rotation involving a non-cereal 

are also helpful. Systemic fungicides would need 

to be applied in sufficient amounts to produce 

an effective concentration at the surface of the 

ovary, and they have been used to control ergot 

in seed crops of Kentucky bluegrass, Poa pratensis 

(Schulz et al., 1993). Fungicide sprays are used at 

present to control C. africana on sorghum in 

Australia (Ryley et al., 2003) but not against 

C. purpurea on cereals. 

Other Claviceps spp. 

Some other species of Claviceps differ in significant 

ways from C. purpurea. For example, 

C. fusiformis has two synanamorphs, a macroand 

a micro-conidial state. Claviceps africana and 

C. paspali may produce secondary phialoconidia 

and these may develop in sufficient quantity on 

the surface of the conidial stroma to be capable 

of dispersal by wind (Luttrell, 1977; Frederickson 

& Mantle, 1989; Alderman, 2003). Claviceps paspali 

which infects dallisgrass (Paspalum dilatatum) is 

the source of alkaloids such as paspalic acid and 

its derivatives. Ingestion of its sclerotia causes 

paspalum staggers in sheep. The salt marsh grass 

Spartina anglica often shows heavy infection by 

a specialized variety, C. purpurea var. spartinae 

(Plate 5e). This fungus appears to be adapted to 

an aquatic environment. Its unusually slender 

sclerotia float on the surface of sea water whilst 

those of other forms of C. purpurea sink. The high 

levels of infection may be related to the fact that 

S. anglica, an allopolyploid grass of recent origin, 

is genetically uniform. Despite the heavy infection, 

seed production by the host plant is not 

severely affected (Raybould et al., 1998; Duncan 

et al., 2002). In contrast, C. phalaridis, which is 

endemic in Australia on the introduced pasture 

grass Phalaris tuberosa, is systemic and when its 

mycelium penetrates the inflorescence, sclerotia 

are formed in all the florets, rendering the host 

plant sterile (Walker, 2004). Its systemic habit 

is shared by other clavicipitaceous endophytes 

such as Epichloe (see below). 

12.5.2 Epichloe 

There are about 10 biological species (i.e. mating 

populations) of Epichloe (Gr. epi ¼ on, upon; 

chloë ¼ young shoots of grass) mainly infecting 

cool-season grasses with the C 3 photosynthetic 

pathway (Leuchtmann, 2003). They grow in 

nature as biotrophic, systemic, parasitic or 

symbiotic endophytes in grass shoots, forming 

at first conidial, then perithecial stromata 

around the uppermost leaf sheaths of tillers 

containing floral primordia. Anamorphic relatives, 

now classified as species of 

Neotyphodium (previously Acremonium Section 

Albo-lanosum; Glenn et al., 1996), are symptomless 

endophytes. Neotyphodium-infected grasses 

contain ergot alkaloids and other mycotoxins 

which are injurious to herbivorous insects and 

mammals and cause economic damage (Schardl, 

1996; Kuldau & Bacon, 2001; Clay & Schardl, 

2002). 

Epichloe typhina (sensu lato) causes ‘choke’ of 

pasture grasses and is common on grasses such 

as Dactylis, Holcus and Agrostis. However, forms 

of Epichloe on certain hosts are distinct from 

E. typhina in dimensions of stromata, ascospores, 

ascospore septation, and in molecular characteristics. 

They have now been accorded different 

species names. The specific name typhina should 

be applied to the forms on eight genera of 

grasses including Dactylis, whilst the name


E. baconii has been given to the fungus on Agrostis 

stolonifera, and E. clarkii to that on Holcus lanatus 

(White, 1993). The form on Festuca rubra and F. 

valesiaca is E. festucae (Leuchtmann et al., 1994). 

The uppermost leaf sheath of flowering tillers 

becomes surrounded by a white mass of mycelium 

2 cm or more in length, and at the surface 

small unicellular phialoconidia are produced 

(Fig. 12.29b). These conidia function as spermatia 

(see below). Later, the conidial stroma becomes 

thicker and turns orange in colour as perithecia 

are formed (Plate 5f). The perithecia produce 

numerous asci, each with a well-defined apical 

cap, and containing eight long narrow ascospores 

which may break up within the ascus to 

form part-spores (Fig. 12.29d). The mycelium is 

for the most part intercellular, unbranched and 

mainly located in the pith, although intracellular 

penetration of the vascular bundles is found 

in the region of the inflorescence primordium. 

Perithecial stromata are formed only on tillers 

containing inflorescence primordia, and by 

manipulating incubation conditions it has been 

shown that the formation of stromata is correlated 

directly with the presence of an inflorescence 

primordium rather than with external 

conditions (Kirby, 1961). 

Epichloe typhina is heterothallic with a unifactorial 

(bipolar) mating system (White & Bultman, 

1987). Throughout its range Epichloe is attacked 

by a parasitic fly, Botanophila phrenione (Phorbia 

phrenione), which feeds on conidia, conidiophores 

and hyphae. The relationship is a symbiotic one. 

Before laying eggs, female flies feed on conidia 

and hyphae from conidial stromata. Possibly they 

are attracted by the white colour and distinctive 

smell of the stroma (Leuchtmann, 2003). The 

conidia remain viable after passing through the 

gut of the flies. After laying an egg in a fresh 

conidial stroma an ovipositing female shows an 

unusual but characteristic pattern of behaviour, 

walking in a linear or spiral path around the 

conidial stroma whilst dragging its abdomen and 

depositing a trail of faecal material with viable 

conidia on the receptive hyphae of its surface, 

so spermatizing them. This track is later marked 

by the development of perithecia (Bultman 

et al., 1998). 

Perithecial ontogeny has been studied by 

White (1997). The perithecial primordium develops 

as a cavity lined by inwardly directed 

branched hyphae. In E. typhina, at the base of the 

cavity a mound of ascogenous tissue appears. 

This is made up of ascogenous hyphae with 

croziers and with lateral paraphyses, but the 

paraphyses do not persist as the asci mature. The 

perithecial ostioles protrude above the surface of 

the stroma and are lined by curved periphyses 

(Fig. 12.29c). The apical apparatus of the ascus 

consists of a thickened ring pierced by a narrow 

canal continuous with the cytoplasm of the ascus 

(Figs. 12.29d, 12.30a) and through the canal the 

ascospores are discharged singly, one after 

another. 

Ascospores may segment into part-spores 

within the ascus or after discharge. It has been 

claimed that they never germinate directly (i.e. 

by germ tube), but only by the production of 

conidia from narrow tapering phialides (Figs. 

12.30b,c; Bacon & Hinton, 1988). However, our 

own observations on ascospores of E. typhina 

from D. glomerata show that direct germination 

may occur (Fig. 12.30d). Primary conidia may 

germinate directly or by forming secondary 

conidia, a process described as microcyclic conidiation 

(Bacon & Hinton, 1991). Tertiary conidia 

may also develop from secondary conidia. 

Attempts to infect grasses from ascospores 

have generally been unsuccessful, so it is likely 

that infection is by conidia. After allowing 

ascospores to be discharged close to emerging 

inflorescences of uninfected Lolium perenne 

plants, about 12% of the seeds gave rise to 

infected progeny, but whether infection was 

directly from ascospores or from primary or 

secondary conidia was not determined (Chung & 

Schardl, 1997a). Experimentally, it has not been 

possible to infect developing seeds of Dactylis, 

and the only effective method of infection is by 

application of ascospores or conidia to the cut 

ends of green stubble (Western & Cavett, 1959). 

If this is the natural route of infection in other 

grasses, it may explain the greater incidence of 

the disease in Agrostis in heavily grazed pastures 

(Bradshaw, 1959). 

The time of release of ascospores coincides 

with the emergence of larvae of the parasitic fly


357 

Fig12.29 Epichloe baconii. (a) T.S. stem and leaf 

sheath of Agrostis surrounded by a perithecial stroma. 

Note the axillary shoots between the leaf sheath and 

the stem. (b) Part of the conidial stroma. (c) A single 

perithecium. Note the periphyses lining the ostiole. 

(d) Ascus and ascospores. Note the apical apparatus 

of the ascus. 

which may feed on perithecia and so reduce 

ascospore production (Welch & Bultman, 1993). 

12.5.3 Epichloe-related grass endophytes 

White (1988) has classified the relationships 

between Epichloe or related endophytes and 

their hosts into three types. In type I associations, 

perithecial stromata are formed on the inflorescences 

of most if not all infected individuals 

so that flowering of the host is suppressed. 

Dactylis glomerata and Agrostis tenuis harbour this 

type of association which should be regarded 

as parasitic. In type II associations, stromata 

are formed on only a few (1 10%) of infected 

individuals in a population, although 50 75% of 

the population may contain the infection. This 

type of association has been found only in the 

sub-family Festucoideae. Agrostis hiemalis, Bromus 

anomalus and Elymus canadensis have associations 

of this type. The endophyte is probably spread 

by clonal (i.e. vegetative) growth of the infected 

host, by ascospores (contagious or horizontal 

transmission) and by seed transmission (vertical 

transmission). In type III associations, stromata 

are not formed on infected plants and apparently 

are never produced. Such associations 

have been found only in festucoid grasses including 

tall fescue (Festuca arundinacea) and perennial 

ryegrass (Lolium perenne). In many of these grasses 

over 90% of individuals are infected. In this type 

of association the endophytes rely on vertical 

transmission which involves mycelial growth 

from the parent plant to the embryo within the 

seed (White et al., 1991). Since the host plant is


Fig12.30 Epichloe typhina. (a) Tip of ascus showing the thickened apical ring pierced by a cytoplasmic canal. (b) Discharged 

ascospore which has germinated to produce several phialides. (c) Phialides with primary conidia. (d) Ascospore showing 

direct germination by hyphal growth. Some phialides are also visible. 

not detrimentally affected and indeed may 

benefit by experiencing reduced herbivory, the 

relationship can be regarded as mutualistic. 

The anamorphic states of Epichloe spp., now 

classified as species of Neotyphodium, grow as 

endophytes, i.e. symptomless symbionts, of 

many grasses. Most species of Neotyphodium 

produce phialoconidia in laboratory culture 

and N. typhinum, the anamorph of E. typhina, 

has been reported to form conidiophores on the 

phylloplane (leaf surfaces) of Poa rigidifolia and 

Agrostis hiemalis, although it is unclear whether 

or not they are involved in horizontal transmission 

in nature (White et al., 1996). What is certain 

is that these endophytes are seed-borne and 

are vertically transmitted. The leaf sheaths of 

infected plants show a characteristic fine, intercellular, 

infrequently branched, contorted mycelium 

with lipid contents, running parallel to the 

vascular bundles, and following the longitudinal 

cell walls of the inner epidermis of the lower 

leaf sheaths (Fig. 12.31). Endophyte mycelium 

is less extensive in leaf blades and it is believed 

that the ligule, lacking intercellular spaces, 

may be a barrier to spread (Hinton & Bacon, 

1985; Christensen et al., 2002). The mycelium of 

Neotyphodium appears indistinguishable from 

that of Epichloe. At flowering, the Neotyphodium 

mycelium grows upwards through the stem, 

extending into the inflorescence and infecting 

the embryos of the developing seeds so that 

a high proportion of them are infected (White 

et al., 1991). In natural infections of Lolium perenne 

by N. lolii, the mycelium is scanty in vascular 

tissues but is occasionally found in smaller 

vascular bundles (Christensen et al., 2001). 

Alkaloids and endophytism 

Intense interest in Neotyphodium has developed 

since the discovery that consumption of 

endophyte-infected grass is associated with disorders 

of grazing livestock caused by mycotoxins, 

including ergot alkaloids. Two associations 

(symbiota) have been particularly well investigated. 

Ingestion of tall fescue (Festuca arundinacea) 

infected with N. coenophialum causes fescue 

toxicosis in cattle and horses in the Southeastern 

USA (Bacon et al., 1977; Blodgett, 2001). The


359 

Fig12.31 Endophytic hyphae of 

Neotyphodium lolii growing 

intercellularly between epidermal 

cells of Lolium perenne. 

Photographed from material kindly 

provided by P. J.Fisher. 

economic impact of fescue toxicosis to livestock 

producers in the USA has been estimated at 

$50 200 million annually (Siegel et al., 1984). 

Perennial ryegrass (Lolium perenne) containing 

N. lolii is associated with ryegrass staggers in 

sheep in New Zealand (Fletcher & Harvey, 1981). 

Various alkaloids are present in Neotyphodiuminfected 

grasses. These belong to several groups, 

including the ergopeptide-type ergot alkaloids 

which we have already encountered in Claviceps 

purpurea (Figs. 12.28, 12.32a), the lolitrems 

(Fig. 12.32b), the lolines (Fig. 12.32c) and peramine 

(Fig. 12.32d). The primary causal agent 

of ryegrass staggers is the neurotoxin lolitrem B 

(Siegel & Bush, 1997; Kuldau & Bacon, 2001). 

In addition to their toxicity to mammals, 

endophyte-infected grasses have deleterious 

effects on insects feeding on them. The loline 

alkaloids are primarily insecticidal. The endophytes 

are therefore regarded as mutualistic 

symbionts with their grass hosts, protecting 

them against mammalian and insect herbivory 

whilst themselves gaining nutrients and a means 

of dissemination (Clay, 1988; Schardl & Clay, 

1997). Endophyte-infected grasses are also more 

resistant than uninfected hosts against attack by 

certain fungal pathogens (Christensen, 1996) and 

nematodes. 

There are other effects of infection on the 

grass hosts. Infection causes enhanced production 

of biomass, increased tillering, drought 

resistance and competitiveness. These are valuable 

attributes of turf grasses and attempts have 

been made to enhance the agronomic value of 

turf grasses by deliberately infecting them with 

endophytic fungi (Bacon et al., 1997), including 

genetically modified strains. Attempts have also 

been made to free seeds and seedlings of pasture 

grasses from endophytes by fungicidal or heat 

treatment. Prolonged storage may also achieve 

this goal because the endophytes do not retain 

viability for as long as the seeds. However, 

endophyte-free plants are often less competitive 

than their infected counterparts. 

The origin of grass endophytes 

The most convincing evidence that Neotyphodium 

species are the anamorphic state of Epichloe is 

molecular (Glenn et al., 1996; Kuldau et al., 1997). 

Some of the endophytic Neotyphodium species are 

believed to be directly related to a species of 

Epichloe, e.g. N. lolii which is apparently derived 

from E. festucae, whilst others are of hybrid 

origin (Tsai et al., 1994; Schardl & Moon, 2003). 

Interspecific heterokaryon formation has been 

observed in culture (Chung & Schardl, 1997b). 

Hyphal anastomosis and heterokaryosis may 

take place within grass shoots infected with 

more than one species of Epichloe, and the parasexual 

origin of some Neotyphodium species is 

a possibility (Tredway et al., 1999).


Fig12.32 Alkaloids produced by Neotyphodium endophytes in grasses. (a) Ergovaline, an ergopeptide similar to ergotamine 

(see Fig.12.28). (b) Lolitrem B, an alkaloid derived from geranylgeranylpyrophosphate and tryptophan.This substance is neurotoxic 

to grazing animals, causing ryegrass staggers. (c) Loline, an insecticidal pyrrolizidine alkaloid derived from ornithine and 

S-adenosylmethionine. (d) Peramine, an insecticidal pyrrolopyrazine-type alkaloid. 

Other evidence comes from the distribution 

of alkaloids in species of Epichloe and 

Neotyphodium. Epichloe festucae is the only sexual 

species known to synthesize representatives of 

three classes of alkaloids, namely ergovaline, 

lolitrem B and lolines (Fig. 12.32). Neotyphodium 

lolii produces the same three alkaloids and it 

seems reasonable to assume that E. festucae 

was the ancestor that contributed the genes for 

synthesis of these three alkaloids (Clay & Schardl, 

2002). 

12.5.4 Cordyceps and its anamorphs 

There are about 400 500 species of Cordyceps 

(Kobayasi, 1982; Liu et al., 2002) with an epicentre 

of species diversity in northeastern Asia and 

Japan. There are 29 species in the United States 

and Canada, and 18 species in Europe (Humber, 

2000). Most species are necrotrophic parasites 

of insect adults, larvae or pupae, but several 

species grow on the ascocarps of Elaphomyces 

(Mains, 1957). There is a wide range of insect 

hosts including moths, ants, beetles, and cicadas. 

Spiders are also attacked. Within the dead body 

of an infected insect a mass of mycelium or a 

sclerotium develops, and from this a perithecial 

stroma grows out. The perithecial stroma is 

usually fleshy and brightly coloured. It may 

bear perithecia over its entire surface or they 

may be restricted to an upper or lateral portion 

so that there is a stalk region lacking perithecia. 

The perithecia are embedded in stromatal tissue 

and tightly packed together. They are elongate, 

with protruding ostioles. They contain numerous 

narrowly cylindrical asci, each with a conspicuous 

swollen cap pierced by a narrow canal. 

There are 4 8 long cylindrical ascospores which 

are typically divided by transverse septa into 

cylindrical or fusoid part-spores which may 

number 16, 32, 64 or 128 (Hywel-Jones, 2002). 

The ascospores escape singly through the narrow 

pore at the tip of the ascus and usually, but not 

invariably, break up into constituent part-spores 

outside the ascus. 

There is an exceptionally wide range of 

conidial forms including the anamorph genera 

Paecilomyces, Hirsutella, Hymenostilbe, Beauveria, 

Metarhizium and Tolypocladium (Hodge, 2003; 

Stensrud et al., 2005). Some of these are 

shown in Fig. 12.35. Evidence for the connection 

between anamorphs and their Cordyceps teleomorphs 

has been obtained in various ways, 

e.g. by the development of anamorphs in cultures 

derived from ascospores or from hyphal 

bodies within a parasitized insect, by the development 

of perithecial stromata on insect larvae


361 

artificially infected with conidia, or by molecular 

comparison of gene sequences (Liu et al., 2002). 

Teleomorphic states may be rare and some of 

the fungi listed above are far better known as 

anamorphs than as teleomorphs. This is especially 

true of Beauveria bassiana and Metarhizium 

anisopliae, both of which are widely distributed 

in soil, probably growing as saprotrophs. 

They have been used in the biological control of 

insect pests. 

Cordyceps 

Cordyceps militaris forms club-shaped orange- or 

red-coloured stromata (Plate 5g) which project 

above the ground in autumn from buried lepidopteran 

larvae and pupae (Winterstein, 2001). 

Species from several genera of Lepidoptera and 

some Hymenoptera are susceptible. If ascospore 

segments or conidia come into contact with the 

integument of a pupa, germination occurs and is 

followed by penetration of the cuticle, aided by 

the secretion of chitinolytic enzymes. Soon after 

penetration, cylindrical hyphal bodies appear 

in the haemocoel. The hyphal bodies increase in 

number by budding, and become distributed 

within the insect’s body. Death of the insect is 

probably associated with the secretion of the 

toxin cordycepin (3’-deoxyadenosine) which also 

accumulates in the perithecial stroma (Yu et al., 

2001; Kim et al., 2002). After death some 5 days 

after infection, mycelial growth takes place and 

the body of the dead insect becomes transformed 

into a sclerotium. Under suitable conditions 

one or more perithecial stromata develop 

above ground, some 45 60 days post infection. 

Perithecial stromata can also form in pure 

culture on rice grain supplemented with haemoglobin 

or casein (Basith & Madelin, 1968). In pure 

cultures derived from single ascospores, a phialidic 

conidial state called Paecilomyces militaris 

is formed (Fig 12.33c). 

It is not known whether C. militaris is homoor 

heterothallic. Perithecial development has 

been studied in C. militaris by Varitchak (1931). 

Coiled septate ascogonia arise in the peripheral 

layers of the perithecial stroma. The segments 

of the ascogonium become multinucleate and 

give rise to ascogenous hyphae from which asci 

develop in a single cluster at the base of the 

Fig12.33 Cordyceps militaris. (a) Two perithecial stromata 

attached to pupae. (b) Ascus and multiseptate ascospores. 

Note the ascus cap. (c) Conidiophores and conidia. 

perithecium. The perithecial wall is derived 

from hyphae which develop from the stalk of 

the ascogonium or from surrounding hyphae. 

Paraphysis-like hyphae grow inwards from the 

perithecial wall, but at maturity these hyphae 

dissolve and disappear. 

Cordyceps sinensis (Fig. 12.34) is highly prized in 

traditional Chinese medicine (Pegler et al., 1994). 

It grows on the larvae of hepialid moths at 

3600 5000 m in mountainous areas in southern


Fig12.34 Stromata of Cordyceps sinensis growing from insect 

larvae. Image kindly supplied byY.-J.Yao. 

and western China, Tibet and Nepal (Jiang & Yao, 

2002). The cylindrical perithecial stromata may 

be 10 cm or more in length and bundles of dried 

stromata are sold commercially. The anamorph 

is Hirsutella sinensis (Liu et al., 2001). The conidiogenous 

cells are tightly packed together on the 

surface of a stroma. 

The ecological role of Cordyceps spp. on insects 

is difficult to evaluate. Evans and Samson (1982, 

1984), judging by the large numbers of stromata 

collected on worker ants in tropical forests, were 

of the opinion that they exerted a controlling 

effect on population size. 

Cordyceps ophioglossoides grows in woods on 

the subterranean ascocarps of the hart’s truffle 

Elaphomyces, forming bright yellow mycelial 

stands over its surface. Brown club-shaped 

perithecial stromata grow above ground in 

autumn (Plate 4f). Cordyceps capitata grows in 

similar situations. Phylogenetic analyses using 

nuclear and mitochondrial ribosomal DNA 

derived from 22 species of Cordyceps and their 

known anamorphs have shown that four species 

of Cordyceps parasitic on Elaphomyces have very 

close similarity to two species which parasitize 

the nymphs of cicadas, and have probably 

evolved from them, an example of ‘interkingdom 

host-jumping’. These related species have been 

grouped together in a ‘truffle cicada clade’ and 

it has been suggested that the truffle cicada 

clade separated from other Cordyceps clades 

about 43 + 13 million years ago (Nikoh & 

Fukatsu, 2000). Cicada nymphs develop for 

several years underground, feeding on xylem 

sap from the host trees with which they are 

associated. In this respect their physiology is 

similar to that of Elaphomyces spp., which are 

mycorrhizal partners of trees, obtaining nutrients 

from them. Nikoh and Fukatsu (2000) have 

speculated that the overlapping niches of the 

species of Cordyceps which parasitize cicadas and 

those which parasitize hart’s truffles may have 

promoted this interkingdom host jumping. 

Species of Cordyceps reproduce asexually, 

some having more than one anamorphic state, 

i.e. with synanamorphs (Hodge, 2003). 

Considerable research attention has been 

focused on the three anamorphs Beauveria 

bassiana, Metarhizium anisopliae and Tolypocladium 

inflatum (Figs. 12.35a c). The first two have 

potential for the biological control of insect 

pests, whereas Tolypocladium inflatum is the 

source of the immunosuppressant drug cyclosporin 

A (Fig. 12.24a). 

Beauveria bassiana 

This is the conidial form of Cordyceps bassiana 

(Huang et al., 2002) and causes the serious white 

muscardine disease of silkworm (Bombyx mori) 

larvae, which is a threat to silk production. This 

species has been known for well over a century 

and is of historical interest because Agostino 

Bassi, who studied the fungus around 1835, 

proposed the germ theory of disease on the 

basis of his results. This preceded by several years 

the publications of Robert Koch, who is usually 

given credit for the formal proof of pathogenesis 

by micro-organisms. Beauveria bassiana is widely 

distributed in the soil, usually associated with 

diseased insects (Domsch et al., 1980). Species of 

Coleoptera, Diptera, Lepidoptera and other 

groups, including Arachnida, are covered by 

white dusty raised tufts of hyphae bearing


363 

conidia. The association has had a long history. A 

worker ant covered with a fungus similar to the 

present-day B. bassiana has been discovered 

embedded in 25 million year-old amber (Poinar 

& Thomas, 1984). Beauveria bassiana grows readily 

in culture, forming dry conidia and, occasionally, 

synnemata. The conidiophores form densely 

clustered whorls of conidiogenous cells which 

are swollen at the base and extend into a zigzag 

shaped rachis forming small, globose, smooth, 

hyaline conidia (Fig. 12.35a). 

Several mycotoxins have been obtained 

from cultures of B. bassiana including beauvericin, 

a cyclic depsipeptide, oosporein and bassianolide, 

all of which are toxic to insect larvae 

(see Boucias & Pendland, 1998). Numerous 

attempts have been made to use commercial 

preparations of conidia in the biological control 

of insect pests, such as the Colorado beetle 

on potatoes or the codling moth on apples. 

Conidia are either applied alone or, in integrated 

control, in conjunction with a chemical insecticide. 

However, dependable success in biocontrol 

using B. bassiana is still awaited. Whilst it 

is possible to produce large quantities of inoculum, 

this cannot be stored for very long, and 

there are also problems in maintaining a 

reproducibly high level of biocontrol of insect 

pathogens in outdoor situations (Boucias & 

Pendland, 1998). 

Metarhizium anisopliae 

This fungus is the cause of green muscardine 

disease of insects. There are three varieties, 

var. anisopliae, var. acridum and var. major. The 

teleomorph of M. anisopliae var. major is C. brittlebankisoides 

(Liu et al., 2001, 2002). Metarhizium 

anisopliae grows in soil (Domsch et al., 1980), but 

it is also one of the most important insect 

pathogens. Metarhizium anisopliae var. anisopliae 

has a wide host range, attacking members of the 

Coleoptera, Orthoptera, Hemiptera and 

Hymenoptera as well as Arachnida. Metarhizium 

anisopliae var. major is more host-specific, mostly 

infecting soil-inhabiting scarabeid beetles 

(Boucias & Pendland, 1998). In culture it grows 

slowly, forming columns of green, shortly cylindrical, 

uninucleate phialoconidia which are rich 

in lipid droplets (Fig. 12.35b). The wall of the 

conidium is three-layered and the outermost 

layer is highly hydrophobic due to impregnation 

by a hydrophobin. There have been extensive and 

detailed studies of the physiology and enzymology 

of germination and penetration by the germ 

tubes, mainly carried out by Charnley and St 

Leger (1991). The brief account which follows 

Fig12.35 Anamorphic states associated with Cordyceps. (a) Beauveria bassiana.(b)Metarhizium anisopliae. (c) Tolypocladium inflatum. 

The phialides have a swollen base and a long neck. (a,b) to same scale.


draws heavily on the summary in Boucias and 

Pendland (1998). Water is required for germination, 

which is followed by attachment to the host 

cuticle by means of an appressorium. 

Appressorium development is stimulated by 

contact with a hard surface and can take place 

on glass or polystyrene, so long as complex 

nitrogenous substances (e.g. yeast extract or 

peptone) are present. In nature it is presumed 

that such compounds are derived from the 

cuticle. The wall of the appressorium is 

surrounded by a coat of mucilage which tightly 

attaches the appressorium to the host integument. 

An infection peg from the appressorium 

penetrates the surface layer of the integument, 

the epicuticle, but when it reaches the procuticle 

(the layer beneath it), the infection peg expands 

to form a penetration plate which grows out 

parallel to the surface of the integument. From 

the penetration plate, penetration hyphal bodies 

develop and, from these, vertical penetration 

hyphae grow through the innermost layer, the 

procuticle, to the hypodermis and the body 

cavity. From the vertical penetration hyphae, 

hyphal bodies in turn develop which become 

dispersed in the haemolymph. The hyphal bodies 

come to rest in the fat bodies of the insect and 

then give rise to mycelium, by which time, 

48 72 h post infection, the host is dead. Death 

is probably brought about by the action of 

secondary metabolites which function as toxins. 

These include a series of depsipeptides 

(destruxins A E), a hydrophobin, cytochalasins 

and alkaloids. 

Metarhizium anisopliae var. acridum (formerly 

known as M. flavoviride) has been used in the 

biological control of grasshoppers and locusts 

by suspending conidia in oil for low volume 

application. As for B. bassiana, however, the 

commercial viability of M. anisopliae as a mainstream 

insecticide remains to be established 

(Hajek et al., 2001). 

Tolypocladium inflatum 

This is the anamorph of Cordyceps subsessilis which 

fruits on the larvae of scarabeid beetles (Hodge 

et al., 1996). It is the commercial source of the 

immuno-suppressant cyclosporin A, which has 

become a crucial drug in the treatment of the 

rejection reaction after organ transplantation 

(Dreyfuss et al., 1976; Borel, 1986). Other secondary 

metabolites are the efrapeptins, compounds 

with anti-fungal and insecticidal properties 

(Krasnoff & Gupta, 1992). Tolypocladium inflatum 

grows in soil. In culture it first forms Acremoniumlike 

conidia on single slender phialides, but 

later copious hyaline conidia are produced 

in slime from clusters of phialides with a 

globose base and a long, narrow tapering neck 

(Fig. 12.35c). 

12.6 Ophiostomatales 

This group contains about 6 genera (110 species) 

of perithecial ascomycetes which are mainly 

saprotrophic or parasitic on woody hosts. The 

perithecia are non-stromatic, generally longnecked 

and solitary. We shall consider only 

Ophiostoma. 

12.6.1 Ophiostoma 

There are about 100 species of Ophiostoma (Grylls 

& Seifert, 1993; Seifert et al., 1993), largely 

confined to wood and bark and associated with 

bark-boring beetles which disperse their ascospores 

and conidia. Some cause fatal diseases 

of trees, notably Dutch elm disease (see below). 

Others, e.g. O. piceae (Fig. 12.36), cause blue-stain 

(¼ sap-stain) of conifer wood (Seifert 1993; 

Gibbs, 1993). The anamorphic fungus Sporothrix 

schenkii, which is closely related to Ophiostoma 

(Berbee & Taylor, 1992b), is a human pathogen 

(Summerbell et al., 1993). 

The perithecia of Ophiostoma are black in 

colour with a bulbous base and a long cylindrical 

neck, the ostiole of which is surmounted by 

a ring of stiff tapering hairs which hold the 

hyaline unicellular ascospores in a mucilaginous 

blob. The asci have thin evanescent walls and 

the ascospores are released into the body of the 

perithecium and move up the narrow tube inside 

the neck. The perithecia closely resemble those 

of Ceratocystis and the two genera are sometimes 

synonymized (see de Hoog & Scheffer, 1984). 

However, molecular and morphological comparisons 

have indicated that, despite their

OPHIOSTOMATALES 

365 

Fig12.36 Ophiostoma piceae. 

(a) Perithecium showing spore drop at tip 

of neck. (b) Details of ostiole with ring of 

setae. (c) Asci. (d) Synnematous 

conidiophore. (e) Details of apex of 

conidiophore. 

similarity, the two genera are not closely related, 

Ophiostoma being in a sister clade to the 

Diaporthales (p. 373) whilst Ceratocystis is allied 

to the Microascales (p. 368; Hausner et al., 1993; 

Spatafora & Blackwell, 1994). The similarity in 

perithecial morphology suggests parallel evolution 

in adaptation to the insect dispersal of 

ascospores (Malloch & Blackwell, 1993). There 

are differences in anamorphs between the two 

groups. In Ceratocystis sensu stricto the anamorphs 

are phialidic, of the Thielaviopsis type (see 

Figs. 8.8, 12.42e), whereas the anamorphs of 

Ophiostoma are annellidic (de Hoog, 1974). Other 

points of difference are listed on p. 369. 

Most species of Ophiostoma are heterothallic 

and the ascospores are of two mating types, 

A and B. Although ascogonia have been described, 

there are no antheridia. When isolates 

of different mating types from the same ascocarp 

of O. ulmi or O. piceae are inoculated near each 

other in agar cultures, the two mycelia intermingle 

and perithecia develop. However, when 

cultures of different origin are opposed to each 

other, a line of barrage analogous to that seen 

in Podospora anserina may develop between the 

approaching mycelia, a phenomenon associated 

with vegetative incompatibility (Brasier, 1993). 

Perithecium development in O. ulmi has 

been described by Rosinski (1961) and the ultrastructure 

of the ascogenous hyphae and ascosporogenesis 

by Jeng and Hubbes (1980). The 

multinucleate coiled ascogonium, differentiated 

by its greater width from the hyphae which 

subtend it, becomes surrounded by a mantle 

of branched hyphae probably derived from the 

ascogonial stalk. Ascogenous hyphae arise as 

buds from the ascogonium which is positioned 

near the base of the ascocarp. A central cavity 

arises as the result of enlargement of the outermost 

cells of the ascocarp, and the ascogenous


hyphae form a lining layer around this cavity 

and develop centripetally towards the centre of 

the cavity. Croziers develop at the tips of the 

ascogenous hyphae and produce a succession 

of asci, indicating the ascohymenial nature of 

the fungus. The asci have extremely thin walls. 

There are no paraphyses and no periphyses. 

Ascospores released into the cavity of the 

perithecium are extruded through the narrow 

neck and accumulate in a mucilaginous blob 

held in place by the ring of ostiolar hairs. Barkboring 

beetles which feed on the ascospores 

(and also conidia) help in their dispersal. The 

beetles are attracted by ‘fruity’ odours emitted 

from the mycelium. These are volatile metabolites, 

mainly short-chain alcohols and esters, as 

well as monoterpenes and sesquiterpenes 

(Hanssen, 1993). 

Some species of Ophiostoma have two or 

more synanamorphs. These vary in structure 

from yeast-like to mononematous or synnematous. 

They have been assigned to several 

anamorph genera including Leptographium, 

Sporothrix, Pesotum and Graphium. For example, 

O. ulmi has a yeast-like anamorph, a mononematous 

anamorph referred to Pesotum and a synnematous 

anamorph, Graphium ulmi. Older hyphae 

may also produce endoconidia (Fig. 12.37). 

Wingfield et al. (1991) have placed Pesotum in 

synonymy with Graphium. 

12.6.2 Dutch elm disease 

Dutch elm disease is a vascular wilt disease 

of Ulmus spp. caused by O. ulmi, O. novo-ulmi and 

O. himal-ulmi. It is best regarded as a disease 

complex because it is invariably associated with 

the activities of bark-boring scolytid beetles such 

as Scolytus scolytus, S. multistriatus and Hylurgopinus 

rufipes. These are the vectors for the disease. 

Elm populations worldwide have been ravaged, 

causing the death of millions of trees in Europe 

and North America and changing the appearance 

of the landscape, particularly where hedgerow 

elms have been killed. Diseased tree leaves 

wilt in dry weather and rapidly turn brown 

and brittle. Defoliation and death of the twigs 

ensues, and eventually the whole tree dies 

(Plate 5h). The fungus persists as a saprotroph 

in the bark of dead trees. Infected twigs show 

a characteristic brown flecking in the sapwood. 

This is associated with the development of 

brown-coloured bladder-like inflated cells of the 

xylem parenchyma called tyloses, which invade 

the xylem vessels and block them. Gums released 

partly by the action of cell wall-degrading enzymes 

of the pathogen impede water flow. Wilting 

is also associated with the production of the 

wilt toxin cerato-ulmin, which is a hydrophobin 

(Richards, 1993). However, since mutants of 

O. novo-ulmi with low cerato-ulmin production 

still retain pathogenicity, an alternative role 

for it has been sought. Temple et al. (1997) have 

shown that cerato-ulmin can enhance the adhesiveness 

of yeast-like propagules of the pathogen 

and also protect them from desiccation. 

Dutch elm disease was first described in 

Holland in the late 1920s and spread to the rest 

of north-western Europe, North America and to 

parts of Asia. The disease declined in severity 

in Europe in the 1940s but persisted in North 

America, possibly because the American elms 

were more susceptible. This first pandemic was 

relatively mild in effect and did not destroy 

the elm tree populations. When first discovered, 

the disease was associated with the synnematal 

conidial state, Graphium ulmi. Later the 

teleomorphic state was discovered and named 

Ceratostomella ulmi, then Ceratocystis ulmi, now 

O. ulmi. In the mid-1960s simultaneous outbreaks 

of a more severe and aggressive form of the 

disease occurred, centred around ports in 

southern England and originating from 

infected elm logs from North America. These 

outbreaks spread rapidly from the original 

infection foci into much of Britain and mainland 

Europe. 

Isolations from trees affected by the aggressive 

form of the disease yielded a strain of 

Ophiostoma distinguished by its fluffy appearance 

and more rapid growth in culture, in contrast 

with the waxy appearance and slower growth 

of the non-aggressive strain. In many places 

where O. ulmi was present, it has now been 

replaced by the more aggressive form (Brasier 

et al., 1998). The aggressive strain is regarded as 

a distinct species, O. novo-ulmi (Brasier, 1991b). 

Closer investigation of isolates of O. novo-ulmi,

OPHIOSTOMATALES 

367 

Fig12.37 Asexual reproduction in Ophiostoma ulmi. (a,b) Synnematous conidiophores (Graphium ulmi). Parallel bundles of dark 

hyphae branch at their tips to produce holoblastic conidia which accumulate in a sticky drop. (c,d) Mononematous synanamorph 

terminating in conidiogenous cells with a succession of holoblastic conidia which, on detachment, leave a protruding scar or denticle. 

In d some of the conidia show yeast-like budding. (e) An older hypha within which a new hypha and endoconidia have developed 

(from Harris & Taber,1973). 

based on their vegetative incompatibility characteristics, 

showed that they can be separated 

into two distinct vc (vegetative compatibility) 

supergroups. One biotype, centred on the 

Romania Moldova Ukraine region of Europe, 

was designated the Eurasian or EAN vc supergroup, 

whilst the other, centred on the Southern 

Great Lakes region of North America, has 

been designated the North American or NAN vc 

supergroup. They have been formally recognized 

as distinct subspecies, O. novo-ulmi subsp. novoulmi 

for the EAN strains and subsp. americana 

for the NAN strains. There are morphological 

differences between the perithecia of the two 

subspecies, those of subspecies novo-ulmi having 

longer necks than those of subspecies americana 

(Brasier & Kirk, 2001). Naturally occurring 

hybrids between the two subspecies have been 

detected. Rare interspecific hybrids between 

O. ulmi and O. novo-ulmi also occur where the 

former species is being replaced by the latter 

(Brasier et al., 1998). Hybridization between introduced 

pathogens permits their rapid evolution 

(Brasier, 2001). Ophiostoma himal-ulmi is endemic 

to the Himalayas and has been distinguished as 

a third species (Brasier & Mehrotra, 1995). 

Fertilized females of bark-boring beetles, 

possibly carrying ascospores or conidia, excavate 

tunnels beneath the bark of living trees, often 

those already weakened by the disease, to lay 

a cluster of eggs. After hatching, the developing 

larvae also make tunnels beneath the bark 

radiating outwards from the egg chamber. They 

feed on the infected wood, and the galleries 

which they excavate are often lined by synnemata 

or perithecia, so that conidia and ascospores 

become attached to their mouthparts and 

bodies. Young, sexually immature adults emerge 

in the spring and summer. They fly to the 

crotches (branch points) of young twigs where 

they feed on bark before maturation and 

mating. During this twig-feeding stage spores 

of the fungal pathogen may be introduced into 

the host sapwood, and from these multiple 

inoculation points the fungus may spread into 

host tissues by mycelial growth or by movement


of conidia in xylem vessels (Webber & Brasier, 

1984; Webber & Gibbs, 1989). By the latter 

method it has been estimated that movement 

can be as much as 10 cm day 1 . In addition to 

being transmitted by insect vectors, the pathogen 

can be passed from tree to tree by natural 

root contact. 

The control of Dutch elm disease has been 

attempted by the combined use of fungicides and 

insecticides but is now based largely on the 

breeding of resistant cultivars. Major genes for 

resistance have been identified in a group of 

Asian species. By crossing some of these with 

European elms, cultivars have been bred and 

released for commercial sale (Smalley & Guries, 

1993). Resistance may be correlated with the 

production of phytoalexins (mansonones) by the 

host in response to infection (Smalley et al., 1993). 

In U. minor a correlation has also been found 

between vessel diameter and susceptibility, trees 

having vessels of large diameter being more 

susceptible to the disease than those with 

smaller diameter vessels (Solla & Gil, 2002). An 

interesting novel potential method of control 

is by the use of hypovirulent strains of the 

pathogen infected by cytoplasmically transmissible 

virus-like agents called d-factors (d for 

disease), now known to consist of doublestranded 

mitochondrial RNA elements. Twelve 

d-factors have been characterized. Strains 

carrying d-factors are hypovirulent and this 

is correlated with a reduced capacity in vitro 

to produce cerato-ulmin (Rogers et al., 1986; 

Sutherland & Brasier, 1995). 

12.7 Microascales 

The Microascales are a small order currently 

containing 67 species (Kirk et al., 2001). 

The taxonomy of the Microascales has seen a 

turbulent history. Species accommodated here 

are characterized by perithecia (rarely cleistothecia) 

which usually have a long neck. The fact that 

asci are scattered throughout the perithecial 

cavity and are not produced by croziers is one 

reason why members of the Microascales have 

been considered in the past to belong to the 

Plectomycetes. Another moot point has been the 

great similarity of perithecia and general ecological 

features between Ceratocystis (Microascales) 

and Ophiostoma (Ophiostomatales), which will be 

discussed in more detail below. In its current 

shape, the order Microascales is monophyletic by 

DNA analyses (Hausner et al., 1993). Because the 

two major lineages, the Ceratocystidaceae and 

Microascaceae, show considerable differences in 

their biology and ecology, we will briefly discuss 

members of both groups. 

12.7.1 Microascus (Microascaceae) 

The family Microascaceae currently contains 

43 species in 8 genera. The conidial forms are 

hyphomycetous, with conidia produced on 

annellides (see Fig. 8.7). The most important 

genus is Microascus with 14 species, which have 

been described in detail by Barron et al. (1961). 

Simple conidiogenous forms of Microascus are 

referable to Scopulariopsis (Fig. 12.38), whereas 

more complex, synnematous forms belong 

to Cephalotrichum (formerly called Doratomyces; 

Fig. 12.39) or Trichurus (Fig. 12.40). In agar culture, 

both Cephalotrichum and Trichurus produce 

simple Scopulariopsis-like forms in addition to 

the striking synnemata. The connection between 

these annellidic forms and Microascus has 

now been confirmed by phylogenetic analyses 

(Issakainen et al., 2003). Just to confuse matters, 

Cephalotrichum stemonitis produces, in addition to 

annelloconidia, a distinct Echinobotryum conidial 

state (Fig. 12.39e). Graphium is another formgenus 

producing synnemata which form annelloconidia 

at their apex (Fig. 12.41), but here the 

conidia are held in a drop of mucilage at the 

tip of the synnema. Certain Graphium-like forms, 

e.g. G. penicillioides (Fig. 12.41a), have affinity with 

Microascus, although others seem to belong to 

the Ophiostomatales (Okada et al., 2000). 

Microascus spp. and members of related 

genera (e.g. Pseudoallescheria, Petriella) are capable 

of metabolizing a wide range of carbon sources, 

including keratin, crude oil, cellulose and even 

phenol, and they are tolerant of wide-ranging 

environmental conditions. Consequently, they 

are found from the Arctic to hot desert soil, in 

salt marshes, bat guano, herbivore dung, food,

MICROASCALES 

369 

Fig12.38 Scopulariopsis brevicaulis. Conidiophores terminating 

in conidiogenous cells (annellides) from which chains of conidia 

develop.The stippled areas at the tips of the annellides indicate 

the region of growth associated with the development of 

successive conidia. 

silage, and on keratin-rich substrates. Because 

of their ability to degrade keratin and grow at 

37°C, some Scopulariopsis spp. can be pathogenic 

to humans, occasionally causing deep-seated 

mycoses (de Hoog et al., 2000a). Not surprisingly 

for such versatile and adaptable fungi, they 

quickly develop resistance against commonly 

used antifungal drugs (Cuenca-Estrella et al., 

2003). This feature, rather than their pathogenicity 

per se, seems to be the main reason why 

they can be troublesome in clinical situations. 

Several well-known Scopulariopsis states 

have only recently been assigned to 

heterothallic Microascus species (Abbott & Sigler, 

2001). Detailed developmental studies of perithecium 

formation in homothallic species have 

been carried out by Corlett (1966). The vegetative 

hyphae of Microascus consist of uninucleate segments. 

Sexual reproduction is initiated when 

a coiled ascogonium forms and becomes 

ensheathed by hyphae arising from the ascogonial 

base as well as the surrounding vegetative 

mycelium. At this primordium stage, the outermost 

layer already becomes melanized, and it 

surrounds the developing pseudoparenchyma. 

The primordium enlarges by further growth of 

the pseudoparenchyma. The ascogonium is positioned 

initially in a cavity in the centre of the 

primordium, but soon sterile hyphae grow 

inwards from the surrounding pseudoparenchyma, 

raising the ascogonium towards the 

apex of the perithecium. From the ascogonium, 

ascogenous hyphae grow between the sterile, 

inwardly radiating hyphae and form asci without 

croziers from their tips which have become 

binucleate. Simultaneously, at the tip of the 

perithecium pseudoparenchymatous hyphae 

begin to grow inwards and then upwards, 

rupturing the apical wall and extending a 

perithecial neck with an ostiole. During maturation 

of the perithecium, the sterile hyphae in 

the perithecial centre lyse, followed by disintegration 

of the ascus walls, so that the mature 

perithecium contains an outer melanized 

layer surrounding a pseudoparenchyma which 

encloses masses of free ascospores. These ooze 

out through the ostiole as a tendril. 

12.7.2 Ceratocystis and Sphaeronaemella 

(Ceratocystidaceae) 

The most important genus of this small family 

is Ceratocystis (14 species) associated with living 

trees. Some species cause vascular wilts, perhaps 

the most important pathogen being C. fagacearum, 

the cause of oak wilt, which is especially 

destructive in the United States. Ceratocystis 

fimbriata attacks an exceptionally wide range of 

plants, including the European plane (Platanus 

acerifolia), Eucalyptus spp., mango, coffee, sweet 

potato and rubber (Kile, 1993). However, infections 

by Ceratocystis spp. need not be destructive 

to the host, and some species produce benign


Fig12.39 Cephalotrichum (Doratomyces) stemonitis. (a) Synnema or macronematous conidiophore consisting of a parallel bundle 

of dark hyphae branching at their tips to form conidiogenous cells (annellides) and chains of conidia. (b) Developing synnema. 

(c) Micronematous conidiophore bearing six annellides.The stippled region is the cylinder of annellide growth. (d) Annellides from 

a synnema showing chains of annelloconidia.The stippled zone represents the growth cylinder of the annellide. (e) Echinobotryum 

conidial state. (b) and (e) to same scale, (c) and (d) to same scale.

MICROASCALES 

371 

Fig12.40 Trichurus sp. on agar. (a) Macronematous 

fructification. Note the melanized curved setae typical of the 

form-genus.Conidia are produced from annellides arising 

from the tips of the parallel hyphae making up the synnema. 

(b) Micronematous fructification with annellidic 

conidiogenesis. 

infections which merely stain the wood. This 

so-called sap-stain can none the less be of 

economic importance as it reduces the market 

value of the infected wood. 

The asci of the Ceratocystidaceae (Fig. 12.42c) 

deliquesce early in the development of the 

perithecium. The perithecium has a very long 

neck (Fig. 12.42a) through which the ascospores 

are exuded single file, accumulating in a sticky 

drop at the tip of the perithecial neck 

(Fig. 12.42b). This is thought to be an adaptation 

to dispersal by insects which may pick up the 

slime containing ascospores upon browsing, 

or by feeding directly on it. Many Ceratocystis 

spp. produce fruity smells (pineapple, banana, 

pear) which attract insects. The substances responsible 

are complex mixtures of alcohols, esters 

and other volatile substances (Soares et al., 2000), 

and industrial processes are being developed to 

produce them under fermentation conditions 

(Bluemke & Schrader, 2001). The conidial forms 

of Ceratocystis are phialidic, and the conidia 

are typically barrel-shaped or cylindrical and 

are produced deep inside the phialide (Figs. 8.8, 

12.42e). This anamorph used to be called Chalara 

but has now been renamed Thielaviopsis (Paulin- 

Mahady et al., 2002). Additionally, dark melanized 

chlamydospores may be present. 

In addition to Ceratocystis spp., which are 

mainly associated with trees, other members of 

this group are soil-borne saprotrophs or weak 

pathogens attacking the roots of herbaceous 

plants. Examples are Thielaviopsis basicola and 

T. thielavioides (Fig. 12.42e), which can cause 

significant post-harvest rots in stored carrots 

(Punja et al., 1992). The genus Sphaeronaemella 

probably also belongs to the Ceratocystidaceae. 

Its perithecium is typical of the family in being 

long-necked and topped by a frill of hyphae 

which hold the ascospore drop in place 

(Figs. 12.42a,b). Sphaeronaemella fimicola grows 

on dung, and its distinctive perithecia are 

commonly found in association with the fructifications 

of other coprophilous fungi. Although 

S. fimicola can be a weak hyphal parasite, it 

also seems to require diffusible metabolites and, 

in turn, supplies other metabolites to fellow 

coprophilous fungi (Weber & Webster, 1998b). 

There is also an interaction of S. fimicola with 

animals because its ascospore drop appears 

to stick to mites brushing past the perithecial 

neck, and the mites in turn hijack rides on 

flies (Malloch & Blackwell, 1993). In contrast, 

S. helvellae is a mycoparasite infecting the fruit 

bodies of Helvella spp. The conidial state of 

Sphaeronaemella is called Gabarnaudia and 

differs from Thielaviopsis mainly in that the 

conidia are formed at the tip of the phialide 

(Fig. 12.42d), not inside.


Fig12.41 Scanning EM of synnemata of Graphium.The annellations are prominently visible. (a) Graphium penicillioides. 

(b) Graphium sp. Both images reprinted from Okada et al. (2000) with kind permission of Centraalbureau voor Schimmelcultures 

(Utrecht).Original prints kindly provided by G.Okada. 

Fig12.42 Ceratocystidaceae. (a) Perithecium of Sphaeronaemella fimicola. Note the extremely long neck and the crown of ostiolar 

hairs. (b) Enlargement of a mature perithecium apex, with the ostiolar hairs supporting a mucilaginous blob containing ascospores. 

The mucilage has a frothy appearance. Arrows indicate two ascospores ascending in the neck canal. (c) Ascus and conidium of 

S. fimicola. (d) The Gabarnaudia state of S. fimicola.The conidia are delimited at the apex of the phialide. (e) Phialide of Thielaviopsis 

basicola. Note that the cylindrical conidia are delimited deep inside the phialide neck. (d,e) to same scale.

DIAPORTHALES 

373 

Aspects of pathogenicity 

Although Ceratocystis spp. are spread by insects, 

they are not normally associated with the 

tunnels of bark-boring beetles. Instead, they 

infect through pruning wounds or the bark, 

and may be introduced by sap-feeding insects. 

Transmission from infected to adjacent healthy 

trees may also occur via root contact. Ceratocystis 

fagacearum causes oak wilt symptoms by invading 

the xylem and blocking the conducting 

vessels with mycelium and a gel- or gum-like 

substance. Additionally, toxins are produced by 

C. fagacearum and other wilt-causing species, 

and these can reproduce many wilt symptoms 

in the absence of the fungus (Pazzagli et al., 1999). 

Upon death of the host, C. fagacearum forms 

compact mycelial mats underneath the bark. 

The hyphae of the mycelial mat produce conidia 

which are dispersed by beetles attracted by the 

fruity smell. The fungus is heterothallic and the 

conidia double up as spermatia. When spermatia 

of compatible mating types are carried to a 

mycelial mat, perithecia are formed. 

There are several Ceratocystis spp. which are 

associated with coniferous trees, partly as pathogens 

but also as sap-staining fungi (Harrington & 

Wingfield, 1998). These belong to a phylogenetically 

clearly defined group around C. coerulescens 

(Witthuhn et al., 1998). Because conifers are 

unusual hosts for Ceratocystis and all known 

species associated with them are closely related, 

it is assumed that Ceratocystis has only recently 

switched hosts from broad-leaved trees. 

Ceratocystis versus Ophiostoma 

Much confusion has arisen in the past between 

the genera Ceratocystis and Ophiostoma which 

are now known not to be closely related phylogenetically 

(Spatafora & Blackwell, 1994). 

Alexopoulos et al. (1996) have summarized the 

main differences, which are as follows. (1) The 

anamorphic state of Ophiostoma is annellidic 

(Graphium; see Fig. 12.41) whereas that of 

Ceratocystis and its allies is phialidic 

(Thielaviopsis, Gabarnaudia; Fig. 12.42). (2) 

Ophiostoma spp. infect through insect tunnels 

whereas Ceratocystis spp. infect through wounds. 

(3) The cell wall of Ophiostoma spp. contains 

rhamnose-based polymers and cellulose, but 

neither kind is found in Ceratocystis. (4) 

Ophiostoma spp. are insensitive to cycloheximide 

whereas Ceratocystis spp. are sensitive. 

12.8 Diaporthales 

The order Diaporthales currently includes some 

447 species in 94 genera (Kirk et al., 2001) and 

is well separated phylogenetically from the 

other orders of perithecial ascomycetes (Zhang 

& Blackwell, 2001). Several clades can be resolved 

within the Diaporthales, although the naming of 

families is problematic at present (Castlebury 

et al., 2002). Members of the Diaporthales grow 

mainly in the bark of trees as saprotrophs or 

parasites. Discula destructiva infects all aboveground 

organs of dogwood (Cornus spp.) causing 

anthracnose (leaf blight, twig dieback, stem 

cankers) which is devastating the native Cornus 

populations of North America (Redlin, 1991). 

Two other important plant-pathogenic genera 

are Diaporthe and Cryphonectria, and these will be 

considered in more detail below. 

Members of the order Diaporthales are 

characterized by perithecia which are produced 

in clusters or stromata, often embedded in the 

host tissue with their long necks protruding 

beyond the surface. The asci are unitunicate 

and contain eight ascospores which have one or 

more septa. Diaporthales may be homothallic or 

heterothallic, in the latter case with a bipolar 

mating type system. The conidia are produced by 

phialide-like structures lining the inside surface 

of pycnidia, i.e. anamorphic Diaporthales were 

formerly classified as coelomycetes. Pycnidia 

are usually dark-walled (melanized) and have 

one or more openings through which the 

conidia exude in slimy drops. They are more 

commonly encountered than the sexual state 

(see Fig. 12.43). 

12.8.1 Diaporthe and its anamorph 

Phomopsis 

Developmental aspects 

Perhaps the only detailed developmental study 

in Diaporthe was carried out by Jensen (1983) on 

D. phaseolorum var. sojae, which is homothallic


Fig12.43 Phomopsis phaseoli.(a)Surfaceviewofa 

conidium-producing stroma formed in agar culture. 

(b) Phialides producing b-conidia. (c) Ovoid a-conidium and 

elongated b-conidium. Both types of conidium are produced 

from similar phialides. (b) and (c) to same scale. 

like all species of Diaporthe examined to date. 

In culture, the mycelium consists of narrow 

hyphae containing 3 4 nuclei per segment, and 

wider ones with up to 15 nuclei per segment. 

Hyphae aggregate and swell to form a pseudoparenchymatous 

stroma which produces both 

pycnidia and perithecia. In nature, the pycnidial 

Phomopsis state is produced earlier than the 

Diaporthe state which is most often seen on 

dead plant material. Conidial locules form in the 

upper region of the stroma (ectostroma) when 

two opposing palisades of hyphae press against 

each other, accompanied by lysis of hyphae 

bordering the developing slit. In consequence, 

the slit becomes convoluted and lined 

by hymenium. Ectostromatic cells proliferate to 

form a neck, resulting in the typical shape of the 

pycnidium consisting of a more or less globose 

structure within which the lobed or folded 

hymenium is located, and one or several necks 

through which conidia are exuded (Fig. 12.43a). 

The conidiogenous cells are interpreted as 

phialides. They are awl-shaped, 20 mm long and 

tapering from 2 3 mm at their base to 1 mm at 

their apex (Fig. 12.43b). Two types of conidia are 

produced, often within the same conidioma 

(Fig. 12.43c). The ovoid a-conidia contain two 

lipid droplets and germinate readily in culture, 

whereas b-conidia are highly elongated and do 

not usually germinate in P. phaseoli or other 

Phomopsis spp. They are therefore interpreted as 

spermatia (Jensen, 1983). 

According to Uecker (1988), Phomopsis typically 

has a dark stroma producing a- and b-conidia, 

the teleomorph being Diaporthe. Unfortunately, 

few typical Phomopsis species exist since many 

produce only either a- or b-conidia, and/or 

lack the Diaporthe state. Further, there are few 

distinguishing features in conidial shape 

between different Phomopsis species, and species 

identification is based mainly on the host species 

with which a given strain is associated. This 

poses problems because the delimitations of host 

ranges are not precisely characterized. Thus, the 

taxonomy of Phomopsis is in a state of confusion, 

with many synonyms probably in existence. 

Uecker (1988) has compiled over 800 Phomopsis 

names in current use, but Kirk et al. (2001) 

have estimated that only about 100 species of 

Phomopsis exist. The genus is thus in urgent need 

of an up-to-date monographic treatment, Grove 

(1935) having been the last mycologist to rise 

to this formidable task. 

In D. phaseolorum, sexual reproduction is 

initiated by the formation of ascogonial coils in 

the lower region of the stroma, termed entostroma 

by Jensen (1983). These coils become

DIAPORTHALES 

375 

enveloped by hyphae which proliferate to form 

the wall (peridium) of the perithecium, and 

by others which form the pseudoparenchymatous 

centrum and paraphyses. A neck lined by 

periphyses is formed relatively early in perithecium 

development. The ascogenous hyphae 

arising from the ascogonial coils form a bowlshaped 

hymenium in the base of the perithecium. 

Shortly before maturity of the 

perithecium, the ascogenous hyphae produce 

croziers. Karyogamy, meiosis and mitosis all 

occur in the usual way, giving rise to eight 

nuclei which divide once more, so that eight 

bicellular ascospores are produced in each ascus. 

A typical feature of Diaporthe is that the asci often 

become detached from the hymenium before or 

after the ascospores are ripe, so that the cavity of 

the perithecium is filled with loose asci or free 

ascospores. Ascospores are usually discharged 

non-violently as sticky tendrils exuding from the 

ostiole of the perithecium. The ascus has a 

prominent apical apparatus which stains with 

iodine. 

Ecology 

Species of Phomopsis and Diaporthe cause serious 

plant diseases of commercial significance, 

such as pod and stem blight of soybeans 

and other pulse fruits (D. phaseolorum, anamorph 

P. phaseoli) or stem canker and leaf necrosis of 

sunflower (D. helianthi, anamorph P. helianthi). 

Many Phomopsis diseases are caused by species 

complexes, i.e. different Phomopsis spp. can be 

isolated from the same diseased plant in the 

field. All species associated with a given disease 

may not be equally pathogenic. A good example 

is dead arm of vines, which is caused primarily 

by P. viticola. Several other Phomopsis species 

which can also be isolated from vines are only 

weakly pathogenic or entirely non-pathogenic 

(Mostert et al., 2001). Fungi colonizing the living 

plant host as permanently asymptomatic infections 

are termed endophytes. The example of 

P. viticola illustrates the diffuse boundary 

between endophytism and parasitism; some 

Phomopsis strains are entirely endophytic whereas 

others initially cause latent infections but later 

become pathogenic (Mostert et al., 2000). Another 

example is provided by Diaporthe toxica 

(anamorph formerly called P. leptostromiformis) 

which infects living lupins as coralloid hyphae 

with a limited spread beneath the cuticle. 

Such latent infections can persist for many 

months until death of the colonized host 

organs occurs by natural causes, e.g. senescence 

at the end of the growing season. Within 

1 2 days of host death, large-scale colonization 

of the infected tissue occurs (Shankar et al., 1998). 

Colonization by saprotrophic and pathogenic 

Phomopsis spp. can be accompanied by the secretion 

of large amounts of cell wall-degrading 

enzymes which indiscriminately macerate the 

plant tissue (Heller & Gierth, 2001). This accounts 

for the strongly necrotic nature of many 

Phomopsis diseases. Toxins may also be produced 

by phytopathogenic species, and these may facilitate 

rapid colonization by killing host cells and 

preventing an immune response. The Phomopsis 

state of D. toxica produces phomopsins, which are 

cyclic peptides comprising six unusual amino 

acids. These can accumulate in lupin stems and 

seeds to such high levels that they cause a serious 

toxicosis called lupinosis in sheep grazing on 

lupin stubble, or fed with lupin seeds (Culvenor 

et al., 1977). They seem to act mainly on the 

microtubular cytoskeleton, and their primary 

effect is on the liver of affected sheep (Edgar 

et al., 1986). Another example is the toxin phomozin 

which is produced by P. helianthi and has 

been shown to be capable of killing host tissue 

(Mazars et al., 1991). 

Recently, Diaporthe ambigua, the cause of 

cankers on roots and stems of fruit trees, 

has been found to be infected by a mycovirus 

which reduces the ability of its fungal host to 

cause disease on plants (Preisig et al., 2000). 

Hypovirulence-causing fungal viruses and their 

implications for biological control are discussed 

in the following section on Cryphonectria 

parasitica. 

12.8.2 Cryphonectria parasitica 

Readable accounts of various aspects of 

C. parasitica have been written by Nuss (1992), 

Heiniger and Rigling (1994) and Dawe and 

Nuss (2001). The origin of C. parasitica is uncertain. 

It was first reported in 1904 as a sudden and


rapidly spreading infection of Castanea dentata 

(American edible chestnut) in North America, 

and in 1938 on C. sativa (European edible chestnut) 

in Italy, from where it spread rapidly to 

other countries. It is also known in Asia, the 

putative centre of origin of C. sativa which was 

brought from the Near East to Western Europe 

by the Romans. It is possible that the pathogen 

was accidentally introduced into the USA and 

Europe with seedlings of Asian C. crenata 

(Anagnostakis, 1987). Other tree species such as 

oak (Quercus spp.) are occasionally attacked, 

although only with minor commercial damage. 

The fungus is a wound pathogen, colonizing 

the bark and cambium tissues as a spreading 

mycelium. The host defence reaction produces 

cankers (see Fig. 12.18), and branches die if 

cankers girdle their circumference. Cankers are 

often coloured reddish-brown due to the abundant 

formation of conidia which ooze out in 

sticky tendrils from the pycnidia producing 

them. Conidia are spread by animals and rainsplash. 

Perithecia are also formed, embedded 

in the bark tissue. The fungus is heterothallic, 

with a bipolar mating system. Conidia function 

as spermatia but can also germinate directly 

to cause fresh infections. The roots are not 

normally affected, and sucker shoots may grow 

from intact rootstocks or from points proximal 

to girdling cankers, but these new shoots also 

become infected in due course. Following the 

establishment of C. parasitica, the American 

chestnut tree has become reduced to a shrublike 

habit, not unlike the way in which the elm 

tree in Europe has been affected by Dutch elm 

disease (see p. 366). The disease caused by 

C. parasitica is known as chestnut blight and 

has had a dramatic effect especially in the 

eastern United States, where C. dentata once 

accounted for 50% of the value of hardwood 

timber (Agrios, 2005). 

Hypovirulence in Cryphonectria parasitica 

Similarly severe outbreaks to those in the United 

States were noted in Europe, but self-healing 

cankers were observed about 15 years after the 

first sighting of the disease. Self-healing was 

shown by Grente and Sauret (1969) to be 

associated with the presence of hypovirulent 

C. parasitica isolates, i.e. strains with a much 

reduced virulence. Moreover, when the hyphae of 

a fully virulent colony were allowed to fuse with 

those of a hypovirulent strain by anastomosis, 

the former became hypovirulent, too. Eventually 

it was discovered that hypovirulence is associated 

with the presence of an unusual fungal 

virus consisting of double-stranded RNA surrounded 

by membranes but without a protein 

coat (Anagnostakis & Day, 1979). This new type 

of virus was named Hypovirus (see Dawe & Nuss, 

2001). There are now three species of Hypovirus 

known from Cryphonectria (Smart et al., 2000), 

the best-examined being CHV-1 (Cryphonectria 

Hypovirus 1). Cryphonectria is also a repository 

for mycoviruses belonging to several other 

taxonomic groups (Hillman & Suzuki, 2004). 

Strains of C. parasitica infected by Hypovirus 

have several phenotypic characteristics that 

distinguish them from uninfected C. parasitica. 

In addition to their hypovirulence on chestnut 

trees, these include a pale rather than orange 

colony colour on agar, reduced production of an 

extracellular laccase and of a cell surface hydrophobin 

protein due to reduced transcription of 

their genes, poor asexual sporulation, and lack of 

sexual reproduction because of female sterility. 

Several genes were thus found to be affected by 

the presence of the virus. This pleiotropic effect 

is thought to be due to the action of the virus on 

various signalling cascades, whereby the stimulation 

of the cAMP pathway due to an inhibition 

of the inhibitory a subunit (CPG-1) of a large 

trimeric G protein has been particularly strongly 

implicated (Chen et al., 1996). 

The CHV-1 virus genome consists of two open 

reading frames which produce altogether three 

proteins (Shapira et al., 1991). It is not yet clear 

how these act to cause the observed symptoms, 

except that the p29 protein is responsible for 

reducing the pigmentation and asexual sporulation 

as well as transcription of the laccase gene. 

However, p29 does not seem to cause hypovirulence 

(Nuss, 1996). In contrast, when the 

CPG-1 protein levels were reduced by the 

presence of the wild-type virus or by genetic 

manipulation of uninfected C. parasitica, or when

MAGNAPORTHACEAE 

377 

cAMP levels were raised by chemical treatment, 

much of the phenotype of hypovirus infection 

including hypovirulence was induced. This 

hints at an interplay between several signalling 

pathways, as outlined for Magnaporthe grisea 

(Fig. 12.48). 

Experiments with CHV-1 have also provided 

an insight into the sexual reproductive system 

of C. parasitica because the virus suppresses the 

genes encoding the mating pheromones which 

could thus be identified (Zhang et al., 1998). Both 

male and female pheromones were suppressed 

by CHV-1 infections. The reason why infection 

leads selectively to female sterility is unclear 

but may be because a certain proportion of 

conidia, which double up as spermatia, remains 

uninfected by the virus during conidiogenesis. 

Biological control of Cryphonectria parasitica 

by Hypovirus 

The transmission of Hypovirus from one strain of 

C. parasitica to another is mediated by anastomosis, 

which requires vegetative compatibility. 

In C. parasitica as in Podospora anserina (p. 320), 

there are several genetic loci controlling vegetative 

compatibility, and anastomosis as well 

as virus transmission occur readily between two 

strains possessing identical alleles at all six vegetative 

incompatibility (vic) loci. Heteroallelism 

at one or more loci restricts anastomosis and 

reduces the percentage of virus transmission, 

whereby mismatches at certain loci have a more 

restrictive effect than those at others (Cortesi 

et al., 2001). Of course, virus transmission in the 

field will be higher in populations containing 

a low diversity of vic alleles. Such is the case 

in Europe, where hypovirulent strains were 

observed to spread rapidly after their discovery. 

There are different strains of Hypovirus which 

may be mildly hypovirulent, i.e. only moderately 

restricting canker development and asexual 

sporulation in Cryphonectria, or may be aggressive. 

The latter permit Cryphonectria to form 

only very small cankers, but also greatly reduce 

asexual sporulation. Since the virus can be disseminated 

at least to a certain extent in conidia 

of C. parasitica, mild virus strains may spread 

faster in nature than aggressive ones. 

In addition to relying on the natural spread 

of hypovirulent strains of C. parasitica in Europe, 

it has proven possible to implement a biological 

control strategy by inoculating active cankers 

with a paste containing a mixture of hypovirulent 

strains differing in their vic alleles. 

Success has been obtained especially in chestnut 

orchards or in regions where hypovirulent 

strains were rare in the field (Heininger & 

Rigling, 1994). Active cankers can be converted 

into healing cankers if one of the inoculated 

hypovirulent strains can anastomose with the 

fully pathogenic strain. In addition, the natural 

spread of hypovirulence was observed around 

sites of release (Heininger & Rigling, 1994). 

In contrast, in the eastern USA where a 

great diversity of vic alleles exists in the wild, 

biological control measures have not generally 

been successful except in isolated forests. 

Another reason for the difficulties may be that 

an aggressive hypovirus strain was chosen for 

initial release experiments, which strongly 

reduced the ability of C. parasitica to produce 

conidia (Nuss, 1992). Current strategies are using 

the fact that cDNA of Hypovirus can be stably 

integrated into the genome of C. parasitica, 

and produces double-stranded viral RNA in the 

fungus. Whereas the RNA of the virus is not 

transmissible via sexual reproduction into ascospores, 

the integrated genomic DNA, of course, 

is transmitted so long as the viral RNA, which 

causes female sterility, is absent from the fungal 

cytoplasm. This strategy promises to be more 

successful than previous release experiments 

because the vic alleles are re-mixed during 

sexual reproduction, thereby facilitating the 

introduction of the virus into a population 

with diverse vic alleles (Dawe & Nuss, 2001). 

12.9 Magnaporthaceae 

This small family (9 genera, 26 species) is 

currently homeless, having been excluded from 

the Diaporthales (see p. 373) with which it 

was formerly thought to be associated (Berbee, 

2001; Castlebury et al., 2002). We include it here


because two members, Magnaporthe grisea and 

Gaeumannomyces graminis, are important plant 

pathogens. Seminal work on developmental and 

molecular aspects of plant pathogenesis has 

been done with M. grisea which will be the 

main focus of this section. 

Magnaporthe grisea causes rice blast disease 

in which individual infections give rise to 

spindle-shaped necrotic lesions on rice leaves. 

The fungus is particularly common in South 

East Asia, its probable centre of origin where 

it has been known for centuries (Rao, 1994). Rice 

blast has spread to virtually all rice-growing 

areas, although it is more severe in cooler 

climates. Considerable research efforts are 

being directed at controlling rice blast, although 

the output in the shape of fungicides against 

M. grisea or the seeds of resistant rice cultivars 

may well be beyond the financial means of the 

small-scale agricultural systems found in many 

countries in Asia and Africa where rice blast is 

a problem. 

In the field, the fungus is encountered mainly 

in the anamorph state which used to be called 

Pyricularia oryzae if growing on rice. In addition 

to rice, M. grisea can attack wheat, barley and 

various wild grasses on which the asexual state is 

called P. grisea. Accordingly, the rice pathogen 

should perhaps be renamed M. oryzae, but we feel 

bound by convention to retain M. grisea since 

that name is universally used. There are several 

strains with different host spectra, and e.g. the 

wheat blast strain in Brazil is genetically distinct 

from rice blast strains present in the same 

regions (Urashima et al., 1993). This is consistent 

with the suggestion by Couch et al. (2005) 

that the rice-infecting lineage of M. grisea arose 

from a single host-switching event from Setaria 

millet early in the history of rice cultivation 

which began around 5000 BC. Sexual reproduction 

is rare in the field especially with the rice 

strains, so that discrete clones of M. grisea 

populations are typically formed in many ricegrowing 

areas (Zeigler, 1998). In tropical climates 

with up to three cropping seasons each year, the 

fungus can continuously infect fresh green 

foliage, whereas in Southern Europe it overwinters 

on rice stubble. Magnaporthe grisea is 

haploid, with each nucleus containing about 

seven chromosomes (Valent, 1997). 

12.9.1 Conidium germination and 

appressorium formation in 

Magnaporthe grisea 

A summary of the disease cycle is given in 

Fig. 12.44. Good reviews have been written by 

Howard and Valent (1996), Valent (1997) and 

Tucker and Talbot (2001). The conidia of M. grisea 

are three-celled, with each cell containing a 

single nucleus. A mature conidium swells upon 

hydration, and this causes the breakage of the 

wall at the tip of the spore, releasing a drop 

of mucilage stored in the periplasmic space 

(Fig. 12.45a). This may already occur while the 

spore is still attached to the conidiophore. 

The exact chemical nature of this mucilage is 

unknown, although it probably contains glycoproteins. 

It attaches the spore firmly to the wax 

of the host cuticle or other hydrophobic surfaces 

(Hamer et al., 1988; Howard, 1994). Mucilage 

release is a purely physical phenomenon which 

does not require any de novo metabolic 

activities. 

Under suitable conditions, a single conidial 

cell usually the basal or apical cell, more rarely 

the central one emits a germ tube. Numerous 

conflicting reports have been published on the 

requirements for germination, but in our experience 

conidia germinate readily in aqueous 

suspension or in contact with any inert surface, 

provided that they have been washed by centrifugation 

and resuspension in water. Washing 

removes an auto-inhibitor which prevents germination 

of spores in dense suspensions (Kono et al., 

1991). Germination on the plant cuticle may 

appear to be stimulated simply because the inhibitor 

is lipophilic and dissolves into the cuticular 

waxes, thereby becoming diluted from the 

spore (Hedge & Kolattukudy, 1997). 

In contrast to spore germination, commitment 

to appressorium formation requires 

the presence of specific environmental signals. 

These are perceived after the germ tube has 

formed a hook-like appressorium initial (Bourett 

& Howard, 1990; deZwaan et al., 1999). 

Appressoria are formed from hooks upon contact


379 

Fig12.44 The infection sequence of 

Magnaporthe grisea.The approximate 

times are indicated, as are developmental 

stages at which signalling cascades are 

known to be involved.


Fig12.45 Microscopy of Magnaporthe grisea. (a) Hydrated conidium of M. grisea showing the drop of mucilage exuded at the apex. 

(b) Ungerminated conidium with dense cytoplasmic contents and developing vacuoles. (c) Conidium on a hydrophobic surface about 

18 h after germination. Most cytoplasmic contents have been translocated into the appressorium which is laying down a dark 

melanized wall. (d) SEM of a mature appressorium of M. grisea.Whereas the conidial cells have collapsed due to the loss of turgor 

pressure, the appressorium is still turgid. (e) TEM of an appressorium penetrating a cellophane membrane.The appressorial wall is 

heavily melanized with the exception of the basal region through which the penetration peg has emerged. A large vacuole (Vac) and 

nucleus (Nuc) are visible inside the appressorium. (f,g) Formation of bulbous hyphae from an appressorium, some 36 h after 

penetration of an onion epidermis. A thinner secondary hypha has already been produced (arrow). Micrographs in (d) and (e) kindly 

provided by R. J. Howard; (d) reprinted fromValent (1997) with kind permission of Springer Science and Business Media; 

(e) reprinted from Bourett and Howard (1990), by copyright permission of the National Research Council of Canada.Original 

micrographs in f and g kindly supplied by A. J.Foster. (a c) to same scale; (f,g) to same scale.


381 

with a hydrophobic surface, or by means of 

chemical cues such as cutin monomers (especially 

1,16-hexadecanediol). Major carbon and 

energy storage products in spores of M. grisea are 

cytoplasmic glycogen deposits and lipid droplets. 

During and after germ tube emergence, the 

glycogen becomes hydrolysed and enters the 

germ tube as soluble sugars. In contrast, lipid 

droplets become mobilized and migrate intact 

into the germ tube (Thines et al., 2000), most 

probably along elements of the cytoskeleton. 

Lipid droplets accumulate in the developing 

appressorium (Figs. 12.45b,c), and their exit 

is prevented by the formation of a septum 

which cuts off the appressorial cytoplasm from 

that of the germ tube. The single nucleus present 

in the germinating conidial cell divides 

once, and one nucleus enters the appressorium 

whereas the other remains in the germ tube. 

After the septum has been completed, the germ 

tube and conidial cell collapse (Fig. 12.45d). 

12.9.2 Appressorium maturation 

and host penetration by 


The maturation of the appressorium is a rapid 

process, and within 12 h of conidia being placed 

on a suitable surface, mature appressoria will 

have formed (Fig. 12.44). Penetration takes place 

about 24 h after spore germination. Several 

processes can be observed with the light microscope, 

e.g. when drops of a conidial suspension 

are placed on plastic coverslips or onion epidermis. 

The lipid droplets which have accumulated 

in the appressorium aggregate into larger drops. 

In the centre of the appressorium, a vacuole 

forms and enlarges, and the lipid droplets enter 

the vacuole by microautophagocytosis and are 

degraded there (Weber et al., 2001). This presumably 

provides the energy needed for the penetration 

events which follow. While the lipid 

droplets are being degraded, a thick brown 

wall forms on the outside of the initially 

hyaline wall. This contains melanin. The melanin 

of M. grisea, like that of most ascomycetes, is 

a polymer of dihydroxynaphthalene (DHN), 

although other pathways exist in other groups 

of fungi, plants and animals. DHN is a 

pentaketide, i.e. it is formed by the head-to-tail 

condensation of five acetate units (Fig. 12.46) 

which may well arise directly from lipid oxidation. 

Melanin biosynthesis in fungi has been 

reviewed by Bell and Wheeler (1986) and Butler 

and Day (1998). In addition to giving strength 

to the appressorial wall, melanin also reduces 

the pore size to less than 1 nm so that molecules 

larger than water cannot traverse the 

melanized wall. 

Soon after the melanin layer has been 

deposited, the appressorium begins to synthesize 

large quantities of solutes, especially glycerol 

(de Jong et al., 1997). Since these solutes cannot 

escape, water moves inwards by osmosis, resulting 

in the generation of a turgor pressure of 

up to 8 MPa (¼ 80 bar). This is one of the highest 

pressures recorded in any living cell (Howard 

et al., 1991). At its base, the appressorium is 

cemented tightly to the surface of the cuticle by 

a very effective adhesive which consists mainly 

of glycoproteins and lipids (Ohtake et al., 1999). 

In the basal plate of the appressorium, there is 

a small non-melanized pore, so that eventually 

the turgor pressure is relieved by driving a penetration 

peg through the surface (Fig. 12.45e). 

The penetration peg contains a conspicuous 

internal skeleton of actin (Bourett & Howard, 

1992), which is almost certainly involved in 

maintaining its shape, akin to the internal 

skeleton at the tip of a growing hypha (see 

Fig. 1.8). 

12.9.3 Colonization of the host 

and sporulation of 


Once the cuticle has been penetrated, the 

infection peg enlarges and branches to form 

hyphae which initially look swollen and are 

therefore called bulbous hyphae. Interestingly, 

at this stage the ultrastructure of an infection by 

M. grisea is similar to that of haustoria produced 

by biotrophic pathogens such as rusts or powdery 

mildews in that the bulbous hyphae do not 

pierce but invaginate the host plasmalemma 

(Heath et al., 1992). This initial biotrophic phase 

is confined to the first epidermal cell encountered; 

hyphae reaching adjacent cells quickly


Fig12.46 The biosynthetic pathway 

of fungal melanin via DHN 

(dihydroxynaphthalene). A polyketide 

synthase fuses five acetate units 

head-to-tail followed by cyclization, 

resulting in the pentaketide 

1,3,6,8 -tetrahydroxynaphthalene. 

This is modified by two reductases 

and two dehydratases to 

1,8 -dihydroxynaphthalene.This melanin 

precursor, which is presumably 

synthesized in the cytoplasm, is 

released into the wall and then 

polymerized to melanin by wall-bound 

oxidases, presumably laccases. 

Melanin biosynthesis is an excellent 

target for fungicides, and the points 

of inhibition of several of them are 

indicated. Based partly on Uesugi (1998) 

and Thompson et al. (2000).


383 

Fig12.47 (a) Conidiophores of 

Magnaporthe grisea emerging from 

a stoma on a rice leaf. Detached 

conidia are also shown (b). 

colonize the plant tissue. These secondary colonizing 

hyphae are thinner and straighter than 

the bulbous hyphae (Figs. 12.45f,g). Within 5 days 

of infection, diamond-shaped lesions of dead 

tissue develop, and these emit conidiophores 

which often grow out through dead stomata 

(Fig. 12.47). 

The interaction between M. grisea and rice 

is governed by a gene-for-gene relationship 

(Valent, 1997; see p. 619). In compatible interactions, 

the host response is delayed because the 

fungus is not immediately recognized by the 

plant. However, even virulent strains of M. grisea 

will eventually be exposed to the toxic products 

(phytoalexins) of the host’s delayed immune 

response, and M. grisea seems to have evolved 

mechanisms to deal with phytoalexins by exclusion. 

It is becoming clear that ABC transporters 

play a crucial role, and we have already come 

across them as a resistance mechanism developed 

by Candida albicans against clinical drugs 

(see p. 278). The report by Urban et al. (1999) 

on M. grisea was one of the first to implicate 

a phytoalexin-excluding ABC transporter as an 

important factor in the colonization of a plant 

host by a fungal pathogen. ABC transporters 

have now been shown to play a crucial role in the 

exclusion of toxic substances as well as fungicides 

in several plant-pathogenic fungi (Hayashi 

et al., 2002; Stergiopoulos et al., 2002).


Fig12.48 The three principal signalling cascades involved in appressorium differentiation in Magnaporthe grisea and in many other 

differentiation processes in other eukaryotes.Cross-talk occurs between the individual pathways, but this is not shown here. 

Abbreviations are as follows: CaM (calmodulin), cAMP (cyclic adenosine monophosphate),Cat. (catalytic), DAG (diacylglycerol), 

GTP (guanosine triphosphate), IP 3 

(inositol trisphosphate), MAPK (mitogen-activated protein kinase), PIP 2 

(phosphatidylinositol 

bisphosphate), Reg. (regulatory), TF (transcription factor). 

12.9.4 Signalling and pathogenesis 

in Magnaporthe grisea 

Both signals for appressorium initiation surface 

hydrophobicity and cutin monomers are 

probably perceived at the plasma membrane of 

the Magnaporthe germ tube. The actual receptors 

are unknown at present, but the Pth11p plasma 

membrane protein is likely to be one of them 

(deZwaan et al., 1999). The transmission of signals 

from the plasma membrane to the nucleus 

occurs along several different routes (Fig. 12.48; 

Dean, 1997; Tucker & Talbot, 2001) which are 

briefly outlined below: 

1. One membrane receptor receiving the 

chemical stimulus 1,16-hexadecanediol acts via 

a trimeric GTP-binding protein to activate an 

adenylate cyclase which converts ATP into the 

second messenger, cyclic AMP (cAMP). This, in 

turn, activates a protein kinase A by releasing 

its monomeric catalytic subunits from the 

inactive tetramer, and the catalytic subunits 

then phosphorylate regulatory proteins (transcription 

factors) which enter the nucleus 

and activate the genes required for specific 

developmental steps. 

2. The involvement of a second common 

eukaryotic signalling cascade in appressorium 

formation was suggested by Thines et al. (1997) 

who noted that diacylglycerols could trigger 

appressorium formation on normally non-inductive 

hydrophilic surfaces such as glass. The 

initial signal (hydrophobicity) is thus likely to 

be transduced via phospholipase C which hydrolyses 

the membrane lipid phosphatidylinositol 

into inositol-triphosphate (IP 3 ) and diacylglycerol 

(DAG). IP 3 acts by releasing Ca 2þ from


385 

intracellular stores such as the endoplasmic 

reticulum; this forms a complex with the 

calcium-binding protein calmodulin, and the 

calcium calmodulin complex activates a calmodulin-dependent 

protein kinase. The DAG component 

directly activates protein kinase C (Fig. 

12.48). Both the IP 3 and DAG branches of this 

signalling pathway thereby lead to the activation 

of protein kinases which phosphorylate transcription 

factors. 

3. Mitogen-activated protein kinase (MAPK) 

pathways have been proposed to be involved at 

various points in appressorium induction and 

maturation in M. grisea (Xu & Hamer, 1996; 

Thines et al., 2000). A mitogen is an extracellular 

substance which stimulates nuclear division 

or cell differentiation; here it is a stimulus 

for appressorium formation. The MAP kinase 

encoded by PMK1 responds to a surface signal and 

interacts with the cAMP pathway in a manner 

not yet entirely understood, to initiate appressorium 

formation (see Fig. 12.48). A second MAP 

kinase, MPS1, is involved in penetration of the 

epidermis from mature appressoria. A third MAP 

kinase, OSM1, is involved in turgor regulation 

during osmotic stress but plays no role in 

appressorium functioning (Dixon et al., 1999). 

MAP kinases are very highly conserved between 

different fungi, to the extent that they are 

functional when their genes are exchanged, 

e.g. between M. grisea, Candida albicans and 

Saccharomyces cerevisiae (Xu, 2000). 

It should be noted that any one of the above 

principal signalling cascades may act repeatedly 

in the course of appressorium development, as 

indicated in Fig. 12.44, and in other events such 

as production of conidiophores and conidia. 

Signal cascades acting repeatedly in the life 

cycle of M. grisea use many shared components 

and only a few specific ones at any one time 

point. There is also considerable cross-talk 

between the three types of signalling cascade 

mentioned here (see Kronstad et al., 1998), and 

equivalent signalling pathways are involved 

in infection processes of many other fungal 

pathogens and in other fundamental processes 

such as yeast hyphal dimorphism, mating and 

osmoregulation in most fungi examined to 

date (Xu, 2000). They are also fundamentally 

conserved across other eukaryotic life forms, 

and some are even found in prokaryotes. For 

this reason, signalling cascades are unlikely to 

provide suitably specific targets for fungicides, 

and interest in this aspect of signalling seems to 

have waned somewhat in recent years. 

12.9.5 Gaeumannomyces graminis 

Gaeumannomyces graminis var. tritici causes take-all 

disease of wheat, barley, rye and numerous 

wild grasses. The pathogen is soil-borne and 

Fig12.49 Melanized hyphopodia of 

Gaeumannomycesgraminis arising from an 

equally strongly melanized runner hypha 

formed on the hydrophobic surface of a 

plastic coverslip.


Fig12.50 Diagrammatic representation of the 

relationship between wheat yield (solid line), the 

severity of take all infection (dashed line) and the 

occurrence of 2,4-diacetylphloroglucinol-producing 

Pseudomonas spp. (dotted line) on a field with successive 

wheat cultivation.The insert shows the molecular 

structure of 2,4-diacetylphloroglucinol. Based partly 

on Parry (1990) and Weller et al.(2002). 

infects the roots, causing blackening and decay. 

As a result, the cereal plants appear stunted and 

produce small, non-fertile heads which appear 

bleached and are therefore called ‘white heads’. 

The fungus overwinters on cereal stubble and 

infects the new crop mainly in spring. The infection 

mechanism is not entirely clear, and the 

fungus may enter host roots directly from dark 

melanized hyphae (runner hyphae) or melanized 

hyphopodia which may be aggregated to form 

infection cushions or mycelial mats (Butler & 

Jones, 1949). A hyphopodium is defined as an 

appressorium produced from a vegetative hypha 

rather than a germinating spore (Fig. 12.49). The 

turgor pressure in hyphopodia is around 1.5 MPa 

(¼ 15 bar), i.e. considerably less than in appressoria 

of M. grisea (Money et al., 1998). 

Like M. grisea, G. graminis is a complex of 

strains with different but overlapping host 

ranges, and varieties tritici, avenae, graminis and 

maydis are distinguished. The conidial state of 

Gaeumannomyces is a Phialophora, but since the 

assignments of anamorphs is difficult, it may be 

best to speak of the Gaeumannomyces Phialophora 

complex (Bryan et al., 1995). Gaeumannomyces 

is closely related to Magnaporthe (Bryan et al., 

1995). 

Take-all is considered to be the most important 

cereal disease in temperate climates. If 

wheat is grown on a field for about four successive 

years, the disease will build up to very 

high levels, causing crop losses in excess of 50% 

(Polley & Clarkson, 1980), but if cultivation is 

continued the disease will decline to an acceptable 

base level (Fig. 12.50). If a crop rotation 

is carried out, the antagonistic properties of 

the soil are lost. The reasons for this remarkable 

phenomenon are now beginning to be understood, 

and it is clear that the establishment of an 

antagonistic soil microflora plays an important 

role. In particular, fluorescent Pseudomonas 

spp., i.e. pseudomonads which produce watersoluble 

substances which fluoresce green 

or yellow, have been implicated as agents of 

take-all decline (Weller et al., 2002). The metabolite 

2,4-diacetylphloroglucinol (Fig. 12.50) 

produced by them seems to be responsible for 

suppression of G. graminis in the rhizosphere 

(Raajmakers & Weller, 1998). Wheat roots injured 

by Gaeumannomyces are colonized extensively 

by Pseudomonas spp., thereby explaining why a 

severe take-all attack must occur in order to 

render the soil suppressive. 

12.10 Glomerellaceae 

Like the Magnaporthaceae, the family 

Glomerellaceae is a group of plant-pathogenic 

fungi which cannot be assigned to any order at 

present, although it is certain that it belongs to 

the core group of Pyrenomycetes like all other 

groups described in this chapter (Wanderlei-Silva 

et al., 2003). The family comprises only one

GLOMERELLACEAE 

387 

Fig12.51 Colletotrichum graminicola. (a) Portion of Sorghum 

grain bearing acervuli. (b) An acervulus. (c) Phialides and 

phialoconidia. 

teleomorph genus, Glomerella, which consists of 

five species, and numerous species belonging 

to the form-genus Colletotrichum. Early workers 

defined Colletotrichum spp. mainly by their association 

with host plants, so that approximately 

750 ‘species’ were described before von Arx (1957) 

tidied them up by synonymizing them into 

11 taxa. For C. gloeosporioides alone, von Arx 

(1957) recognized 600 synonyms. A more recent 

treatment is that by Sutton (1992) in which 

39 species are described. Many of these are 

probably species complexes, and for example 

six formae speciales have been described for 

C. gloeosporioides. 

Glomerella forms dark-walled perithecia which 

occur singly. They are long-necked and release 

ascospores passively. The Colletotrichum state is an 

acervulus, i.e. a saucer-shaped conidioma which 

develops within the host tissue, rupturing 

the cuticle at maturity (Fig. 12.51a). The 

conidiogenous cells form a closely packed palisade 

of phialides (Fig. 12.51c). The curved 

elongated phialoconidia are produced in a 

slimy droplet which is held in place by stiff 

dark setae surrounding the acervulus (Fig. 

12.51b). This mucilage contains the autoinhibitor 

mycosporine-alanine which prevents the 

germination of conidia until it has been diluted 

out (Leite & Nicholson, 1992). Other germination 

autoinhibitors are localized within the conidial 

cytoplasm of diverse Colletotrichum spp. (García- 

Pajón & Collado, 2003). The presence of such 

substances explains why the spores of many 

fungi germinate better after they have been 

washed. 

Mating systems are complex and variable in 

Glomerella. For example, in G. cingulata (anamorph 

C. gloeosporioides), both homothallic and heterothallic 

strains occur, and there may be more 

than two mating type idiomorphs (Cisar & 

TeBeest, 1999). The occurrence of multiple alleles 

at one mating type locus is common in the 

Basidiomycota but has apparently not been 

found in any ascomycete other than Glomerella. 

Many strains belonging to a given species


complex appear to be reproductively isolated; for 

instance, the sexual state of C. lindemuthianum 

(teleomorph G. cingulata f. sp. phaseoli) has not 

been found in nature but can be readily induced 

in agar culture by the pairing of compatible 

isolates (Roca et al., 2003). 

Species of Colletotrichum cause serious diseases 

on a wide range of plants. These are often referred 

to as anthracnose because of the appearance 

of sunken necrotic lesions, as exemplified by 

C. lindemuthianum which causes anthracnose of 

beans, peas and other legumes (Plate 5i). These 

necrotic lesions contain the acervuli. Other 

important pathogenic species are C. gloeosporioides 

(anthracnose of a range of tropical fruits and 

many other plants), C. coffeanum (coffee berry 

disease), C. gossypii (boll rot and anthracnose of 

cotton), C. musae (post-harvest fruit anthracnose 

on banana), C. graminicola (anthracnose of maize 

and sorghum), and C. coccodes (anthracnose of 

tomato, black dot disease of potato). Many of 

these produce phytotoxic substances which are 

involved in causing disease symptoms (García- 

Pajón & Collado, 2003). Whilst diseases in the 

field are important, post-harvest rots probably 

cause even greater economic damage, especially 

in the tropics. This comes about because 

Colletotrichum spp. can cause latent infections 

which give rise to disease symptoms only during 

fruit ripening in storage. Good descriptions of 

anthracnose diseases may be found in two 

volumes dedicated to Colletotrichum, which is 

one of the most important genera of fungal 

plant pathogens worldwide (Bailey & Jeger, 1992; 

Prusky et al., 2000). Several Colletotrichum spp. have 

been developed with limited success as biocontrol 

agents against weeds (Watson et al., 2000). 

12.10.1 Infection strategies in Colletotrichum 

Most species infect their host from germinating 

conidia which emit germ tubes terminating in a 

melanized appressorium. The details of appressorium 

formation and function are very similar 

to those in Magnaporthe grisea (see pp. 378 381), 

as far as they are known (Bailey et al., 1992). 

One of the fascinations of the genus 

Colletotrichum lies in the range of postappressorial 

infection strategies which various 

species have evolved. These have been well 

described by O’Connell et al. (2000) and 

Latunde-Dada (2001), and are briefly summarized 

below. 

Necrotrophic pathogens 

Colletotrichum capsici is a necrotrophic pathogen 

infecting red peppers. It shows intercellular 

growth which commences immediately after 

penetration and is accompanied by the secretion 

of cell wall-degrading enzymes (Pring et al., 

1995). 

Hemibiotrophic pathogens 

The pattern of infection by numerous species 

(exemplified by C. lindemuthianum) is very similar 

to that in Magnaporthe grisea (p. 381). The penetration 

peg arising from an appressorium forms 

a vesicle which emits swollen primary hyphae 

inside the first-colonized epidermal cell and in 

adjacent cells (see Figs. 12.45f,g). The primary 

hyphae do not breach the plant plasma membrane 

but invaginate it, and there is evidence of 

a distinct matrix between the fungal hypha and 

the host membrane, in analogy to the haustorium 

formed by biotrophic fungal pathogens 

(O’Connell et al., 1985; Mendgen & Hahn, 2002). 

After 1 3 days, the biotrophic phase breaks 

down and thinner secondary hyphae are 

formed which spread the infection, forming 

a necrotrophic lesion. Secondary hyphae differ 

fundamentally in surface properties from primary 

hyphae and are not surrounded by an 

extracellular matrix (Perfect et al., 2001). A 

modification of this pattern is observed, e.g. in 

C. destructivum on cowpea (Vigna unguiculata), 

in which the biotrophic stage is confined to 

one epidermal cell containing a multi-lobed 

vesicle, from which secondary hyphae initiate 

the necrotrophic phase (Latunde-Dada et al., 

1996). 

Post-harvest pathogens 

This group of Colletotrichum spp. is responsible for 

most of the diseases of ripe fruits, especially in 

tropical areas. An example is C. musae on banana 

fruits. Spores alighting on unripe fruits prior 

to harvest may germinate and form appressoria 

and even penetration pegs, but there the

GLOMERELLACEAE 

389 

infection process stalls. Infection is continued on 

the ripened fruits after a period of storage. 

This infection strategy enables the pathogen to 

avoid the high levels of phytoalexins in unripe 

fruits (Latunde-Dada, 2001). Resumption of development 

is triggered by the strong increase in 

ethylene levels associated with fruit ripening 

(Flaishman & Kolattukudy, 1994). 

Endophytic colonization 

Several anthracnose pathogens including 

C. musae, C. coccodes and strains of C. gloeosporioides 

develop a prolonged latent phase inside their 

host plant (Rodriguez & Redman, 1997). 

Colonization during the endophytic phase may 

begin by infection through stomata rather than 

direct penetration of the epidermis, and intercellular 

colonization of host tissue. During 

senescence of the host plant, the host’s 

immune system degenerates and active colonization 

may ensue, resulting in the development of 

sporulating anthracnose-type lesions. Freeman 

and Rodriguez (1993) and Redman et al. (1999a) 

have shown that the deletion of a single gene 

can convert an aggressive pathogen (C. magna) 

to a permanently symptomless endophyte. 

This finding emphasizes the possibility that 

‘endophytic mutualism is only a gene away 

from pathogenicity’ (Latunde-Dada, 2001), and 

also indicates one mechanism by which endophytes 

may evolve in nature. A further fundamental 

point of interest is that colonization by 

such symptomless endophytes renders the host 

plant resistant against infection by pathogenic 

strains of the same species, and also other fungal 

pathogens (Redman et al., 1999b).

13 

Hymenoascomycetes: Erysiphales 


The Erysiphales are a clearly defined, monophyletic 

order of about 500 species, all of which are 

obligately biotrophic pathogens of plants. Braun 

(1987, 1995) has provided thorough monographic 

treatments of this group, including descriptions 

of most known species. There is only one family, 

the Erysiphaceae. The species grouped here cause 

symptoms readily recognized as ‘powdery mildews’ 

because the conidia produced in abundance 

on the shoots of infected host plants give 

them a whitish powdery appearance. The term 

‘powdery mildews’ is often also applied to the 

organisms causing them. Only angiosperms are 

attacked, almost always belonging to the dicotyledons. 

One notable exception is the powdery 

mildew of cereals and grasses caused by Blumeria 

graminis (formerly Erysiphe graminis). Other 

economically relevant species are Podosphaera 

leucotricha causing apple mildew, Podosphaera 

(formerly Sphaerotheca) mors-uvae causing 

American gooseberry mildew, and Uncinula necator 

(now Erysiphe necator) causing the powdery 

mildew of grapes. Many other species produce 

less destructive infections and are ubiquitous in 

nature, e.g. Microsphaera alphitoides (now Erysiphe 

alphitoides) on the leaves of oak (Quercus spp.) and 

Phyllactinia guttata on hazel and many other 

broad-leaved trees. Being obligate biotrophs, 

powdery mildews cannot be kept in axenic 

culture, although Arabi and Jawhar (2002) have 

recently grown B. graminis on agar augmented 

with shredded barley leaves. The possibility of 

infecting Arabidopsis thaliana with several different 

powdery mildew species holds promise for 

future investigations (Vogel & Somerville, 2002). 

In the Erysiphales, the mycelium generally 

consists of uninucleate haploid segments. It is 

almost always confined to the leaf surface, and 

infections are limited to the epidermal cells 

which are penetrated from the outside following 

the formation of appressoria. Inside the host cell, 

haustoria are formed which provide a large area 

of contact with the host. Only relatively few 

powdery mildews (e.g. Phyllactinia spp.) are able 

to penetrate more deeply into the host tissue. 

Either way, soon after infection conidia are 

produced at the infected leaf surface from a 

foot cell, either in basipetal chains or singly as in 

Erysiphe if a conidium is released before the next 

one is formed. Conidial states of the Erysiphales 

are referable to the anamorphic genus Oidium, 

barring a few specialized genera such as the 

Ovulariopsis state of Phyllactinia. A division of 

Oidium into subgenera has been proposed (Cook 

et al., 1997; Braun et al., 2002; see Fig. 13.1). The 

conidia of Erysiphales are generally described as 

meristem arthroconidia because the conidiogenous 

cell is not homologous to a rudimentary 

phialide (Hughes, 1953). Numerous crops of 

conidia can be produced in a growing season, 

and they are the main carriers of infection. 

The conidia of Erysiphales are unusual 

because unlike most fungal spores they are 

fully hydrated. Germination does not require 

the uptake of exogenous water and can proceed 

even in atmospheres with low relative humidity 

(Somers & Horsfall, 1966). In fact, germination

INTRODUCTION 

391 

Fig13.1 Summary of the key features of the most important genera of Erysiphales.Based on the results of Saenz and Taylor (1999a) 

and Braun et al.(2002). Note that Erysiphe is a polyphyletic genus at present.

392 HYMENOASCOMYCETES: ERYSIPHALES 

in some species is inhibited by free water. Ultrastructurally, 

conidia are highly vacuolated (see 

Fig. 13.11). The major carbon and energy reserve 

seems to be glycogen (McKeen et al., 1967; Roberts 

et al., 1996), although lipid droplets have also 

been reported, and lipids may contribute about 

10% of the dry weight of conidia (Lösel, 1988). 

The conidia of Erysiphales are uninucleate. 

Ascocarps are usually formed late in the vegetation 

period. These have traditionally been 

termed cleistothecia, although they differ fundamentally 

from those of the Plectomycetes because 

the asci of Erysiphales are club-shaped, not globose, 

and are formed at one level at the bottom of 

the ascocarp rather than being scattered throughout. 

Further, at maturity the ascocarp breaks 

open by a pre-determined line of weakness, 

exposing the asci which forcibly discharge their 

spores by a squirt mechanism. In contrast, the 

ascospores of Plectomycetes are released passively 

when the ascus wall disintegrates. Braun et al. 

(2002) have proposed the term chasmothecium 

(Gr. chasma ¼ an opening, open mouth) for the 

ascocarp of the Erysiphales. Chasmothecia are 

brown globose bodies which have no ostiole. 

Depending on species, they may contain one or 

several asci, and their line of weakness may run 

around the equator of the chasmothecium, or 

through its apex. Chasmothecia are often ornamented 

by highly characteristic appendages 

(Fig. 13.1) which are usually sufficient to permit 

unambiguous species identification, together 

with the number of asci in the ascocarp (one or 

several), the number of ascospores per ascus, and 

the identity of the host plant. However, the 

phylogenetic value of chasmothecial appendages 

appears limited (see Fig. 13.1). In Northern 

European climates, the asci are usually fully 

formed in late autumn, but chasmothecia do 

not open until the following spring when the 

host plants begin to grow. They are therefore 

thought of primarily as overwintering structures, 

even if their viability may be low. In countries 

with dry hot summers, chasmothecia may serve as 

oversummering structures, being formed in late 

spring and releasing ascospores in the autumn. 

The developmental events taking place during 

chasmothecium formation are immensely complex 

and have been described by Luttrell (1951) 

and Gordon (1966). They are probably similar in 

most species. Initially, two superficial uninucleate 

hyphae meet and one encircles the other. 

The central cell receives a nucleus and enlarges 

somewhat. The central cell has been termed the 

pseudoascogonial cell because it does not seem 

to play any direct role in ascus formation. The 

pseudoantheridial cells which encircle the pseudoascogonium 

divide to form the peripheral cells 

of the ascocarp. Some outer peripheral cells 

(‘mother cells’) develop short septate receptive 

hyphae which make contact with vegetative 

hyphae on the host surface. Following plasmogamy, 

one nucleus is taken up by the receptive 

hypha and divides in each segment of the receptive 

hypha until one nucleus derived from the 

vegetative hypha reaches the mother cell. The 

mother cell then divides repeatedly. 

At this stage, the immature ascocarp consists 

of a pseudoparenchymatous centrum composed 

largely of binucleate cells derived from the 

mother cells intermixed with some uninucleate 

cells, and surrounded by a peridium, some 4 6 

cell layers thick. The peridium becomes darkly 

pigmented. Uninucleate and binucleate cells 

above the middle part of the centrum lyse. Karyogamy 

occurs only within certain of the binucleate 

cells which are more or less isolated from 

the surrounding cells by lysis. These cells then 

enlarge to form asci. The asci appear to grow at 

the expense of the uninucleate and binucleate 

cells of the centrum, so that eventually the asci 

(or a single ascus, depending on the genus) 

occupy almost the entire centrum. Meiosis of the 

fusion nucleus in developing asci is usually 

delayed until the centrum cells have all been 

absorbed, although it tends to be completed 

before the winter dormancy. 

13.2 Phylogenetic aspects 

The Erysiphales are clearly delimited and defined 

as a group, but the question where to position 

this order within the Ascomycota has aroused 

considerable controversy over the past 150 years 

or so and is still undecided. Braun et al. (2002) 

have given an overview of the taxonomic history

BLUMERIA GRAMINIS 

393 

of the Erysiphales. Affinities with Pyrenomycetes 

or Plectomycetes have been proposed in the past 

but are not now thought to be true. Instead, the 

phylogenetic position of the Erysiphales is fairly 

isolated, possibly associated weakly with the 

Helotiales (Saenz & Taylor, 1999b). 

For many years, the taxonomy of genera 

and species was based on the system proposed 

by Léveillé (1851) who emphasized the features 

of the chasmothecium, especially the number of 

asci (one or several) and the type of appendage 

which may be simple, uncinate (¼ recurved or 

hooked), dichotomously branched, or bulbous 

(see Fig. 13.1). Recent phylogenetic studies based 

on a variety of DNA sequences have revealed that 

in the Erysiphales, unlike most other groups of 

organisms, the features of asexual reproduction 

are more clearly diagnostic than those associated 

with sexual reproduction. There is a good correlation 

between the anamorphic state and the 

groupings obtained by DNA sequence analysis 

(Saenz & Taylor, 1999a), and the gross anamorphic 

features also correlate with the surface 

ornamentations of the conidia as seen by scanning 

electron microscopy (Fig. 13.3; Cook et al., 

1997). Thus, the genera of Erysiphales are currently 

defined mainly by their anamorphs. In 

contrast, the striking chasmothecial appendages 

do not correspond well to the individual groups 

because notably the dichotomous and simple 

mycelioid appendages are found in more than 

one taxon (Saenz & Taylor, 1999a). One casualty 

of these findings is the genus Sphaerotheca with 

simple appendages and one ascus per chasmothecium, 

which has been incorporated into Podosphaera, 

formerly comprising only species with 

chasmothecia containing one ascus but bearing 

appendages with dichotomously branched tips 

(Braun et al., 2002). 

We have encountered a great plasticity of 

appendages on ascocarps before, especially in the 

Plectomycetes where they may be involved in 

insect dispersal (see p. 289). In contrast, in the 

Erysiphales the chasmothecial appendages seem 

to be related to the type of host infected. 

According to the analyses of Mori et al. (2000), 

the most basal species among the Erysiphales is 

Parauncinula septata which has uncinate (hooked) 

appendages. This species occurs on oak (Fagaceae), 

and Mori et al. (2000) have speculated that the 

Erysiphales originated on members of the Fagaceae 

because that host family hosts by far the 

greatest diversity of powdery mildews (Amano, 

1986; Braun, 1987, 1995). Together with another 

ancestral species possessing chasmothecia with 

uncinate appendages, Caespitotheca forestalis, 

P. septata may have diverged from other powdery 

mildews some 80 90 million years ago 

(Takamatsu et al., 2005). 

Many of the powdery mildews associated 

with the leaves of deciduous trees have hooked 

or branched appendages, whereas those on evergreen 

or herbaceous plants often have simple 

(mycelioid) appendages. It is known that complex 

appendages facilitate the attachment of chasmothecia 

to twigs or the bark of host trees for 

overwintering (see p. 407; Gadoury & Pearson, 

1988; Cortesi et al., 1995), and it must be advantageous 

for the primary inoculum in spring to be 

close to the budding leaves, rather than falling 

to the ground. Mori et al. (2000) proposed that no 

such selection pressure may hold for species parasitizing 

herbaceous plants, which might have 

permitted a reduction in the complexity of appendages 

to simple mycelioid ones. Such changes 

from woody to herbaceous hosts accompanied by 

the reduction in the complexity of appendages 

may have occurred several times independently 

within the Erysiphales (Takamatsu et al., 2000). 

13.3 Blumeria graminis 

Although Blumeria graminis is somewhat atypical 

of a powdery mildew in being a pathogen of 

grasses and cereals, we shall describe it in detail 

because more is known about it than any other 

member of the Erysiphales. Blumeria is separated 

from Erysiphe on several grounds. The haustorium 

of B. graminis is digitate, i.e. it has striking 

finger-like projections (Fig. 13.2c), whereas the 

haustoria are knob-like in most members of 

the Erysiphales. Upon closer inspection, they 

also have lobes, but these are tightly folded 

round the main haustorial body, giving it a 

globose appearance (Bushnell & Gay, 1978). 

A second distinguishing feature of B. graminis


Fig13.2 Blumeria graminis. (a) Two-day-old germinating conidium on wheat leaf, showing penetration point surrounded by a‘halo’ 

(stippled). A haustorium has developed beneath the penetration point. (b) Penetration from an established mycelium. (c) Section of 

an epidermal cell showing two penetration points and two haustoria. Note the thickening of the epidermal cell beneath the 

penetration point. (d) Mycelium and conidia, showing the swollen flask-shaped foot cell (‘mother cell’). 

is that the conidial foot cell is swollen (Fig. 13.2d). 

Thirdly, scanning electron microscopy studies by 

Cook et al. (1997) have shown that the surface of 

the conidium of B. graminis is distinct from that of 

other Erysiphales because of the spiny wall and 

the raised septum surrounded by a depressed ring 

(Figs. 13.3a,b). These differences are matched by 

DNA sequence data (Saenz & Taylor, 1999a).


395 

Fig13.3 An example of the use of scanning electron microscopy in fungal taxonomy, separating Blumeria graminis (a,b) from other 

members of the Erysiphales (c,d). (a) Whole conidium of B. graminis showing the spiny surface of the wall. (b) The‘annular’ septum 

of the conidium.The actual septum is raised and warty, but it is surrounded by a depressed annulus. (c) Conidium of Golovinomyces 

(Erysiphe) cynoglossi showing a slightly roughened wall. (d) Conidium of Neoerysiphe (Erysiphe) galeopsidis with its striate conidial wall. 

Micrographs kindly provided by R.T. A.Cook. Reprinted from Cook et al. (1997), British Crown copyright1997. 

The genus Blumeria contains only one species, 

B. graminis, which is separable into several 

formae speciales distinguishable by their different 

grass (Agropyron, Bromus, Poa) or cereal hosts 

(barley, oat, rye, wheat). Thus, B. graminis f. sp. 

tritici infects wheat (Triticum) but not barley, 

whilst B. graminis f. sp. hordei infects barley 

(Hordeum) but not wheat. Blumeria graminis is heterothallic 

and hybrids between certain formae 

speciales may arise, especially if the hosts themselves 

can hybridize. For example, it has been 

shown that hybridization between B. graminis ff. 

spp. agropyri, tritici and secalis can occur, resulting 

in viable ascospores. The three host genera 

Agropyron (couch grass), Triticum (wheat) and 

Secale (rye) can also hybridize (Hiura, 1978). 

Recently, it has become obvious that the definition 

of formae speciales is less clear-cut than previously 

thought. Extensive overlaps in host spectra 

occur especially on wild hosts in the Middle East 

where Hordeum spontaneum, the presumed ancestor 

species of cultivated barley, is endemic and 

where B. graminis probably originated (Clarke & 

Akhkha, 2002; Wyand & Brown, 2003). Further, 

within a given forma specialis, numerous races 

can be distinguished by specific features such 

as resistance to fungicides or ability to infect 

a given host cultivar. 

13.3.1 The infection process 

A conidium of B. graminis alighting on the surface 

of a grass or cereal leaf will initially come to rest 

by the tips of its spines. Within seconds of contact 

with hydrophobic (but not with hydrophilic) 

surfaces, an extracellular matrix is released by 

those spines touching the surface. The matrix 

contains proteins, including enzymes such as 

cutinases and non-specific esterases, and it may 

serve in the initial attachment of the conidium to 

the surface (Carver et al., 1999; Nielsen et al., 2000).


About 15 min later, a further batch of matrix 

material is released from the conidium, but 

unlike the initial secretion this second wave 

requires de novo protein biosynthesis. Within 

2 h, a primary germ tube emerges. In all powdery 

mildews except B. graminis, this develops an 

appressorium under suitable conditions, but in 

B. graminis the primary germ tube grows only to 

a limited distance (up to 10 mm). An appressorium 

is formed by a separate secondary germ tube 

which is much longer than the primary germ 

tube (up to 40 mm) and becomes septate. If the 

primary germ tube fails to make contact with 

a suitable surface, further short germ tubes may 

be emitted. Upon contact with the host surface, 

the primary germ tube secretes an adhesive pad 

which provides more secure anchorage to the 

surface. By suspending conidia on a spider’s 

thread over different kinds of surface, Carver 

and Ingerson (1987) observed that a long appressorial 

germ tube is emitted only if the primary 

germ tube has made contact with an inductive 

surface such as a host leaf. The primary germ tube 

therefore functions as a probe. Signals perceived 

by the primary germ tube may be the hydrophobicity 

of the surface, or minute quantities of 

cutin or cellulose degradation products released 

by appropriate hydrolytic enzymes which are 

secreted by the primary germ tube (Green et al., 

2002). The signals are probably transduced by 

cascades containing cAMP and cAMP-dependent 

protein kinase A (cPKA), similar to those described 

in more detail for Magnaporthe grisea (Fig. 12.48). 

The primary germ tube may penetrate the surface 

of the epidermis to a limited extent but does not 

achieve successful infection of the host cell. It 

may, however, take up water and dissolved substances 

from the plant surface (Kunoh & Ishizaki, 

1981; Carver & Bushnell, 1983). 

Under optimal conditions, the appressoriumforming 

germ tube emerges about 3 h after the 

primary germ tube. It elongates and its tip 

swells to form an appressorium which is lobed 

(Fig. 13.4b) and non-melanized, in contrast to 

the hemispherical melanized appressorium of 

M. grisea described on p. 381. Appressoria 

of other species of the Erysiphales may have 

different shapes, and these are of taxonomic 

significance (see Braun et al., 2002). The sequence 

Fig13.4 Penetration events in Blumeria graminis. (a) Conidium 

incubated on a cellulose membrane for12 h. After contact of 

the primary germ tube (pgt) with the surface, the appressorial 

germtube(agt)wasemittedandhasformedanincipient 

appressorium. (b) A lobed mature appressorium on the 

surface of a wheat leaf. (a) reprinted from Carver et al. (1999), 

with permission from Elsevier; original print kindly provided 

byT.L.W.Carver.(b)reprintedfromHoward(1997),withkind 

permission of Springer Science and Business Media; original 

print kindly provided by R. J. Howard. 

of infection-related morphogenetic events up to 

this stage is shown in Fig. 13.4. 

Penetration is achieved by means of a thin 

penetration peg which originates from the underside 

of the appressorium. In all probability, both 

the activity of secreted wall-degrading enzymes 

(cutinases and cellulases) and appressorial turgor 

pressure contribute to successful penetration 

events, with the former predominating (Edwards 

& Allen, 1970). Penetration can be achieved within 

about 12 h of the conidium landing on the


397 

leaf surface. The tip of the penetration peg then 

enlarges to form the haustorium initial which 

differentiates in the course of 2 3 days, invaginating 

but not breaching the host plasmalemma. 

As a nutrient supply is established, surface 

hyphae grow from the appressorium or the 

appressorial germ tube and further epidermis 

cells are penetrated. It is also possible for the same 

host cell to be penetrated repeatedly so that it 

contains several haustoria. Haustorium formation 

represents the end-point of in planta growth; 

further penetration occurs from epidermal 

hyphae. 

13.3.2 Self-defence of the host plant 

against infection 

Good summaries of this vast topic may be found 

in Carver et al. (1995), Giese et al. (1997) and Zeyen 

et al. (2002). Although the ungerminated conidium 

already emits signals perceived by the epidermis 

cell, it is the contact of the primary germ 

tube with the host cell surface which elicits initial 

defence reactions. These are visible as a dramatic 

re-organization of the cytoplasm of the attacked 

epidermal cell, with dense cytoplasm aggregating 

beneath the point of contact of the primary germ 

tube with the leaf surface. This is followed by 

a modification of the epidermal cell wall by 

secreted substances. The altered cell wall region is 

visible as a halo (Fig. 13.2a). Phenolic substances 

and hydrolytic enzymes become incorporated 

into the cell wall within the halo region. This is 

a non-specific defence reaction because it is elicited 

by both virulent and avirulent strains of the 

pathogen. A further such halo is produced by the 

epidermal cell when the appressorial penetration 

peg attempts to penetrate. A papilla is then 

formed around the penetration peg between the 

host cell wall and the host plasma membrane, and 

this may succeed in plugging the peg and preventing 

infection. Papillae are easily seen with an 

epifluorescence microscope because they show 

strong autofluorescence, a general indicator of an 

attempt by the host plant to resist infection. 

Autofluorescence is due mainly to the accumulation 

of phenolic substances which have antimicrobial 

activity (von Röpenack et al., 1998). 

Additionally, hydrolytic enzymes, callose and 

silica may be deposited in the papilla. Papilla 

formation is an important mechanism of general 

resistance, although it is unknown why some 

strains of B. graminis can penetrate the papillae 

and others fail. Even if a susceptible host is 

infected, only about 70% of the penetration 

events succeed beyond the papilla stage. In certain 

barley cultivars, particularly thick papillae 

are formed because of mutations in which restrictions 

of the resistance response are lifted; only 

0.5% of infection pegs get through the epidermis 

of these mlo mutants, and barley cultivars homozygous 

for the mlo allele show broad-spectrum 

resistance to all strains of B. graminis f. sp. hordei 

(Jørgensen, 1994; Collins et al., 2002). It should be 

noted here that papillae are not particularly 

prominent in infections of dicotyledons by other 

powdery mildews. 

In cereals attacked by B. graminis, most strainspecific 

resistance mechanisms are initiated later, 

when the tip of the penetration peg enlarges and 

begins to differentiate into the first haustorium. 

At this point the infected epidermal cell of 

a resistant cultivar displays an oxidative burst, 

i.e. it releases H 2 O 2 and various enzymes into its 

own cytoplasm and dies (Zhou et al., 1998). This 

phenomenon is known as the hypersensitive 

response. Since B. graminis is an obligate biotroph, 

penetration ending in a haustorium inside a dead 

cell is a wasted effort. The haustorium itself may 

also be directly affected by the oxidative burst, 

with first signs of degeneration appearing in the 

mitochondria (Hippe-Sanwald et al., 1992). If sufficient 

nutrient reserves are present in the appressorial 

germ tube, further appressoria may be 

formed, each resulting in failure to establish a 

functional haustorium in resistant cultivars. 

Successful infection results if the host cell 

tolerates the establishment of the initial haustorium. 

Curiously, therefore, it is sensitivity rather 

than tolerance which leads to resistance. Numerous 

genes are involved in the various lines of 

defence which barley plants possess against 

B. graminis f. sp. hordei (Collinge et al., 2002). 

13.3.3 Genetics of plant resistance against 

B. graminis 

The fact that only certain strains of B. graminis 

f. sp. hordei can elicit the hypersensitive response


in a given barley cultivar indicates that specific 

recognition mechanisms between host and pathogen 

must be involved. The molecular basis of 

recognition is still obscure, but the genetics are 

well understood. They are based on the genefor-gene 

concept first formulated by Flor (1955) 

for an interaction between the rust fungus 

Melampsora lini and flax, but soon after also 

demonstrated for B. graminis and cereal hosts (see 

Moseman, 1966). Given that in strain-specific 

interactions recognition leads to resistance via 

the hypersensitive response, every avirulence 

gene of the pathogen (e.g. encoding a surface 

protein recognized by the host) is matched by 

a specific resistance gene of the host (e.g. a 

receptor). It follows that avirulence alleles should 

be dominant to virulence alleles in diploid or 

dikaryotic pathogens (not, of course, applicable 

to the haploid B. graminis), whereas resistance 

should be dominant to susceptibility in the host. 

Successful infection occurs only if the avirulence 

gene is modified so that the host can no longer 

recognize the pathogen. Numerous resistance 

genes have been identified especially in barley 

and are being used for breeding programmes, 

although it is relatively easy for the pathogen 

to overcome such single-gene resistance (Brown 

et al., 1993; Collins et al., 2002). It should be noted 

that there are deviations from the classical genefor-gene 

concept in the interaction between 

B. graminis f. sp. hordei and barley. Further, interactions 

between a given race of B. graminis and its 

host can take various courses with intermediates 

between complete resistance and full development 

of symptoms, due to the influence of minor 

genes depending on the host’s genetic make-up, 

and also due to environmental parameters. 

A good summary of this complicated topic has 

been written by Brown (2002). In general terms, 

research on the molecular biology of B. graminis 

would benefit greatly from the availability of 

a reliable DNA transformation method for this 

important pathogen. 

13.3.4 The haustorium of B. graminis 

In compatible interactions, a functional haustorium 

is formed by the enlarging tip of the 

penetration peg. The papilla remains as a collar 

around the peg at the point where it penetrated 

the epidermis wall. The host plasmalemma is 

invaginated around the haustorium, but it is not 

in direct contact with the plasma membrane of 

the haustorium. Instead, the two membranes are 

separated by the haustorial wall, and surrounding 

it by the extrahaustorial matrix which is of 

host origin. It is a compartment with a gelatinous 

texture, sealed by the host and pathogen 

plasma membranes, and at the epidermal wall by 

a collar (Manners, 1989). The host plasmalemma 

is strongly modified and seems to lack H þ 

ATPases, so that the host cell may not be able 

to control leakage of solutes into the extrahaustorial 

matrix (Gay et al., 1987). The escape of 

solutes from the extrahaustorial matrix to the 

cell surface is prevented by the collar seal. Haustoria 

of the Erysiphales contain a full complement 

of organelles including a single nucleus. 

The haustorium is separated from the surface 

hypha by a septum which is perforated, thus 

permitting nutrient transfer. Ultrastructural 

details are summarized in Fig. 13.5 and 

have been described by Bracker (1968b) and 

Hippe-Sanwald et al. (1992). 

Whereas in other biotrophic plant pathogens 

nutrients can, to a certain extent, be absorbed by 

intercellular hyphae in addition to haustoria, in 

the Erysiphales the haustorium seems to be the 

sole means of nutrient uptake. Not surprisingly, 

the haustorial membrane differs from that of 

surface hyphae in terms of protein composition 

and physiology (Manners, 1989; Mendgen & 

Deising, 1993; Green et al., 2002). Nutrient 

uptake has traditionally been studied with the 

haustoria of E. pisi which can be isolated intact 

from infected pea plants (Gil & Gay, 1977). Sutton 

et al. (1999) have shown that glucose is the sugar 

which is taken up by haustoria of B. graminis f. sp. 

tritici, and that the plant hydrolyses the transport 

sugar sucrose before this reaches the epidermal 

cells and the haustoria contained within them. 

Glucose probably diffuses passively into the 

extrahaustorial matrix and is then taken up 

across the haustorial membrane by a proton 

uniport mechanism (Sutton et al., 1999). This is 

in line with the situation in most other 

fungi examined to date, which generally take 

up glucose but not sucrose (Jennings, 1995).


399 

Fig13.5 Interpretation of the 

fine structure of the haustorium 

of B. graminis f. sp. hordei 

(redrawn from Bracker,1968b). 

(a) Section of host leaf at point 

of penetration.The body of the 

haustorium (bo) containing 

asinglenucleus(nu)lies 

immediately beneath the point 

of penetration.The body of the 

haustorium is enclosed in a sheath 

with extensive matrix (MAT).The 

sheath membrane (SM) is close 

to the host tonoplast (T). 

The sheath membrane bears 

invaginations (SI). A single lobe 

(lo) of another haustorium 

enclosed in an extension of the 

sheath is shown to the left of the 

diagram, and four lobes enclosed 

in a common sheath to the right. 

(b) Enlargement of the neck of a 

haustorium. Note the thickened 

collar (C) deposited on the host 

cell wall (W).The sheath 

membrane (SM) is continuous 

with the host plasmalemma (E). 

Other abbreviations: XW 

(cross-wall),CH (channel), 

H (host cytoplasm). 

The difference is that other fungi are capable of 

hydrolysing sucrose externally by the activity of 

their own secreted invertases. 

13.3.5 Life cycle and epidemiology of 

B. graminis 

About 7 10 days after infection by B. graminis, the 

haploid surface mycelium can produce conidia 

under field conditions. Conidia develop from 

a flask-shaped foot cell within which mitotic 

nuclear division occurs. The foot cell elongates 

away from the host leaf and a cross-wall cuts off 

the hyphal tip. Further cross-walls develop so that 

a chain of cells is formed, increasing in length 

at its base by further divisions of the foot cell. 

Such conidia are said to be catenate (Fig. 13.2d). 

Each conidium is uninucleate. In successful infections, 

a dense stand of conidiophores is produced 

so that the lesion appears as a white powdery 

pustule (Fig. 13.6a). Aust (1981) has estimated 

that a single pustule can release about 1.5 10 4 

conidia day 1 . A high spore inoculum can be built 

up very quickly, and numerous infection cycles 

can occur during one growing season. Dispersal 

of powdery mildew conidia is mainly by wind, 

whereby short gusts of wind are ideal for spore


dispersal (Hammett & Manners, 1971, 1974). This 

ties in with the duration of conidium production 

(about 3 h for each conidium) and the fact that 

usually only the terminal, most mature spore 

becomes detached from the conidial chain. Thus, 

the observed diurnal rhythm of spore abundance 

in the air, with a peak usually in early 

afternoon, can probably be explained by factors 

affecting release, rather than formation, of 

spores (Hammett & Manners, 1971, 1974). Both 

the formation and release of spores are strongly 

inhibited by rain (Hirst, 1953). 

The conidia of B. graminis can travel considerable 

distances with the prevailing wind. For 

instance, Hermansen et al. (1978) have demonstrated 

the migration of spores from Northeastern 

England and Scotland to Denmark, a 

journey which would have taken approximately 

48 h. In an extensive survey undertaken across the 

whole of Europe, Limpert et al. (1999) found that 

B. graminis is a nomadic species, with the 

prevailing westerly winds driving waves of populations 

eastwards at a rate of about 100 km 

year 1 . Since such populations encounter hosts 

with different spectra of resistance genes, they 

face a selective pressure to adapt, and this may 

explain why the complexity of virulence alleles in 

B. graminis populations was found to increase 

from west to east by about one virulence factor 

every 1000 km. Ultra-long distance (intercontinental) 

dispersal of viable conidia, as found e.g. 

for urediniospores of rust fungi (see p. 632) or 

teliospores of smut fungi (p. 639), has not been 

reported for powdery mildews. 

Whereas conidium formation and release by 

B. graminis are favoured by dry windy conditions, 

infection proceeds best at 98 100% relative 

humidity but is inhibited by free water. The optimum 

infection temperature is about 15 20°C. 

Thus, the conditions in Northwestern Europe are 

ideal for B. graminis in terms of rapidly changing 

weather conditions (Smith et al., 1988). Crop 

losses of up to 40% have been reported, with 

barley the most seriously affected cereal. The 

timing of infection is important, early infections 

reducing the number of ears and later infections 

reducing the size of the grain. Crop damage is 

due to a decrease in photosynthesis in infected 

leaves, meaning that they are unable to 

Fig13.6 Blumeria graminis. (a) Conidial pustules on wheat. 

(b) Dark spherical chasmothecia nestling in a felt of surface 

hyphae on a wheat leaf sheath. 

export carbohydrates to the developing grains. 

Heavily infected leaves may even act as a sink 

for photosynthetic product (sucrose) from other 

leaves. 

The chasmothecia of B. graminis are dark 

brown and globose, and nestle in a dense mass 

of mycelium formed on the basal leaves and 

leaf-sheaths of cereals (Fig. 13.6b). In contrast to 

the chasmothecia of most Erysiphales, those of 

B. graminis do not bear any conspicuous thickwalled 

appendages (Fig. 13.7a). Each chasmothecium 

has a wall made up of several layers of cells, 

surrounding a number of asci. At maturity, 

it cracks open by swelling of the contents, and 

the asci discharge their spores. In Europe, 

chasmothecia are formed in late summer and 

it is unclear what their exact role in the disease 

cycle is. Ascospores of B. graminis formed in the 

current season are capable of infection, and 

dried chasmothecia can survive under herbarium 

conditions for up to 13 years (Moseman & 

Powers, 1957). However, it is generally assumed

ERYSIPHE 

401 

that B. graminis survives mainly in the vegetative 

state on overwintering host plants, especially 

winter varieties of cereals (Jenkyn & Bainbridge, 

1978). To survive a single growing season, 

B. graminis may have to switch four times between 

winter barley and summer barley main 

crops and their volunteers germinating after 

harvest (Limpert et al., 1999). The availability of 

living shoots for infection throughout the year is 

called the ‘green bridge’. In contrast, in hot and 

arid regions such as the Mediterranean, chasmothecia 

play a role in the oversummering of the 

pathogen on wild grasses such as Hordeum 

spontaneum, discharging ascospores when the 

host seeds germinate in autumn (Clarke & 

Akhkhra, 2002). Since B. graminis seems to have 

its centre of origin in the Middle East, it is 

possible that the chasmothecia are primarily 

oversummering rather than overwintering 

structures. 

13.4 Erysiphe 

The genus Erysiphe is currently subject to 

major taxonomic rearrangements. Erysiphe has 

traditionally been defined by chasmothecia 

with undifferentiated mycelioid appendages 

(Fig. 13.8a), and was later distinguished from 

Blumeria by its knob-like haustoria and a cylindrical 

(non-swollen) conidial foot cell (Fig. 13.8b). 

This anamorph gives rise to one conidium at a 

time, i.e. it is non-catenate. It is called Pseudoidium. 

Erysiphe spp. now fall into several branches of 

phylogenetic trees, and they are interspersed by 

species which have similar anamorphs but chasmothecia 

with uncinate or lobed appendages 

(Saenz & Taylor, 1999a; Mori et al., 2000). Braun 

et al. (2002) therefore proposed the absorption of 

genera such as Microsphaera and Uncinula into 

Erysiphe. The most important species of Erysiphe in 

an agricultural context (Spencer, 1978; Smith 

et al., 1988) are mentioned below. They seem to 

share the fundamental biological principles of 

infecting by wind-dispersed conidia which do not 

require or even tolerate free water, and causing 

disease symptoms as a superficial mycelium 

producing haustoria only in epidermal cells. 

13.4.1 Erysiphe sensu stricto 

Erysiphe cruciferarum (formerly part of E. polygoni 

sensu lato or E. communis) is a pathogen of 

Fig13.7 Blumeria graminis. (a) Mat of superficial hyphae with 

a sectioned chasmothecium containing several asci. (b) Ascus.


Fig13.8 Erysiphe polygoni. (a) Chasmothecium showing dark, free-ended equatorial appendages, and the hyaline superficial 

mycelium anchoring the chasmothecium to the host leaf. (b) T.S. host leaf showing simple haustorium, superficial mycelium and 

conidial chain arising from a foot cell which does not appear bulbous. 

crucifers, causing severe infections on cabbage 

and Brussels sprouts. It is morphologically 

similar to E. betae which is a specialized pathogen 

of sugar beet and related hosts (Beta spp.). Erysiphe 

polygoni is now considered a separate species of 

no commercial interest, forming powdery 

mildew on Rumex and Polygonum. Erysiphe pisi is 

a cosmopolitan pathogen of leguminous plants 

including peas and lucerne. There are several 

formae speciales. This species is of particular 

interest because much physiological work has 

been done on its haustoria which can be isolated 

from infected leaves (Gil & Gay, 1977). Another 

powdery mildew fungus on Leguminosae is 

Erysiphe trifolii infecting mainly clover and with 

formae speciales on Trifolium, Lathyrus, Melilotus 

and Lotus. Erysiphe heraclei (¼ E. umbelliferarum) 

infects umbellifers such as carrot and celery 

and is of limited importance in winter crops in 

the Mediterranean. It is exceedingly common 

on hogweed (Heracleum sphondylium). 

All the above species belong to the redescribed 

genus Erysiphe, possess a Pseudoidium 

anamorph and cluster together in phylogenetic 

analyses (Saenz & Taylor, 1999a; Mori et al., 2000). 

13.4.2 Microsphaera and Uncinula 

Both these genera group together with the main 

Erysiphe cluster around E. pisi, E. cruciferarum and 

other species described above (Saenz & Taylor, 

1999a) and will in due course be called Erysiphe 

(Braun et al., 2002) possibly with the addition of 

further names reflecting distinct phylogenetic 

sub-groups rather than characteristics of chasmothecial 

appendages. Anamorphic states belong to 

Pseudoidium. 

Microsphaera 

Chasmothecia of Microsphaera (now Erysiphe sect. 

Uncinula) contain several asci, but they carry 

appendages with tips showing a highly diagnostic 

dichotomous branching (see Fig. 13.10a). 

Microsphaera (now Erysiphe) alphitoides is the 

cause of oak mildew which is extremely 

common, especially on Quercus robur. It appears 

from June onwards, infecting mainly leaves 

which are produced on sucker shoots and 

seedlings, and causing distortions to growing 

shoots until growth finally stalls for the rest of 

the growing season (Fig. 13.9). The chasmothecial 

stage is not always present but may be more

ERYSIPHE 

403 

Fig13.9 Summer shoot of oak (Quercus)infectedbyoak 

powdery mildew, Microsphaera (now Erysiphe) alphitoides. 

Contrast the stunted appearance of the infected foliage with 

the healthy basal leaves formed in spring. 

common during hot summers or in hot climatic 

zones. 

Uncinula 

Members of the genus Uncinula (now Erysiphe sect. 

Uncinula) also produce several asci in each 

chasmothecium but are distinguished by their 

chasmothecial appendages which are uncinate, 

i.e. they have recurved tips. Strikingly similar 

appendages are found in the unrelated genus 

Sawadaea (see Fig. 13.10b). Undoubtedly the bestknown 

species is U. necator, the cause of powdery 

mildew of vines. Chasmothecia are quite rare, 

and when the fungus first appeared in Europe 

in a glasshouse in Kent in 1845 it was known 

only in its anamorphic state and given the name 

Oidium tuckeri, after Mr Tucker, the gardener 

who discovered it. An accidental introduction 

from North America, U. necator quickly spread 

throughout the major vine-growing regions of 

Europe, causing such severe damage especially in 

France that the entire wine industry was 

threatened. By 1854, the French wine production 

had fallen from 54 million to 10 million hectolitres. 

Fortunately, Mr Tucker had also discovered 

that a mixture of sulphur dust and lime 

provided good control of the disease, and this 

simple fungicide is still used today (Smith et al., 

1988). An excellent account of the arrival of vine 

powdery mildew (and many other fungal 

diseases) has been given by Large (1940). 

Because of the extremely high value of the 

vine crop, extensive epidemiological data have 

been compiled and are used for disease forecasting 

models (Jarvis et al., 2002). Conidia are, 

of course, the major inoculum, and they are 

dispersed by wind movements and also by the 

air currents generated by high-pressure spraying 

equipment (Willocquet & Clerjeau, 1998). 

Infections are mainly found on the upper 

(adaxial) surface of leaves, in contrast to the 

grape downy mildew (Plasmopara viticola; see 

p. 120) which is more common on the underside 

(abaxial surface). The grapes themselves are 

also readily infected by U. necator; if they are 

young, they will be aborted altogether whereas 

older grapes suffer skin damage, and moulds 

such as Botrytis cinerea can easily infect through 

these cracks. Uncinula necator overwinters as 

mycelium in dormant buds (Rugner et al., 2002), 

although chasmothecia formed in autumn can 

survive the winter on twigs and give rise to 

sizeable quantities of ascospores capable of 

causing new infections in spring (Jailloux et al., 

1998, 1999). 

13.4.3 Species previously attributed to 

Erysiphe 

Species of Golovinomyces (formerly Erysiphe cichoracearum 

sensu lato) are not closely related to the 

Erysiphe as circumscribed above. They have an 

anamorph (Oidium subgenus Reticuloidium; Cook 

et al., 1997) that has catenate conidia with slightly 

roughened conidial surfaces as seen under the 

scanning electron microscope (see Fig. 13.13c). 

Braun (1987) has placed the forms affecting 

Asteraceae (including lettuce) in G. cichoracearum 

and most of the plurivorous forms in the morphologically 

very similar G. orontii. Important crops


13.5 Podosphaera and Sphaerotheca 

These two genera, although easily distinguished 

from each other with the light microscope by 

their chasmothecial appendages, have now been 

grouped together, and Podosphaera takes precedence 

over Sphaerotheca (Braun et al., 2002). Both 

produce chasmothecia containing only a single 

ascus. The important features of the conidia 

of all species grouped here are that they are 

catenate and contain conspicuous fibrosin 

bodies. These are also seen in some other 

genera, e.g. Sawadaea (see p. 405). Fibrosin 

bodies are filamentous organelles up to 8 mm 

long which appear highly light-refractile or 

sparkling when viewed with the light microscope 

(Fig. 13.11). Their biochemical composition 

and function appear to be unknown. 

Fig13.10 Chasmothecial appendages of Erysiphales. 

(a) Flattened dichotomously branched appendages of 

Podosphaera clandestina. (b) Branched appendages of Sawadaea 

(formerly Uncinula), bicornis with recurved tips. 

stated to be attacked by the plurivorous species 

are those belonging to Solanaceae (e.g. tobacco) 

and Cucurbitaceae (especially melon, cucumber, 

squash and pumpkin). However, it is unclear 

whether the same species attacks both families. 

On cucurbits it has been described as G. cucurbitacearum 

but here it seems to be of lesser significance 

than Sphaerotheca fuliginea (¼ Podosphaera 

xanthii) and might have been confused with it in 

the past (Jahn et al., 2002). Molecular data indicate 

that both Golovinomyces spp. are polyphyletic, 

and that the clades do not obviously relate to 

their host ranges. Another catenate species, 

Neoerysiphe (formerly Erysiphe) galeopsidis affecting 

mainly Lamiaceae differs from Golovinomyces in 

having conidia with a minutely striated conidial 

surface (Fig. 13.3d). 

13.5.1 Sphaerotheca (now Podosphaera) 

Common species are S. fuliginea on dandelion 

(Taraxacum officinale) and other Asteraceae, 

S. macularis causing powdery mildew of hops 

(Humulus lupulus), S. mors-uvae (American gooseberry 

mildew) and S. pannosa, the common rose 

mildew. The chasmothecial structure of Sphaerotheca 

closely resembles that of Erysiphe with its 

simple appendages, the only notable microscopic 

difference being that the chasmothecium contains 

only one ascus in Sphaerotheca (Fig. 13.12). 

The fine structure of developing and mature 

chasmothecia of S. mors-uvae has been studied by 

Martin et al. (1976). They have shown that the 

darker melanized cells forming the peridium 

are, like those of vegetative hyphae, uninucleate. 

Most of the inner cells of the chasmothecium are 

binucleate, suggesting that they may have arisen 

from a binucleate ascogonial fusion cell. Another 

interesting discovery was that fibrosin bodies, 

previously reported from conidia, are also 

present in the ascospores. 

The mycelium and conidia of S. pannosa are 

common on leaves and shoots of cultivated and 

wild roses. Chasmothecia are formed on twigs, 

embedded in a dense mycelial felt. Overwintering 

is not only by means of ascospores, but 

particularly as mycelium within dormant

PHYLLACTINIA AND LEVEILLULA 

405 

Fig13.11 Sphaerotheca (now Podosphaera) pannosa.(a)Conidial 

foot cell producing a chain of conidia. (b) Close-up of mature 

conidia. Note the large vacuoles and the elongated 

light-refractile fibrosin bodies (arrowheads). 

buds, and the chasmothecia may not play any 

significant role in perennation. In the case of 

S. mors-uvae from blackcurrants, only a small 

proportion (


Fig13.12 Sphaerotheca (now Podosphaera) 

pannosa. (a) Chasmothecium crushed to show 

a single ascus. (b) Chasmothecium with 

discharged ascospores. 

gives rise to very large and distinctly shaped 

conidia. 

13.7.1 Phyllactinia 

Phyllactinia guttata (¼ P. corylea) grows on the 

leaves of hazel (Corylus avellana) and other woody 

plants, forming chasmothecia on the lower leaf 

surface in late summer and autumn. In this 

species the superficial mycelium produces short 

lateral appressoria which emit penetration 

hyphae through the stomata into the mesophyll 

(Fig. 13.13b). Directly beneath the stoma, the 

penetration peg swells to produce a substomatal 

vesicle from which septate hyphae grow into the 

leaf mesophyll, penetrating mesophyll cells and 

forming haustoria within them. The conidia are 

club-shaped and are formed singly (Fig. 13.13a). 

However, in a damp chamber pseudo-chains of 

up to four conidia may hang together. Conidia 

of this type are classified in the anamorphic 

genus Ovulariopsis. 

Phyllactinia guttata presents a most intriguing 

spore dispersal mechanism which is easily demonstrated 

in mycology classes because the same 

hazel trees are reliably infected each year and, 

once a source has been located, leaves can be

PHYLLACTINIA AND LEVEILLULA 

407 

Fig13.13 Phyllactinia guttata. 

(a) Conidiophores showing the 

single terminal conidium. (b) T.S. 

leaf of Corylus avellana showing 

penetration of stoma in lower 

epidermis, formation of a 

substomatal vesicle (arrow) and 

extension of the mycelium into 

the mesophyll. 

collected and kept dry until required for classes 

(Weber & Webster, 2001a). Chasmothecia are 

formed only on the lower leaf surface. They bear 

two types of appendage, an equatorial group of 

radiating unbranched appendages with bulbous 

bases, and a crown of highly branched appendages 

which secrete mucilage (Fig. 13.14). The base 

of the bulbous appendage is thin-walled in the 

region facing the leaf surface, but thick-walled 

facing away from the leaf. On drying, the 

appendage bends towards the leaf surface as 

the thin part buckles inwards, and the pressure 

of the appendage tip levers the chasmothecium 

free from the superficial mycelium (for a video 

sequence, see Webster, 2006b). The bulbous 

appendages now function as ‘flights’ or vanes, 

and the chasmothecium plummets downwards 

like a shuttlecock, orientated during its fall with 

the sticky mucilage on the lower side. The blob of 

mucilage between the apical crown of branched 

appendages helps to stick the chasmothecium 

onto twigs and leaves. The asci usually contain 

only two spores (Fig. 13.14e). Overwintered ascocarps 

open by means of an equatorial line of 

dehiscence, and the base of the ascocarp hinges 

back to place the asci in a suitable position for 

ascus discharge to occur (Cullum & Webster, 

1977; Weber & Webster, 2001a). 

For historical interest, we may note that in 

1861 the Tulasne brothers, working on P. guttata 

and other powdery mildews, were among the first 

to demonstrate and illustrate in timeless beauty 

the connection between a conidial state and a 

morphologically very different-looking sexual 

state (see Tulasne & Tulasne, 1931). 

13.7.2 Leveillula 

This genus is related to Phyllactinia. Its members 

are common in warmer countries and occasionally 

in glasshouses in cooler areas. Leveillula 

taurica attacks a wide range of mainly herbaceous 

plants including tomato and pepper. It is


distinguished from Phyllactinia by its rare chasmothecia 

bearing only mycelioid appendages 

and by its spear-shaped conidia (Oidiopsis 

anamorph). 

13.8 Controlofpowderymildew 

diseases 

Several different strategies are employed to control 

powdery mildew diseases in various crops, 

chemical control and breeding for resistance 

being by far the most important in commercial 

terms. We describe them here in detail because 

the fundamental principles apply to diseases 

caused by many other groups of fungi within 

the Eumycota, as mentioned elsewhere in this 

book. 

13.8.1 Breeding for resistance 

Wheat and barley were among the first crop 

plants for which resistance breeding programmes 

were initiated almost a century ago, 

following Biffen’s (1905) seminal work on the 

genetics of resistance to wheat stripe rust, 

Puccinia striiformis. Initial attempts at resistance 

breeding against B. graminis as well as other 

biotrophic plant pathogens used major gene 

resistance based on introducing single resistance 

genes into the cultivar of choice. Numerous such 

major resistance genes originating from cereal 

cultivars as well as wild grasses related to wheat 

or barley are now available for breeding purposes 

(Hsam & Zeller, 2002). Breeding for major gene 

resistance has also been pursued in many other 

crops susceptible to powdery mildew diseases, 

such as melons and cucumbers (Podosphaera 

xanthii and Golovinomyces cichoracearum; Jahn 

et al., 2002), or clover (Erysiphe trifolii), hops 

(Sphaerotheca macularis) and gooseberries 

(Sphaerotheca mors-uvae) (see Smith et al., 1988). 

Breeding for resistance in slow-growing perennial 

crops such as apple or vines is obviously 

rather more difficult. 

Major gene resistance is usually based on 

a recognition mechanism involving the hypersensitive 

response (see pp. 397 398). The danger 

inherent in major gene resistance breeding is 

that the pathogen can overcome resistance by 

mutation of its corresponding avirulence allele 

to virulence. This is a frequent occurrence, e.g. in 

B. graminis. On the other hand, the frequency of 

virulence alleles in the field may decrease again 

in pathogen populations no longer exposed to 

the cultivar and its resistance gene. Further, by 

co-ordinating the release of resistant cultivars, 

the effect of major gene resistance in crop 

protection can be maximized. For instance, the 

‘green bridge’ of B. graminis (see p. 399) can be 

broken if the summer and winter cereal cultivars 

sown in any one year carry different resistance 

genes. Further, it is possible to combine several 

resistance genes in one host variety, a process 

known as ‘pyramiding’. This requires the pathogen 

to develop multiple virulence alleles before 

it can infect such a crop variety (Hsam & Zeller, 

2002). The danger, of course, lies in the creation 

of multiply resistant ‘super-races’ of B. graminis 

or other powdery mildews. 

An interesting type of resistance in barley is 

mediated by the mlo allele which, as mentioned 

on p. 397, mediates the formation of very thick 

papillae, restricting infection by all races of 

B. graminis f. sp. hordei. This resistance is unusual 

for a broad-spectrum resistance in giving 

almost total control, and it is exceptional for 

a single-gene resistance in that it has remained 

stable in barley cultivars since it was 

introduced about 20 years ago (Jørgensen, 1994; 

Collins et al., 2002). In 1990, 30% of the spring 

barley acreage was sown with mlo resistant 

barley cultivars (Jørgensen, 1992). More 

commonly, broad-spectrum resistance is based 

on the combined effects of several minor genes 

and it is only partial, i.e. it retards infection 

and sporulation of the pathogen but does not 

altogether prevent disease. It is sometimes 

termed horizontal resistance because it controls 

many different races of the pathogen to the 

same limited level, in contrast to vertical 

resistance mediated by major resistance genes 

in which individual races are controlled totally, 

and others not at all. Although the molecular 

basis of most resistance genes is still unknown, 

it is noteworthy that some genes involved in 

horizontal resistance become more effective in

CONTROL OF POWDERY MILDEW DISEASES 

409 

Fig13.14 Phyllactinia guttata. (a) Chasmothecium on lower side of hazel (Corylus) leaf.The radiating bulbous appendages are 

horizontal.The branched secretory appendages which crown the chasmothecium are on the morphologically upper side, i.e. the 

side to which the ascus apices point. (b) Position of chasmothecium during its fall from the host leaf.The bulbous appendages are now 

folded to form flight vanes, ensuring that the sticky mass of mucilage faces downwards. (c) Diagrammatic representation of an open 

chasmothecium.The chasmothecium is shown attachedby mucilage to a surface.The chasmothecium has openedby a circumscissile 

line of weakness, and has hinged back so that the apices of the asci now point outwards. Arrows indicate the direction of ascospore 

discharge. (d) A bulbous appendage, showing the differential thickening of the wall of the bulb.Collapse of the thinner walls result 

in movement of the appendage. (e) Two-spored ascus. (f) Branched secretory appendage. (a,b) to same scale; (d f) to same scale.


adult plants. This phenomenon is called adult 

plant resistance (Hsam & Zeller, 2002). Thus, 

it can be envisaged that the products of horizontal 

resistance genes may be involved, for 

example, in producing a thicker cuticle, cell 

wall or papilla. 

Resistance breeding will certainly remain one 

of the key methods for controlling powdery 

mildews, and it is likely that major and minor 

genes will be combined to produce cultivars 

with more durable and effective resistance to 

B. graminis and other powdery mildews. Further, 

genetic engineering may enable breeders to produce 

cultivars with overexpresssed pathogenesisrelated 

(PR) genes (Salmeron et al., 2002). The 

principles of PR genes are explained briefly on 

p. 116. 

13.8.2 Chemical control 

A good overview of fungicides against powdery 

mildews has been given by Holloman and 

Wheeler (2002). By far the oldest remedy against 

powdery mildew is powdered elemental sulphur, 

which was mentioned by Homer in about 

1000 BC (Agrios, 2005) and was rediscovered in 

the nineteenth century and combined with lime 

for enhanced efficacy (Large, 1940). Sulphur 

lime mixtures saved the French wine industry 

from ruin in the mid nineteenth century when 

U. necator appeared in Europe, just as Bordeaux 

mixture (based on copper sulphate and lime) 

played a crucial role in protecting vines against 

Plasmopara viticola later that century (see p. 120). 

In the early twentieth century, as described 

above, efforts to control B. graminis on 

cereals shifted to breeding for resistance. 

Dithiocarbamate (see Fig. 5.27) was released in 

1934 and, like sulphur, had a purely protectant 

activity. 

The first systemic fungicide against powdery 

mildews was the benzimidazole benomyl 

(Fig. 13.15a) which is converted to the active 

molecule carbendazim inside the plant. Carbendazim 

binds to tubulin proteins, interfering 

with their assembly into microtubules and 

especially with the nuclear spindle during 

mitosis (Davidse & Ishii, 1995). Resistance against 

benomyl is common among plant-pathogenic 

fungi and is usually due to a mutation in the 

b-tubulin gene at the site where carbendazim 

binds, thereby reducing its affinity (Davidse & 

Ishii, 1995). 

The next two important groups of systemic 

fungicides to be released against powdery mildews 

were the morpholines (Pommer, 1995) and 

2-aminopyrimidines introduced in the 1960s 

(Hollomon & Schmidt, 1995). Both are used more 

or less exclusively against powdery mildews. 

Fig13.15 Fungicides against powdery mildews. (a) The benzimidazole benomyl.The active substance, carbendazim, is 

produced in planta by removal of the side chain at the position indicated by the arrow. (b) The morpholine tridemorph. (c) The 

2-aminopyrimidine ethirimol. (d) The triazole triadimefon.The molecule becomes reduced to its more active alcohol in planta and 

by fungi at the position indicated by the arrow. (e) Strobilurin A, an antifungal substance from Strobilurus tenacellus. (f) Kresoxim 

methyl, the first strobilurin-based fungicide. (g) Quinoxyfen. (h) Benzothiadiazole (¼ benzo(1,2,3)thiadiazole-7-carbothioic acid 

S-methyl ester), an inducer of systemic acquired resistance.


411 

Fig13.16 One of several possible sterol biosynthesis pathways 

in fungi. Most fungi have ergosterol as their major membrane 

sterol, but in the Erysiphales it is ergosta-5,24(28)-dien-3b-ol 

(Loeffler et al.,1992). Putative targets of various sterol 

biosynthesis inhibitors are indicated as follows. (1) Allylamines, 

e.g. terbinafine (against Candida albicans;seeFig.10.9). 

(2) Triazoles (against fungi pathogenic to humans as well as 

plants). A specific demethylation step is inhibited at C14. 

(3) Morpholines, e.g. fenpropimorph (against plant-pathogenic 

fungi).These compounds seem to inhibit two different steps 

in sterol biosynthesis. Re-drawn and modified from 

Kerkenaar (1995). 

Morpholines (e.g. tridemorph; Fig. 13.15b) were 

the first sterol biosynthesis inhibitors, acting by 

inhibiting two sterol-modifying enzymes in fungi 

(Fig. 13.16) whilst not affecting sterol biosynthesis 

in plants (Kerkenaar, 1995; Uesugi, 1998). A more 

recent fungicide, fenpropimorph, is derived 

from tridemorph and has a similar mode of 

action but is used against other fungi as well. 

In contrast, the 2-aminopyrimidines (Fig. 13.15c) 

act by inhibiting the incorporation of adenine 

into nucleic acids, thereby halting DNA synthesis. 

The effects are visible early, usually at the stage of 

formation of the first haustorium (Holloman & 

Schmidt, 1995). 

Triazoles, which we have already encountered 

as drugs in the treatment of Candida 

infections (Fig. 10.9), are also extensively used 

in agriculture because of their selective action in 

sterol biosynthesis. There is a huge diversity of 

structures (Kuck et al., 1995; Uesugi, 1998), but 

they all seem to act as inhibitors of a cytochrome 

P-450 involved in demethylating sterols at the C- 

14 position (Fig. 13.16). These compounds are 

therefore collectively called demethylation inhibitors 

(DMIs). The target organism is unable to 

produce a functional membrane. Triazoles are 

active against a very wide range of fungal 

pathogens and are systemic fungicides with 

curative properties. One of the first important 

examples against powdery mildews and other 

biotrophic plant pathogens was triadimefon, 

which is reduced in plants and fungi to its 

more active alcohol (Fig. 13.15d). However, 

resistance has arisen on numerous occasions, 

and various resistance mechanisms have been


implicated, such as exclusion or reduced uptake 

of the fungicides, altered membrane lipid 

composition with reduced sterol content, or 

mutation of the fungicide-binding site on the 

cytochrome P-450 enzyme. 

One of the most important recently introduced 

classes of fungicides are the strobilurins. 

They are based on strobilurin A (Fig. 13.15e), 

a natural product from the basidiomycete 

Strobilurus tenacellus initially described by Anke 

et al. (1977) as a strongly and selectively antifungal 

substance. This was derivatized to give 

kresoxim methyl, the first commercial strobilurin-type 

fungicide (Fig. 13.15f). The mode of 

action is based on an inhibition of complex III 

of the mitochondrial respiratory chain (Anke, 

1997). Resistance of Strobilurus tenacellus to its 

own product is based on a mutation of three 

amino acids in the target polypeptide, and resistance 

based on similar mechanisms has arisen 

in many fungal plant pathogens. In consequence, 

strobilurins are not currently recommended for 

control of powdery mildews on cereals and 

cucumber/melon crops (Hollomon & Wheeler, 

2002). 

A recently released compound with exclusive 

activity against powdery mildews is quinoxyfen 

(Fig. 13.15g). The mode of action is interesting 

because this compound selectively inhibits 

morphogenetic events related to infection, such 

as germination or appressorium formation, but 

not vegetative growth. It is therefore non-toxic to 

other fungi. Quinoxyfen is not systemic but is 

distributed in the vapour phase and binds to 

the surface waxes of the epidermis. It is thus 

ideally placed for activity against the germinating 

powdery mildew conidium (Hollomon & 

Wheeler, 2002). Non-fungicidal compounds 

with such a highly specific mode of action 

have fewer side effects against non-target organisms 

such as saprotrophic or mycorrhizal fungi, 

and are likely to increase in importance in 

future. 

Activators of systemic acquired resistance 

(SAR; see p. 116), especially the salicylic acid 

derivative benzothiadiazole (Fig. 13.15h), may 

prove their worth in the prevention of powdery 

mildew infections as well as many other plant 

diseases (Salmeron et al., 2002), although they 

cannot cure existing infections. Since SAR activators 

trigger the expression of a multitude of 

defence-related proteins and other mechanisms 

in the crop plant, powdery mildews are unlikely 

to develop resistance against them, like they 

have done against most of the currently used 

fungicides, many of which target a single site in 

the physiology of the pathogen. Therefore, fungicides 

must be used as cocktails containing 

chemicals with different modes of action, and 

following strict recommendations (Hollomon & 

Wheeler, 2002). 

13.8.3 Biological control 

Their exposed habitat on the leaf surface renders 

powdery mildews potentially susceptible to parasitism 

by phylloplane fungi. Perhaps the bestknown 

of them is Ampelomyces quisqualis, which 

produces conidia within pycnidial fruit bodies 

associated with the hyphae, conidia and, less 

frequently, chasmothecia of powdery mildews. 

It is commonly found in nature (Falk et al., 1995; 

Kiss, 1997). Attempts are being made to develop 

it as a biological control agent (see Bélanger & 

Labbé, 2002), but success is limited by the ability 

of powdery mildews to grow at lower humidities 

than A. quisqualis. This may be alleviated by 

the application of the fungus in paraffin oil 

(Bélanger & Labbé, 2002). One positive aspect is 

that A. quisqualis is tolerant of several fungicides 

used against powdery mildews, so that integrated 

control is possible in principle (Sundheim, 

1982). 

In general, however, the biological control of 

powdery mildews, like that of most other 

airborne pathogens, would appear to be limited 

to greenhouses because there the environment 

can be controlled to a certain extent. With powdery 

mildews, humidity appears to be the crucial 

parameter not only in interactions with 

A. quisqualis, but also other potential control 

fungi such as Verticillium lecanii or basidiomycete 

yeasts, e.g. Tilletiopsis and Pseudozyma (summarized 

in Bélanger & Labbé, 2002). All these, in 

contrast to A. quisqualis, control powdery 

mildews through the production of biologically 

active substances rather than by direct parasitism. 

Fatty acid derivatives seem to be the main 

active compounds, and these may act by

Plate1 Slimemoulds(Myxomycota).(a)White coralloidsporocarps ofCeratiomyxafruticulosa (Protosteliomycetes) onrotting wood. 

(b) Developing aethalia of Lycogala epidendron on rotting wood. (c) Aethalium of Reticularialycoperdon with a silvery grey peridium. 

(d) Aethalium of R.lycoperdonwithitsperidiumruptured toreveala darkbrownpowderymass of spores. (e) Arcyriadenudata onrotting 

wood.The sporangia have openedup, releasing their dullred spores.The capillitium network is exposed. (f) Phaneroplasmodium of 

Physarumpolycephalum producing numerous stalked sporangia on an agar surface. (g) Slightly immature aethalium of Fuligo septica. 

(h) Clustered stalked sporangia of Stemonitisaxifera. (e) and (h) kindly providedby G.L.Barron.

Plate 2 Oomycota. (a) Salmon infected by Saprolegnia sp. (b) Damping-off of cress caused by Pythium sp. (c) Sudden death of a 

20 -year-old Pseudotsuga menziesii plantation caused by Pythium undulatum (¼Phytophthora undulata) due to root rot following heavy 

summer rains. (d) Phytophthora rootrotsymptomsofAbies procera. (e) Late blight symptoms on potato leaf caused by Phytophthora 

infestans. (f) Pink rot of potato tuber caused by Phytophthora erythroseptica. Killed tissue shows a pink discoloration after cutting and 

exposure to air for 30 min. (g) Peronospora parasitica on wallflower (Cheiranthus cheiri) showing the distorted host shoot and 

downy appearance of sporulating regions. (h) Cauliflower leaf infected with Albugo candida, showing the typical white blister rust 

symptoms caused by the eruption of sporangia through the epidermis.

Plate 3 Chytridiomycota (a c) and Zygomycota (d i). (a,b) Synchytrium endobioticum. (a) Excavated potato plant showing a gall at 

the base of a shoot. (b) Leafy gall stage at the soil surface. (c) Synchytrium taraxaci, sporangial sori on dandelion (Taraxacum officinale). 

(d) Strawberry infected by Rhizopus stolonifer. (e) Sporangiophores of Spinellus fusiger on an old basidiocarp of Mycena pura. 

(f) Sporangiophore of Piloboluscrystallinus producing a hemispherical black sporangium. Ayellow band below the base of the swollen 

subsporangial vesicle, the ocellus, is enriched in carotenoids.The stalk and vesicle bear droplets of liquid. (g) Entomophthora muscae. 

Dead fly attached to a window pane, surrounded by a halo of discharged conidia. (h) Furia americana. Dead blowflies attached to a 

leaf.Conidiophores have penetrated between the abdominal segments. (i) Sporocarp of the pea truffle Endogone lactiflua,cutopen 

to reveal the zygospores.

Plate 4 Archiascomycetes (a c) and Plectomycetes (d f). (a) Peach leaf infected withTaphrina deformans.(b)Taphrina betulina 

causing witches’ broom disease on birch. (c) Taphrina amentorum causing abnormal enlargement of individual catkin segments on 

Alnus glutinosa.(d)Aspergillus parasiticus. Petri dish with parasexual recombinants deficient in melanin biosynthesis leading to 

colourless spores, and/or in aflatoxin biosynthesis which leads to the accumulation of bright yellow or orange pigments. (e) Orange 

rotted by Penicillium digitatum. (f) Excavated cleistothecium of Elaphomyces infected by Cordyceps ophioglossoides.Germinating 

ascospores have accumulated as whitish pustules around the perithecial ostioles. (d) kindly provided by J.F. Peberdy, (f) by J. Benn.

Plate 5 Pyrenomycetes. (a) Daldinia concentrica on an old log of ash.One stroma has been cut open. (b) Stromata of Xylaria longipes 

on a buried sycamore trunk. (c) Hypocrea pulvinata, perithecial crust on the underside of an old fruit body of Piptoporus betulinus. 

(d) Nectria cinnabarina with conidial pustules and dark red perithecial stromata. (e) Orange-coloured sporodochia of Fusarium 

heterosporum parasitizing sclerotia of Claviceps purpurea var. spartinae on Spartina anglica. (f) Perithecial stroma of Epichloe typhina 

‘choking’ a shoot of Dactylisglomerata.(g)Cordyceps militaris, perithecial stromata emerging from a buried insect pupa. (h) Dutch elm 

disease. (i) Anthracnose on broad bean caused by Colletotrichum lindemuthianum. (c) kindly provided by J. Benn.

Plate 6 Apothecia of operculate discomycetes (Pezizales). (a) Pyronema domesticum fruiting on autoclaved pottery. (b) Aleuria 

aurantia.(c)Peziza vesiculosa on freshly manured garden soil. (d) Ascobolus furfuraceus on agar.The purple dots represent ripe asci. 

(e) Sarcoscypha australis on an old log of ash (Fraxinus). (f) Helvella crispa.(g)Morchella esculenta. (g) kindly provided by P. Davoli.

Plate 7 Inoperculate Discomycetes (Helotiales). (a,b) Sclerotinia curreyana. (a) Sclerotia formed inside culms of Juncus effusus. 

(b) Stalked apothecia of S. curreyana arising from a sclerotium in spring. (c) Rutstroemia echinophila on the shell of edible chestnuts. 

(d) Mollisiacinerea, a common saprotroph on twigs. (e) Dasyscyphusvirgineus producing small apothecia with a hairy margin on rotting 

wood. (f) Leotia lubrica, a saprotroph soil fungus with stalked apothecia. (g) Chlorociboria aeruginascens on a decaying sycamore twig. 

Sections of the colonized wood show its green discolouration. (h) Bisporellacitrina on a beech twig. (i) Bulgariainquinans forming black 

gelatinous apothecia on freshly felled oak trunks. (j) Apothecial stromata of Cyttaria darwinii on living twigs of the southern beech 

Nothofagus pumilio. (d) and (e) kindly provided by H. Anke, (f) by P. Davoli. (a,b) reprinted from Weber and Webster (2003), with 

permission from Elsevier.

Plate 8 Thalli of lichens. (a) The crustose lichen Lecanora muralis. Numerous apothecia are seen in the centre of the thallus. (b) The 

crustose Rhizocarpon geographicum. Its mosaic-like appearance is due to greenish-yellow vegetative thalli with small dark apothecial 

areas, and larger black prothalli. (c) The crustose foliose lichen Xanthoria parietina.The yellow colour is due to the pigment parietin. 

Numerous apothecia are seen in the centre of the thallus. (d) Peltigeracanina on mossy boulders.The foliose fleshy thallus is coloured 

dark blue green by the cyanobacterium Nostoc. Note the white rhizinae and the reddish apothecial areas. (e) Cladonia floerkiana. 

Fruticose upright podetia arise from a squamulose horizontal thallus. (f) The reindeer lichen Cladina rangiferina growing among 

ground vegetation. (g) Usnea florida, a fruticose lichen hanging down from tree branches. (b) kindly provided by B. Bu«del.

Plate 9 Fruit bodies of Homobasidiomycetes: euagarics and boletoid clades. (a) Amanita muscaria, probably the best-known of all 

mushrooms. (b) Amanita caesarea, a prized delicacy in Mediterranean countries. (c) The scarlet waxcap, Hygrocybe coccinea. (d) The 

winter fungus, Flammulina velutipes.(e)Pholiota squarrosa.(f)Boletus erythropus.(g)Suillus granulatus.(h)Boletus badius. Healthy fruit 

body (left) and others attacked by the mycoparasitic mould, Sepedonium chrysospermum. (e) kindly provided by P. Davoli.

Plate10 Fruitbodies of Homobasidiomycetes: other clades. (a) Trametes versicolor, the artist’s fungus or turkey tail on a birchbranch. 

Note the bleached (white-rot) appearance of the wood at the broken end. (b) Laetiporussulphureus, the chicken of the woods. 

(c) Lactariusdeliciosus.(d)Chondrostereum purpureum, cause of silver-leaf disease on plum trees. (e) Thelephoraterrestris,an 

ectomycorrhizalspecies.(f)Phellinusigniarius fruitingon an oldwillow tree. (g) Cantharelluscibarius,thechanterelle.(h)Ramariabotrytis.

Plate11 Gasteromycetes (a f) and Heterobasidiomycetes (g i). (a) Calvatia excipuliformis.(b)Pisolithus tinctorius, one gasterocarp 

cut open to reveal the peridioles. (c) Rhizopogon sp.; excavated gasterocarp which has been cut open. (d) Phallus impudicus,the 

common stinkhorn. (e) Clathrusruber.(f)Aseroe rubra.(g)Calocera viscosa.(h)Auricularia auricula-judae.(i)Tremella mesenterica. 

(f) reprinted from Fuhrer (2005), with permission by Bloomings Books Pty Ltd. Image kindly provided by B.Fuhrer.

Plate12 Urediniomycetes (a g) and Ustilaginomycetes (h j). (a) Aeciospore of Puccinia distincta.Lipid droplets have been displayed 

by the two nuclei in the upper spore. (b) Aecial infection of Pucciniacaricina on stinging nettle. (c) Uredinia (orange pustules) and telia 

(dark purple lesions) of Phragmidiumviolaceum on theunderside of a leaf ofbramble. (d f)Gymnosporangiumfuscum. (d) Telial horns on 

aswollencankeronJuniperus in spring. (e) Spermogonial infection on a pear leaf in midsummer. (f) Roestelioid aecia on the underside 

of a pear leaf in autumn.The aecial caps are connected to the aecialbase by trellis-like threads. (g) Uredinia of Melampsora sp. on 

Populus tremula. (h) Maize smutcausedby Ustilago maydis. Swollen kernels have become convertedinto teliospore-bearing tumours. 

(i) Exobasidium sp. on an ornamental Azalea.Infectedleaves are strongly hypertrophied. (j) Systemic Exobasidiumvaccinii infection of 

blueberry (Vaccinium myrtillus).The infected shoot (left) shows a reddish discolouration. (d) and (i) kindly providedby H.Weber.


413 

inserting themselves into the powdery mildew 

plasma membrane, disrupting its structural 

integrity (Avis & Bélanger, 2002; Urquhart & 

Punja, 2002). Other explanations for the strongly 

inhibitory effect of specific fatty acids (especially 

cis-monounsaturated ones) against powdery mildews 

are, however, also possible (Wang et al., 

2002). Unsaturated fatty acids could also be the 

basis for the anti-powdery mildew activity of 

cow’s milk described by Bettiol (1999).

14 

Hymenoascomycetes: Pezizales (operculate 

discomycetes) 


The order Pezizales contains the operculate 

discomycetes which are the most readily recognized 

cup fungi. The order is large, containing 

some 15 families, about 160 genera and over 

1100 species (Kirk et al., 2001). Most are terrestrial 

and saprotrophic on soil, burnt ground, decaying 

wood, compost or dung, but some form sheathing 

mycorrhiza (ectomycorrhiza) with trees 

(Maia et al., 1996). A somewhat exceptional 

case is Rhizina undulata, which causes root rot 

of conifers in plantation situations, usually starting 

from areas affected by recent fires (Callan, 

1993). Whilst most species of Pezizales produce 

epigeous fruit bodies above ground level and 

have active ascus discharge mechanisms with 

wind-dispersed ascospores, the truffles (e.g. Tuber 

and Terfezia) form subterranean (hypogeous) 

ascomata. The dispersal of truffles relies on 

the ripe ascomata being eaten by rodents and 

other mammals attracted by their strong odour. 

The ascospores survive digestion and defaecation. 

There are also aquatic Pezizales, growing on 

wood in streams or other wet places. An overview 

of the Pezizales may be found in Pfister and 

Kimbrough (2001). Keys to genera are given 

by Korf (1972) and Dissing et al. (2000). 

The ascocarp is generally an apothecium 

(p. 245) which can range in diameter from less 

than one millimetre to several centimetres. It is 

often cup-shaped or disc-like, fleshy, sometimes 

stalked, and frequently brightly coloured. 

The asci are, in most cases, cylindrical with 

a well-defined lid called operculum (see 

pp. 239 241) which is the characteristic feature 

of the Pezizales. Members of this order are 

therefore often referred to as ‘operculate discomycetes’. 

The asci are interspersed by filamentous 

paraphyses, the tips of which often contain 

carotenoids giving the apothecia their striking 

yellow, orange or red colours. Several unusual 

carotenoids are known in nature only from 

apothecia of Pezizales (Gill & Steglich, 1987). 

The ascus wall appears distinctly two-layered 

under the light microscope, but the two layers do 

not separate during ascospore discharge as they 

do in functionally bitunicate (i.e. fissitunicate) 

ascomycetes (see p. 239). The ascus of the 

Pezizales is thus bitunicate but non-fissitunicate. 

In many Pezizales the ascus wall is amyloid, i.e. it 

stains blue or purple with Melzer’s iodine 

(an aqueous solution of iodine and KI). The 

blue-staining properties are associated with an 

outer mucilaginous layer which may extend for 

the whole length of the ascus or may be confined 

to an apical region (Samuelson, 1978a,b). The 

presence or absence of the amyloid staining 

property may help in distinguishing certain 

genera (see Hansen et al., 2001). The septal pore 

formed at the base of the ascus has characteristic 

features which may be useful in classification 

(Kimbrough, 1994). The ascospores are colourless 

to reddish-brown, globose to ellipsoidal, unicellular 

(i.e. non-septate) and may be uninucleate,

PYRONEMA (PYRONEMATACEAE) 

415 

Table 14.1. Families of the Pezizales which are commonly encountered in nature. Data from Kirk et al. (2001). 

Families printed in bold are considered in more detail in this chapter. 

Family Number of species Examples 

Ascobolaceae (p.419) 118 Ascobolus, Saccobolus 

Discinaceae 25 Gyromitra 

Helvellaceae (p.423) 68 Helvella 

Morchellaceae (p.427) 38 Morchella,Verpa 

Pezizaceae (p.419) 160 Peziza 

Pyronemataceae (p.415) 462 Aleuria,Otidea, Pyronema, Scutellinia 

Rhizinaceae 2 Rhizina 

Sarcoscyphaceae 36 Sarcoscypha 

Sarcosomataceae 31 Galiella, Urnula 

Terfeziaceae 15 Terfezia 

Tuberaceae (p.423) 87 Tuber 

quadrinucleate or multinucleate. They contain 

one or several large lipid globules and may have 

smooth or ornamented walls. Individual asci 

may discharge their spores asynchronously, or 

large numbers of asci may shoot off their spores 

simultaneously. In this case, the spores may be 

released in a visible cloud in a process known as 

‘puffing’ (see Fig. 8.14). Buller (1934) investigated 

this phenomenon in detail and reported that 

ascospore puffing produces an audible hissing 

sound. The asci of truffles, in contrast, are saclike 

or globose, with no functional operculum, 

and the spores are released passively. 

The fruit bodies of some members of the 

group are highly prized culinary delicacies, notably 

truffles (Tuber spp.) and morels (Morchella 

spp.). Gyromitra esculenta, the false morel, was 

formerly also widely consumed but, following 

a series of often fatal mushroom poisonings, 

was eventually found to contain the heat-labile 

toxin gyromitrin. This is readily converted 

into hydrazine derivatives such as the rocket 

fuel methylhydrazine, which are highly toxic 

and carcinogenic (Bresinsky & Besl, 1990). Illustrations 

of the ascomata of commonly occurring 

Pezizales have been provided by Breitenbach 

and Kränzlin (1984) and Dennis (1981). Selected 

examples are presented on Plate 6. 

Molecular phylogenetic analyses indicate 

that the Pezizales are probably a primitive 

group ancestral to other Euascomycete orders 

(Fig. 8.17; Gargas & Taylor, 1995; Landvik 

et al., 1997). This implies that apothecia are 

an ancient type of ascoma, with cleistothecia 

and perithecia representing later developments. 

Whilst the Pezizales as a whole are monophyletic, 

the arrangement into families within this order 

is still tentative (Harrington et al., 1999). The more 

important of the currently recognized families 

are listed in Table 14.1. Since the morphological 

and ecological features of pezizalean fungi 

often transcend the family boundaries, we will 

describe a few characteristic genera in more 

detail by their biological features, merely 

indicating their family assignment where 

appropriate. 

14.2 Pyronema (Pyronemataceae) 

The apothecia of Pyronema develop on burnt 

soil and on heat-sterilized composts in glasshouses. 

There are two species, P. omphalodes (¼ 

P. confluens) and P. domesticum (Moore & Korf, 

1963). In P. omphalodes the apothecia are confluent 

and lack marginal hairs, whilst in 

P. domesticum the apothecia are more discrete, 

and surrounded by tapering hairs (Fig. 14.1a). 

Pyronema domesticum forms sclerotia in culture 

(Moore, 1962), whilst P. omphalodes does not. 

In earlier studies the distinction between the 

two species was sometimes not appreciated and

416 HYMENOASCOMYCETES: PEZIZALES (OPERCULATE DISCOMYCETES) 

Fig14.1 Pyronema domesticum. 

(a) Apothecium showing hymenium 

and excipular hairs. (b) Group of 

ascogonia and antheridia. (c) V.S. 

through developing apothecium 

showing several ascogonia 

producing ascogenous hyphae, and 

the development of paraphyses and 

excipulum from the ascogonial 

stalks. (d) Enlarged view of the 

ascogonium and developing 

ascogenous hyphae. (e j) Stages 

in the development of asci. 

(e) Binucleate tip of ascogenous 

hypha beginning to form a crozier. 

(f) Quadrinucleate stage. 

(g) Septation of crozier to form 

a binucleate penultimate cell. 

(h) Development of ascus from 

binucleate cell. (i) Completion of 

first meiotic division. 

(j) Completion of second meiotic 

division. Note the proliferation of 

a new ascogenous hypha from the 

stalk cell. 

some reports purporting to be on P. confluens 

may well have been based on P. domesticum. 

These earlier studies include classical accounts 

of the cytology of the development of ascogenous 

hyphae, croziers and asci (see Moore, 1963). 

14.2.1 Development of asci in Pyronema 

Both species of Pyronema are homothallic and 

grow rapidly in agar culture or on sterilized soil 

and within 4 5 days form pink apothecia about 

1 2 mm in diameter (Plate 6a; Webster & Weber, 

2001). Apothecia of P. domesticum arise from 

clusters of ascogonia and antheridia formed 

by repeated dichotomy of a single hypha. The 

ascogonia are fatter than the antheridia and 

each ascogonium is surmounted by a tubular 

recurved trichogyne which grows to make contact 

with the tip of an antheridium (Fig. 14.1b). 

Both antheridia and ascogonia are multinucleate 

and, following fusion of the trichogyne with the 

antheridium by breakdown of the walls separating 

them (plasmogamy), antheridial nuclei 

stream into the ascogonium and each antheridial 

nucleus becomes paired with an ascogonial 

nucleus. Nuclear fusion (karyogamy) does not 

occur at this stage, but the paired nuclei remain 

associated with each other. Branched investing 

hyphae develop from the ascogonial stalks and 

envelop the cluster of fertilized ascogonia, ultimately 

making up the tissues of the apothecium, 

i.e. the medullary and ectal excipulum. Several 

ascogenous hyphae extend from each ascogonium 

and grow between the surrounding 

investing hyphae (Figs. 14.1c,d). 

Further development follows the common 

ascomycete pattern outlined in Fig. 8.10 (I. M. 

Wilson, 1952; Hung & Wells, 1971). The ascogenous 

hyphae are branched and septate at their 

tips, which recurve to form croziers. The tip of 

the crozier is binucleate and the two nuclei

ALEURIA (PYRONEMATACEAE) 

417 

simultaneously divide by mitosis (conjugate 

mitosis). Two septa cut off a uninucleate terminal 

cell, a binucleate penultimate cell and 

a uninucleate antepenultimate cell (the stalk 

cell). The binucleate penultimate cell is the ascus 

mother cell and the two nuclei within it fuse, 

i.e. karyogamy now occurs. The diploid fusion 

nucleus undergoes meiosis and the four resulting 

haploid nuclei then divide mitotically so 

that eight haploid nuclei result around which 

the eight ascospores are subsequently cleaved 

(Reeves, 1967). No further nuclear divisions occur 

so that each ascospore contains one haploid 

nucleus. No special inclusions are seen in the 

septa of the crozier, but electron-dense plugs are 

formed at the base of the ascus (Hung & Wells, 

1971; Kimbrough, 1994). When the uninucleate 

terminal cell grows backwards and makes 

contact with the stalk cell, their walls break 

down and a new binucleate cell is formed which 

grows on to form a further crozier and another 

ascus, a process which is repeated so that a single 

ascogenous hypha may produce several asci 

(Fig. 14.2b). The ascus mother cell elongates and 

acquires a cylindrical shape. It is surrounded by 

filamentous paraphyses. These develop from the 

stalks of the ascogonia (I. M. Wilson, 1952) and 

also appear to arise from ascogenous hyphae 

(Fig. 14.2c). As the ascus matures it extends above 

the layer of paraphyses and explodes, throwing 

out its ascospores. The operculum may persist 

as a hinged lid (Fig. 14.2c) or may be blown 

off. During the development of asci, before 

the ascospores are cleaved out, the operculum 

becomes apparent as a thickened rim of wall 

material at the upper end of the ascus. 

Mature ascospores have three wall layers, 

a thicker, electron-transparent inner layer (the 

endospore), a thinner electron-opaque epispore, 

and an outer fibrous perispore of variable thickness. 

The perispore lies immediately within 

the ascospore-investing membrane, and, as ascospores 

mature, this membrane continues to 

produce vesicles, leading to degradation of the 

perispore. At discharge, the ascospores do not 

stick together but remain separate from each 

other (Hung, 1977). Merkus (1976) has described 

the development and structure of the ascospores 

of P. omphalodes in similar terms. 

Much is known about the conditions under 

which P. domesticum forms apothecia and sclerotia 

(Moore-Landecker, 1975, 1992). Light is 

required for apothecium development, with 

white, blue and far-red light being particularly 

effective. Sclerotium formation is inhibited by 

intense blue light. 

14.2.2 Ecology of Pyronema 

In nature, the apothecia of both species of 

Pyronema are among the first to appear on 

burnt ground following volcanic eruptions, wildfires, 

controlled burns and bonfires. Pyronema 

forms part of a characteristic group of ‘phoenicoid 

fungi’, i.e. fungi arising from ashes. Many 

other operculate discomycetes are also phoenicoid 

(Carpenter & Trappe, 1985; Dix & Webster, 

1995). The ascospores of P. domesticum germinate 

readily at 20°C, although a short exposure to 

50°C enhances germination. Apothecium formation 

is inhibited by the presence of other 

soil-inhabiting organisms and it is possible that 

the preference for burnt ground and steamsterilized 

soil is associated with its rapid growth 

and inability to compete with other soil biota 

(El-Abyad & Webster, 1968a,b). 

Unnatural (i.e. man-made) situations in which 

P. domesticum fruits are steam-sterilized soils 

and composts used in horticulture, and plaster 

prepared by slaking lime, a process which generates 

heat. Supposedly sterile surgical gauzes 

manufactured from Chinese cotton have been 

found to be contaminated with P. domesticum 

due to insufficient radiation treatment during 

manufacture. The source is likely to be raw 

cotton materials possibly already contaminated 

in the field (Yan, 1998). Laboratory experiments 

have shown that the g-irradiation resistance 

of P. domesticum ascospores is higher even than 

that of Bacillus endospores (Richter & Barnard, 

2002). 

14.3 Aleuria (Pyronemataceae) 

Aleuria seems to be closely related to Pyronema 

(Landvik et al., 1997). There are about 10 species 

of Aleuria, growing especially on forest soil.


Fig14.2 Pyronemadomesticum. (a) An immature ascus (left).The ascogenous hypha fromwhich itdeveloped continues to proliferate. 

(b) More magnified view of the tip of an ascogenous hypha showing repeated proliferation.The three stippled cells represent 

penultimate cells of croziers probably destined to develop into asci. (c) Mature asci, one discharged and showing an operculum. A 

paraphysis is also shown apparently arising from the ascogenous hypha.

ASCOBOLUS (ASCOBOLACEAE) 

419 

Aleuria is similar in appearance to Peziza (see 

below) but is distinguished from it in having 

non-amyloid asci. The best-known species is A. 

aurantia, the so-called orange-peel fungus which 

forms strikingly orange-coloured cup-shaped 

apothecia from about 1 10 cm in diameter in 

woodland and grassland soil during autumn 

(Plate 6b). Isotopic analyses of ascocarps using 

15 N and 13 C isotopes indicate that the fungus 

may be mycorrhizal (Hobbie et al., 2001). The 

orange colour of the hymenium is due to 

carotenoid-enriched granules in the club-shaped 

tips of the paraphyses (Fig. 14.3). The main 

carotenoids are b-carotene, g-carotene and aleuriaxanthin 

(Gill & Steglich, 1987). 

The ascospores contain two lipid globules and 

the ascospore wall is ornamented by a honeycomb-like 

series of raised ridges which represent 

secondary wall material. It is derived from 

granules in the perisporic sac which condense 

into larger spherical dense bodies. These accumulate 

and become attached to the epispore 

(Merkus, 1976; Wu & Kimbrough, 1993). 

14.4 Peziza (Pezizaceae) 

Peziza is a large genus containing around 

100 species. Analyses based on a combination 

of morphological and molecular evidence indicate 

that this genus is polyphyletic, i.e. it 

contains a number of unrelated taxa which 

have been grouped together artificially. Peziza 

in its traditional sense can be differentiated 

into at least eight clades (Hansen et al., 2005). 

Hohmeyer (1986) has provided a key to European 

species. For descriptions and illustrations see 

Dennis (1981), Breitenbach and Kränzlin (1984) 

and Dissing et al. (2000). The apothecia are cupshaped, 

often large (2 5 cm or more), usually 

pale brown and fleshy (Plate 6c). They are 

commonly encountered in a very wide range 

of habitats including soil, manure heaps, dung, 

rotting wood or straw, burnt ground and sand 

dunes. About six species have hypogeous ascocarps 

(Trappe, 1979). The ascus wall is, in general, 

amyloid. In P. succosa the blue-staining by I 2 /KI 

is confined to the ascus apex (Samuelson, 1978a). 

Fig14.3 Aleuria aurantia. Asci, ascospores and paraphyses. 

The tips of the paraphyses are filled with granules containing 

orange-coloured carotenoids. 

The conidial states of Peziza spp., where known, 

have been classified in the anamorph genus 

Oedocephalum (Fig. 14.4). 

A genus with more strikingly coloured apothecia 

is Sarcoscypha (Plate 6e). Although similar 

in appearance to Peziza, these two genera are not 

closely related (Landvik et al., 1997). 

14.5 Ascobolus (Ascobolaceae) 

There are about 80 species of Ascobolus 

(van Brummelen, 1967). Most of them are


Fig14.4 Oedocephalum conidial state of Peziza subviolacea 

(¼ P. praetervisa). (a) Conidiophores terminating in a 

club-shaped vesicle bearing numerous dry blastoconidia. 

(b) Details of developing conidia (top) and a vesicle from which 

the conidia have been detached (bottom). (c) Conidia, two of 

which are germinating. Scale bar ¼ 40mm (a,b) and 20 mm(c). 

From Webster et al. (1964), with permission from Elsevier. 

coprophilous, growing on the dung of herbivorous 

animals, but A. carbonarius grows on old 

bonfire sites. Common coprophilous species 

are A. furfuraceus (¼ A. stercorarius) which is very 

commonly found on old cattle dung, often 

along with A. immersus (Figs. 14.5 and 14.6, 

respectively). Whilst these species are heterothallic, 

some others, e.g. A. crenulatus (¼ A. viridulus), 

are homothallic. Characteristic features of all 

species are the purple colour of the ascospores 

and the protruding, operculate asci. Ascobolus 

furfuraceus forms yellowish saucer-shaped apothecia 

up to 5 mm in diameter, and when mature 

the surface of the apothecium is studded with 

purple dots which mark the ripe asci (Plate 6d). 

As the asci mature they elongate above the 

general level of the hymenium. The ascus tips 

are phototropic and this ensures that when they 

explode the spores are thrown away from 

the dung. The ascospores have a mucilaginous 

perispore which aids attachment. Ascobolus 

immersus has yellow globose apothecia about 

1 2 mm in diameter, with very large ascospores 

(about 70 30 mm). The perispores cause all 

the eight ascospores to adhere to form a single 

projectile about 250 mm long, capable of being 

discharged for up to 30 cm horizontally. In 

general, multi-spored projectiles have a lower 

surface-to-volume ratio and are projected further 

than single spores (see p. 317 for Sordaria). 

There is a general trend among coprophilous 

fungi towards multi-spored projectiles. In the 

genus Saccobolus, which also belongs to the 

Ascobolaceae, all eight spores are firmly cemented 

together by their perispores. 

The spores of Ascobolus become attached to 

herbage and, when eaten by a herbivore, germinate 

in the faeces. It is likely that digestion 

stimulates spore germination. Most spores fail 

to germinate on nutrient media but can be 

triggered to do so by treatment with 0.4% NaOH 

or bile salts, and incubation at 37°C. The purple 

pigment in the spore wall develops late and is 

deposited within the perispore from the ascus 

epiplasm. Immature spores are colourless. The 

spore wall bears longitudinal colourless striations 

in some species, e.g. A. immersus (Fig. 14.5) 

and A. furfuraceus (Fig. 14.6). Both species can be 

grown and induced to form apothecia in culture 

(see Webster & Weber, 2001). 

14.5.1 Mating behaviour 

There is variation in the mating behaviour of 

different species of Ascobolus. A single ascospore 

culture of A. scatigenus (¼ A. magnificus) does not 

produce apothecia. Sex organs (coiled ascogonia 

and antheridia) are formed only when mycelia 

of different mating types are grown together. 

Each strain is hermaphroditic, i.e. is capable 

of developing both ascogonia and antheridia. 

However, A. scatigenus is self-incompatible, 

i.e. the antheridia of one strain do not fertilize 

the ascogonia borne on the same mycelium. 

The ascospores of this fungus are of two types, A

ASCOBOLUS (ASCOBOLACEAE) 

421 

Fig14.5 Ascobolus immersus.(a)Apothecium 

showing two projecting asci. Immature asci can 

be seen below the general level of the surface. 

A single projectile consisting of eight adhering 

ascospores is shown above the apothecium. 

Note the operculum which has also been 

projected. (b) Tip of ripe ascus showing the 

operculum. (c) Tip of discharged ascus. In this 

case the operculum has remained attached to 

the ascus tip. 

and a, and fertilization can only occur between 

an A ascogonium and an a antheridium, or 

vice versa. There is thus a gene for mating 

type represented in two idiomorphs A and a, 

and incompatibility is controlled by this gene 

irrespective of the presence of both types of 

sex organ on each strain. There is no morphological 

difference between the two different 

mating type strains. 

A similar situation occurs in A. furfuraceus, 

but here there are no antheridia. Instead, each 

strain at first produces chains of arthrospores 

or oidia (see Fig. 14.6c). The oidia can germinate 

to form a fresh mycelium, i.e. they can function 

asexually as conidia, but they also play a part 

in sexual reproduction. Mites and flies may 

transport oidia of one strain to the mycelium 

of the opposite strain, and following this, 

apothecia develop. The process of fertilization 

has been studied by Bistis (1956, 1957) and Bistis 

and Raper (1963). If an A oidium is transferred 

to an a mycelium, the oidium fails to germinate 

and within 10 h an ascogonial primordium 

appears on the a mycelium (Fig. 14.6d). The 

ascogonium consists of a broad coiled base and 

a narrow apical trichogyne which shows chemotropic 

growth towards the oidium and eventually 

fuses with it. There is evidence that this sequence 

of events is under hormonal control, and it 

has been suggested that a fresh A oidium is not 

immediately capable of inducing development 

of ascogonial primordia, but must itself at first 

be sexually activated by a messenger secreted 

by the a mycelium. Following activation, the 

oidium can induce ascogonial development. 

By substitution experiments, it has been shown 

that an A ascogonium can be induced to fuse 

with an A oidium, i.e. an oidium of the same 

mating type, but apothecia fail to develop 

from such fusions. In compatible crosses, fertile 

apothecia develop within about 10 days of fertilization, 

each ascus producing four A and four 

a spores. 

In A. immersus there are no morphologically 

distinguishable antheridia and there are 

no oidia. When A and a mating type mycelia 

are grown together in culture, multinucleate 

ascogonia develop which are fertilized by fusion 

with slender multinucleate hyphae of the 

opposite strain. Experimentally, fertilization 

can also be achieved using homogenized mycelial 

fragments of one strain to spermatize a 

strain of opposite mating type (Lewis & Decaris, 

1974).


Fig14.6 Ascobolus furfuraceus. (a) Group of asci and 

paraphyses.One ascus is mature and contains 

purple-pigmented ascospores. (b) The same ascus as 

shown in a after discharge.The ascus has decreased in size 

during discharge. Note the operculum. (c) Arthrospores 

(oidia) developed in five-day-old culture. (d) Coiled 

ascogonium formed in a single ascospore culture within 

48 h of adding oidia of the opposite mating type. 

The trichogyne of the ascogonium has grown towards 

the oidium and has fused with it. 

14.5.2 Apothecium development 

The development of apothecia of A. furfuraceus 

has been studied by various authors, including 

Wells (1970, 1972) and O’Donnell et al. (1974). 

The fertilized ascogonium becomes surrounded 

by sheath hyphae which develop from the 

ascogonial stalk, and the paraphyses and excipular 

tissues develop from the sheath hyphae. 

The ascogonium gives rise to numerous ascogenous 

hyphae. Van Brummelen (1967) has 

distinguished two kinds of ascocarp development 

in Ascobolus. In gymnohymenial forms, 

the hymenium is exposed from the beginning 

until the maturation of the asci. In cleistohymenial 

forms the hymenium is enclosed during 

its early development. Ascobolus furfuraceus and 

A. immersus are examples of cleistohymenial 

development. 

14.5.3 Ascosporogenesis 

The details of ascosporogenesis have been 

studied in A. immersus by Wu and Kimbrough 

(1992) and in A. stictoideus by Wu and Kimbrough 

(2001). Although A. immersus has smooth ascospores 

and A. stictoideus has ornamented spores, 

development is very similar. As in most ascomycetes, 

invagination of the ascus vesicle encloses 

the young ascospores by a two-layered sporedelimiting 

membrane. The inner layer forms the 

plasmalemma of the ascospore, whilst the outer 

membrane forms a perisporic sac. The primary 

spore wall is laid down between these two 

membranes. It consists of an electron-transparent 

endospore and a laminated epispore. The 

perisporic sac is variable in thickness and 

projects into the epiplasm of the ascus. 

At points of contact with the perisporic sac

TUBER (TUBERACEAE) 

423 

of neighbouring ascospores, the perisporic sac 

may be lined by vesicles. Secondary wall formation 

results from deposition of material derived 

from the epiplasm onto the epispore. Dense, 

vesicle-bound bodies originally present in the 

epiplasm are responsible for the purple coloration 

of the secondary spore wall. The pigmented 

secondary wall layer is not uniformly thick and 

the hyaline striations in the spore wall represent 

crevices in the material deposited. 

14.5.4 Studies on gene recombination 

Ascobolus immersus has proved a useful tool 

for interpreting the mechanism of gene 

recombination through crossing-over during 

meiosis using ascospore colour as a marker. 

Recombination is detected by the simple technique 

of scoring the ratio of the spores of different 

colour in octads of spores shot away from hybrid 

apothecia. Although the wild-type strains have 

purple ascospores, several series of mutants 

with pale spores have been found. When crosses 

are made using certain non-allelic spore colour 

mutants, recombinants develop resulting from 

two types of event: (1) crossing-over, giving 

reciprocal recombinants and (2) gene conversion, 

yielding non-reciprocal recombinants corresponding 

to only one of the four products 

of meiosis. Gene conversion is a process where 

one allele of a gene converts another allele at the 

same locus to its own type. Crossing-over results 

in a 4 : 4 ratio of coloured to colourless spores 

whilst a conversion is detected by the presence 

of coloured and colourless spores in different 

ratios e.g. 7 : 1, 6 : 2 or 5 : 3. Conversions have 

been interpreted as implying a double-strand 

replication of one part of a chromatid whilst 

the corresponding part of the other is not 

replicated (Lamb, 1996). 

14.6 Helvella (Helvellaceae) 

Helvella, a genus containing about 40 species, is 

mainly distributed in northern temperate areas 

(Dissing, 1986; Abbott & Currah, 1997). Helvella 

spp. are known as saddle fungi because the 

ascocarp is differentiated into a hollow, nonfertile 

stipe and a curved, saddle-shaped fertile 

part folded over it. They are also called false 

morels. Common species are H. crispa (Plate 6f) 

and H. lacunosa. Some species form ectomycorrhiza, 

and e.g. H. crispa is a mycorrhizal 

partner with beech, Fagus sylvatica. A characteristic 

feature of the Helvellaceae is that their 

ascospores are quadrinucleate. This feature, 

also found in certain truffle-like fungi with 

hypogeous ascocarps, has been used as evidence 

placing genera such as Hydnotrya, species of 

which also form sheathing mycorrhizae, into 

the Pezizales instead of the Tuberales where 

they were previously classified (Trappe, 1979). 

More recent molecular phylogenetic studies 

have confirmed a close relationship between 

the Helvellaceae and the Tuberaceae, the main 

truffle-containing family (Percudani et al., 1999). 

14.7 Tuber (Tuberaceae) 

About 100 species of Tuber are known. They 

are called the ‘true truffles’, ascomycetes which 

form subterranean fruit bodies in which the 

hymenium is not open to the exterior. It has 

been suggested that hypogeous fruiting is an 

adaptation for surviving drought and that the 

genera of fungi which have adopted this strategy 

(including ascomycetes and basidiomycetes) 

have evolved from ancestors with epigeous fruit 

bodies. According to this view the subterranean 

ascocarps of Tuber and other ascomycetous 

truffle genera are modified apothecia. The term 

stereothecium, defined as a more or less solid 

fleshy ascoma with asci which are either solitary, 

i.e. scattered relatively evenly throughout 

the medullary excipulum, or grouped in dispersed 

pockets, has been proposed for this 

type of ascoma (O’Donnell et al., 1997; Hansen 

et al., 2001). Supporting evidence that stereothecia 

are modified apothecia is that, during 

their ontogeny, ascocarps are at first open to 

the exterior and close over later as the hymenium 

develops (Barry et al., 1993; Callot, 1999; 

Janex-Favre & Parguey-Leduc, 2002). This morphological 

evidence has been corroborated by


molecular phylogenetic data (Spatafora, 1995; 

Percudani et al., 1999; Hansen et al., 2001). 

Although Tuber and other ascomycetes were formerly 

classified in a separate order (Tuberales), 

they are now placed in the Pezizales (Trappe, 

1979) as a separate family, the Tuberaceae. 

This family is closely related to the Helvellaceae 

(see above). 

14.7.1 The truffle ascocarp 

The ascocarp is generally globose, varying in size 

from about 1 to 8 cm in diameter and, exceptionally, 

may weigh up to 1000 g. It is differentiated 

into an outer, usually dark peridium 

which in some species, e.g. T. melanosporum or 

T. aestivum, may bear pyramidal scales, and an 

inner, fertile gleba. The appearance of the gleba 

is marbled because it is traversed by light- and 

dark-coloured veins (Fig. 14.7a). The lightcoloured 

veins are sterile, consisting of a loose 

network of hyphae and air, whilst the darker 

veins are fertile, made up of more closely packed 

hyphae, paraphyses and asci (Parguey-Leduc 

et al., 1991; Barry et al., 1995; Callot, 1999; 

Janex-Favre & Parguey-Leduc, 2002). 

The asci are unitunicate, subglobose and 

contain 2 6 ascospores. They do not discharge 

their spores violently, and lack a specialized 

apical apparatus or operculum. The ascospores 

are at first hyaline, but later develop yellow to 

dark brown (melanized) thick walls which may 

be spiny or thrown into reticulate, honeycomblike 

folds (Figs. 14.7b, 14.8). Many of the fruit 

bodies have a strong smell and flavour, and are 

excavated and eaten by animals such as badgers, 

wild boar, mice, moles, shrews, squirrels and 

rabbits (Trappe & Maser, 1977). Hypogeous 

ascocarps (and basidiocarps) form an important 

component of their diet. Spore dispersal is 

brought about in this way and ascospore germination 

is probably enhanced by passage through 

the gut of the mammal. Several different volatile 

chemical substances have been detected from 

truffle fruit bodies, but the most common 

and abundant is dimethyl sulphide, attractive 

to ‘truffle flies’ (Suillia spp.) which lay their eggs 

on the ascocarps (Pacioni et al., 1990, 1991). 

Similar substances are emitted by stinkhorns 

(Phallus spp.), which likewise attract flies (see 

p. 590). Claus et al. (1981) have shown that the 

steroid hormone 5a-androst-16-en-3a-ol is also 

produced by Tuber spp. Since this is the main 

sex hormone produced by boars, its presence in 

truffles may account for the enthusiasm and 

efficiency with which sows locate and excavate 

truffles. It is possible that some of the odoriferous 

substances are produced by the activity of 

microbes associated with ascocarp. 

14.7.2 The life cycle of true truffles 

Surprise discoveries may happen even in 

seemingly well-studied life cycles such as those 

of Tuber spp., in which a sympodulosporic conidial 

state somewhat resembling Geniculosporium 

(see Fig. 12.13) has been described recently (Urban 

et al., 2004). It is as yet unclear how frequent 

this state is in nature or among other Tuber 

spp. and which role, if any, it might play in their 

ecology. 

The traditional life cycle of Tuber is based 

solely on sexual reproduction (see Giovannetti 

et al., 1994). The haploid ascospores germinate 

to form hyphae with monokaryotic segments, 

and the mycelium grows towards the roots of 

potential mycorrhizal partners, usually trees, 

but is unable to form mycorrhiza. Anastomosis 

between monokaryotic mycelia derived from 

different ascospores results in the formation 

of a dikaryotic mycelium which forms sheathing 

mycorrhiza with suitable hosts (Fasolo- 

Bonfante & Brunel, 1972). Ascocarp development 

is initiated by the aggregation and differentiation 

of hyphae which at this stage remain 

attached to long roots and obtain nutrients 

from the host tree. According to Janex-Favre 

and Parguey-Leduc (2002), in T. melanosporum 

the primordium of the ascocarp consists of an 

ascogonium with its trichogyne, surrounded at 

the base by an envelope of sterile investing 

hyphae. Within the glebal tissues to the inside 

of the primordium, fertile cells develop. At the 

tips of these fertile cells, the two nuclei of the 

dikaryon fuse to give a diploid nucleus. This 

is followed by meiosis and one or more mitoses 

so that the ascospores may be uni- or multinucleate 

(Delmas, 1978). Ultrastructural studies

TUBER (TUBERACEAE) 

425 

Fig14.7 Tubermelanosporum,theblackorPe¤rigord truffle. (a) Two fruit bodies, weighing 60 g (left) and 40 g (right).One has been cut 

open to reveal the black fertile (ascospore-containing) regions interspersed by white (sterile) veins. (b) Ascus containing three 

mature ascospores. 

Fig14.8 (a c) Tuber rufum. (a) Fruit body in surface view and in section showing the veins. (b) Portion of hymenium. (c) Ascus with 

four spiny-walled ascospores. (d,e) Tuber puberulum. (d) V.S. ascocarp showing the structure of the peridium and developing asci. 

(e) Mature four-spored ascus showing ascospores with reticulate walls.


have shown that ascosporogenesis resembles 

that found in most other Euascomycetes, but 

instead of being delimited by the invagination of 

an ascus vesicle the ascospores become delimited 

individually by vesicles formed by material 

derived from lomasomes or from invaginations 

of the ascus plasma membrane (Berta & Fusconi, 

1983). 

At first, the developing ascocarp is attached 

by hyphal connections to a host tree, i.e. it grows 

symbiotically. Eventually it breaks free and 

continues to develop independently during a 

saprotrophic phase of growth. In T. melanosporum, 

tufts of hyphae extend into the surrounding soil 

from the pyramidal scales on the outside of 

the peridium. Application of radioactive tracers 

(e.g. 

32 PO 4 , 

3 H 2 O and 14 C-labelled mannose) to 

these hyphae is rapidly followed by the appearance 

of radioactive material in the inner portions 

of the gleba and especially in the fertile 

veins (i.e. the dark regions of the ascocarp 

interior; see Fig. 14.7a) at rates and in patterns 

which could not be accounted for by simple diffusion 

(Barry et al., 1994, 1995). This finding 

and reports that fruit bodies of truffles may be 

found a considerable distance away from living 

tree roots suggest that mature ascocarps may 

be autonomous and can obtain water and nutrients 

directly from the soil, from decaying 

roots and faecal deposits from the soil fauna 

(Callot, 1999). 

The species of Tuber which have been investigated 

have a wide mycorrhizal host range, 

including Angiosperms and some Gymnosperms. 

The host ranges of four species of Tuber are 

shown in Table 14.2. 

14.7.3 Truffle collecting 

The truffles of greatest commercial value are 

Tuber melanosporum (the black truffle of Périgord) 

and T. magnatum (the white truffle of Piedmont), 

which can command prices of up to E2000 kg 1 

in Continental Europe. Several other species 

are also traded. The only common British truffle 

which can be used for culinary purposes is 

T. aestivum. Périgord and Piedmont truffles are 

most abundant in Southern Europe (France, 

Spain and Italy) within latitudes 40° and 50° 

North in well-drained calcareous soils (Callot, 

1999). Both are collected with the aid of pigs 

and dogs trained to detect them by smell. 

The Périgord truffle can also be detected by 

the presence of a ‘burnt’ ring-like zone (brûlé) 

Table14.2. Host species relationships of four species of Tuber. The main hosts are indicated by black symbols. 

Marks in brackets indicate the formation of mycorrhiza with some, but not all members of the host genus 

tested. Data summarized from Giovannetti et al. (1994). 

Tubermagnatum T.melanosporum T.aestivumgroup T. albidum group 

Alnus cordata 

Carpinus betulus 

Castanea sativa 

Cistus (2 spp.) 

Corylus avellana 

Fagus sylvatica 

Ostrya carpinifolia 

Populus (2 spp.) 

Quercus (6 spp.) () 

Salix (2 spp.) 

Tilia (3 spp.) 

Abies alba 

Cedrus (2 spp.) 

Pinus (7 spp.) () () ()

MORCHELLA (MORCHELLACEAE) 

427 

surrounding a tree with roots with mycorrhizal 

connections, in which associated herbaceous 

plants are wilting or dead. This is partly due 

to deleterious volatile metabolites from the 

Tuber mycelium (Pacioni, 1991) and possibly 

also to parasitic attack by the mycelium on 

roots of herbs. The Périgord truffle is associated 

in the wild with the roots of oaks (Quercus spp.) 

in France. Truffles are cultivated there in 

plantations (truffières) of appropriate species 

of oak or on hazel (Corylus avellana). Clonal 

material of suitable hazel cultivars may be 

used to ensure greater yield and uniformity of 

cropping (Mamoun & Olivier, 1996). The seedling 

roots of potential hosts are inoculated by 

dipping them in a suspension of ascospores, or 

seedlings can be naturally infected by growing 

them close to mature mycorrhizal trees where 

infection occurs by mycelial contact. Despite 

this, truffle yields have fallen continuously, with 

about 1000 tons harvested annually in France 

around the year 1900 but less than one-tenth 

of that yield collected 100 years later (Hall et al., 

2003). A method to cultivate truffles on a large 

scale under axenic conditions would be a 

marvellous achievement, but this is not yet 

in sight. 

The literature on truffles, stimulated by 

their gourmet and high commercial value, is 

enormous. Guides to identification have been 

provided by Gross (1987), Pegler et al. (1993), 

Riousset et al. (2001), and a computer-based 

interactive key by Zambonelli et al. (2000). More 

general accounts of truffle biology and cultivation 

have been written by Delmas (1978), Hall 

et al. (1994) and Callot (1999). 

The ‘desert truffles’, Terfezia spp., are not 

closely related to Tuber but may instead have 

an affinity with the Pezizaceae (Percudani et al., 

1999). Terfezia occurs as a mycorrhizal associate 

of shrubs in arid regions of Southern Europe 

and the Middle East, where it is consumed as 

food and traded on markets. The association 

of Terfezia with the roots of shrubs such as 

Helianthemum almeriense can greatly improve the 

ability of the plant to withstand drought stress 

and may play an important role in mediterranean 

ecosystems (Morte et al., 2000). 

14.8 Morchella (Morchellaceae) 

The fruit bodies of Morchella spp., the true morels, 

are among the most popular and highly prized 

edible fungi (Plate 6g). They appear for a few 

weeks in spring in cold-temperate regions soon 

after snow-melt as the soil becomes warmer and 

drier, but they are not confined to such areas. 

Morchella spp. have two ecological strategies; as 

saprotrophic ruderals, fruiting for a relatively 

short period (a few years) on disturbed or burnt 

ground, or in mycorrhizal association with tree 

roots, fruiting over a longer period. The validity 

of the alternative lifestyles has been confirmed 

by comparative analyses of the isotopes 15 N and 

13 C, showing some populations to be saprotrophs 

whilst others are mycorrhizal (Hobbie et al., 

2001). Opinions on taxonomy vary, with some 

authors recognizing about 50 species and others 

as few as 3 5 species showing wide phenotypic 

variation. Three broad groups of species 

have been distinguished, i.e. the half-free morel 

(M. semilibera), the black morels (M. elata, M. conica 

and M. angusticeps), and the common or yellow 

morels (M. esculenta, M. crassipes and M. deliciosa). 

Molecular analysis indicates that the black 

morels and yellow morels are separate taxonomic 

groups (Bunyard et al., 1995; Gessner, 

1995). The ascoma of a Morchella consists of 

a hollow stipe and a fertile cap thrown into 

shallow cup-like depressions or alveoli. The 

alveoli are lined by asci and paraphyses but 

the ridges or ribs which separate the alveoli are 

sterile, containing only paraphyses (Janex-Favre 

et al., 1998). 

The cylindrical, unitunicate, operculate asci 

contain eight unicellular ascospores. Karyogamy 

occurs prior to ascus formation, but croziers 

are apparently absent. Following meiosis in 

the ascus, there are four successive mitoses so 

that the ascospores are multinucleate (Volk & 

Leonard, 1990). The tips of the asci are phototropic 

and are directed towards the opening 

of the alveolus. The ascospores are often discharged 

simultaneously by puffing, generating 

air currents which carry clouds of spores well 

away from the fruit body (Buller, 1934). They


germinate soon after discharge to form a septate 

mycelium with multinucleate segments. Frequent 

anastomosis may result in the formation 

of heterokaryons. Later in the season sclerotia 

develop, and it is in this form that the fungus 

survives the winter. Ascospores themselves do 

not remain viable in the soil for very long 

(Schmidt, 1983). The mycelium may also develop 

‘muffs’ around the roots of various hosts, mostly 

young trees, and within such muffs the mycelium 

may penetrate as far as the phloem, an 

association which is probably non-mycorrhizal 

(Buscot & Roux, 1987; Buscot, 1989). However, 

in association with spruce (Picea abies) rootlets 

already infected with basidiomycetous mycorrhizal 

fungi, the mycelium of Morchella is weakly 

mycorrhizal, forming a Hartig net of intercellular 

mycelium around one layer of cortical cells of 

the host (Buscot & Kottke, 1990). Several morphologically 

distinctive types of such secondary 

ectomycorrhiza have been observed, often in 

association with endobacteria which invade 

the hyphae of M. elata making up the Hartig 

net and also the host plant cells (Buscot, 1994). 

Pure culture synthesis of sheathing mycorrhizae 

between Morchella spp. and four species of 

Pinaceae has been reported (Dahlstrom et al., 

2000). 

The mating system of Morchella is not fully 

understood, and it is as yet uncertain whether 

it is homo- or heterothallic. A conidial state, 

Costantinella cristata, has been reported to develop 

following ascospore germination of M. esculenta. 

The conidiogenous cells (phialides?) are formed 

in verticils arising from lateral branches of the 

erect conidiophores. They give rise to minute 

spherical conidia which do not germinate readily 

(Costantin, 1936). Possibly they function as spermatia. 

When certain mycelial isolates derived 

from single ascospores are confronted in pure 

culture, a barrage phenomenon occurs (Hervey 

et al., 1978), and this may be due to heterokaryon 

incompatibility (Volk & Leonard, 1989). The 

assumption that sexual reproduction occurs, in 

the sense that different parental genomes are 

involved in ascocarp formation, is supported 

by electrophoretic data confirming that allelic 

variation exists in natural populations. It is also 

possible that the fertilization events leading to 

the production of different asci within one fruit 

body may involve several individuals (Gessner 

et al., 1987). 

The possibility of cultivating morel ascocarps 

commercially is being explored and patents 

have been taken out to protect the techniques 

involved. They are based on the observations by 

Ower (1982) that sclerotial development followed 

by ascocarp differentiation can be encouraged 

by growth of the mycelium on sterilized wheat 

grain.

15 

Hymenoascomycetes: Helotiales (inoperculate 

discomycetes) 


In contrast to the Pezizales (see preceding 

chapter) which produce apothecia with asci discharging 

their spores through a detachable lid at 

their apex, the asci of inoperculate discomycetes 

liberate their spores either through a valve or 

a slit. In the inoperculate as well as operculate 

discomycetes, the asci may contain two or more 

layers, i.e. they are often described as bitunicate. 

However, these layers do not separate during 

ascus discharge, i.e. they are non-fissitunicate. 

Fine structural details of the asci of Helotiales 

have been described by Verkley (1993, 1994, 

1996). Two large ecological groups of inoperculate 

discomycetes can be distinguished: the 

lichenized and non-lichenized species. This feature 

correlates approximately with the taxonomy 

at the level of orders, and here we shall 

discuss the Helotiales (sometimes alternatively 

called Leotiales) which contain mostly 

non-lichenized fungi. The Lecanorales and other 

orders with mainly or exclusively lichen-forming 

fungi are described in Chapter 16. 

Those relatively few phylogenetic studies that 

have so far been performed on the Helotiales 

lack the necessary power of resolution to delimit 

natural groups. Thus, it is not clear at present 

whether this order is monophyletic or not, 

and several different classification schemes are 

in use (Gernandt et al., 2001; Kirk et al., 2001; 

Pfister & Kimbrough, 2001). The families 

currently associated with the Helotiales are 

listed in Table 15.1. Thus circumscribed, the 

order Helotiales contains some 2300 species. 

The Orbiliaceae, formerly included here (Pfister, 

1997), are now considered to be more closely 

related to the Pezizales. Since the conidial forms 

of some of them are of interest as nematodetrapping 

and aquatic fungi, they will be considered 

in Chapter 25. 

Fungi belonging to the Helotiales have 

adapted to several different ecological situations. 

Many species are necrotrophic, hemibiotrophic or 

biotrophic plant pathogens, and some can cause 

considerable damage in economically important 

crops. Other species are saprotrophic, colonizing 

dead leaves and shoots of herbaceous and woody 

plants. Endophytic species are also known, and 

it would not be too surprising if many of the 

inoperculate discomycetes known as saprotrophs 

were found to be already present in the living 

plant as endophytes. Some species fruit on plant 

debris submerged in freshwater streams and have 

adapted to this habitat by producing conidia of 

unusual shapes (Chapter 25). Other species form 

ericoid mycorrhizal associations with the roots of 

Ericaceae (p. 442). The Thelebolaceae are a group 

of coprophilous species. 

15.2 Sclerotiniaceae 

The Sclerotiniaceae and Rutstroemiaceae are 

closely related but can be separated by

430 HYMENOASCOMYCETES: HELOTIALES (INOPERCULATE DISCOMYCETES) 

Table 15.1. The families currently placed in or near the Helotiales. Data from Gernandt et al. (2001), Kirk et al. 

(2001) and Pfister and Kimbrough (2001). Three families printed in bold are considered in more detail in 

this chapter. 

Family No. of species Examples 

Ascocorticiaceae 3 

Bulgariaceae 1 Bulgaria inquinans 

Cudoniaceae 10 

Cyttariaceae 11 Cyttaria 

Dermateaceae (p. 439) 385 Mollisia, Pyrenopeziza, Rhynchosporium,Tapesia 

Geoglossaceae 48 Geoglossum,Trichoglossum 

Helotiaceae 623 Ascocoryne, Hymenoscyphus, Neobulgaria 

Hemiphacidiaceae 12 

Hyaloscyphaceae 541 Hyaloscypha, Lachnum (¼ Dasyscyphus) 

Leotiaceae 13 Leotia 

Loramycetaceae 2 

Phacidiaceae 3 Phacidium 

Rhytismataceae (p. 440) 219 Rhytisma 

Rutstroemiaceae 100 Rutstroemia 

Sclerotiniaceae (p. 429) 124 Sclerotinia 

Thelebolaceae 15 Thelebolus 

Vibrisseaceae 14 

DNA-based phylogenetic analyses (Holst-Jensen 

et al., 1997). Members of both families produce 

stalked apothecia which grow from stromata 

located within the colonized host plant tissue. 

The apothecia usually develop in spring from 

overwintered stromata. The stroma is a food 

storage organ and is usually differentiated into 

two parts, a rind (cortex) of dark, thick-walled 

cells and a medulla of hyaline cells. Two generalized 

types of stroma have been distinguished. 

To quote from Whetzel (1945), 

The sclerotial stroma (commonly called the 

sclerotium) has a more or less characteristic form 

and a strictly hyphal structure under the natural 

conditions of its development. While elements of the 

substrate may be embedded in its medulla, they 

occur there only incidentally and do not constitute 

part of the reserve food supply. The substratal 

stroma is of a diffuse or indefinite form, its medulla 

being composed of a loose hyphal weft or network 

permeating and preserving as a food supply a 

portion of the suscept or other substrate (e.g. culture 

media). 

It is now clear that the sclerotial stroma is typical 

of the Sclerotiniaceae where it is often 

conspicuous (Plates 7a,b). Fungi belonging to 

the Rutstroemiaceae (Plate 7c) produce the less 

obvious substratal stroma. The Rutstroemiaceae 

grow mainly as saprotrophs, but the Sclerotiniaceae 

include some important plant-pathogenic 

species. We shall only consider the latter family 

further because much more is known about it. 

Various types of macroconidia with or without 

accompanying microconidia are formed within 

the genus Sclerotinia in its widest sense, and species 

with different types of conidia are regarded 

by many mycologists as belonging to distinct 

genera. Since these are very closely related, 

Sclerotinia is a good example to illustrate the flexibility 

of asexual reproduction in fungi (Weber & 

Webster, 2003). For instance, Sclerotinia fuckeliana 

has Botrytis cinerea with polyblastic conidia as its 

asexual state (Figs. 15.5a,b) and is thus currently 

called Botryotinia fuckeliana. It also produces microconidia 

from clustered phialides (Fig. 15.5c). 

Sclerotinia (Monilinia) fructigena produces Moniliatype 

blastoconidia in chains (Fig. 15.3b) and lacks 

a microconidial state, whereas S. (Myriosclerotinia) 

curreyana produces only Myrioconium-like microconidia 

(Figs. 15.1d f) but has no macroconidial

SCLEROTINIACEAE 

431 

Fig15.1 Sclerotinia 

curreyana.(a)T.S. 

sclerotium. Note the 

stellate pith cells of 

the host, Juncus effusus. 

(b) T.S. sclerotium 

showing 

an ascogonium. 

(c) Ascus and 

ascospores. 

(d) Microconidia in 

culture. (e) T.S. 

spermodochidium on 

Juncus effusus.Note 

the cavity lined by 

phialides. 

(f) Microconidia 

from host. 

state. All of these species can produce apothecia. 

This is also true of Sclerotinia sclerotiorum, which 

is considered to represent Sclerotinia sensu stricto 

(Kohn, 1979). Sclerotium cepivorum produces neither 

functional conidia nor apothecia, and the 

sclerotia function purely as vegetative propagules, 

germinating by hyphal growth. Microconidia 

are sometimes produced by germinating 

sclerotia, but these do not appear to have any 

function. The relationship of S. cepivorum with the 

Sclerotiniaceae has been deduced from DNAbased 

studies (Carbone & Kohn, 1993). Whereas 

macroconidia generally germinate readily and 

play important roles in the spread of diseases, 

microconidia may or may not germinate and 

are considered to function mainly as spermatia, 

i.e. agents of fertilization in sexual reproduction. 

15.2.1 Sclerotinia curreyana and S. tuberosa 

The apothecia of Sclerotinia (Myriosclerotinia) 

curreyana, a pathogen of the rush Juncus effusus, 

are common in May. They arise from black sclerotia 

in the pith at the base of the Juncus stem 

(Plates 7a,b). Infected stems look paler than 

healthy stems, and by feeling down to the base 

of an infected stem the sclerotium can be felt 

as a swelling between finger and thumb. 

The sclerotium has an outer layer of dark cells 

and a pink interior which includes some of the 

stellate pith cells of the host (Fig. 15.1a; Plate 7a). 

One or several apothecia may grow from a single 

sclerotium. The ascospores are released in late 

spring and infect the new season’s stems. In 

culture, germinated ascospores form a mycelium 

which produces microconidia from small phialides 

(Fig. 15.1d). Similar clusters of microconidia 

can be found on infected Juncus later in 

the season (Fig. 15.1f) where they line cavities 

beneath the epidermis in the upper part of 

infected culms. Whetzel (1946) has used the 

term spermodochidium for these microconidial 

fructifications (Fig. 15.1e). It is probable that 

microconidia play a role in fertilization. 

The apothecia of S. (Dumontinia) tuberosa 

(Fig. 15.2) are about 2 cm in diameter and arise 

from sclerotia within rhizomes of Anemone 

nemorosa (Pepin, 1980). They may also occur on 

garden Anemone where they are associated with 

black rot disease. Microconidia are formed in 

culture. Electron microscopy studies of the ascus 

wall show that it has a two-layered wall, but the 

two layers do not separate from each other, 

i.e. the ascus is non-fissitunicate. The ascus apex 

contains a thickened dome of wall material with 

a central canal. As the ascus explodes, the apical 

apparatus is everted (Verkley, 1993).


Fig15.2 Apothecia of Sclerotinia tuberosa rising from 

subterranean sclerotia formed on rhizomes of Anemone 

nemorosa. 

15.2.2 Monilinia fructigena and M. laxa 

Monilinia fructigena is the cause of a brown fruit 

rot of apples, pears, plums and other stone fruits 

(Byrde & Willetts, 1977). Although the apothecial 

state is only rarely formed, the disease is 

common and is transmitted by means of conidia. 

Apples and pears showing brown rot bear buffcoloured 

pustules of conidia often in concentric 

zones (Fig. 15.3a). Sporulation is stimulated by 

light, and adjacent zones correspond to daily 

periods of illumination. The conidia are blastoconidia 

formed in chains which extend in length 

at their apices by budding of the terminal conidium. 

Occasionally more than one bud is formed, 

and this results in branched chains (Fig. 15.3b). 

Conidiogenesis of this type is characteristic 

of the anamorphic genus Monilia. Infection of 

the fruit is commonly through wounds caused 

mechanically or by insects such as codling 

moth, wasps or earwigs (Croxall et al., 1951; 

Xu & Robinson, 2000). Fruits left lying on the 

ground are the source of infection in the following 

season. During the winter, infected fruits 

become mummified, and the shrivelled fruit 

thoroughly colonized by mycelium is interpreted 

as the sclerotium. In the following year the 

sclerotium may produce further conidial pustules. 

Infections can develop as a post-harvest 

disease in stored apples, and in some varieties 

a twig infection (spur canker) may also occur. 

A similar group of diseases of apple and 

plum is caused by Monilinia laxa which also has 

a Monilia conidial state. In addition to fruit rot, 

this species causes blossom and shoot blight, 

in which infected fresh shoots wilt and become 

coated by conidial pustules. Monilinia fructicola 

causes brown rot especially of peaches and nectarines 

in North and South America, South Africa, 

Australia and the Far East, but has not been 

reported from Europe. It produces the apothecial 

state more readily than the other species (Holtz 

et al., 1998), and ascospores released from overwintered 

mummified fruits can be a source of 

inoculum in the field (Tate & Wood, 2000). These 

and a fourth species of the brown fruit rot 

complex, M. polystroma, can be distinguished by 

means of morphological features and DNA 

sequences (van Leeuwen et al., 2002). 

15.2.3 Sclerotinia sclerotiorum 

This species causes a range of diseases (Sclerotinia 

rot, white mould, stalk break) in over 400 

cultivated and wild plant species belonging to 

some 75 different families (Boland & Hall, 1994). 

The most important crop plants affected are 

sunflower, soybean and oilseed rape, with crop 

losses approaching 100% under conditions favourable 

to the disease. Sclerotia are formed on 

decaying crop debris and remain viable in a 

dormant state in the soil for many years, especially 

if deep-ploughed. Sclerotia located within 

the top 3 cm of soil germinate to produce hyphae 

or apothecia in spring. Plants can be infected 

either from mycelium or from ascospores; there is 

no macroconidial state. Phialidic microconidia 

are formed and probably serve as spermatia. 

Infection by S. sclerotiorum is often initiated by 

a saprotrophic phase on dead leaves or petals 

during which mycelial biomass is generated, 

prior to the attack on the living plant tissue. 

Above-ground shoots and, to a lesser extent, roots 

can be infected, and infections of living tissues 

are strongly necrotrophic. This necrotrophic 

phase is followed by further saprotrophic 

growth and the formation of sclerotia. The 

infection cycle in S. sclerotiorum is therefore 

tri-phasic. Reviews of the general biology and 

pathology of S. sclerotiorum have been written by


433 

Fig15.3 Monilinia fructigena. (a) Apple showing brown rot caused by this fungus, and bearing conidial pustules.The wound serving 

as entry point is indicated by an arrow. (b) Blastoconidia of the Monilia type. 

Purdy (1979), Hegedus and Rimmer (2005) and 

Bolton et al. (2006). 

Sclerotinia sclerotiorum can infect pollen grains 

of crop plants but can also become genuinely 

seed-borne, surviving systemically in the embryo 

for several years and replacing the rotten tissues 

with mycelium and sclerotia (Tu, 1988). Such 

seed-borne infections are readily eliminated by 

fungicidal seed-dressings, but infections of growing 

crops are less easily controlled. Hence, 

biological control of S. sclerotiorum has been 

attempted. A promising biocontrol agent is the 

pycnidial fungus Coniothyrium minitans which 

infects and parasitizes hyphae and sclerotia of 

S. sclerotiorum in the soil and in plant tissue 

(Tribe, 1957; de Vrije et al., 2001). The ability of 

C. minitans to destroy dormant S. sclerotiorum 

sclerotia in the soil is particularly interesting, as 

it offers a chance to decontaminate infected soil 

on which susceptible crop plants could not 

otherwise be grown for several years. Gerlagh 

et al. (2003) have demonstrated that one or two 

conidia of C. minitans are sufficient to initiate 

infection of a sclerotium. Conidia of C. minitans 

can be spread rapidly by the activity of soil 

invertebrates, including mites (Williams et al., 

1998). These properties have led to the registration 

of C. minitans as a commercial biocontrol 

agent against S. sclerotiorum. Since C. minitans 

colonizing the soil can tolerate many fungicides 

used against S. sclerotiorum, the integrated 

control of Sclerotinia rot is also possible in some 

crops (Budge & Whipps, 2001). 

Oxalic acid and pH regulation 

Like other fungi such as Botrytis cinerea (see 

p. 435) and brown-rot basidiomycetes (p. 527), 

S. sclerotiorum releases large amounts of oxalic 

acid into the infected plant tissue, and this is an 

important pathogenicity factor (Godoy et al., 

1990). Oxalic acid may chelate Ca 2þ ions released 

from cell wall degradation, and it also suppresses 

the host’s hypersensitive response (Cessna et al., 

2000). Most importantly, however, it acidifies the 

infected plant tissue. There is good evidence that 

S. sclerotiorum can sense the pH of its environment, 

and that it can adjust the production rate 

of oxalic acid accordingly. In this way, optimum 

conditions are created for the activity of its 

pectin-degrading enzymes, especially endopolygalacturonases, 

which macerate colonized host 

tissues (Rollins & Dickman, 2001). A transcription 

factor encoded by the pac1 gene seems to be 

involved in regulating the expression of genes 

controlled by external pH (Rollins, 2003). 

Transgenic sunflower or soybean plants 

containing an oxalate oxidase gene from 

cereals show good resistance to infection by 

S. sclerotiorum. This appears to be a promising 

control strategy for the future, but is currently 

still slow in gaining public acceptance (Lu, 2003). 

Conventional resistance breeding is also possible,


although resistance is not usually due to major 

genes and is only partial. The underlying principle 

in runner bean (Phaseolus vulgaris) seems 

to be an enhanced tolerance of oxalic acid or a 

restriction of its diffusion through the infected 

tissue (Tu, 1985). 

Sclerotia 

Sclerotia of S. sclerotiorum form readily in culture 

and have been the subject of investigations into 

the physiology of their development (Willetts & 

Wong, 1980; Willetts & Bullock, 1992). They are 

of the terminal type. General aspects of sclerotial 

development have been summarized on 

pp. 18 21. The regulation of sclerotium formation 

is interesting because it, too, is stimulated 

by acid pH, and the Pac1 transcription factor is 

involved (Rollins, 2003). Another signal known to 

be a trigger of sclerotium development is 

oxidative stress, e.g. lipid peroxidation or irradiation 

with light. Excessive oxidation is prevented 

by the synthesis of antioxidants such as b- 

carotene or ascorbic acid (vitamin C), and if 

high concentrations of these are added to 

cultures of S. sclerotiorum, sclerotium formation 

is inhibited (Georgiou & Petropoulou, 2001; 

Georgiou et al., 2001). 

15.2.4 Sclerotium cepivorum 

This fungus causes white rot, the most serious 

disease, of Allium spp., especially onions and 

garlic. Sclerotia germinate by emitting hyphae 

which grow towards the roots of the host plant 

and cause necrotrophic infections with maceration 

of the root and bulb base tissue. Large 

quantities of various pectinolytic enzymes are 

secreted (Metcalf & Wilson, 1999). New sclerotia 

are formed on and in the decaying bulb tissues. 

Sclerotia of S. cepivorum can survive in the soil for 

many years or even decades (Coley-Smith, 1959), 

and as little as one sclerotium per kg of soil can 

cause serious disease losses (Crowe et al., 1980). 

Apart from soil fumigation, no effective treatment 

of infections or contaminated soil is 

available (but see below), and fields may need to 

be abandoned for Allium cultivation once 

S. cepivorum has become established. 

The root exudates of Allium spp. have long 

been known to trigger germination of sclerotia 

of S. cepivorum. Substances such as alkyl-cysteine 

sulphoxides are themselves inactive but are 

probably metabolized by soil microbes to release 

volatile compounds which act as the stimulants 

(Coley-Smith & King, 1969; King & Coley-Smith, 

1969). One such substance, which is also produced 

directly by Allium spp., is diallyl disulphide 

(Storsberg et al., 2003). If this is sprayed onto an 

infested field, it will trigger the germination of 

sclerotia which is followed by their death if no 

host plants are present. This idea seems to hold 

potential for the control of S. cepivorum (Coley- 

Smith, 1986; Coley-Smith & Parfitt, 1986). Garlic 

powder worked into the soil seems to have 

similar effects, most probably because of the 

release of volatile substances from the nonvolatile 

water-soluble alkyl cysteine sulphonates, 

catalysed by soil bacteria (Fig. 15.4). Biological 

control using Trichoderma spp., which secrete 

chitinases capable of lysing hyphae 

of S. cepivorum, may also be possible (Metcalf & 

Wilson, 2001). 

15.2.5 The life cycle of Botryotinia 

(Sclerotinia) fuckeliana,anamorph 

Botrytis cinerea 

Because the apothecia of B. fuckeliana are not 

commonly seen, the fungus is better known 

by its macroconidial state, Botrytis cinerea. This 

is ubiquitous on all kinds of moribund plant 

material and is also associated with a wide range 

of diseases often referred to as grey mould. 

The name Botrytis cinerea is now known to be a 

collective name used to describe a number of 

closely similar, but genetically distinct, strains 

(Giraud et al., 1999; Beever & Weeds, 2004). For 

this reason some authors prefer to write of 

a Botrytis of the cinerea type. In-depth treatments 

of the biology of Botrytis cinerea have been 

compiled by Coley-Smith et al. (1980) and Elad 

et al. (2004). In addition to B. cinerea, there are 

some 20 other Botrytis spp. causing diseases on 

a wide range of host plants (Staats et al., 2005). 

Macroconidia of B. cinerea are formed on 

infected host tissue from dark-coloured branched 

conidiophores. The tips of the branches are


435 

Fig15.4 Non-volatile water-soluble 

Allium metabolites (left) and their 

volatile breakdown products (right). 

S-Methyl-L-cysteine sulphoxide (methiin) 

is common in many plants, and its 

sulphide breakdown products do not 

trigger sclerotium germination in 

Sclerotium cepivorum. Alliin 

(S-2-propenyl-L-cysteine sulphoxide 

¼ S-allyl-L-cysteine sulphoxide), isoalliin 

and propiin are typical of members of 

the genus Allium.Their volatilebreakdown 

products, especially mercaptans, 

sulphides and disulphides, are potent 

triggers of sclerotium germination. 

Diallyl disulphide is the major flavour 

component of garlic. 

thin-walled and bud out to form numerous 

elliptical multinucleate conidia which are 

blastospores (Hughes, 1953). These are easily 

detached by the wind, or are thrown off as 

the conidiophores twist hygroscopically 

(Figs. 15.5a,b). Conidia can also be dispersed by 

the fruitfly Drosophila melanogaster (Louis et al., 

1996) and other insect vectors. Uninucleate 

microconidia are formed by clusters of phialides 

which arise directly from the mycelium (Weber & 

Webster, 2003) or from germinating macroconidia 

(Fig. 15.5c). The microconidia have been 

claimed to be capable of germination (Brierley, 

1918) but do not do so in our experience. They 

are probably mainly involved in sexual reproduction, 

i.e. they function as spermatia. Sclerotia 

are formed at the surface of infected tissues and 

the fungus overwinters in this form. In spring 

the sclerotia may develop to give rise to tufts 

of macroconidia or, much less commonly, to 

apothecia. One or several stalked apothecia may 

arise from one sclerotium, with the stalk 1 cm 

or more in length and the apothecial disc a few 

millimeters in diameter. Botryotinia fuckeliana is 

heterothallic with a bipolar mating system. In a 

single-ascospore culture, macroconidia, microconidia 

and sclerotia can be formed on the same 

agar plate (Weber & Webster, 2003), but apothecia 

never develop. However, apothecia will form 

if microconidia of one mating type are applied 

to sclerotia of the opposite mating type (Faretra 

et al., 1988). Like the great majority of ascomycetes 

(Bistis, 1998), B. fuckeliana therefore shows 

physiological heterothallism. The life cycle of 

this fungus is summarized in Fig. 15.6. 

15.2.6 Other life cycles in Sclerotinia 

A deviation from the typical ascomycete life 

cycle of B. cinerea (Fig. 15.6) is found in Sclerotinia 

(Stromatinia) narcissi (Drayton & Groves, 1952). 

Of the eight spores formed in the asci of this 

fungus, four germinate to produce mycelia


Fig15.5 Botrytiscinerea. (a) Conidiophores developing from a 

sclerotium. (b) Apex of conidiophore showing origin of conidia 

as blastospores. (c) Conidium germinating to produce phialides 

and microconidia (after Brierley,1918). 

bearing microconidia but no sclerotia, whilst the 

other four produce mycelia bearing sclerotial 

stromata. Apothecia develop on the strains forming 

sclerotia if microconidia are transferred to 

them. Thus the mating behaviour of S. narcissi 

differs from that of B. fuckeliana and we can say 

that S. narcissi is sexually dimorphic. This type of 

behaviour is not common in ascomycetes and it 

is possible that such an incompatibility system 

has been derived from the more usual system 

exemplified by B. fuckeliana by aberrations which 

prevent the normal sequence of development of 

sexual organs in basically hermaphrodite forms 

(Raper, 1959). 

A somewhat related phenomenon is found 

in Sclerotinia trifoliorum, in which each ascus 

contains ascospores of two different sizes. The 

four large ascospores germinate to give rise to 

homothallic (self-fertile) mycelia, whereas the 

four smaller ascospores produce self-sterile 

mycelia (Uhm & Fujii, 1983a,b). As discussed earlier 

in detail for Saccharomyces cerevisiae (see 

Fig. 10.5), the two mating type alleles of ascomycetes 

differ strongly in the genes they encode 

and are thus termed idiomorphs. Although no 

detailed studies seem to have been carried out 

on the Sclerotiniaceae, in other filamentous 

ascomycetes such as Pyrenopeziza brassicae (see 

p. 439), heterothallic strains carry either one or 

the other of the two idiomorphs whereas in 

homothallic species both are fused together 

and expressed simultaneously. In Sclerotinia 

trifoliorum, the formation of small ascospores 

may be preceded by a unidirectional switch from 

homothallic to heterothallic, i.e. the deletion of 

one of the two mating types during meiosis 

(Harrington & McNew, 1997). 

Yet another kind of mating behaviour is seen 

in Sclerotinia sclerotiorum, which is homothallic. 

A single ascospore culture produces microconidia 

and sclerotia which bear ascogonial coils 

beneath the rind. The transfer of microconidia to 

the sclerotia on the same mycelium results in 

the formation of apothecia (Drayton & Groves, 

1952). A similar process of self-fertilization also 

occurs in Sclerotinia (Botryotinia) porri. 

15.2.7 Pathogenicity of Botrytis cinerea 

Botrytis cinerea is pathogenic on over 200 species 

of plants. Serious diseases of crops are grey 

mould of lettuce, tomato, strawberry and raspberry, 

die-back of gooseberry and damping-off 

of conifer seedlings. A special case is bunch rot 

of grapes. Under normal circumstances, infected 

grapes shrivel and ultimately fall to the ground, 

forming mummies in which the fungus can 

survive the winter. Mummies give rise to 

infective macroconidia in the following spring. 

This type of bunch rot causes serious 

crop losses in both white and red grapes. 

Under certain circumstances and with certain 

grape varieties, however, Botrytis causes the 

‘noble rot’ in which infections take a milder 

course and allow the grape to dry out gently, 

concentrating its sugar and flavours in the process. 

The resulting wine is much sweeter and 

richer than normal table wine and is consumed


437 

Fig15.6 Life cycle of Botryotinia fuckeliana (anamorph Botrytis cinerea).Innature,thisfungusoverwintersbymeansofsclerotia 

which may germinate in either of two ways.Conidiogenic germination gives rise to the macroconidial state which can be formed also 

from mycelium.The blastic macroconidia are multinucleate, as are mycelial segments. Phialidic microconidia are formed from 

vegetative mycelium or from macroconidia.They are uninucleate, serving mainly as fertilizing agents for sclerotia of opposite mating 

type.Fertilization leads to carpogenic germination of a sclerotium, i.e. to the formation of apothecia, resulting in eight uninucleate 

ascospores of either of two mating types.The diploid state is confined to the tip of the ascogenous hypha (not shown; see Fig. 8.10). 

Open and closed circles represent haploid nuclei of opposite mating type. Key events in the life cycle are plasmogamy (P), 



as a dessert wine. Probably the most famous 

example is produced in the Sauternes region of 

France, using the thin-skinned Sémillon grape 

which is particularly susceptible to B. cinerea. 

Botrytis cinerea can kill its host’s tissue 

rapidly and then carries on growing on the 

dead remains. It is thus a classical necrotrophic 

pathogen. Several research groups have examined 

factors which may be involved in the 

pathogenicity of B. cinerea, but it is as yet 

impossible to say which ones are the most 

important. Quite possibly B. cinerea employs 

different strategies for the colonization and 

killing of different hosts. This subject has been 

reviewed by Prins et al. (2000) and Kars and van 

Kan (2004) and is summarized below. 

Attachment 

Macroconidia of B. cinerea have a hydrophobic 

surface, but this is apparently not due to the 

presence of hydrophobin-type proteins (Doss et al., 

1997). Initial attachment of the macroconidium 

to the host surface is by weak hydrophobic interactions. 

When the germ tube emerges, it secretes 

a polysaccharide-based matrix which acts as 

a much stronger glue (Doss et al., 1995). This 

polysaccharide may be the same as cinerean, a 

b-(1,3)-glucan with frequent b-(1,6) cross-linkages 

which is produced by B. cinerea from excess 

glucose in liquid culture and in infected grapes 

(Dubourdieu et al., 1978b; Monschau et al., 1997). 

When free glucose becomes scarce, cinerean is 

hydrolysed again by extracellular glucanases 

(Stahmann et al., 1993). On the plant surface, 

the glucan matrix may thus serve in attachment, 

as an external carbohydrate reservoir, and as 

a matrix for hydrolytic enzymes (Doss, 1999). 

Lytic enzymes 

After a short period of growth, the germ 

tube terminates in a slightly swollen infection 

structure which may be considered a rudimentary 

appressorium. This is non-melanized, and 

thus penetration of the cuticle is probably 

mediated mainly by lytic enzymes rather than 

turgor pressure (see pp. 381 and 395). 

Cutin-degrading enzymes are secreted by 

B. cinerea during the initial infection stages 

(Comménil et al., 1998), and proteases may also 

play a role in pathogenesis (Movahedi & Heale, 

1990). Later, a battery of cell wall-degrading 

enzymes (especially pectinolytic enzymes) is 

produced during the colonization of the host 

tissue beyond the initial necrotic lesion. Pectin 

seems to be a major carbohydrate source for 

B. cinerea (Prins et al., 2000). The degradation of 

pectin from the middle lamella may also be a 

contributing factor to host cell death (Tribe, 1955) 

and causes rapid and widespread maceration 

of host tissue (Kapat et al., 1998; Kars & van Kan, 

2004), which is typical of the necrotrophic 

appearance of B. cinerea infections. Oxalic acid is 

secreted by B. cinerea as it is by many other fungi, 

and its presence is also correlated with tissue 

necrosis. However, rather than acting directly as 

a toxin, it is more likely to enhance the activity 

of the pectinolytic enzymes which have an acidic 

pH optimum, and to chelate Ca 2þ ions (Prins et al., 

2000). Substantial quantities of Ca 2þ ions can 

be released during pectin degradation from the 

carboxylic acid groups of the monomers, galacturonic 

acid, which often form calcium salts. 

Hypersensitive response 

Biotrophic pathogens such as downy or powdery 

mildews or rust fungi fail to infect incompatible 

host plants because these recognize their presence. 

One important mechanism of defence is the 

hypersensitive response (see pp. 115 and 397) in 

which epidermal cells in the vicinity of the 

infection site undergo programmed cell death 

(Mayer et al., 2001). The hypersensitive response is 

accompanied by an ‘oxidative burst’ followed by 

the synthesis of phytoalexins. With biotrophic 

pathogens which require living host cells for 

their nutrition, the hypersensitive response is 

often sufficient to kill the infection unit. If the 

necrotrophic B. cinerea attempts to infect a host 

plant, the hypersensitive response also takes 

place, but it fails to control the infection because 

B. cinerea can exploit the dead cells for nutrition 

and initial growth (Govrin & Levine, 2000). 

The reactive oxygen intermediates (especially 

superoxide and H 2 O 2 ) released during the oxidative 

burst may be detoxified by the enzymes 

superoxide dismutase and catalase, respectively, 

which are secreted by B. cinerea and are probably 

localized in the glucan matrix surrounding 

the infection hypha (Gil-ad et al., 2001).

DERMATEACEAE 

439 

Further, B. cinerea is known to produce laccase 

and other enzymes which can degrade or 

detoxify phytoalexins (Prins et al., 2000). ABC 

transporters capable of excluding phytoalexins 

from the hyphal cytoplasm have also been 

reported from B. cinerea (Schoonbeek et al., 2001; 

see also p. 278). Hence, Govrin and Levine (2000) 

have suggested that the hypersensitive response 

launched by the host actually facilitates, rather 

than represses, infection by B. cinerea. 

Fungicide resistance 

Although biological control strategies against 

B. cinerea are being attempted, especially in the 

greenhouse and in post-harvest storage of certain 

fruit crops, control in agricultural situations 

relies chiefly on the application of fungicides. 

This is especially the case for the control of grey 

mould on grapevines. Botrytis cinerea has developed 

resistance against almost all fungicides in 

current use, and this may be due to several 

factors, e.g. the occurrence of sexual reproduction 

in the field, the existence of at least two 

genetically distinct ‘species’, and the presence 

and spread of transposable genetic elements in 

one of them (Giraud et al., 1999). All of these 

factors enhance the genetic diversity of populations 

of the pathogen, and thus the chances of 

development of fungicide resistance. Mechanisms 

of resistance of B. cinerea to fungicides 

have been discussed by Leroux et al. (2002) and 

seem to involve strategies also described from 

other fungi, i.e. reduced fungicide penetration 

into or enhanced export from the hyphae by 

means of ABC transporters, enzyme-mediated 

detoxification and degradation of fungicides, 

and mutations leading to a reduced binding of 

the fungicide to its modified target protein. 

15.3 Dermateaceae 

This family (385 species) is almost certainly 

polyphyletic and it will take some time and 

numerous further name changes before the 

genera are circumscribed to the phylogeneticists’ 

satisfaction. The species included here produce 

their apothecia directly on the substratum. 

Stromata are absent. The apothecia are small 

(less than 1 mm in diameter) and rather inconspicuous, 

being coloured in grey, brown or black 

tones. The development of apothecia has been 

described by Gilles et al. (2001) for Pyrenopeziza 

brassicae (Fig. 15.7). Apothecia are formed from 

hyphae aggregating into small globular structures 

resembling sclerotia or cleistothecia. Later 

a pore develops at the apex (Fig. 15.7a), and this 

increases in diameter by lateral expansion of the 

basal disc (Fig. 15.7b) Meanwhile the asci mature 

in the hymenium. Ultimately, a flat apothecium 

is formed which possesses a clearly defined 

margin typical of the Dermateaceae (Fig. 15.7c). 

This developmental pattern has been termed 

hemiangiocarpic by Corner (1929). The anamorphs 

of Dermateaceae are variable. One very 

common form (Cadophora) is Phialophora-like, 

i.e. the phialides bear an apical collarette 

(Harrington & McNew, 2003). Other forms do 

not have phialides, and instead long and transversely 

septate conidia are produced more or less 

directly from vegetative hyphae. 

One large genus (Mollisia) is chiefly saprotrophic 

and forms apothecia on dead leaves 

and fallen twigs, as exemplified by the ubiquitous 

Mollisia cinerea which fruits on dead wood 

(Plate 7d). Other members of the family are 

hemibiotrophic plant pathogens causing limited 

lesions on agricultural crops. Pyrenopeziza 

brassicae (anamorph Cylindrosporium concentricum) 

causes light leaf spot on winter oilseed rape 

(Fig. 15.7) whereas Tapesia yallundae (anamorph 

Pseudocercospora herpotrichoides) is the cause of 

eyespot at the base of cereal stems, especially 

winter wheat, and its sister species, T. acuformis, 

causes a similar disease especially on rye. The 

conidial Rhynchosporium secalis is the agent of 

leaf blotch on a range of cereals. All of these 

pathogenic species are phylogenetically closely 

related (Goodwin, 2002). 

15.3.1 Tapesia yallundae and T. acuformis 

Apothecia have been found only recently for 

both Tapesia species (see Lucas et al., 2000) and 

Pyrenopeziza brassicae (see Gilles et al., 2001). They 

have not yet been found for Rhynchosporium 

secalis, although the high genetic diversity of 

field isolates of this species indicates that 

sexual reproduction should occur in nature


Fig15.7 Development of Pyrenopeziza brassicae ascocarps. (a) Immature apothecium,10 days old on oilseed rape.The apical 

pore has just formed. (b) 14-day-old apothecium on oilseed rape.The opening is widening due to the expansion of the basal disc. 

(c) Mature apothecium 46 days after inoculation onto agar. Reprinted from Gilles et al. (2001), with permission from Elsevier. 

Images kindly provided by N. Evans. 

(Salamati et al., 2000). The mating type idiomorphs 

have been characterized for all species 

except Tapesia acuformis (Foster & Fitt, 2004), and 

they are of the usual heterothallic/bipolar type. 

The biology of the two sister species Tapesia 

yallundae on wheat and T. acuformis on rye 

(formerly called T. yallundae W and R pathotypes, 

respectively) is very similar and has been 

reviewed by Fitt et al. (1988) and Lucas et al. 

(2000). Eyespot is a major disease in winter 

cereals growing in cool climates. Infection is 

probably mainly by the needle-shaped conidia 

which are formed on overwintered stubble and 

spread by rain splash. However, ascospores 

released from apothecia (Fig. 15.8a) in early 

spring are also infectious. If a spore lands on 

the coleoptile of a host plant, it germinates and 

produces an aggregate of hyphae termed an 

infection plaque (Fig. 15.8b). Numerous melanized 

appressoria are formed at the interface 

of this structure with the host epidermis, so that 

infection of susceptible hosts occurs at several 

points (Fig. 15.8c). Penetration is probably 

mediated by a combination of turgor pressure 

and hydrolytic enzymes. The typical eyespot 

(Fig. 15.8d) develops as a greyish-brown lesion 

around clusters of infection plaques which may 

be visible as the ‘pupil’ of the eyespot. Detailed 

studies of infection mechanisms have been 

published by Daniels et al. (1991, 1995). The presence 

of eyespots at the haulm bases renders the 

cereal shoots prone to collapsing. Further infections 

can affect the vascular system, resulting 

in poorly developed ‘whiteheads’ containing 

inferior grain. 

Resistance breeding seems to be a promising 

strategy for the control of eyespot in cereals 

(Lucas et al., 2000). Chemical control is also practised, 

but Tapesia spp. have developed resistance 

against several types of fungicide (Leroux & 

Gredt, 1997). 

15.4 Rhytismataceae 

The taxonomy of this family is still in a state of 

flux (Gernandt et al., 2001). It is sometimes given 

ordinal status (Rhytismatales or Phacidiales). 

The apothecia are immersed in host tissue or 

embedded in a flat stroma. Individual apothecia 

become evident when the upper surface breaks 

open to reveal the hymenium. There are 

219 species in this group at present (Kirk et al., 

2001). Most of them are associated with broadleaved 

trees or conifers (Cannon & Minter, 1986; 

Johnston, 1997). Particularly difficult genera

RHYTISMATACEAE 

441 

Fig15.8 Infection biology of Tapesia yallundae (a,c,d) and T. acuformis (b). (a) Production of apothecia on overwintered wheat 

stubble. (b) SEM of infection plaques on a rye leaf. Runner hyphae (arrows) extend from established plaques onto the surrounding 

leaf surface. (c) SEM view of a wheat leaf after removal of an infection plaque. Penetration has occurred at numerous points. 

(d) Eyespot lesions at the stem bases of wheat plants. (a) kindly provided by P. S. Dyer. (b) and (c) reprinted from Daniels et al.(1991) 

with permission from Elsevier; original images of (b d) kindly provided by J. A. Lucas. 

in taxonomic terms are Lophodermium and 

Lophodermiella which cause needlecast diseases 

of Pinus spp. As with many other fungi, there is 

a gradient of interactions within the Rhytismataceae, 

ranging from the purely endophytic way 

of life (Deckert et al., 2001) through saprotrophy 

to severely pathogenic species. Ortiz-García et al. 

(2003) have suggested that at least some 

pathogenic species have evolved from endophytic 

ancestors. 

15.4.1 Rhytisma acerinum 

Rhytisma acerinum is common on the leaves of 

sycamore, Acer pseudoplatanus, forming black 

shiny lesions (tar spots) about 1 2 cm wide 

(Fig. 15.9). The lesions arise from infections by


ascospores released from apothecia on overwintered 

leaves. Lesions become visible to the naked 

eye in June or July, some 2 months after infection, 

as yellowish spots which eventually turn 

black. Sections of the leaf at this stage show 

an extensive mycelium filling the cells of the 

mesophyll, and especially the cells of the upper 

epidermis. Between the epidermal cells, a conidial 

state called Melasmia acerina develops. 

This consists of flask-shaped cavities (spermogonia) 

which give rise to uninucleate curved 

club-shaped conidia (spermatia) measuring about 

6 1 mm (Figs. 15.10a,b). The spermatia are 

exuded from the upper surface of the centre 

of the lesion through ostioles in the spermogonial 

wall. The spermatia do not germinate, even 

on sycamore leaves, and it is believed that they 

play a sexual role (Jones, 1925), although this has 

not yet been proven. Apothecia begin development 

in the portion previously occupied by 

spermogonia, and the hymenium is roofed over 

by several layers of dark cells formed within the 

upper epidermis. The asci complete their development 

on the fallen leaves and are ripe about 

March to April when sycamore leaves of the 

new season unfold. The hymenium is exposed by 

means of cracks in the surface layer of the fungal 

stroma (Fig. 15.9b) and the asci discharge their 

spores, sometimes by puffing. Since the ascospores 

are very large, their discharge can be 

viewed with a dissecting microscope. Although 

the ascospores are only projected to a height of 

about 1 mm above the surface of the stroma, they 

are carried by air currents to leaves several 

metres above the ground. The ascospores are 

needle-shaped and have a mucilaginous epispore 

which is especially well developed at the upper 

end (Fig. 15.10d). This probably helps in attaching 

them to leaves. Infection occurs by penetration 

of the germ tubes through stomata on the 

lower epidermis. 

Rhytisma acerinum is absent from densely 

populated areas, probably because the germination 

of ascospores is inhibited by sulphur 

dioxide. Greenhalgh and Bevan (1978) have 

suggested that the incidence and frequency of 

colonization of sycamore leaves by the tar spot 

fungus can be used as an accurate visual index of 

air pollution, although other interpretations are 

possible, such as the removal of fallen leaves 

from municipal parks or the drier microclimate 

in city centres (Leith & Fowler, 1988). 

15.5 Other representatives of the 

Helotiales 

Many members of the Helotiales are encountered 

during fungus forays because they produce 

Fig15.9 Rhytisma acerinum. (a) Leaf of sycamore (Acer pseudoplatanus) with developing tar spot lesions. (b) Tarspot from an 

overwinteredleaf showing cracking of the surface to reveal the hymenia of the apothecia.The flat central zones indicate areas where 

spermogonia had been formed during the previous summer.

OTHER REPRESENTATIVES OF THE HELOTIALES 

443 

Fig15.10 Rhytisma acerinum. (a) T.S. living leaf of Acer pseudoplatanus in June showing spermogonium. (b) Details of cells forming 

spermatia. (c) T.S. overwintered leaf of Acer showing the opening of lips of the stromatal surface to reveal the apothecial hymenium. 

(d) Asci, paraphyses and ascospores. Note the mucilaginous appendage at the upper end of the ascospore. 

unusually shaped or brightly coloured fruit 

bodies. Good images and keys are given in 

Dennis (1981), Breitenbach and Kränzlin (1984) 

and Hansen and Knudsen (2000). Very little 

is known about Helotiales with small or inconspicuous 

apothecia, such as the Hyaloscyphaceae 

(Plate 7e). 

15.5.1 Geoglossaceae 

Trichoglossum is a representative of the Geoglossaceae 

(earth-tongues) which form club-shaped 

stalked apothecia. Members of this family grow 

saprotrophically on the ground, but sometimes 

also on dead leaves or amongst Sphagnum 

(e.g. Mitrula). An account of the family has been 

given by Nannfeldt (1942). Trichoglossum hirsutum 

has black, somewhat flattened fruit bodies up 

to 8 cm high, and grows in pastures and lawns. 

The ascospores are long, dark and septate, and 

the asci are interspersed by black, thick-walled, 

pointed hymenial setae whose function is not 

known (Fig. 15.11b). The presence of hymenial 

setae separates Trichoglossum from Geoglossum 

which grows in similar habitats. The elongated 

ascospores of Geoglossum and Trichoglossum are 

discharged singly through a minute pore at the 

tip of the ascus. When the ascus is ripe, the 

pore bursts and one ascospore is squeezed into 

it, blocking it. The pressure of the ascus sap 

behind the spore causes the spore to protrude, 

at first slowly. When about half the spore is 

projecting, the spore gathers velocity and is


Fig15.11 Trichoglossum hirsutum. (a) Apothecia. (b) Asci, 

ascospores, paraphyses and a hymenial seta. 

rapidly discharged. Another ascospore immediately 

takes the place of the first spore and the 

process of discharge is continued until all eight 

ascospores have been released in single-file 

(Ingold, 1953). 

15.5.2 Leotiaceae 

Following the separation of the Helotiaceae 

(see below), the Leotiaceae now represent only 

a small group (13 species) of saprotrophic fungi. 

They can be distinguished from the Geoglossaceae 

by their brightly coloured ascocarps 

and hyaline ascospores (Lizoň et al., 1998). 

A well-known example is Leotia lubrica (Plate 7f), 

a species colonizing woodland humus and 

known colloquially as ‘jelly babies’. 

15.5.3 Helotiaceae 

Even after the separation of the Leotiaceae, this 

is still a very large (4600 spp.) and probably 

polyphyletic group. Well-known and widely distributed 

saprotrophic genera are Ascocoryne and 

Neobulgaria which produce gelatinous pinkish 

apothecia on relatively fresh dead wood, or 

Chlorociboria with its bright green apothecia 

(Plate 7g). Chlorociboria spp. stain the colonized 

wood, and this is sometimes used in furniture 

making for ornamental inlays. Bisporella citrina 

(Plate 7h) is another commonly encountered 

species on relatively freshly fallen twigs. 

Some members of the Helotiaceae, 

notably Hymenoscyphus ericae, as well as some 

other ascomycetes belonging to the Plectomycetes 

(e.g. Pseudogymnoascus, Myxotrichum, Oidiodendron; 

see p. 295), can form mycorrhizal 

associations with ericaceous plants such as Erica 

and Vaccinium. This association is called ericoid 

mycorrhiza and has fundamentally different 

properties from the vesicular arbuscular 

(p. 202), ectomycorrhizal (pp. 525 and 581) and 

orchid mycorrhizal types (p. 596). Ericaceous 

plants form numerous small lateral roots called 

hair roots which consist of a narrow vascular 

bundle surrounded by a thin cortex and a thick 

epidermal monolayer. When H. ericae infects 

individual epidermal cells of its host’s hair 

roots, it invaginates the plasmalemma and 

forms hyphal coils which superficially resemble 

those seen in orchid mycorrhiza (see Fig. 21.2). 

Hymenoscyphus ericae is credited with making

OTHER REPRESENTATIVES OF THE HELOTIALES 

445 

nitrogen and phosphorus available to its host 

plants which typically grow in situations characterized 

by poor soils with acid pH. Good 

accounts of ericoid mycorrhiza have been given 

by Read (1996), Smith and Read (1997), Berch et al. 

(2002) and Peterson et al. (2004). 

15.5.4 Bulgariaceae 

Bulgaria inquinans forms gelatinous black apothecia 

on the bark of recently felled trees (Plate 7i), 

especially oak (Quercus), chestnut (Castanea) and 

beech (Fagus). Most unusually, the ripe ascus 

always seems to contain melanized as well as 

hyaline spores (Verkley, 1992). This species is 

cosmopolitan, and it is possible that it 

pre-colonizes the bark of the living tree as an 

endophyte. 

15.5.5 Cyttariaceae 

This family contains some of the most unusual 

and striking members of the Helotiales. 

Cyttaria spp. live biotrophically on the southern 

beech (Nothofagus). Orange-coloured apothecial 

stromata which can attain the size of golf balls 

arise singly or in clusters from galls on living 

tree branches (Plate 7j). Each of the dimples at 

the surface of the stroma represents a single 

apothecium. The ascospores are dark grey to 

black and continue to be discharged in great 

numbers even after several days of storage of 

detached stromata in dry conditions. Cyttaria spp. 

occur wherever Nothofagus grows, especially in 

South America, Australia and New Zealand. The 

fruit bodies of some species are edible (Minter 

et al., 1987). A review of this enigmatic family of 

fungi has been given by Gamundí (1991).

16 

Lichenized fungi (chiefly Hymenoascomycetes: 

Lecanorales) 


The dual nature of lichens was first hinted at 

by de Bary (1866) and clearly recognized by 

Schwendener (1867). A lichen is now defined as 

a ‘self-supporting association of a fungus (mycobiont) 

and a green alga or cyanobacterium 

(photobiont)’ (Kirk et al., 2001), ‘resulting in a 

stable thallus of specific structure’ (Ahmadjian, 

1993). The fungal partner usually contributes 

most of the biomass to this symbiosis, including 

the external surface. It is thus termed the 

exhabitant, whereas the unicellular or filamentous 

photobiont cells are collectively called the 

inhabitant because they are located inside 

the lichen thallus (see Ahmadjian, 1993). Most 

lichens have a characteristic appearance which 

permits their identification if suitable keys are 

available (e.g. Purvis et al., 1992; Wirth, 1995a,b; 

Brodo et al., 2001). Since the structure of lichens 

is almost entirely due to the fungal partner, 

lichen taxonomy is synonymous with the taxonomy 

of the mycobiont. 

It is possible to grow the algal and fungal 

partners of many lichens separately in pure culture 

(Ahmadjian, 1993; Crittenden et al., 1995). 

Whereas most photobionts multiply readily in 

pure culture, the fungal partner, if it grows at 

all, typically shows slow growth as a sterile 

leathery mycelium but does not produce the 

characteristic lichen thallus. This is in marked 

contrast to the natural thallus where the 

mycobiont displays its full sexual and asexual 

cycle, whereas the photobiont cells often appear 

swollen and are arrested in their cell cycle, i.e. 

their cell division is controlled by the mycobiont. 

The nature of the morphogenetic signals 

exchanged between the symbiotic partners is as 

yet unknown (Honegger, 2001). 

Some 13 500 species of lichenized fungi have 

been described to date. Since lichens are often 

conspicuous and have been relatively well 

researched over the past 200 years, this number 

is not far below the estimated worldwide total of 

some 18 000 species (Sipman & Aptroot, 2001). 

In contrast, only about 100 species (40 genera) of 

photobionts are known, although this number 

may rise because photobionts are rarely formally 

and fully identified by lichenologists. The most 

common photobiont genera are the green algae 

Trebouxia (found in about 50% of all lichens) 

and Trentepohlia, and the cyanobacterium Nostoc. 

About 85% of lichenized fungi have a green algal 

photobiont, and 10% are associated with a cyanobacterium. 

The remaining lichens contain both 

a green alga and a cyanobacterium (Honegger, 

2001). Most lichenized fungi (498%) belong to 

the Euascomycetes, with only a few imperfect 

fungi and some 20 species of Basidiomycota also 

entering this type of symbiosis. 

Because of their ability to tolerate repeated 

cycles of drying and rehydration and to survive 

extreme temperatures, high solar irradiation 

and other adverse conditions, lichens can colonize 

a range of terrestrial habitats not accessible

GENERAL ASPECTS OF LICHEN BIOLOGY 

447 

to higher plants. Lichens are classical pioneer 

organisms, e.g. on bare rocks or infertile soils. 

Lichens can cause the weathering of rocks by 

secreting oxalic acid which reacts chemically 

with the rock surface; the rate of degradation 

may be 0.5 3.0 mm century 1 (Hale, 1983). Dirina 

massiliensis f. sorediata has been shown to cause 

much more rapid weathering of limestone surfaces, 

including those of historical monuments, 

at a rate of up to 2 mm in 12 years (Seaward & 

Edwards, 1997). Extensive lichen communities 

also exist on the bark and foliage of trees (corticolous 

lichens). Additionally, freshwater and 

marine species have been described. Lichens 

occur in all climatic zones from the Arctic and 

Antarctica, where they provide the dominant 

vegetation (Seppelt, 1995), to the tropics. 

Some lichen thalli live for over 1000 years 

and can be used for determining the age of rock 

surfaces because of their slow growth rate. This 

discipline is known as lichenometry (Hale, 1983; 

Innes, 1988). It has been applied, for example, to 

date the standing stones on Easter Island or the 

time point of exposure of rock surfaces caused by 

avalanches or earthquakes. Crustose lichens are 

commonly used for lichenometry because they 

have the slowest growth rate. An example is the 

‘map lichen’, Rhizocarpon geographicum (Plate 8b; 

O’Neal & Schoenenberger, 2003). 

A wide range of lichens has been examined 

by different research groups. Therefore, in the 

present chapter we will give an introduction to 

the general features of lichen biology, followed 

by brief profiles of common examples taken from 

the Lecanorales, which is by far the largest order 

of lichenized fungi. Good general textbooks on 

lichens are those by Hale (1983), Ahmadjian 

(1993) and Nash (1996a). Richardson (1975) has 

written a stimulating account of the importance 

of lichens to mankind and in natural ecosystems. 

16.2 General aspects of lichen 

biology 

16.2.1 Morphology of the lichen thallus 

Lichen thalli come in three basic shapes 

crustose (crust-like), fruticose (shaped like a 

miniature shrub) or foliose (leaf-like). It should 

be noted that these are purely descriptive terms 

which have no taxonomic meaning. Intermediate 

forms also exist. Good summaries are those by 

Büdel and Scheidegger (1996) and Honegger 

(2001). 

By far the most common type is the crustose 

thallus which forms a thin spreading crust 

firmly attached to the substratum by its entire 

lower surface (Plate 8a,b). In the morphologically 

simplest crustose lichens, fungal hyphae are 

loosely associated with photobiont cells but do 

not form a protective upper cortex. Such lichen 

thalli appear powdery and are referred to as 

leprose. They often have a highly hydrophobic 

surface. Other crustose lichens produce a thicker 

thallus often held together by mucilage, as in the 

gelatinous lichens. In more highly differentiated 

crustose thalli, the photobiont cells are positioned 

in a defined layer located underneath an 

upper cortex formed exclusively by the mycobiont. 

The photobiont cells are thus protected 

from adverse environmental factors. Air spaces 

in the photobiont layer and the medulla underneath 

permit gas exchange (see Fig. 16.1). The 

differentiation of the lichen thallus into horizontal 

layers is called stratification. Insquamulose 

lichens (Plate 8e), the crustose thallus forms 

small scales (squamules) which become partially 

raised from the substratum, giving the surface a 

scurfy appearance. 

The stratification is developed further in the 

second thallus type, the foliose lichens (Plate 

8c,d) by the development of a lower cortex. 

Attachment to the substratum is often by bundles 

of hyphae termed rhizinae. As a result, the 

thallus appears leaf-like or lobed and can be 

detached from the substratum without being 

damaged. 

The third thallus type is called fruticose. Here 

the thallus has a shrub-like or branched appearance 

and is raised from the substratum (Plate 8f) 

or hangs down from it (Plate 8g). In some cases 

a fruticose thallus may develop from a basal 

crustose or foliose thallus (Plate 8e). Stratification 

in fruticose thalli is often tubular/ 

concentric rather than horizontal, and it resembles 

the more complex crustose types in possessing 

an outer cortex overlying a photobiont layer

448 LICHENIZED FUNGI (CHIEFLY HYMENOASCOMYCETES: LECANORALES) 

Fig16.1 SEM view of a section of 

the stratified fruticose thallus of 

Anaptychiaciliaris.The globose cells 

of the photobiont (Trebouxia)are 

located in a loose layer underneath 

the thick mucilaginous cortex 

produced exclusively by the 

mycobiont hyphae. From Bu«del & 

Scheidegger (1996), by permission 

of Cambridge University Press. 

Original image kindly provided by 

C. Scheidegger. 

and a medulla, but lacking an inner cortex 

(Fig. 16.1). 

16.2.2 Reproduction of lichens 

Sexual reproductive features of lichenized ascomycetes 

are largely equivalent to those found 

in non-lichenized groups. Both homothallic 

and heterothallic mating systems are known. 

Apothecia with inoperculate asci are especially 

common, but perithecia and pseudothecia also 

occur. In contrast, no cleistothecia or apothecia 

with operculate asci are known among lichenized 

fungi. The taxonomic affinities of the 

various orders of lichenized ascomycetes are 

summarized in Table 16.1. Conidial states, if produced, 

are often pycnidial. In most cases, the 

photobiont is excluded from the fertile regions 

of the mycobiont so that ascospores or conidia 

are released without photobiont cells. A new 

lichen thallus can be established from fungal 

spores only by re-lichenization with suitable 

photobiont cells. It is unclear how frequent this 

is in nature. 

Most lichen thalli therefore produce vegetative 

propagules containing both symbionts. 

These can be very variable, and an extensive 

terminology has evolved to describe them (see 

Büdel & Scheidegger, 1996). The most common 

vegetative propagules are soredia, i.e. small 

clumps of hyphae enclosing a few algal cells 

(Fig. 16.2). They are produced over the entire 

surface of the thallus (Plate 8e; Fig. 16.8) or in 

differentiated structures called soralia. Soredia 

are usually hydrophobic and are dispersed by 

wind, perhaps following their initial detachment 

by the impact of a rain drop. Isidia are larger, 

upright cylindrical structures which contain 

both symbionts. They serve to increase the 

surface area of the lichen thallus but can also 

become detached and then function as vegetative 

propagules. In some lichens such as Cladonia, 

squamules broken off a vegetative thallus are 

capable of establishing a new thallus. Animals 

can also play a role in dispersing lichens. Meier 

et al. (2002) have shown for Xanthoria parietina 

(Plate 8c) that mites feeding on lichen thalli can 

spread both the mycobiont and photobiont via 

their faecal pellets. Since this lichen does not 

produce soredia or isidia, dispersal by invertebrates 

could be significant. 

16.2.3 Establishment of a lichen thallus 

A germinated mycobiont spore in nature may 

be able to survive for a while as a mycelium 

of limited spread, or it can undergo a loose 

association with free-living algae not suitable for 

an intimate and permanent lichen symbiosis 

(Ahmadjian & Jacobs, 1981; Ott, 1987). The initial 

stage of the lichen symbiosis is therefore nonspecific. 

It results in mycobiont hyphae making 

contact with and growing around individual 

photobiont cells (Figs. 16.3a,b).

Table 16.1. Summary of the most important orders of lichenized ascomycetes and their characteristic features. Orders have been grouped approximately 

according to the phylogenetic summary by Grube and Winka (2002). 

Order Number of species Features of sexual 

reproduction 

Lichen thallus Photobiont Taxonomic reference 

Lichinales 237 (alllichenized) ascohymenial/apothecial 

with prototunicate asci 

crustose, foliose or 

fruticose (often 

gelatinous) 

cyanobacteria Schultz et al.(2001) 

Agyriales 98 (mostly lichenized) ascohymenial/apothecial 

with bitunicate (nonfissitunicate) 

asci 

crustose or 

squamulose 

green algae (with 

cyanobacteria in 

cephalodia) 

Lumbsch et al.(2001) 

Gyalectales 108 (alllichenized) ascohymenial/apothecial 

with unitunicate asci 

mainly crustose mainly green 

algae (especially 

Trentepohlia) 

Lumbsch et al.(2004) 

Ostropales 

(incl.Graphidales) 

1854 (mainly 

non-lichenized) 

ascohymenial/apothecial 


crustose green algae Lumbsch et al.(2004) 

Pertusariales 47 (alllichenized) ascohymenial/apothecial 


mainly crustose green algae Stenroos and DePriest 

(1998) 

Lecanorales 7108 (mostly lichenized) ascohymenial/apothecial 

with rostrate 

(non-fissitunicate) asci 

all shapes green algae and/or 

cyanobacteria 


Pyrenulales 286 (two-thirds 

lichenized) 

ascohymenial/perithecial 

with bitunicate 

(fissitunicate) asci 

crustose green algae 

Verrucariales 720 (mostly lichenized) ascohymenial/perithecial 


(non-fissitunicate) asci 

crustose or foliose green algae Wedin et al.(2005) 

Arthoniales 1200 (mostly lichenized) ascohymenial/apothecial 


(fissitunicate) asci 

mainly crustose green algae Myllys et al.(1998)


Fig16.2 Cladonia pyxidata. Soredia containing algal cells 

surrounded by fungal hyphae. 

Fig16.3 Interactions between photobiontcells (Trebouxia) and mycobiont hyphae. (a,b) Early stages in the establishment of a lichen 

thallus in Cladonia cristatella. (a) Single algal cell at point of contact with the mycobiont. (b) Ensheathment of algal cell by the 

mycobiont. Both images redrawn and modified from SEM images of Ahmadjian and Jacobs (1981). (c) Formation of tubular 

intracellular haustoria by the mycobiont of a simple crustose lichen (e.g. Lecanora conizaeoides).The same photobiont cell may be 

penetrated repeatedly. (d) Formation of an intraparietal haustorium by the mycobiont of a stratified lichen. Exchange of nutrients 

occurs apoplastically; the walls of both mycobiont and photobiont are surrounded by a common hydrophobin sheath produced by 

the former. (c,d) schematic drawings based on the results of Honegger (1986). 

If partners are compatible, a pre-thallus 

is formed, i.e. a crustose non-stratified cluster 

of photobiont cells ensheathed by hyphae of 

the mycobiont (Trembley et al., 2002). A prethallus 

is also formed by germinating isidia 

or soredia. Under suitable conditions, the prethallus 

enlarges and stratifies into a mature 

thallus; the first sign of this step is the secretion 

of mucilage by hyphae at the periphery of the 

pre-thallus (Honegger, 1993). 

The factors determining photobiont 

mycobiont specificity and thus permitting the 

development of a pre-thallus and mature thallus 

are not yet known. In addition to genetic determinants, 

environmental factors must also play 

a crucial role as indicated by the difficulties 

encountered when trying to grow pre-thalli 

into fully differentiated thalli in the laboratory 

(Ahmadjian, 1993). Recognition is probably a 

continuous and multi-step process mediated 

by surface molecules such as lectins, and facilitated 

by the embedding of both bionts in a 

gelatinous matrix of fungal origin (Ahmadjian, 

1993).


451 

A pre-thallus can be formed by fusion of 

several genetically distinct isidia, soredia or 

photo- and mycobionts, and likewise several 

pre-thalli can fuse in the process of thallus 

maturation. Thus, a mature thallus may contain 

a jigsaw of genetically heterogeneous myco- and 

photobionts (Fahselt, 1996). In other cases, e.g. 

the map lichen Rhizocarpon geographicum, the 

borders between incompatible thalli are demarcated 

by black barrage lines. In some lichens with 

a green alga as photobiont, the situation is 

further complicated by the inclusion of a second 

(cyanobacterial) photobiont. This is then usually 

confined to discrete regions termed cephalodia 

which often differ in their morphology from the 

thallus containing the green photobiont (Fig. 

16.4). 

16.2.4 Lichenicolous fungi 

The capture of a compatible photobiont partner 

by a germinating fungus spore can be problematic, 

especially if the photobiont belongs to the 

genus Trebouxia which does not seem to be 

widespread as a free-living organism. One solution 

to the problem is the recovery of photobionts 

from the propagules of other lichen 

species. Certain photobiont strains are favoured 

by many taxonomically unrelated mycobionts 

(Rikkinen et al., 2002). If these lichens grow 

in similar ecological situations, communities are 

formed which have a high mycobiont diversity 

but share the same or closely related photobiont 

strains. Thus, the chances for a germinating 

spore to salvage compatible photobionts from 

soredia or isidia of other lichen species may be 

quite high (Rikkinen, 2003). 

Several mycobionts have taken the ultimate 

step of poaching their photobiont from an 

existing lichen thallus in order to establish 

their own independent thallus (Ott et al., 1995). 

Such organisms are called lichenicolous lichens, 

and the phenomenon has been aptly named 

‘cleptobiosis’ (Honegger, 1993). Numerous other 

fungi feed on the photosynthetic products of a 

lichenized photobiont without ever establishing 

an independent thallus, while yet others destructively 

parasitize the host lichen (Rambold 

& Triebel, 1992; Richardson, 1999; Lawrey & 

Diederich, 2003). Such fungi are collectively 

called lichenicolous fungi, and they are often 

taxonomically related to lichenized fungi. 

16.2.5 The nutritional basis of the 

lichen symbiosis 

Hill and Smith (1972) devised a simple and 

elegant method termed the ‘inhibition technique’ 

which has permitted the identification of 

carbohydrates secreted by the photobiont. Lichen 

thalli are exposed to radiolabelled CO 2 , and 

after a while an excess of a single unlabelled 

Fig16.4 Placopsisgelida, a foliose lichen.The 

brightly coloured main thallus containing the 

primary (algal) photobiont has produced a 

dark central gall-like cephalodium in which 

the secondary (cyanobacterial) photobiont is 

localized. From Bu«del and Scheidegger (1996), 

by permission of Cambridge University Press. 

Original image kindly provided by 

C. Scheidegger.


carbohydrate is added. This will saturate the 

uptake system of the mycobiont; only if it is 

identical to the radiolabelled mobile carbohydrate 

exported by the photobiont will the latter 

accumulate in the incubation medium, where 

its radioactivity can be measured. Such studies 

have shown that cyanobacterial photobionts 

export glucose to the mycobiont, whereas green 

algae export polyols such as erythritol (Trentepohlia), 

sorbitol (Hyalococcus, Stichococcus) or ribitol 

(Trebouxia, Coccomyxa, Myrmecia) (Ahmadjian, 

1993). Tapper (1981) estimated that at least 70% 

of the total photosynthetically fixed carbon is 

transferred from the photobiont to the mycobiont 

in Cladonia convoluta. Once taken up by the 

fungus, the transport carbohydrate is rapidly 

converted to mannitol (Lines et al., 1989; 

Ahmadjian, 1993). 

Cultured algal photobionts do not secrete 

polyols into the medium, and if they are separated 

from a fresh lichen thallus, polyol secretion 

ceases within a few hours. Nothing appears 

to be known about the mechanism by which 

carbohydrate export from the photobiont is 

regulated (Ahmadjian, 1993). Contact of the 

mycobiont with its photobiont partner takes 

various shapes. The gelatinous extracellular 

sheath of cyanobacteria is penetrated by hyphal 

protrusions, whereas direct wall-to-wall contact 

occurs between mycobionts and green algal 

photobionts. Appressorium-like structures presumably 

facilitate attachment, and haustoria 

may also be formed within the photobiont cells 

especially in simple, non-stratified crustose 

lichens (Fig. 16.3c). In more highly differentiated 

lichens, haustoria are often reduced to a pad-like 

infection peg appressed to but not breaking the 

algal wall (Fig. 16.3d). Such structures have been 

called intraparietal haustoria (Honegger, 1986). 

Fungal hyphae and attached photobiont cells 

are often coated by hydrophobin-type proteins 

and other hydrophobic molecules secreted by the 

mycobiont (Honegger, 1997; Scherrer et al., 2000). 

Thus, the main transport route from the photobiont 

to the mycobiont, in the absence of large 

haustorial interfaces, must be through the 

apoplast by cell wall contact (Ahmadjian, 1993). 

This is different from the elaborate membraneto-membrane 

contact as found in the haustorial 

complexes of arbuscular mycorrhizal fungi (see 

Fig. 7.46c) and biotrophic parasites (see Fig. 13.5). 

The reason for the reduction in membrane 

contact in the lichen symbiosis may lie in the 

fact that membranes are among the most easily 

damaged structures during the drying and rehydration 

cycles to which lichens are exposed. 

Large haustoria might thus reduce cell viability. 

Presumably sufficient carbohydrate leaks out 

of the photobiont cells during the frequent 

drying rehydration cycles without the need for 

intracellular haustoria (Honegger, 1997). 

Fungi with a cyanobacterium as their primary 

or secondary photobiont benefit by receiving 

nitrogen in addition to carbohydrates. Nitrogen 

fixed by cyanobacterial photobionts is released 

to the mycobiont as ammonium (NH þ 4 ) and 

is incorporated into the amino acid pool as 

glutamate (Nash, 1996b). 

Whilst the advantages of the lichen symbiosis 

to the mycobiont are obviously nutritional, there 

is no clear evidence of the transfer of any 

minerals or other nutrients from the mycobiont 

to the photobiont. The benefits to the photobiont 

may include the buffering against adverse 

environmental conditions such as high solar 

irradiation. The upper cortex of many lichens is 

brightly coloured due to the presence of 

pigments which screen out UV light (see Plate 

8b,c). In fact, cortical pigments may filter out as 

much as 50% of the incoming light, and this is 

particularly important with Trebouxia spp. as 

photobiont because these algae favour low light 

intensities (Masuch, 1993). Lichen thalli growing 

at higher altitudes or on surfaces facing 

the sun often contain higher pigment concentrations 

than less-exposed thalli. An example of a 

light-screen pigment is the polyketide usnic acid 

(Fig. 16.5) which is also toxic against bacteria, 

fungi and other organisms (Elix, 1996; Cocchietto 

et al., 2002). This substance is produced by several 

taxonomically unrelated lichens, but has not yet 

been isolated from any non-lichenized fungus. 

Another example is the pulvinic acid derivative 

vulpinic acid (Fig. 16.5) produced by the wolf’s 

lichen, Letharia vulpina. This species is so toxic 

that its thalli have been used in the past to 

poison foxes and wolves, by laying out animal 

carcasses spiked with ground lichen thalli


453 

Fig16.5 The main routes of secondary metabolism in lichenized fungi.The shikimic acid pathway (top) gives rise to vulpinic acid 

(¼ pulvinic acid methyl ester) and other pulvinic acid-derived metabolites (see also Fig.19.22).The mevalonic acid pathway gives rise 

to triterpenes such as sterols (see Fig.13.16) and tetraterpenes such as carotenoids (see Fig. 24.8).The most typical lichen metabolites 

are polyketides, especially those synthesized by polymerization of phenolic acids (orsellinic acid) or orcinols derived from them, 

giving rise to a wide range of depsides (e.g. lecanoric acid) or depsidones (e.g. psoromic acid).This biosynthetic route, although 

taking place in the mycobiont, is thought to be encouraged by the production of an orsellinic acid decarboxylase inhibitor produced 

by the photobiont.Usnic acid is also the product of oxidative coupling of two phenolic-type rings, although the biosynthetic route 

does not proceed via orsellinic acid and orcinol.Yet other lichen polyketides (e.g. parietin) arise by cyclization of a single long 

polyketide chain; this metabolic pattern is also common in non-lichenized fungi (see Fig.12.46). Modified from Hale (1983), 

Masuch(1993)andElix(1996). 

(Richardson, 1988; Brodo et al., 2001). Not 

surprisingly, lichens containing these and other 

toxic substances appear to be avoided by lichengrazing 

animals (Masuch, 1993). Many secondary 

metabolites of lichens have acidic properties 

and are therefore sometimes collectively called 

lichen acids. Most of them are produced by the 

mycobiont only in the intact lichen thallus but 

not in isolation, indicating that the photobiont 

may exert a subtle influence on the secondary 

metabolism of the mycobiont. As an example, 

Culberson and Ahmadjian (1980) have proposed 

that a putative decarboxylase inhibitor secreted 

by lichen algae inhibits the conversion of 

orsellinic acid to phenolic substances which is 

common in free-living fungi, leading instead to 

esterification of orsellinic acid or orcinol, and 

the accumulation of depside-type lichen acids 

(see Fig. 16.5). The topic of secondary metabolism 

in lichens is vast and has been reviewed by 

Lawrey (1986), Fahselt (1994) and Elix (1996). 

The main biosynthetic routes towards secondary 

metabolism in lichens are the shikimic acid, 

terpenoid and polyketide pathways, of which 

the polyketide route is particularly important 

(Fig. 16.5). 

The benefit conveyed by the mycobiont may 

thus be the provision of a ‘photobiont cultivation 

chamber’ (Honegger, 2001) which permits the 

growth of photobionts in situations which might


be too hostile for free-living forms. The lichen 

symbiosis can thus be considered an alternative 

adaptation to terrestrial life as compared to 

higher plants. 

16.2.6 Lichens and pollution 

Lichens are particularly sensitive to aerial pollutants, 

and especially to sulphur dioxide, SO 2 

(Seaward, 1993; Gries, 1996; Nash & Gries, 2002). 

The photobiont appears to be generally more 

sensitive than the mycobiont. The disappearance 

of lichens from the centres of urban and 

industrial areas was first recognized by Nylander 

(1866), who had already correlated this phenomenon 

with aerial pollution. Because different 

lichens show a differential sensitivity to SO 2 , 

the presence or absence of key species can be 

used as an index of the level of air pollution 

(Hawksworth & Rose, 1970). The most SO 2 - 

tolerant lichen, Lecanora conizaeoides, may have 

evolved in SO 2 -polluted areas and went on to 

become Northern Europe’s most abundant lichen 

by the 1950s (Richardson, 1975). This lichen may 

actually require elevated SO 2 levels for good 

growth (Nash & Gries, 2002), as shown by its 

disappearance from some areas after the implementation 

of legislation to curb SO 2 emissions. 

At the same time, formerly polluted areas are 

being re-colonized by many SO 2 -sensitive species 

(Rose & Hawksworth, 1981; Seaward, 1993). An 

example of this trend has been given by Masuch 

(1993) for the city of Munich. Between 1891 and 

1956, the ‘lichen desert’ (i.e. lichen-free zone) in 

the city centre increased from 8 to 56 km 2 , and 

then it decreased again, disappearing altogether 

by 1983. The size of the ‘lichen desert’ has been 

correlated with the degree of SO 2 pollution in 

the air. Careful studies of lichen population 

dynamics have revealed that lichen species recolonizing 

a lichen desert may be different from 

those initially present. This phenomenon has 

been explained by the eutrophication of urban 

habitats, i.e. their enrichment especially with 

nitrogen (Seaward, 1997; Seaward & Coppins, 

2004). One of these newcomers in urban lichen 

deserts is Dirina massiliensis f. sorediata, which is 

the cause of a rapid decay of limestone monuments 

(Seaward & Edwards, 1997). 

Lichens obtain most of their mineral nutrients 

from the air and rainwater in which these 

are present only in very low concentrations. 

Not surprisingly, therefore, lichens can accumulate 

dissolved substances from very dilute 

solutions. For instance, lichens concentrate 

radioactive nuclides which enter the food chain 

lichen!reindeer!man, leading to their accumulation 

in human tissues (Richardson, 1991). 

Lichens are also being used to monitor the 

radioactive contamination resulting, for example, 

from the explosion of the Chernobyl nuclear 

reactor in 1986 (Seaward, 2004). 

16.2.7 Taxonomy of lichens 

The discovery of a fossilized cyanolichen in the 

Rhynie chert sediments (Taylor et al., 1997) 

indicates that lichens were present some 

400 million years ago when the terrestrial habitat 

was first colonized. Indeed, there is evidence of 

even older lichen-like associations (Yuan et al., 

2005). A huge diversity of lichens exists today, 

and there is good phylogenetic evidence that the 

lichenized habit has been developed and lost 

independently on several occasions in the course 

of evolution (Gargas et al., 1995; Lutzoni et al., 

2001). This is also evident from the scattered 

placement of lichenized fungi in a wider ascomycete 

context. Lutzoni et al. (2001) even suggested 

that some of today’s groups consisting 

entirely of non-lichenized species, notably the 

Plectomycete lineage (Chapter 11), originated 

from lichenized ancestors. Part of the proposed 

argument is a chemotaxonomic one, i.e. the 

presence of numerous secondary metabolites 

(especially polyketides) in the lichens and 

Plectomycetes, but their absence or less-frequent 

occurrence in certain other groups of fungi. As 

with many DNA-based analyses, the phylogenetic 

arrangement of taxa may vary with the kinds 

of sequences used, and other schemes showing a 

less scattered distribution of lichenized fungi 

within the Ascomycota have been put forward 

(Fig. 8.17; Liu & Hall, 2004). 

Whereas much work remains to be done on 

the taxonomy of ascomycetes in general and 

lichenized ascomycetes in particular, some 

orders are beginning to take shape. These are

LECANORALES 

455 

listed in Table 16.1, summarizing data from 

Tehler (1996), Kirk et al. (2001), Ott and Lumbsch 

(2001) and Grube and Winka (2002). The orders 

Dothideales (Section 17.3), Hypocreales (Section 

12.4) and Helotiales (Chapter 15) are not considered 

here because they contain only a small 

proportion of lichenized species. Some small 

families of lichenized fungi (e.g. Baeomycetaceae, 

Icmadophilaceae, Umbilicariaceae) are incertae 

sedes at the moment, and their accurate placement 

will be determined in further studies. Such 

studies will have to be based on the combined 

analysis of several different genes in order to 

obtain a greater degree of confidence in the 

resulting phylogenetic trees (Myllys et al., 2002). 

Most results so far have been obtained with the 

small subunit (18S) ribosomal RNA sequence. 

The data summarized in Table 16.1 are too 

diffuse to be fully understood at present, but we 

note in passing that the occurrence of fissitunicate 

asci is not always correlated with ascolocular 

development (see p. 459 for an explanation), 

i.e. that fissitunicate asci can be found in 

perithecia and apothecia, not just pseudothecia 

(see Chapter 17). Further, many orders, and 

especially the Lecanorales, produce bitunicate 

but non-fissitunicate asci, as do some other 

Ascomycota, e.g. Helotiales and Pezizales (see 

pp. 414. and 429). 

16.3 Lecanorales 

Members of the Lecanorales produce inoperculate 

asci in apothecia. The asci are bitunicate but 

non-fissitunicate. The ascus apex is thickened, 

and ascospores are discharged when the outermost 

wall layer breaks and the innermost layer 

protrudes through the pore thus generated, to 

produce an apical beak called rostrum (Figs. 

8.12e,f). Rostrate ascus dehiscence is typical of 

the Lecanorales. 

Over 75% of all lichenized fungi belong to 

this order, making it one of the largest in 

the Ascomycota. Most of the best-known and 

most readily collected lichens belong to the 

Lecanorales. Only a few non-lichenized members 

of the Lecanorales are known; these are usually 

lichenicolous. This order has been divided into 

42 families (Kirk et al., 2001), of which many still 

have an uncertain phylogenetic position and are 

currently being circumscribed by DNA sequence 

comparisons. Stenroos and DePriest (1998) have 

identified five suborders which together make 

up a monophyletic order. We shall consider just 

a few representatives to indicate the astonishing 

morphological and ecological variability of lecanoralean 

lichens. 

16.3.1 Lecanora 

About 300 species of Lecanora have been described, 

mainly from temperate climates. Thalli 

are usually crustose and are very common on 

rock surfaces, including ancient monuments, 

dry stone walls and roof tiles, as well as on the 

bark of trees. The photobiont usually belongs to 

the genus Trentepohlia. We have already come 

across L. conizaeoides as a particularly SO 2 -tolerant 

species (p. 454). Because of their exposed habitats, 

Lecanora spp. often deposit light-screen 

pigments in their upper cortex which give 

them a bright yellow coloration. An example is 

the xanthone lichexanthone; usnic acid and 

pulvinic acid derivatives have also been detected. 

The quantity and diversity of pigments may be 

greater in thalli exposed to higher levels of 

irradiation (Obermayer & Poelt, 1992). A common 

example of the genus is L. muralis, showing a 

typical crustose thallus with apothecia (Plate 8a). 

The thalli of Lecanora (Sphaerothallia) esculenta, 

a species found from northern Africa to western 

Central Asia, may roll up and become detached 

upon maturity, being blown about by the wind. 

They are said to be edible. On occasions, windborne 

lichen thalli have been so abundant that 

the common name ‘manna lichen’ has been 

coined for L. esculenta (Richardson, 1988). 

16.3.2 Xanthoria 

The most abundant species is X. parietina, which 

forms bright yellow foliose thalli (Plate 8c) on the 

surface of rocks, roofs, trees and farm buildings, 

especially near the sea. It is particularly common 

in places enriched by manure, e.g. dust from 

cattle yards, or from birds. The thallus is lobed 

and is attached to the substratum by short 

rhizinae. The photobiont is the green alga


Trebouxia, which forms single globose cells in a 

defined layer beneath the upper cortex of the 

stratified thallus (Fig. 16.6c). The apothecia are 

saucer-shaped and about 2 3 mm in diameter. 

They are located on the upper surface of the 

thallus, and the algal zone extends into the 

apothecial margin (Fig. 16.6a). The ascospores are 

at first one-celled, but ingrowth from the wall of 

the ascospore eventually divides the contents 

of the spore into two. The yellow colour of the 

thallus is due to the presence of the anthraquinone 

parietin (Fig. 16.5) in the upper cortex. 

Unusual carotenoids are also produced by 

Xanthoria spp. (Czeczuga, 1983). Xanthoria parietina 

does not produce soredia, but it is very 

abundant none the less. One reason for this may 

be that germinating ascospores display a tendency 

towards cleptobiosis, i.e. the theft of 

photobiont cells from soredia or mature thalli 

of other lichens (Ott, 1987). Another means of 

dispersal may be by mite browsing and feeding 

as mentioned earlier. 

16.3.3 Peltigera 

About 45 60 species are known, and the genus 

has been thoroughly examined by Miadlikowska 

and Lutzoni (2004). They and many other workers 

now consider it to be part of a separate order, 

Peltigerales, which is closely related to Lecanorales. 

Species of Peltigera form large lobed leaf-like 

thalli attached to the ground or to rocks by 

groups of white rhizinae. The thallus is rather 

fleshy and is highly stratified (Fig. 16.7a). The 

commonest species are P. polydactyla and P. canina 

(Plate 8d), both of which have now been split up 

into several species. They grow among grass on 

heaths, on sand dunes and on rocks amongst 

moss. The usual photobiont is the cyanobacterium 

Nostoc. In some species, however, the 

primary photobiont can be either a Nostoc, 

giving rise to the usual greyish-black thallus, or 

a green alga (Coccomyxa), in which case the 

thallus is vividly green, with Nostoc sometimes 

present as a secondary photobiont in cephalodia 

(Brodo & Richardson, 1978). The two different 

Fig16.6 Xanthoria parietina. (a) V.S. thallus and apothecium showing the extension of the algal zone into the apothecium. (b) Asci, 

paraphyses and two germinating ascospores. (c) V.S. thallus.

LECANORALES 

457 

Fig16.8 Cladonia pyxidata. Primary squamulose thallus 

bearing funnel-shaped podetia. Note the granular soredia 

outside and inside the podetia. 

contain algal cells. The red colour of the 

apothecia is due to pigments in the tips of the 

paraphyses (Fig. 16.7b). 

Fig16.7 Peltigera polydactyla. (a) V.S. thallus. (b) Ascus, 

ascospores and paraphyses. 

forms of the same lichen are then termed a 

morphotype pair or ‘lichen chimera’. The 

apothecia of Peltigera are reddish-brown, folded 

extensions of the thallus (Plate 8d) which do not 

16.3.4 Cladonia 

There are about 400 species of Cladonia, some of 

them extremely common, growing in heaths, 

moors and elsewhere on rocks and walls. There 

are two kinds of thallus. The primary thallus is 

squamulose, and the secondary thallus is upright 

and cylindrical (fruticose), often consisting of a 

hollow stalk which bears the apothecium at its 

tip. Such an apothecium-bearing vertical thallus 

arising from a horizontal primary thallus is 

called a podetium and is typical of the genus 

Cladonia. InC. pyxidata, the podetium opens out 

into a cup (Fig. 16.8), and the apothecia ultimately 

develop at the rim of the podetium. In C. 

floerkiana (Plate 8e), the podetia are shrub-like 

and bear their red apothecia as terminal heads. 

The colloquial name for this species is ‘British 

soldiers’. The podetia frequently bear the granular 

soredia which contain algal cells surrounded 

by fungal hyphae (Fig. 16.2). In windtunnel 

experiments using C. pyxidata, Brodie and 

Gregory (1953) showed that soredia were blown 

away from the funnel-shaped podetia at wind 

speeds as low as 5.4 7.2 km h 1 although they 

were not removed from horizontal glass slides at 

the same wind speeds. They suggested that 

funnel-shaped structures generate eddy currents


when placed in a windstream and that eddy 

currents effectively remove soredia. 

Usnic acids (Fig. 16.5) are particularly common 

in Cladonia spp., and their concentration in the 

lichen thallus has been shown to increase linearly 

with the intensity of UV light, supporting a 

possible role as a light screen (Rundel, 1969). 

Further, sun-exposed thalli of Cladonia spp. appear 

yellowish whereas those in more shaded habitats 

are greyish-green, although the pigment responsible 

is not usnic acid. 

The reindeer lichen genus Cladina is closely 

related to Cladonia (Stenroos & DePriest, 1998). 

The most common species are C. rangiferina (Plate 

8f) and C. stellaris, which are a major winter food 

for grazing animals such as reindeer or caribou 

in northern boreal forests (Richardson, 1988). 

These lichens provide an important component 

of the ground cover grazed by animals, and are 

also used by Laplanders to make hay for their 

animals. Reindeer lichens are popular in 

Germany as decorations on wreaths and are 

also well-known among model railway enthusiasts 

and architects who use the highly 

branched fruticose thalli as miniature trees 

(Kauppi, 1979; Richardson, 1988).

17 

Loculoascomycetes 


The characteristic feature of this group is that 

the ascus is bitunicate and fissitunicate; it has 

two separable walls (see p. 240). The outer wall 

(ectotunica or ectoascus) does not stretch readily, 

but ruptures laterally or at its apex to allow 

the stretching of the thinner inner layer, the 

endotunica or endoascus (Figs. 17.1a c). Asci 

are generally non-amyloid. The fruit body with 

asci is regarded as an ascostroma, and each 

cavity in which asci develop is termed a locule. 

In contrast to the Hymenoascomycetes, in which 

ascocarps develop following plasmogamy and 

the pairing up of two genetically dissimilar 

nuclei (ascohymenial development), in the 

Loculoascomycetes the ascoma is already present 

before the compatible nuclei are brought together 

(Barr & Huhndorf, 2001). The development of 

asci in pre-formed locules is called ascolocular. 

The ascostroma has therefore been defined as 

an aggregation of vegetative hyphae not resulting 

from a sexual stimulus (Wehmeyer, 1926). 

However, Holm (1959) has questioned the accuracy 

of this definition, since examples are known 

where the ascocarps do develop following the 

pairing of nuclei (Shoemaker, 1955). Within the 

developing ascocarp, one or more locules are 

formed by the downgrowth of pseudoparaphyses 

(see below) and the development of asci. One or 

more ostioles then develop by the breakdown 

(lysis) of a pre-formed mass of tissue (lysigenous 

development). Where a single locule develops, a 

structure resembling a perithecium results and, 

although this term is commonly used for such 

loculoascomycete fruit bodies, they should 

strictly be called pseudothecia (see p. 245). 

Although a mature ascostroma with several 

locules can be superficially similar to the perithecial 

stroma of Pyrenomycetes such as 

Hypoxylon (Fig. 12.11) or Claviceps (Fig. 12.27), the 

difference is that in the pyrenomycete stroma 

each fertile region (perithecium) is surrounded 

by a wall whereas the locules of the ascostroma 

are not (Alexopoulos et al., 1996). However, the 

ascocarp of Loculoascomycetes does not always 

take the form of a pseudothecium. In some groups 

it may be an apothecium, a hysterothecium (an 

elongate ascoma with a slit-like opening) or a 

cleistothecium (Barr & Huhndorf, 2001). These 

deviations from the classical pseudothecium are 

found for example in lichenized Loculoascomycetes 

(see Table 16.1). 

The name Loculoascomycetes was coined 

by Luttrell (1955) and corresponds to the 

Ascoloculares of Nannfeldt (1932). The group 

has also been named the Dothideomycetidae (see 

Kirk et al., 2001). It is very large, with about 900 

genera and over 7000 species. Most members are 

terrestrial, growing as saprotrophs, endophytes 

or parasites on the shoots and leaves of herbaceous 

or woody plants and may cause diseases of 

economic significance, but some grow in freshwater 

or the sea and others in dung or soil. 

There is a very wide range of anamorphs, some 

hyphomycetous, others pycnidial (Sivanesan, 

1984; Seifert & Gams, 2001). 

It is most unlikely that the Loculoascomycetes, 

as currently classified, are monophyletic

460 LOCULOASCOMYCETES 

Fig17.1 Sexualreproductionin Pleosporascirpicola. (a) Young ascus withundifferentiated cytoplasm.Note the thick ascus wall. 

(b)Maturingasciwithcytoplasmcleavedintoascospores.(c)Matureascuswithmuriformascospores.Theascusis shownafewseconds 

before discharge; the ectotunica hasruptured (arrow), and themore flexible endotunica hasbeenforced to expandby theincreasing 

turgor pressure. (d) Discharged ascospore mountedin Indian ink to show the mucilaginous extensions. Allimages to same scale. 

(Berbee, 1996; Dong et al., 1998; Silva-Hanlin & 

Hanlin, 1999). Molecular analyses based on a relatively 

small number of representatives of ascomycete 

groups suggest that the most closely related 

groups are Pyrenomycetes (perithecioid fungi) 

belonging to Diaporthales, Hypocreales, Microascales 

and Sordariales (see Chapter 12; Spatafora, 

1995). Several orders are currently included in 

the Loculoascomycetes (Barr & Huhndorf, 2001; 

Kirk et al., 2001) but we shall consider representatives 

only of the two most important, the 

Pleosporales and Dothideales. Because the 

arrangement of orders and especially families 

is still in a state of flux, we shall not discuss it. 

17.2 Pleosporales 

This is a large group of ascomycetes believed to 

be monophyletic on the basis of molecular 

evidence (Berbee, 1996). Several economically 

important genera of plant pathogens are 

included, such as Cochliobolus, Phaeosphaeria and 

Pyrenophora, parasitic on grasses and cereals. 

Pleospora, Lewia and Leptosphaeria are common 

endophytes, saprotrophs or parasites of other 

herbaceous plants. They and their anamorphs 

may also have significance as human allergens, 

as human pathogens and in the production 

of mycotoxins. Sporormiella fruits on herbivore 

dung. 

The development of pseudothecia in these 

forms conforms to the Pleospora type of Luttrell 

(1951). Ascogonia arise within a stroma and, 

in the region of the ascogonia, a group of 

vertically arranged septate hyphae appears, 

each hypha arising as an outgrowth from a 

stromatal cell. These hyphae are capable of 

elongating by intercalary growth and are 

termed pseudoparaphyses (Luttrell, 1965).

PLEOSPORALES 

461 

Pseudoparaphyses arise near the upper end of 

the cavity and grow downwards. Their tips soon 

intertwine and push between the other cells of 

the stroma so that free ends are seldom found. 

They may thus be distinguished from the true 

paraphyses of other fungi (e.g. Sordaria) which are 

formed from hyphae attached at the base of the 

cavity, extend upwards and are free at their 

upper ends. They may also be distinguished from 

apical paraphyses which are attached above, 

arising from a clearly defined meristem near 

the apex of a perithecium, and form a welldefined 

palisade of hyphae free at their lower 

ends (see the Nectria type of development, p. 337). 

In the Pleospora type of development, asci arise 

amongst the pseudoparaphyses at the base of the 

cavity and grow up between them. The ostiole 

develops lysigenously, i.e. by breakdown of preexisting 

cells. Development of this general type 

has been described in P. herbarum (Wehmeyer, 

1955; Corlett, 1973), Leptosphaeria (Dodge, 1937), 

Sporormiella (Arnold, 1928) and other fungi (see 

Luttrell, 1951, 1973). A more recent discussion 

of pseudoparaphyses development in the Pleosporales 

and its taxonomic implications has been 

written by Liew et al. (2000). 

17.2.1 Leptosphaeria 

Leptosphaeria species fruit on moribund leaves 

and stems of herbaceous plants. There are 

probably some 100 species, many growing on a 

wide range of hosts, but others are confined to 

one host plant. Although most are saprotrophic 

or only weakly pathogenic, some are troublesome 

pathogens, e.g. L. coniothyrium, the cause of 

cane blight of raspberry, and L. maculans which 

causes blackleg of oilseed rape and other 

brassicas. Characteristic features are the fusoid, 

yellow or pale brown ascospores with two or 

more transverse septa. Anamorphic states are 

pycnidial (see Table 17.1). 

Leptosphaeria acuta fruits in abundance in 

spring at the base of overwintered, decorticated 

stems of stinging nettles (Urtica dioica). The black 

shining pseudothecia are somewhat conical and 

flattened at the base (Fig. 17.2a). Bitunicate asci 

elongate within a pre-existing group of branching 

pseudoparaphyses, and close examination of 

the direction of growth and branching indicates 

that the pseudoparaphyses may be ascending 

and descending. The ostiole of the perithecium 

is formed lysigenously by breakdown of a preexisting 

mass of thin-walled cells (Fig. 17.3a). 

The bitunicate structure of mature asci is 

difficult to discern because, as the ascus expands, 

the inner wall protrudes through a thin area 

in the outer wall at the ascus tip (Fig. 17.3e) 

and then the inner wall extends. Thus the 

ascus tip in expanded asci is single-walled. 

The ascospores have about 11 transverse septa 

and are discharged successively at intervals of 

about 5 s. 

Associated with the thick-walled conical 

pseudothecia on the nettle stem are thinnerwalled, 

slightly smaller, globose pycnidia with 

cylindrical necks (Figs. 17.2b and 17.3b). The 

cavity of the pycnidia is lined by small spherical 

cells which give rise to numerous rod-shaped 

conidia (Fig. 17.3c). These are dispersed by rain 

splash or in water films and are capable of 

germination, which suggests that they do not 

function as spermatia. Such pycnidia have been 

Table 17.1. Anamorphic states of some species of Leptosphaeria and Phaeosphaeria. 

Teleomorph Anamorph Disease 

L. bicolor Stagonospora sp. Sugarcane leaf scorch 

L. coniothyrium Coniothyrium fuckelii Raspberry cane blight 

L. maculans Phoma lingam Blackleg of oilseed rape and other brassicas 

P. avenaria Stagonospora avenae Oatleaf blotch 

P. microscopica Phaeoseptoria festucae Leaf spot of fescue and other grasses 

P. nodorum Stagonospora nodorum Glume and leaf blotch of wheat and barley


Fig17.2 Leptosphaeriaacuta on overwinterednettle stem. 

(a) Pseudothecia. (b) Phoma anamorph.Bothimages to same 

scale. 

named Phoma acuta, and culture studies have 

confirmed that this stage is the conidial state of 

L. acuta (Müller & Tomasevic, 1957). Pseudothecia 

of L. acuta ripen in the spring and discharge 

ascospores as the new season’s nettle shoots are 

elongating. There are no obvious disease symptoms 

on infected plants during the summer and 

the fungus persists as a symptomless endophyte, 

with the pseudothecia and pycnidia developing 

during the winter on dead stems of the past 

season’s growth. 

17.2.2 Leptosphaeria and Phaeosphaeria 

An unusually high degree of taxonomic confusion 

has arisen in attempts to delimit and define 

several important plant-pathogenic species 

which clearly belong to the Pleosporales but 

show immense variations in their anamorph 

and teleomorph features. One example is a group 

of coelomycetous species comprising Septoria 

with multiseptate conidia more than 10 times 

longer than wide, Stagonospora with multiseptate 

conidia less than 10 times longer than wide 

(Fig. 17.4), and Phoma with aseptate globose 

or slightly elongated conidia (Figs. 17.6 and 

17.7). The most common sexual states associated 

with Septoria and Stagonospora are Leptosphaeria 

and Phaeosphaeria (Leuchtmann, 1984). As with 

the anamorphs, the morphological features of 

these teleomorphs show transitions, but a broad 

distinction can be made by Leptosphaeria being 

associated mainly with dicotyledons whereas 

Phaeosphaeria is pathogenic on monocotyledons 

(Cunfer & Ueng, 1999). These two genera have 

also been separated by critical DNA sequence 

analyses (Câmara et al., 2002). 

Among the cereal pathogens belonging here, 

Phaeosphaeria (Stagonospora) nodorum has two 

formae speciales, one on wheat and the other on 

barley, whereas Phaeosphaeria avenaria 

(Stagonospora avenae) is a more diverse species 

complex (Ueng et al., 1998) but is not as serious a 

pathogen in most agricultural situations. These 

fungi cause leaf blotch diseases which are very 

common in most cereal-growing regions and 

often become the major cereal leaf disease in wet 

and cool conditions. Epidemics are slowed 

during periods of dry weather. Serious infections 

can cause heavy crop losses if they start early and 

affect the uppermost leaves, which contribute 

most photosynthetic product to the developing 

grains. Stagonospora nodorum also infects the 

heads of wheat, causing glume blotch. Lesions 

develop as small brown spots which enlarge into 

irregular brownish necrotic areas, giving the leaf 

a speckled appearance. Within the necrotic 

areas, pycnidia develop beneath the epidermis 

which they eventually pierce, releasing a tendril 

of cylindrical, three-septate pycnidiospores 

(Fig. 17.4d). These can spread the disease to 

neighbouring plants by rainsplash. In S. nodorum, 

a second pycnidial state containing minute 

unicellular conidia has also been discovered 

(Harrower, 1976). These infect host leaves via 

germ tubes which penetrate the stomata, 

whereas penetration from Stagonospora-type conidia 

is directly through the cuticle (Karjalainen & 

Lounatmaa, 1986). There is no evidence that 

either type of conidium plays a sexual (spermatial) 

role. Low temperatures (5 10°C) and irradiation 

with ultraviolet light favour conidium 

production. Both S. avenae and S. nodorum survive 

the winter either on living volunteer plants or as 

pycnidia and pseudothecia on stubble. Epidemics 

can also be started from infected seeds, and from 

ascospores which are released from pseudothecia

PLEOSPORALES 

463 

Fig17.3 Leptosphaeria acuta.(a)L.S.immature 

pseudothecium. Note the young asci (stippled) 

elongating between a pre-formed mass of 

pseudoparaphyses, and the thin-walled cells 

which block the ostiole at this stage but later 

dissolve.The centrum subsequently enlarges, 

dissolving the pseudoparenchyma surrounding it. 

(b) L.S. pycnidium. (c) High-power drawing of cells 

lining the pycnidium, showing the origin of the 

conidia. (d) Cluster of developing asci from a young 

pseudothecium. Note the branching of the 

pseudoparaphyses. (e) Stretched bitunicate ascus 

showing rupture of the outer wall at its apex. 

in the spring and autumn. Good reviews of 

S. avenae and S. nodorum have been written by 

Eyal (1999) and Cunfer (2000). 

An important disease caused by Leptosphaeria 

maculans (anamorph Phoma lingam) is blackleg 

disease of winter oilseed rape (Brassica napus) and 

other brassicas. As the name suggests, the disease 

symptoms are seen mainly at the stem bases and 

main roots, although the foliage can also be 

affected. Infection may occur through leaves, 

followed by an endophytic phase lasting several 

months, before the blackleg symptoms manifest 

themselves. Lesions eventually turn pale and 

necrotic, and pycnidia are produced within 

them. Where the cortex of infected stems 

cracks open, cankers develop. Rain-splashed 

pycnidiospores spread the disease during the 

growing season. The fungus overwinters on 

stubble and infects the new crop by ascospores 

released from pseudothecia, although it can also 

be seed-borne. The biology of this fungus has been 

reviewed by Rouxel and Balesdent (2005). 

Leptosphaeria maculans comprises several 

morphologically similar species which can be 

assigned to two groups, the highly destructive 

A group which forms cankers and a less damaging 

B group which is confined to infections of 

leaves and the pith (Williams & Fitt, 1999). 

The B pathotype has recently been named 

L. biglobosa (Shoemaker & Brun, 2001). Some of 

the disease symptoms are probably caused by 

toxins produced by the A pathotype in planta


Fig17.4 Stagonospora nodorum. (a) Pycnidia seen from above. (b) Pycnidia in section in agar culture. (c) Portion of wall of pycnidium 

showing origin of conidia. (d) Conidia. (a,b) to same scale; (c,d) to same scale. 

(Pedras & Biesenthal, 1998; Howlett et al., 2001). 

In addition, L. maculans is able to detoxify phytoalexins 

produced by the host plant (Pedras et al., 

2000). Since P. lingam is not closely related to 

most other Phoma spp., it has been re-named 

Plenodomus (Reddy et al., 1998). 

Diverse anamorphic states are known in 

other species of Leptosphaeria and Phaeosphaeria, 

and some examples of important pathogens are 

summarized in Table 17.1. 

17.2.3 Ascochyta and Phoma 

Several related Ascochyta-type anamorphs infect 

legumes, causing diseases such as blight of 

chickpea (A. rabiei), foot rot and blight of peas 

(A. pinodes), and leaf- and pod-spot of broad beans 

(A. fabae) and peas (A. pisi). The pseudothecial 

state, where present, is now called Didymella 

(formerly Mycosphaerella). These species usually 

overwinter on crop residues, infecting new crops 

in spring as ascospores, but they are also seedborne. 

During the growing season, the infection 

is spread by rainsplash of pycnidiospores. An 

excellent review of the biology of Ascochyta, 

highlighting the severity of diseases which can 

be caused, has been written by Pande et al. (2005) 

for A. rabiei. Pycnidia contain hyaline, two-celled 

conidia which, according to Brewer and Boerema 

(1965), arise by septation from the conidiogenous 

cell. A few conidia with no, two or three 

septa may be produced occasionally (Fig. 17.5). 

Extensive work has been carried out on characterizing 

the mating type idiomorphs of 

Ascochyta spp. These data and analyses of other 

sequences have shown that Ascochyta spp. belong 

to the Pleosporales and are not closely related 

to Mycosphaerella, which is in the Dothideales 

(Barve et al., 2003). 

Phoma medicaginis (Fig. 17.6) has also been 

shown to be related to Ascochyta spp. (Fatehi et al., 

2003). Unfortunately, little information is available 

to circumscribe the very large genus Phoma 

which is almost certainly polyphyletic, being 

associated with several different teleomorphs. 

However, a valuable and much-needed monograph 

of this difficult group has been written by 

Boerema et al. (2004). The conidial fructification 

of Phoma is a pycnidium which usually has only 

one ostiole, rarely two (Figs. 17.6a and 17.7b). 

Like most pycnidia, its outermost wall layer is 

pigmented and consists of cells of distinct shape, 

which is a useful feature in species identification. 

In the case of Phoma spp., it is called a 

textura angularis (Fig. 17.6a). The cavity of the 

pycnidium is lined by a hymenium of conidiogenous 

cells from which one-celled hyaline 

pycnidiospores develop. The absence of filiform

PLEOSPORALES 

465 

Fig17.5 Ascochyta pisi. (a) Pycnidium seen from above, showing a cirrhus of conidia oozing from the ostiole. (b) Conidia 

(pycnidiospores). (c) Portion of pycnidium wall in section, showing origin of pycnidiospores. 

Fig17.6 Phoma medicaginis. (a) View of the ostiole of a pycnidium from above, showing the angular appearance of the wall surface 

comprising a textura angularis. (b) Conidia (pycnidiospores), most of them containing two lipid droplets. (c) Pigmented chlamydospores 

formed by old hyphae embedded in agar.The light-refractive globose bodies inside the chlamydospores are lipid droplets. 

b-conidia distinguishes Phoma from Phomopsis, 

which belongs to an altogether different group 

(see p. 373). The pycnidiospores often ooze out 

from the ostiole as a tendril (cirrhus). 

The conidiogenous cells of Phoma are very 

small, and details of conidium development are 

difficult to discern with the light microscope 

(Fig. 17.7b). Brewer and Boerema (1965) have 

therefore studied spore development with the 

electron microscope. They described the process 

of spore formation as a monopolar, repetitive 

budding of the small, undifferentiated cells of 

the pycnidial wall. As repeated spore formation 

occurs, the apex of the conidiogenous cell


Fig17.7 Phoma betae. (a) L.S. pycnidium. (b) Portion of 

pycnidium wall, showing conidiogenous cells and conidia. 

develops a thickened rim which resembles a 

phialide or an annellophore (annellide). Sutton 

(1980) has interpreted these spores as 

phialoconidia. 

Phoma epicoccina is an unusual species because 

it possesses a hyphomycetous synanamorph, 

Epicoccum nigrum (Fig. 17.8), which is very 

common on decaying plant material and in the 

soil. The Epicoccum state takes the form of 

cushion-shaped sporodochia, which are black or 

purplish-red in colour and covered with roughwalled, 

warted, segmented, brownish-red conidia 

(Fig. 17.8a). The conidia may be violently 

projected from the sporodochium, probably by 

the rounding off of the two turgid cells on either 

side of the septum which separates the conidium 

from its conidiophore (Fig. 17.8c; Webster, 1966). 

It is possible that conidial discharge is stimulated 

by drying because the peak concentration 

of Epicoccum spores in air occurs shortly before 

noon (Meredith, 1966). The synanamorphic 

nature of P. epicoccina and E. nigrum has been 

conclusively demonstrated only relatively 

recently (Arenal et al., 2000). 

17.2.4 Pleospora 

Estimates of the number of species of Pleospora 

vary, and Kirk et al. (2001) suggested that there 

are about 50. Most species form fruit bodies on 

moribund herbaceous stems apparently as saprotrophs, 

but some are weak pathogens. Of these, 

P. bjoerlingii (¼ P. betae) is the cause of blackleg 

of sugar beet. Pleospora scirpicola forms its pseudothecia 

on the underwater parts of the culms 

of the bulrush, Schoenoplectus lacustris, and was 

the first fungus in which the ‘jack-in-the-box’ 

mechanism of discharge of bitunicate asci was 

illustrated (see Fig. 17.1). 

Pleospora herbarum attacks a wide range of 

cultivated hosts, causing such diseases as net 

blotch of broad bean and leaf spot of clover, 

lucerne and other hosts. It may be seed-borne.

PLEOSPORALES 

467 

Fig17.8 Epicoccum nigrum. (a) Young sporodochium. (b) Conidiophores and conidia. (c) Conidium almost separated from the 

conidiophore. Note the bulging septum of the conidiophore. (d) Two detached conidia. 

The pseudothecia are common on overwintered 

stems of herbaceous maritime plants. The 

large, black, somewhat flattened pseudothecia 

contain broad, sac-like bitunicate asci, with 

eight yellowish-brown, slipper-shaped ascospores 

with transverse and longitudinal septa 

(Fig. 17.9a). The anamorphic state, Stemphylium, 

produces pigmented muriform conidia and is 

often associated with the pseudothecia. The 

connection between the teleomorphic and 

anamorphic states is readily demonstrated by 

shooting ascospores onto an agar surface 

where they germinate and the resulting mycelium 

develops conidia within a few days. 

Conversely, cultures started from a single conidium 

develop pseudothecia within a few weeks


Fig17.9 Pleospora herbarum. (a) Ascus and ascospores showing mucilaginous epispore. (b) Stretched bitunicate ascus showing 

rupture of outer wall. (c) Developing asci and pseudoparaphyses.The arrows (p) indicate points of branching of ascending and 

descending pseudoparaphyses. (d) Conidia of Stemphylium type. 

(Weber & Webster, 2000b). The P. herbarum 

complex includes a number of similar species 

forming conidia which are critically different 

from each other in morphology and dimensions 

(Simmons, 1969). A distinctive form, 

S. vesicarium, is associated with leaf blight of 

onions and garlic. 

Stemphylium conidia develop singly from the 

tips of conidiophores swollen at their apices, 

as blown-out ends. A narrow neck of cytoplasm 

connects the developing spore to its conidiophore 

through a pore, and Hughes (1953) has 

termed conidia of this type porospores 

(Fig. 17.9d), but the term poroconidium is also

PLEOSPORALES 

469 

used (Ellis, 1971b). Electron microscopy studies 

(Carroll & Carroll, 1971) have shown that 

conidial development is blastic, involving the 

whole of the wall at the apex of the conidiogenous 

cell. The cytoplasmic connection between the 

conidiogenous cell and the conidium is narrow, 

and is surrounded by two layers of thickened 

wall material. Following the detachment of the 

first-formed conidium, the conidiophore may 

grow out through the detachment scar to form 

a second conidium, a process described as 

percurrent conidiogenesis. The conidia of 

P. herbarum are formed more readily in cultures 

illuminated by near-UV light (Leach, 1968), 

whereas daylight and low temperature stimulate 

pseudothecial development (Leach, 1971). The 

fungus is homothallic. According to Meredith 

(1965) the conidia are violently jolted from the 

tip of the conidiophores. 

17.2.5 Lewia 

The genus Lewia was named in honour of L. E. 

Wehmeyer by Simmons (1986) for Pleospora-like 

fungi with Alternaria anamorphs. Six ascocarpic 

species have been recognized, fruiting on grasses 

(including cereals) and on dicotyledonous hosts 

(including Brassica and Pastinaca) (Kwasna & 

Kosiak, 2003). The separation of Lewia from 

Pleospora is supported by molecular evidence 

(Pryor & Gilbertson, 2000). 

Lewia infectoria (¼ Pleospora infectoria) forms 

black, shining, subepidermal pseudothecia on 

overwintered grass and cereal culms. It has 

golden-brown muriform ascospores with up to 

five transverse septa. The central cells of the 

ascospores also contain one or rarely two longitudinal 

septa (Fig. 17.10a). In culture, this 

fungus forms branching chains of obclavate, 

brown-coloured (melanized), muriform, beaked 

spores (dictyospores or dictyoconidia) and new 

spores are formed at the tip of the chain 

(Fig. 17.10c). A darkly pigmented thickened 

annulus is visible at the base of the conidium 

and at the apex of the conidiophore surrounding 

the point of spore separation and, if the spore 

has occupied an intercalary position on the spore 

chain, there is also an annulus at the opposite 

end. Chain branching occurs where a conidium 

produces more than one spore. Conidia of this 

type have been classified in the anamorph genus 

Alternaria, and are poroconidia. The conidial state 

of L. infectoria is A. infectoria. 

17.2.6 Alternaria 

About 50 species of Alternaria are known which 

have not been connected to a teleomorph 

(Neergaard, 1945; Joly, 1964; Simmons, 1986; 

Kirk et al., 2001). The taxonomy of Alternaria is 

difficult. Simmons (1992) has given a key to 10 

species-groups and Ellis (1971a, 1976) has 

described and figured some common species. 

Despite the absence of formal evidence for sexual 

reproduction in many species of Alternaria, 

Berbee et al. (2003) have shown that three species 

of Alternaria not known to have sexual states, 

A. brassicae, A. brassicicola and A. tenuissima, have 

mating type gene sequences. In any one isolate of 

these species, only one mating type idiomorph 

was found, but in other isolates of the same 

species the opposite idiomorph was detected. 

This suggests that these currently asexual species 

were derived from sexually reproducing 

ancestors. 

The fine structure of conidial development 

from a pre-existing conidium in A. brassicae has 

been studied by Campbell (1968). The mature 

spore has a two-layered wall, the outer of which 

is melanized. A pore develops in the outer wall, 

probably by enzymatic activity, and the inner 

wall layer expands through the pore to become 

the primary wall of the new conidium. Later, this 

in turn becomes two-layered. Transverse and 

longitudinal septa develop within the spore, 

but these are incomplete; a pore in each 

septum allows cytoplasmic continuity between 

adjacent cells and flow of cytoplasm through the 

spore to provide material for the formation of 

new spores at the tip of the chain. 

The shape of the conidium in Alternaria 

affects its aerodynamic properties. Several 

species have conidia with long beaks, e.g. 

A. solani and A. brassicae (Fig. 17.11). It has been 

suggested that the long beaks increase the 

chance of wind-dispersal as compared to species 

with smaller, non-beaked conidia (Chou & Wu, 

2002). Long beaks also increase the drag on the


Fig17.10 Lewiainfectoria. (a) Asci, one intact, the 

other stretched by expansion of the endotunica. 

(b) Germinating ascospore. (c) Alternaria 

infectoria conidial state developed in culture 

from a germinating ascospore. (d) A conidium 

from an intercalary position in a spore chain 

showing a scar at each end of the conidium. 

(e) A conidium from the end of a spore chain 

with only one basal scar. 

spore, reducing its settling velocity (McCartney 

et al., 1993). 

Some species of Alternaria are of considerable 

economic significance (Chelkowski & Visconti, 

1992; Rotem, 1994). Alternaria alternata (¼ A. 

tenuis) is the name given to a widespread and 

cosmopolitan opportunistic saprotroph, reported 

on all kinds of senescent plant material. 

Unfortunately, because of difficulties in identification, 

it is probable that the name encompasses 

several distinct taxa (Roberts et al., 2000). 

Alternaria spp. are associated with diseases of 

crops, often showing a degree of host specificity 

as indicated in Table 17.2. Most of these diseases 

are seed-borne; seeds become infected from the 

flowering stage onwards (Rotem, 1994). The hostspecific 

pathogens may have evolved from nonspecific 

saprotrophic forms of ‘A. alternata’ by the 

selection and multiplication of mutants capable 

of secreting host-specific toxins (Scheffer, 1992; 

Rotem, 1994; Thomma, 2003). Many of these 

host-specific toxins have been characterized 

chemically (Otani & Kohmoto, 1992). Numerous 

mycotoxins are also produced by Alternaria spp. 

(Montemurro & Visconti, 1992), and some have 

severe and fatal consequences if they accumulate

PLEOSPORALES 

471 

Fig17.11 

Alternaria brassicae. (a) Conidiophores and conidia. (b) Conidia. Note the long conidial beaks. 

in human food and animal feed. Spores of 

Alternaria spp. are abundant in the air in late 

summer and autumn and may be a cause of 

inhalant allergy causing asthma. Some species, 

e.g. ‘A. alternata’, A. infectoria and A. longipes are 

rare opportunistic human pathogens, associated 

with diseases of bone, cutaneous tissue, ears, 

eyes, nose and the urinary tract (Schell, 2003). 

Other species are insect pathogens. 

17.2.7 Cochliobolus 

In Cochliobolus, the pseudothecium is long-necked 

and contains elongate, transversely septate 

ascospores spirally coiled around each other 

within a vestigially bitunicate ascus (see 

Figs. 8.15b d). 

Anamorphs associated with Cochliobolus 

The genus Cochliobolus contains some of the 

best-studied and most highly damaging plant 

pathogens. As in other Loculoascomycetes, 

the taxonomic history of this genus has 

been tortuous (Sivanesan, 1987; Alcorn, 1988); 

the anamorphs were formerly classified in 

Helminthosporium, then transferred to Drechslera, 

and are now called Bipolaris (Fig. 17.13) and


Table 17.2. Selected plant-pathogenic species of Alternaria (from Holliday, 1998). 

Species of Alternaria Disease Comments 

‘A. alternata’ 

Widerangeofhostsanddiseases 

‘A. alternata’f. sp. lycopersici Tomato stem canker 

A. brassicae Brassica greyleaf spot Seed-borne 

A. brassicicola Brassica blackleaf spot Seed-borne 

A. carthami Safflower leaf spot Seed-borne 

A. dauci Carrot leaf blight Seed-borne 

A. dianthi Carnationleaf blight Seed-borne 

A. linicola Linseed seedling blight Seed-borne 

A. macrospora Cottonleaf spot Seed-borne 

A. mali Apple core rot 

A. porri Onion purple blotch Seed-borne 

A. radicina Carrot black rot; also infects celery and parsnip 

A. solani Potato early blight and tuber rot 

Tomato early blight and fruit rot 

Curvularia (Fig. 17.14). The revised genus 

Helminthosporium is now rather small, with 

about 20 species and H. velutinum as the typespecies 

(Fig. 17.12). It has affinities to 

Leptosphaeria (Olivier et al., 2000). Drechslera, in 

contrast, is the anamorphic state of Pyrenophora 

(Fig. 17.16; see p. 477). All these anamorphic 

forms produce pigmented (melanized) spores 

with only transverse septa, but they differ in 

their pattern of conidiogenesis and in the 

ultrastructural appearance of their cell walls. 

Sporogenesis by Helminthosporium is tretic, i.e. 

porospores are formed as described for 

Stemphylium by the digestion of a small hole 

into the conidiophore cell wall, followed by an 

extension of the inner wall to form the conidium 

which then lays down its outer wall (Fig. 17.12c). 

In contrast to Pleospora, each site can produce 

only one conidium, and conidia can develop 

apically or laterally on the conidiophore. If the 

conidium is produced apically, the conidiophore 

cannot grow further. The sequence of conidium 

development in Bipolaris and Curvularia is not 

of this type. In Bipolaris, the first conidium 

always develops apically, and subsequent 

conidia are formed either by growing through 

the scar left by the first conidium, or by the 

conidiophore growing past the first conidium to 

form a new apex producing the second conidium 

(B. sorokiniana; Fig. 17.13b). Bipolaris is so named 

because the conidia germinate by emitting two 

germ tubes, one at either end (Fig. 17.13d), and 

these grow as extensions of the long axis of the 

spore. This is in contrast to Helminthosporium 

conidia in which each cell is principally capable 

of germination, and the germ tubes grow 

perpendicular to the long axis of the spore. 

In Curvularia, the conidia are curved because 

of an unevenly swollen central cell. The end cells 

are usually less strongly pigmented than the 

central cell (Figs. 17.14b,c). The first conidium 

also develops at the apex of the conidiophore as 

a poroconidium extending through a tiny pore, 

and then the conidiophore develops a new 

subterminal growing point from which a 

second conidium initial arises. The process is 

repeated so that a succession of new apices, each 

terminated by a conidium, is formed (Fig. 17.14a). 

The term sympodula has been applied to such 

a conidiophore producing conidia sympodially 

(Kendrick & Cole, 1968). In some Curvularia spp., 

such as C. cymbopogonis (Fig. 17.14c), the base of 

the conidium bears a protuberant hilum. 

A feature of the conidia of Drechslera, 

Helminthosporium and Bipolaris, but not 

Curvularia, is that they are distoseptate 

(Luttrell, 1963). This means that the wall separating 

adjacent conidial segments is visibly

PLEOSPORALES 

473 

Fig17.12 Helminthosporium velutinum. (a) Conidiophores and conidia. (b) Detached conidia. (c) Details of conidial development. 

Note the narrow channels in the wall through which cytoplasm passes to the developing conidia.This type of development is tretic. 

(b)and(c)tosamescale. 

different from the outer wall surrounding the 

entire conidium (White et al., 1973). This can be 

readily seen even with the light microscope 

because the individual conidial cells of 

Drechslera, Helminthosporium and Bipolaris appear 

like peas in a pod (Figs. 17.12, 17.13, 17.16). In 

Curvularia, the conidial septa are of the normal 

(euseptate) type (Fig. 17.14).


Fig17.13 Bipolaris sorokiniana, the conidial state of Cochliobolus sativus. (a) Developing conidia.The arrows point to developing septa. 

(b) Conidiophore showing the development of a second conidium lateral to the first. (c) Mature conidia. (d) Two germinating 

conidia showing emergence of germ tubes from each end of the conidium.

PLEOSPORALES 

475 

Fig17.14 Curvularia spp. (a) Curvularia lunata, the conidial state of Cochliobolus lunatus.Conidiophores showing sequence of conidial 

development. (b) Mature detached conidia of C. lunata. Note the paler end cells. (c) Mature detached conidia of C. cymbopogonis 

showing the protuberant hilum. 

The pathology of Cochliobolus 

Cochliobolus has been examined by DNA sequencing 

methods (Berbee et al., 1999), which revealed 

two separate groups. All important pathogens 

belong to one group and have Bipolaris 

anamorphs. In general, the teleomorphs are 

rare or absent in nature, and the diseases are 

carried mainly by the thick-walled conidia, 

which can survive in the soil but can also infect 

seeds. Cochliobolus sativus (B. sorokiniana) is the 

cause of a variety of root and leaf necroses of 

cereals (especially wheat and barley) in warm 

humid climates of South East Asia, Australia, 

North and South America. A good review of its 

biology has been written by Kumar et al. (2002). 

It is a typical hemibiotrophic pathogen which 

forms quiescent infections in the first-infected 

epidermal cell, followed by a necrotrophic phase 

in which the surrounding tissue is aggressively 

invaded. This pathogen shares with Botrytis 

cinerea (see p. 435) the ability to evade the 

oxidative burst launched as a defence response 

by the newly infected host (Kumar et al., 2001). 

Several sesquiterpene-type toxins are produced 

and contribute to a weakening of the host; 

prehelminthosporol (Fig. 17.15a) seems to be 

the most potent. These toxins act in a nonspecific 

manner on several different cellular 

processes. Interestingly, barley cultivars possessing 

the mlo-type resistance against powdery


Fig17.15 Toxins produced by Cochliobolus spp. a.The sesquiterpene prehelminthosporol produced by C. sativus.b.Thechlorinated 

pentapeptide victorin C produced by C. victoriae. c.The dominant form of T-toxin, a polyketide produced by C. heterostrophus. 

d.The major form of HC-toxin, a tetrapeptide produced by C. carbonum. 

Fig17.16 Pyrenophora tritici-repentis. (a) Immature pseudothecial stroma on overwintered barley stubble, with conidia produced 

on the setae and on separate conidiophores. (b,c) Conidia of Drechslera tritici-repentis mounted in lactic acid (b) showing the typical 

‘peas-in-a-pod’ appearance, and mounted in water (c). (b) and (c) to same scale. 

mildew (see p. 408) are highly susceptible 

to C. sativus. A hypersensitive response which 

effectively suppresses biotrophic pathogens may 

thus actually enhance pathogenicity by others 

with a necrotrophic potential. 

A similar feature was observed with 

C. victoriae, which became pathogenic on the 

Victoria cultivar of oats bred for resistance 

against the crown rust, Puccinia coronata 

(Meehan & Murphy, 1946). The main toxin 

produced by C. victoriae, victorin C (Fig. 17.15b), 

is one of several related cyclic pentapeptides 

which are absolutely essential and sufficient for 

pathogenesis, i.e. the purified toxin can reproduce 

the disease symptoms which consist of 

widespread leaf necrosis, and strains of 

C. victoriae not synthesizing this toxin do not 

cause the disease. It now seems that victorin 

triggers a form of hypersensitive response, i.e. 

widespread host cell death (Navarre & Wolpert,

PLEOSPORALES 

477 

1999). Victorin binds to mitochondrial proteins, 

and it is possible that it initiates cell death via 

mitochondrial dysfunction (Curtis & Wolpert, 

2002). Intriguingly, in the mammalian equivalent 

of the hypersensitive response (i.e. apoptosis), 

mitochondria are also among the first 

organelles to break down. 

Mitochondria are also the target of the 

specific toxin produced by C. heterostrophus 

(B. maydis), which caused the well-described 

southern leaf blight of corn in the United 

States in 1970 (Ullstrup, 1972; Schuman, 1991). 

Prior to that epidemic, maize breeders had relied 

heavily on male-sterile cultivars, i.e. cultivars 

which do not produce viable pollen and are 

therefore dependent on pollen from another 

cultivar for seed production. This facilitated 

the production of hybrids, i.e. the F1 progeny of 

genetically dissimilar parents. These often 

produce particularly high yields, a phenomenon 

known as hybrid vigour. Male sterility was 

achieved by a mitochondrial mutation called 

cms-T (cytoplasmic male sterility). The plant line 

used as the pollen donor did not contain the 

cms-T mutation, so that the hybrid seeds grew 

into plants capable of producing pollen in the 

field of the farmers. In 1970, about 80% of the 

maize crop contained cms-T cytoplasm. At about 

the same time a mutation in a minor leaf 

spot pathogen, C. heterostrophus race O, spread 

in the field. This new race produced several 

related polyketides collectively called T-toxin 

(Fig. 17.15c), which specifically affected the 

mitochondria of hybrid maize. The epidemic 

of 1970 resulted in crop losses totalling over 

US $1 billion for that year. The target site of 

T-toxin in cms-T maize mitochondria is now 

known to reside in a small protein present 

as a tetramer in the outer mitochondrial membrane. 

T-toxin binds directly to this protein, 

causing conformational changes which open 

up pores and render mitochondria leaky 

(Levings et al., 1995; Wolpert et al., 2002). Race O 

causes only minor leaf spots on cms-T as well as 

other cultivars of maize. 

Cochliobolus carbonum is the cause of northern 

leaf spot and ear rot of maize. There are three 

races, of which only race 1 is a serious pathogen 

on all those cultivars of maize containing two 

recessive alleles of the Hm1 resistance gene. This 

strongly enhanced pathogenicity is caused by a 

group of cyclic tetrapeptides collectively called 

HC-toxin (Fig. 17.15d), where HC stands for 

Helminthosporium carbonum, the former name of 

the anamorph. Resistant cultivars produce an 

enzyme which detoxifies HC-toxin. The susceptibility 

of certain maize cultivars was caused 

by a simultaneous inactivation of both duplicate 

genes encoding the enzyme, HC-toxin reductase 

(Multani et al., 1998). The mode of action of HCtoxin 

is not yet clear; it seems to inhibit, rather 

than induce, defence responses (Wolpert et al., 

2002). 

As we have seen, certain strains of 

C. carbonum, C. heterostrophus and C. victoriae have 

caused catastrophic epidemics on particular 

cereal hosts employing biochemically unrelated 

toxins. This specificity of action i.e. a specific 

pathogen race being pathogenic only against 

certain host cultivars paved the way towards 

an understanding of the gene-for-gene concept 

(see pp. 112 and 397). A further question of 

interest is the origin of these highly aggressive 

strains. A partial answer was found somewhat 

fortuitously by an examination of the mating 

type genes in all three pathogens. Both idiomorphs 

MAT-1 and MAT-2 have been found in 

various field isolates of C. heterostrophus and 

C. carbonum, but all known isolates of C. victoriae 

belong to MAT-2. Further, C. victoriae and MAT-1 

strains of C. carbonum are interfertile. These 

observations have led to the suggestion that 

C. victoriae arose from a MAT-2 strain of C. 

carbonum which received the gene cluster for 

pathogenicity on oats (i.e. the genes encoding the 

enzymes necessary for toxin synthesis) by horizontal 

gene transfer (Christiansen et al., 1998). 

The integration of this gene cluster must have 

been close to the MAT-2 locus, so that it did 

not spread to MAT-1 strains of C. carbonum by 

crossing-over. 

17.2.8 Pyrenophora (anamorph Drechslera) 

In its taxonomically restricted use, the Drechslera 

state (Fig. 17.16b) is the conidial form of 

Pyrenophora and is clearly defined as a monophyletic 

group (Zhang & Berbee, 2001). Drechslera


is commonly found in the field, whereas 

Pyrenophora-type pseudothecia are uncommon. 

Species belonging to this group are pathogens 

of cereals and grasses, and some of them cause 

significant diseases in agricultural situations. 

The disease symptoms are similar to those 

caused by other members of the Pleosporales, 

and phytotoxic substances are produced by 

several members of the genus. 

Pyrenophora tritici-repentis (anamorph Drechslera 

tritici-repentis) occurs on a range of grasses, 

including, as the name suggests, Agropyron 

(formerly Triticum) repens and wheat (Triticum 

aestivum). The disease caused is known as yellow 

leaf spot or tan spot of wheat (De Wolf et al., 

1998). Pyrenophora tritici-repentis is spread as seedborne 

infections but also overwinters on infected 

stubble, which is the most important source of 

inoculum, giving rise to pseudothecia and 

conidia in spring. Pseudothecia can be identified 

by their large size and by the presence of dark 

setae around the pseudothecial neck (Fig. 17.16a). 

The ascospores are transversely septate, with a 

longitudinal septum also present in one of the 

central cells. The conidia of Drechslera triticirepentis 

are very large and have a variable 

number of distosepta (Fig. 17.16b). They are 

sometimes produced on the pseudothecial 

setae, or they arise directly from stubble or 

from necrotic leaf lesions. Phytotoxins are 

involved in causing disease symptoms. Most 

unusually, they consist of at least two extracellular 

proteins synthesized by ribosomes 

(Wolpert et al., 2002). They are a critical factor 

in determining the host specificity of infections. 

Pyrenophora teres is common wherever barley 

is grown, and is the major barley pathogen, 

especially in humid regions. This species exists in 

two forms which are distinguished by their 

symptoms, P. teres f. teres causing net blotch on 

barley leaves and P. teres f. maculata causing 

brown leaf spots. These two forms can hybridize 

in the laboratory and also in the field (Campbell 

& Crous, 2003). In addition to ascospores and 

Drechslera-type macroconidia similar to those of 

P. tritici-repentis, a pycnidial state producing 

unicellular conidia is also apparently associated 

with P. teres, although its role in the disease 

cycle is uncertain (Smith et al., 1988). The 

epidemiology of the disease is similar to P. 

tritici-repentis, as is the involvement of phytotoxins 

in causing leaf necrosis. Leaf chlorosis and 

necrosis can be reproduced by phytotoxins 

purified from cultures of P. teres. However, 

biochemically the phytotoxins involved are 

rather different, the most potent of them being 

the aspartic acid derivative aspergillomarasmine 

A (Weiergang et al., 2002). 

17.2.9 Venturia 

The genus Venturia contains some 50 species 

which cause scabs, i.e. limited lesions with a 

scurfy appearance, on the leaves and fruits of 

various trees. The genus is an unusual member 

of the Pleosporales in producing asci with oneseptate 

ascospores, but Silva-Hanlin and Hanlin 

(1999) have confirmed its position within this 

order. The most important species is V. inaequalis 

which parasitizes apple (Malus spp.) and hosts 

related to it. This fungus is cosmopolitan and 

extremely common on apple fruits and leaves if 

fungicide treatments are not carried out 

(Fig. 17.17a). In many regions, scab is the most 

serious apple disease. The fungus overwinters on 

fallen leaves which, in spring, give rise to 

pseudothecia (Fig. 17.17b) releasing ascospores 

during periods of wetness. The ascospores 

require surface wetness in order to infect apple 

leaves. Infection is mediated by appressoria, but 

the invasion is limited to the space between the 

cuticle and the epidermis; the latter is not 

pierced, and haustoria are not formed. In this 

way, the fungus persists for several weeks. 

Conidia are eventually produced from such 

subcuticular stromata, and they spread the 

disease during the growing season. Invasion of 

host tissue takes place only on dead leaves in the 

autumn when V. inaequalis switches to a saprotrophic 

growth phase and produces pseudothecial 

initials. The biology of Venturia, which 

has been summarized by MacHardy et al. (2001), 

is thus very unusual for members of the 

Pleosporales. 

From the above summary of the infection 

biology of Venturia it is apparent that the key to 

apple scab management lies in controlling the 

ascospore inoculum in spring. One commonly

PLEOSPORALES 

479 

Fig17.17 Venturia inaequalis. (a) Apples showing scab symptoms. 

(b) Section through a pseudothecium in an overwintered 

apple leaf. 

practised approach is disease forecasting, 

based on the knowledge that ascospore 

discharge occurs within 1 2 h of wetting ripe 

pseudothecia, and that infection requires leaf 

surface wetness for some 25 h at 6°C or9hat 

16 24°C (Smith et al., 1988). Under certain 

circumstances, e.g. after a prolonged dry 

period, some time will elapse before the pseudothecia 

have produced a fresh crop of ascospores 

after the onset of rain, and this can be 

integrated into forecasting systems (Stensvand 

et al., 2005). Protective fungicide sprays have to be 

applied as soon as possible after the onset of 

conditions conducive to infection, and especially 

if a high density of air-borne ascospores has 

already been detected by spore traps or other 

means (Kollar, 1998). Curative fungicides can be 

applied one or a few days after infection. 

Numerous fungicides are in use against apple 

scab. Protective agents include copper-based 

formulations which are registered in some 

countries even for organic farming, or the thiol 

reactant captan. Important curative fungicides 

include strobilurins (respiration inhibitors), and 

myclobutanil and imidazoles (demethylation 

inhibitors of ergosterol biosynthesis). 

A different control strategy is to reduce the 

available ascospore inoculum in the spring by 

encouraging the decomposition of leaves during 

winter. This can be achieved by applying urea to 

the leaf litter, or by using a flail mower to shred 

the leaves (Sutton et al., 2000). It may also prove 

possible to spray leaves before leaf-fall with 

spores of fungi antagonistic to Venturia (Carisse 

et al., 2000). Yet another approach is the breeding 

of resistant cultivars. 

17.2.10 Sporormiella 

There are about 70 species of Sporormiella (Ahmed 

& Cain, 1972). Molecular studies indicate that the 

genus has affinities with Pleosporales (Liu et al., 

1999). Most species form pseudothecia on the 

dung of herbivores, but some are isolated from 

the soil or as endophytes. Characteristic features 

are dark, transversely septate ascospores which 

may disarticulate into separate part-spores, each 

of which is capable of germination, and whose 

walls are often marked by a hyaline longitudinal 

or oblique germ slit. Sporormiella intermedia is one 

of the common species and has thin transparent 

pseudothecial walls through which asci can be 

seen (Fig. 17.18a). The ascospores of S. intermedia 

are four-celled and surrounded by a mucilaginous 

envelope. Spore discharge is nocturnal 

(Walkey & Harvey, 1966b). 

Because of the unmistakable shape of its 

ascospores and its association with dung, 

Sporormiella has been used in an archaeological


Fig17.18 Sporormiella intermedia. (a) Pseudothecium with asci visible through the transparent wall. (b) Ripe unextended ascus 

showing the double wall. (c) Elongating ascus showing rupture of the outer wall (ectotunica) and extension of the inner (endotunica). 

(d) Ascospore separated into its four component cells. (e) Intact ascospore. 

context as an indicator of changes in vegetation 

and land management. Thus, Burney et al. (2003) 

have shown for the island of Madagascar that 

Sporormiella was very common before the settlement 

of humans which occurred after ad 200 

and then declined in abundance along with the 

extinction of several groups of large herbivores. 

After ad 1100, spore densities of Sporormiella 

in sediments showed an increase, coinciding 

with the introduction of grazing domesticated 

livestock. 

17.3 Dothideales 

This is a large group of ascomycetes containing 

an enormous variety of conidial forms, both 

hyphomycetous and pycnidial. Where present, 

the teleomorph consists of dark-celled pseudothecial 

ascomata, usually developing as 

locules within an ascostroma. The asci are 

bitunicate (fissitunicate). In contrast to the 

Pleosporales, inter-ascal tissue (hamathecium 

with pseudoparaphyses) is generally lacking. A 

relationship between the Dothideales and the 

Pleosporales has been suggested on the basis of 

molecular data (Silva-Hanlin & Hanlin, 1999; 

Lumbsch & Lindemuth, 2001). Many members 

are saprotrophic on dead plant material, but 

some grow as endophytes and some are plant 

pathogens. The single ascocarpic example which 

we shall study is Mycosphaerella. 

17.3.1 Mycosphaerella 

Mycosphaerella is one of the largest genera of 

ascomycetes, containing over 2000 described 

species (Corlett, 1991). However, many of the 

names are based mainly on the association of a 

Mycosphaerella with a particular host plant. Given 

the lack of critical inoculation experiments to 

clarify their host range, mating experiments or 

DNA sequence comparisons with similar forms 

on other plants, it is likely that many names 

are synonyms. Some species are plurivorous, 

growing on a broad range of monocotyledonous 

and dicotyledonous hosts. Many species of 

Mycosphaerella cause diseases of economic significance, 

and some of them are listed in Table 17.3. 

Most of these diseases involve the necrosis of 

host plant tissue, and the toxins produced by 

the pathogens are commonly associated with 

the disease symptoms (e.g. Cercospora beticola; see 

p. 481).

DOTHIDEALES 

481 

Table 17.3. Some anamorph genera with Mycosphaerella teleomorphs. 

Mycosphaerella Anamorph Diseases caused 

M. graminicola Septoria tritici Leaf blotch of wheat 

M. brassicicola Asteromella brassicae Ring spot of brassicas 

M. tassiana Cladosporium herbarum 

M. berkeleyi Passalora personata Groundnut defoliation 

(unknown) Cercospora beticola Leaf spotof sugar beet 

M. fijiensis Paracercospora fijiensis Leaf spot of banana 

M. musicola Pseudocercospora musae Sigatoka disease of banana 

Crous et al. (2000, 2001) and Goodwin and 

Zismann (2001) listed and discussed the bewildering 

diversity of anamorph genera (about 23) 

connected with Mycosphaerella teleomorphs, and 

performed phylogenetic analyses on representatives 

of most of them. The list includes pycnidial 

forms such as Septoria and Asteromella, but also 

numerous hyphomycetous form-genera such as 

Cercospora, Pseudocercospora and Cladosporium 

(Table 17.3). Despite this range of anamorphs, 

molecular evidence has somewhat surprisingly 

indicated that the genus Mycosphaerella is monophyletic 

(Crous et al., 2000, 2001; Goodwin & 

Zismann, 2001). Pseudothecia of Mycosphaerella 

are globose and small, rarely more than 100 mm 

in diameter. Because they show relatively little 

variation, they are difficult to identify to species 

level. Pseudothecia develop subepidermally, 

usually on leaves. The asci develop in a basal 

fascicle. The ascospores are hyaline with a single 

transverse septum (Fig. 17.19). In these features 

Mycosphaerella is similar to Venturia, although 

these two genera are not closely related. 

17.3.2 Mycosphaerella graminicola 

(anamorph Septoria tritici) 

The leaf blotch disease of wheat caused by 

M. graminicola (Fig. 17.20) is very similar to that 

caused by the wheat strain of Phaeosphaeria 

nodorum (see p. 17.2.2), and the two diseases 

often co-occur on wheat crops and are controlled 

in the same way, especially by the application of 

fungicides. The most important fungicides are 

strobilurin-type compounds and ergosterol 

biosynthesis inhibitors. The ascospores of 

M. graminicola, produced from pseudothecia 

initially on overwintering stubble and later 

from infected leaves, are the main source of 

inoculum, and conidia are thought to be of lesser 

importance as propagules of the disease (Eyal, 

1999). In consequence, the genetic diversity of 

M. graminicola in the field is often very high, 

with one square metre of infected wheat shown 

to contain about 70 genetically different strains 

(Zhan et al., 2001). Infection by germinating 

ascospores and conidia of M. graminicola is 

almost always through stomata (Duncan & 

Howard, 2000), in contrast to Phaeosphaeria 

nodorum where it occurs directly through the 

cuticle. Following penetration, intercellular 

colonization of the surrounding leaf tissue by 

hyphae of M. graminicola occurs, but the onset 

of symptom development is delayed. Recent 

reviews of M. graminicola have been written by 

Eyal (1999) and Palmer and Skinner (2002). 

17.3.3 Cercospora 

This very large form-genus (41000 species) 

contains numerous important plant pathogens 

associated with a wide range of host plants (Farr 

et al., 1989). Examples are C. beticola causing leaf 

spot of sugar beet, C. zea-maydis (grey leaf spot of 

corn), and C. coffeicola (brown eyespot of coffee). 

It is difficult to estimate the real number of 

species; Johnson and Valleau (1949) isolated 

Cercospora from 28 host plants in 16 families, 

and all seemed to belong to the same species. 

Further, the dimensions of conidia and conidiophores 

can vary in response to changes in 

humidity. Where known, the teleomorphs of 

Cercospora spp. belong to Mycosphaerella (Goodwin 

et al., 2001). The conidia of Cercospora are


Fig17.19 Mycosphaerella brassicicola. (a) Section of 

a brassica leaf with a subepidermal 

pseudothecium containing asci. Note that there is 

no hamathecium. (b) Pseudothecium as seen from 

above, showing the ostiole. (c) Intact bitunicate 

ascus. (d) Stretched ascus resulting from extension 

of the endotunica. (e) Ascospores. Scale bar: 

40mm (a,b) and10 mm(c e). 

hyphomycetous, being produced from pigmented 

aerial hyphae. They are long and tapering, as 

shown by C. beticola (Fig. 17.21), which is seedborne. 

It has long been known that Cercospora 

infections are much less severe in shaded 

plants as compared to those growing in direct 

sunlight. The reason for this lies in the production 

of a potent photosensitizing toxin, cercosporin 

(Fig. 17.22), by many Cercospora spp. A 

fascinating and lucid account of cercosporin has 

been written by Daub and Ehrenshaft (2000). 

Cercosporin, upon absorption of light energy, 

is activated to an energized state in which it 

reacts with molecular oxygen, converting it into 

various radicals but especially into singlet 

oxygen ( 1 O 2 ). This energized form of oxygen 

is highly reactive, rapidly destroying organic 

molecules and especially membrane lipids. 

Cercosporin is a non-selective toxin, affecting 

bacteria, plants, fungi and animals unless these 

produce protective antioxidants such as carotenoids. 

It is not yet entirely clear how Cercospora 

spp. protect themselves against their own toxin, 

but part of the answer may lie in keeping it in a 

non-reactive (reduced) state. Another mechanism 

is the synthesis of vitamin B 6 (pyridoxine) and 

its derivatives which can act as antioxidants. 

Cercosporin has been found only in Cercospora 

species (Goodwin et al., 2001), but biosynthetically 

related photosensitizers are produced by a 

range of plant-pathogenic fungi, especially in the 

Loculoascomycetes (e.g. Cladosporium, Alternaria, 

Stemphylium spp.). 

17.3.4 Cladosporium 

The anamorph genus Cladosporium is large, 

containing about 60 species. A key to species in 

culture collections has been published by Ho 

et al. (1999). Several species have Mycosphaerella 

teleomorphs, e.g. C. herbarum is the anamorph 

of M. tassiana (von Arx, 1950; Barr, 1958), 

C. echinulatum is the anamorph of M. dianthicola 

and C. humile the anamorph of M. macrospora. The 

association of Cladosporium with Mycosphaerella 

has been supported by molecular studies (Crous 

et al., 2001). However, most species are without 

known teleomorphs. Mycosphaerella tassiana forms

DOTHIDEALES 

483 

Fig17.20 Wheat leaf blotch symptoms caused by 

Mycosphaerella graminicola. (a) Infected leaf showing a necrotic 

lesion, in the centre of which pycnidia of Septoria tritici have 

formed (arrows). (b) Septate conidia of S. tritici,morethan 

10 times longer than wide. 

its pseudothecia on overwintered stalks and 

leaves of numerous monocotyledons and dicotyledons 

in subarctic and subalpine regions, and a 

period of cold is required for ascocarp initiation 

in culture (Barr, 1958; Corlett, 1991). In contrast, 

C. herbarum is ubiquitous and common in 

temperate regions on senescent and dead plant 

material, and in soil. Conidia of this and other 

Cladosporium spp. are the most abundant component 

of the fungal air spora (Gregory, 1973), and 

they are probably the most frequent contaminant 

of foodstuffs, textiles and paintwork. 

They also frequently contaminate cultures of 

other fungi in the laboratory. The conidia of 

C. herbarum and other common moulds such as 

Alternaria alternata and Aspergillus fumigatus are 

associated with severe asthma (Zureik et al., 

2002). Over 30 antigens causing mould allergy 

have been described from C. herbarum, and most 

of them are secretory or cytoplasmic glycoproteins, 

often representing common enzymes such 

as enolase or aldehyde dehydrogenase 

(Breitenbach & Simon-Nobbe, 2002). 

Colonies of C. herbarum are dull olive green 

to black in colour, and appear as a network 

of hyphae or a plate-like mass (stroma) of 

tightly packed, dark, thick-walled cells (McKemy 

& Morgan-Jones, 1991). The conidiophores are 

branched or unbranched and conidiogenesis is 

holoblastic (Fig. 17.23a). The tip of the conidiophore 

bulges out to form the first conidium and 

it is presumed that all the wall layers of the apex 

are involved (Hashmi et al., 1973). The first 

conidium buds to form a further conidium and 

this process continues so that a chain of conidia 

develops in acropetal succession, the youngest 

conidium at the end of the chain. Most conidia 

have a scar (hilum) at each end, but occasionally 

a conidium may form two daughter conidia 

at its tip so that, as further conidial development 

proceeds, a branched chain develops (see 

Fig. 17.23a). Such branch-point conidia have been 

termed ramoconidia (Lat. ramus ¼ branch) and 

are marked by having a single scar at the base 

and two scars at the apex. The conidia of 

C. herbarum have dark (melanized) walls which 

are slightly roughened. They may remain unicellular 

or develop 1 3 transverse septa. Another 

common species of Cladosporium is C. cladosporioides, 

which has smooth conidium walls. 

Cladosporium fulvum (also called Fulvia fulva 

or Mycovellosiella fulva) is probably not closely 

related to other Cladosporium spp. No sexual state 

has been reported, but other Mycovellosiella 

spp., like Cladosporium spp., belong to 

Mycosphaerella (Crous et al., 2001). In contrast to 

most other plant-pathogenic members of the 

Loculoascomycetes, C. fulvum is biotrophic. It is 

a pathogen of tomato plants, especially in 

greenhouses. Conidia infect their host through 

stomata, and hyphae spread in the leaf apoplast 

in close contact with mesophyll cells, but without 

producing haustoria. Sucrose, the major 

plant transport sugar, is hydrolysed and taken 

up, being converted to mannitol by the fungus 

(Joosten et al., 1990). Conspicuous yellow


incompatible interactions results if the product 

of the Avr gene is recognized by the host plant. 

Several Avr genes have been characterized, and 

their products are usually small proteins 

secreted by C. fulvum into the apoplast. Many of 

the corresponding Cf genes of tomato are also 

known; they encode proteins anchored in the 

plasma membrane of tomato cells, with large 

extracellular domains. The examination of the 

products of matching avirulence and resistance 

genes should provide an opportunity to examine 

their interactions, and thus the molecular basis 

of recognition events involved in specific resistance 

(Rivas & Thomas, 2005). This work is still 

ongoing. 

Fig17.21 Cercospora beticola.Conidiophores and conidia from 

sugar beet seed. 

(chlorotic) leaf areas are produced as a result of 

such systemic infections (Fig. 17.24), and eventually 

conidiophores are emitted through 

stomata especially on the lower leaf surface, 

forming a lawn of spores resembling powdery 

mildews but being light brown in colour. 

The interaction between C. fulvum and its 

tomato host is governed by a classical genefor-gene 

relationship based on dominant host 

resistance genes (Cf genes, for C. fulvum) and 

dominant avirulence (Avr) genes in C. fulvum, 

i.e. virulence is a recessive trait (Joosten et al., 

1997). The hypersensitive response of 

17.3.5 Aureobasidium and black yeasts 

Aureobasidium pullulans is a ubiquitous saprotroph 

whose main habitats are the phylloplane 

and other surfaces of living and senescent plants, 

but it can also occur as a symptomless endophyte. 

It grows in soil, but is often not recorded 

because it is temperature-sensitive and is not 

seen on soil plates prepared with warm agar. It 

has been isolated from fresh water, estuarine 

and marine sediments, sea water, sewage and 

other liquid waste (Domsch et al., 1980). Its 

teleomorph is Discosphaerina fulvida, a relative of 

Mycosphaerella (Yurlova et al., 1999). The fungus 

can be readily isolated from leaf washings. It is 

pleomorphic, and in culture it forms a rapidly 

growing mycelium with wide, septate hyphae 

from which intercalary and occasionally terminal 

cells give rise to single or clustered hyaline 

blastoconidia by a process of budding. Budding is 

associated with local lysis of the wall of the 

conidiogenous cell, the inner wall of which then 

balloons out and forms the wall of the conidium 

(Ramos et al., 1975). Repeated conidium development 

from the same or closely adjacent conidiogenous 

loci results in the formation of 

slimy clusters of hyaline conidia (Fig. 17.25a). 

Intercalary cells may enlarge and develop 

thicker, dark, melanized walls to become 

chlamydospores (Fig. 17.25b). Conidia bud in a 

yeast-like manner when the fungus is grown 

in liquid culture with high inoculum densities. 

The yeast cells can continue to bud

DOTHIDEALES 

485 

Fig17.22 Cercosporin.This compound is synthesized as two 

polyketide halves which are then fused, accounting for the 

symmetric appearance of the molecule. 

or may germinate by germ tube. Conidia are 

dispersed by rain splash and by air currents. The 

fungus may be involved in the biodeterioration 

of paint. 

Aureobasidium pullulans has a number of 

potential applications. It is being investigated 

as a possible biocontrol agent against fungi like 

Botrytis and Monilia which cause post-harvest 

storage rots of fruit such as grapes, cherries 

and strawberries. It is a source of gluconic acid 

and of the dextran pullulan, an extracellular 

polysaccharide which has uses as an adhesive in 

laminates and in fabrics. Pullulan is also used as 

Fig17.23 Cladosporium.(a)Cladosporium herbarum; conidiophore with branching chain of blastoconidia.The terminal spores 

of the chain continue to develop blastoconidia. (b,c) Cladosporium macrocarpum. (b) Conidiophores and conidia. (c) Conidiophores 

developing from a sclerotium.


Fig17.24 Cladosporium fulvum. Symptoms on 

greenhouse-grown tomato leaves as seen from above. 

The pale leaf areas are chlorotic spots, at the underside of 

which a pale greyish-brown felt of conidiophores is produced. 

Fig17.25 Aureobasidium pullulans. (a) Blastoconidia developing 

from an undifferentiated hypha. Several conidia can form 

from the same point, i.e. conidiogenesis is polyblastic. 

(b) Thick-walled melanized chlamydospores formed from 

hyphal segments in an older agar culture. 

a low-calorie ingredient of foodstuffs and in 

pharmaceutical applications (Deshpande et al., 

1992; Leathers, 2003). 

Aureobasidium is a member of a group loosely 

called black yeasts. This is not a taxonomic term 

but simply describes melanized fungi which 

produce yeast states, especially in culture. 

Several species of black yeasts, notably species 

of Exophiala, Cladophialophora and Ramichloridium, 

are known as opportunistic human pathogens 

causing infections of the brain and other organs 

which can be fatal (Horré & de Hoog, 1999; de 

Hoog et al., 2000b). The microscopic features 

of these species have been described by de 

Hoog (1977) and, together with supplementary 

information, in an excellent compendium by 

de Hoog et al. (2000a). Although formerly considered 

to belong to the Loculoascomycetes, they 

are now recognized to be related to Capronia 

which is grouped in the Chaetothyriales (Haase 

et al., 1999; Untereiner, 2000), an order quite 

remote from the Loculoascomycetes but with 

possible affinities with Plectomycetes or 

Lecanorales (Winka et al., 1998). Black yeasts 

belonging to the Chaetothyriales are similar to 

those of the Dothideales not only in microscopic 

features, but also in their ecology, 

commonly occurring on living and decaying 

vegetation.

18 

Basidiomycota 


The Basidiomycota (colloquially basidiomycetes) 

are a large group of fungi with over 30 000 

species. They include many familiar mushrooms 

and toadstools, bracket fungi, puffballs, earth 

balls, earth stars, stinkhorns, false truffles, jelly 

fungi and some less familiar forms. Also classified 

here are the rust and smut fungi, which are 

pathogens of higher plants and may cause 

serious crop diseases. Most basidiomycetes are 

terrestrial with wind-dispersed spores, but some 

grow in freshwater or marine habitats. Many are 

saprotrophic and are involved in litter and wood 

decay, but there are also pathogens of trees such 

as the honey fungus, Armillaria, which attacks 

numerous tree species, and Heterobasidion annosum, 

which can seriously damage conifer plantations. 

Common woodland mushrooms such as 

species of Amanita, Boletus and their allies grow 

in a mutually symbiotic relationship with the 

roots of trees, forming ectotrophic (sheathing) 

mycorrhiza. Species of Rhizoctonia, representing 

mycelial forms of basidiomycetes, behave as 

pathogens towards a wide range of plants but 

are mycorrhizal associates of orchids. As saprotrophs, 

basidiomycetes play a vital role in 

recycling nutrients but they also cause severe 

damage as agents of timber decay, e.g. dry rot of 

house timbers by Serpula lacrymans. The fruit 

bodies (basidiocarps) of many mushrooms are 

edible, and some are grown commercially for 

food, notably Agaricus bisporus (¼ A. brunnescens, 

the white button mushroom), Pleurotus spp. 

(oyster mushrooms) and Lentinula edodes (shiitake). 

It is also well known that the basidiocarps 

of certain mushrooms are poisonous to eat, e.g. 

Amanita phalloides (the death cap). Some species 

have basidiocarps which are hallucinogenic, 

e.g. Amanita muscaria (the fly agaric) and 

Psilocybe spp. (‘magic mushrooms’). 

The mycelium of basidiomycetes may be very 

long-lived. Estimates based on the rate of growth 

and the diameter of circles of the fairy ring 

fungus Marasmius oreades growing in permanent 

pasture show that they may be centuries old. It 

has been estimated that the age of an individual 

mycelium of Armillaria in a Canadian forest is 

at least 1500 years, with an extent of 15 hectares 

and a probable biomass in excess of 10 tonnes, 

making it one of the largest organisms on earth 

(Smith et al., 1992). 

Not all basidiomycetes grow in the mycelial 

form; some are yeast-like and others are dimorphic, 

i.e. capable of switching between mycelial 

and yeast-like growth. A dimorphic species which 

is a dangerous human pathogen to immunocompromised 

patients is Filobasidiella (¼ Cryptococcus) 

neoformans causing cryptococcosis, a fatal disease 

of the brain (see pp. 661 664). 

18.2 Basidium morphology 

The characteristic structure of sexually reproducing 

basidiomycetes is the basidium. It is a 

spore-bearing cell which produces basidiospores 

externally through curved, tapering sterigmata

488 BASIDIOMYCOTA 

(Figs. 18.1d,e). Usually there are four spores but in 

some cases there are one, two or more than four 

basidiospores per basidium. Itersonilia perplexans 

has one-spored basidium-like structures (see 

Fig. 18.6a), the cultivated mushroom (Agaricus 

bisporus) has two-spored basidia, whilst basidia 

of the stinkhorn (Phallus impudicus) have as many 

as nine spores (see Fig. 20.9b). The form of the 

basidium varies, and this has taxonomic significance, 

different groups of basidiomycetes having 

distinctive types of basidium. In the mushrooms 

and their allies, the basidium is a cylindrical cell, 

undivided by septa (Fig. 18.1). Such basidia are 

termed holobasidia. InDacrymyces and Calocera 

(Dacrymycetales) the basidium is undivided by 

septa, but the body of the basidium is forked into 

two, with each arm of the fork developing a single 

basidiospore. The basidia of the Jew’s ear fungus, 

Auricularia auricula-judae, and related species 

are divided by transverse septa, whilst Tremella 

and its relatives have basidia with longitudinal 

septa. Basidia divided by septa are 

termed phragmobasidia or heterobasidia 

(Gr. phragmos ¼ a hedge or barricade; heteros ¼ 

other, different). In rust fungi (Uredinales) and 

smut fungi (Ustilaginales) the basidia develop 

from thick-walled, originally dikaryotic resting 

cells termed teliospores or chlamydospores. A 

thin-walled tubular structure, the promycelium, 

develops from this resting cell and becomes 

divided by transverse septa, each of the resulting 

cells producing one basidiospore (in rusts) or 

several basidiospores (sporidia) in smuts. Some of 

these different kinds of basidia are illustrated in 

Fig. 18.2. 

18.3 Development of basidia 

The development of a holobasidium is readily 

observed with the light microscope in the 

gill-bearing fungus Oudemansiella radicata which 

fruits on dead tree stumps (Figs. 18.1 and 19.18c) 

Fig18.1 Oudemansiella radicata. Stages in the development of basidia. (a) Young basidium with numerous vacuoles. Note the clamp 

connection at its base and the formation of a further basidial initial. (b) A later stage showing the appearance of a clear apical cap. 

(c) Localization of vacuoles towards the base of the basidium. (d) Development of sterigmata and spore initials. A basal vacuole is 

enlarging. (e) Fully developed basidium.The spores are full of cytoplasm, whilst the body of the basidium contains only a thin lining of 

cytoplasm surrounding an enlarged vacuole. (f) Discharged basidiospores.

DEVELOPMENT OF BASIDIA 

489 

Fig18.2 Some different kinds of basidia. (a) Longitudinally divided basidium of Exidiaglandulosa (Tremellales). (b) Tuning-fork type 

of basidium of Calocera viscosa (Dacrymycetales). (c) Transversely divided basidium of Auricularia auricula-judae (Auriculariales). 

(d) Germinating chlamydospore of Ustilago avenae (Ustilaginales). A transversely septate promycelium has developed and each 

segment is forming sporidia. (e) Germinating teliospore of Puccinia graminis (Uredinales). A transversely septate promycelium has 

developed and each segment is producing a single basidiospore. 

and has particularly large basidia. A detailed 

description of the process has been given by 

Corner (1948) for O. canarii. Ultrastructural 

studies have also been made on a range of 

fungi with holobasidia, e.g. the split-gill 

(Schizophyllum commune; Wells, 1965), the agarics 

Coprinus cinereus (McLaughlin, 1973, 1977, 1982) 

and Panellus stypticus (Lingle et al., 1992), the 

clavarioid fungus Clavicorona pyxidata (Berbee & 

Wells, 1989) and the bolete Boletus rubinellus 

(McLaughlin, 1973; Yoon & McLaughlin, 1979, 

1984). 

18.3.1 Cytological aspects 

In Oudemansiella radicata the basidium arises as 

the terminal cell of a hypha making up the gill 

tissue on the underside of the cap of the fruit body 

(basidiocarp). Basidia are packed tightly together 

in the hymenium at the surface of the gill. A 

basidium is at first filled with dense cytoplasm, 

but soon several small vacuoles appear near its 

base. Later these coalesce into a single large 

vacuole at the base of the basidium and, by 

enlargement of this vacuole, cytoplasm is pushed 

towards the apex of the basidium. A clear cap is 

differentiated at the tip and it is in this region 

that the sterigmata develop. Corner (1948) postulated 

that there must be four elastic areas in the 

upper part of the basidium wall from which 

the sterigmata extend. The wall of the upper part 

of the basidium consists of two layers, the outer of 

which is mucilaginous, the inner firmer. In the 

areas where the sterigmata are about to bulge 

out, a new layer of wall material is deposited 

between these two original layers. The outer 

mucilaginous layer of the basidial wall bursts 

and the apex of the sterigma grows out. It is 

surrounded by two wall layers, the inner of which 

is continuous with the inner wall layer of the 

basidium (Clémençon, 2004). Ultrastructural 

studies of Boletus rubinellus show that, in the 

region where the sterigmata appear, the basidial


wall is indeed thinner and differs in structure 

from the other parts of the wall (Yoon & 

McLaughlin, 1984). Beneath these areas there is 

some evidence of cytoplasmic differentiation, 

such as the presence of microtubules and vesicles. 

The growth of sterigmata can be compared to 

hyphal tip growth, except that a Spitzenkörper 

is absent (McLaughlin, 1973). At the tips of the 

sterigmata of Coprinus cinereus, vesicles apparently 

fusing with the plasma membrane have been 

observed by transmission electron microscopy 

studies, and vesicles of similar size were also 

found in the basidium (McLaughlin, 1973). Corner 

(1948) suggested that the force for the development 

of basidia comes from the expansion of the 

basal vacuole which acts as a piston, ramming 

the cytoplasm into the spores. Ripe basidia thus 

contain a large vacuole but very little cytoplasm 

(Fig. 18.1e). The vacuole, which is filled with 

liquid, keeps the basidium turgid until spore 

discharge has occurred. 

The tip of the sterigma expands to form a 

small spherical knob, the apophysis (Gr. apo- ¼ 

away from, separate; physis ¼ growth). Further 

development of basidiospores is asymmetric, 

expansion being more rapid towards the outside 

of the long axis of the basidium. The narrow 

point of attachment of the spore at the tip of the 

sterigma is the eventual point of spore separation 

and is termed the hilum. The non-expanded 

part of the apophysis persists as the hilar 

appendix (Fig. 18.3a). 

18.3.2 Nuclear events 

Typically, a basidium is at first binucleate; it is 

formed on a dikaryotic mycelium, i.e. a mycelium 

with segments containing two haploid nuclei 

which are usually genetically different (see 

Section 18.9). In this cell nuclear fusion (karyogamy) 

occurs (see Fig. 18.4) and is followed immediately 

by meiosis, giving rise to four haploid 

nuclei. As in most fungi, division is intranuclear; 

the nuclear membrane remains intact. Meiosis 

occurs in the upper part of the basidium. In 

narrow basidia the plane of the second meiotic 

nuclear division lies parallel to the long axis of 

the basidium. This type of nuclear division is 

termed chiastic (Gr. chiastos ¼ crossed, arranged 

diagonally) and basidia with nuclear division of 

this sort are termed chiastobasidia. In contrast, 

in broader basidia, the plane of both meiotic 

nuclear divisions is transverse to the long 

axis. Nuclear divisions of this type are stichic 

(Gr. stichos ¼ a line or row of things) and the 

corresponding term for basidia with such division 

is stichobasidium. The plane of nuclear 

division has relevance to taxonomy; chiastobasidia 

are found in mushrooms and toadstools 

whilst stichobasidia are more characteristic of 

certain genera of bracket fungi in the polyporoid 

clade. Terms used to define different parts of 

a basidium are probasidium, the part within 

which karyogamy occurs, and metabasidium, 

the part within which meiosis occurs (see Kirk 

et al., 2001). The four haploid nuclei formed 

during meiosis move into the basidiospores 

which are therefore usually four in number. As 

they pass through the sterigmata, the nuclei 

are often elongated and tapered apically. They 

may be led through the sterigmata by microtubules 

attached to the nuclear spindle pole 

bodies (Thielke, 1982; Lingle et al., 1992). 

In many basidiomycetes, meiosis is followed 

by a post-meiotic mitosis (Duncan & Galbraith, 

1972; Clémençon, 2004) which may happen in 

different places: (1) In the upper part of the 

basidium. Four of the eight nuclei enter the 

spores, and those remaining in the basidium 

abort. The ripe spores are thus uninucleate, e.g. 

in Cantharellus cibarius. (2) At the base of or inside 

the sterigmata. One nucleus enters each spore 

and the other four remain in the basidium 

and degenerate, e.g. in Collybia butyracea. (3) In 

the young spore. Four of the daughter nuclei 

migrate back into the basidium where they 

degenerate, e.g. in Paxillus involutus. (4) In the 

young spore, but all eight nuclei remain in the 

four spores and none abort; the basidium is left 

devoid of nuclei. 

18.4 Basidiospore development 

On the adaxial side of the apophysis, an electrondense 

cytoplasmic region appears at the moment

BASIDIOSPORE DEVELOPMENT 

491 

Fig18.3 Coprinus cinereus.Transmission electron micrographs 

of sections illustrating development of basidiospores. (a) Stage 

4 basidiospore expanding at the tip of its sterigma.The hilar 

appendix body (HAB) is appressed to a wall thickening. (b) An 

early stage 4 basidiospore with the conical hilar appendix body 

in firm contact with the spore plasmalemma.For further 

explanation see p. 490. Photomicrographs kindly provided by 

D. J. McLaughlin. 

of its initiation and, in most cases, persists 

throughout the development of the basidiospore, 

disappearing only shortly before spore discharge. 

It is hemispherical or conical, lying immediately 

within the plasma membrane of the apophysis 

and closely appressed to the wall of the hilar 

appendix (see Figs. 18.3a,b). This structure is 

the hilar appendix body and has been reported 

from several basidiomycetes, including Boletus 

rubinellus, Coprinus cinereus (McLaughlin, 1973, 

1977), Lactarius lignyotellus (Miller, 1988) and 

Panellus stypticus (Lingle et al., 1992). It is probably 

present in all ballistosporic species. Its function 

is not understood. Possibly it is involved in the 

softening of the closely adjoining wall layers 

of the hilar appendix or in the extrusion of 

material related to the expansion of Buller’s 

drop (see Fig. 18.8). Another possibility is that it 

blocks the movement of wall vesicles into the 

adaxial side of the spore, so possibly contributing 

to the asymmetric shape of the spore. During 

further development, the wall of the hilar 

appendix thickens considerably, and uneven 

expansion of the wall of the developing spore 

occurs. Expansion of the abaxial face is more 

rapid, leaving the spore asymmetrically perched 

on the sterigma, attached at the hilum and with 

the remains of the apophysis forming the hilar 

appendix (see Fig. 1.20). In Coprinus cinereus, 

McLaughlin (1977) has distinguished four successive 

stages of basidiospore expansion (see 

Fig. 18.5a). 

Stage 1, inception. This is characterized by 

the spherical enlargement of the sterigma apex 

to form a basidiospore primordium 0.6 0.8 mm 

in diameter. The hilar appendix body is already 

differentiated. The thin basidiospore wall is 

three-layered at first. Microtubules are occasionally 

present in the sterigma, being orientated 

parallel to its long axis. 

Stage 2, asymmetric growth. The basidiospore 

initial grows asymmetrically on its abaxial side, 

and the hilar appendix develops. The hilar 

appendix body becomes conical and appressed 

to the plasma membrane of the spore initial. The 

hilar appendix is initiated adjacent to the hilar 

appendix body. The basidiospore wall thickens, 

being thickest at the apex of the spore, and is sixlayered.


Fig18.4 Life cycle of the basidiomycete Coprinus (diagrammatic and not to scale).The basidiocarp develops from a dikaryotic 

secondary mycelium and produces numerous basidia on the surface of its gills beneath the cap. Progressive stages of basidium 

maturation involving karyogamy (K) and meiosis (M) are indicated. Eventually, each basidium forms four basidiospores, each 

containing a single haploid nucleus. In many basidiomycetes there is a post-meiotic mitosis, giving rise to two identical haploid nuclei 

in each basidiospore (not shown here). Basidiospores are discharged by the surface-tension catapult mechanism involving Buller’s 

drop. Discharged basidiospores germinate to form haploid (monokaryotic) mycelia with simple transverse septa. In Coprinus,these 

often produce upright conidiophores which form numerous sticky haploid oidia.The apex of a monokaryotic hypha in the vicinity of 

an oidium of compatible mating type will respond chemotropically by growing towards the compatible oidium (homing reaction). 

Fusion (plasmogamy, P) between the hypha and the oidium initiates the formation of a dikaryotic mycelium bearing clamp 

connections. Nuclear fusion does not occur at this stage.The dikaryotic mycelium can develop basidiocarps under appropriate 

environmental conditions.Open and closed circles represent haploid nuclei of opposite mating type; the diploid nucleus is drawn 

larger and half-filled. 

Stage 3, equal enlargement. This is characterized 

by spherical enlargement of the basidiospore. 

Growth is at an angle of about 45° to the 

sterigma apex (see Fig. 18.5a). The hilar appendix 

body projects further into the spore wall. It is 

conical or hemispherical, with the apex of the 

cone or base of the hemisphere projecting 

towards the hilar appendix. The outermost 

layer of the basidiospore wall is sticky. 

Stage 4, elongation. Basidiospores grow in 

length and a pore cap is formed at the upper end 

of the spore. The spore wall becomes darkly 

pigmented, starting at the upper end. 

Similar asymmetric changes in spore expansion 

have been reported by Yoon and McLaughlin 

(1984) for basidiospores of Boletus rubinellus 

(Fig. 18.5b). Elongation of the spore occurs 

mainly at later stages of development. 

In certain basidiomycetes, e.g. Amanita 

vaginata, the basidiospore is spherical. This 

involves even wall expansion during development 

and implies that the wall structure is

THE MECHANISM OF BASIDIOSPORE DISCHARGE 

493 

point of abscission (Yoon & McLaughlin, 1986; 

Money, 1998). 

18.5 The mechanism of 

basidiospore discharge 

Fig18.5 Asymmetric expansion of basidiospores during 

development. (a) Coprinus cinereus.Changes in shape and the 

axis of growth (shown on the right) at successive stages in 

basidiospore development.The numbers on the left indicate 

spore stages. (b) Boletusrubinellus.Changes in shape and the 

major axis of growth (long arrows) at successive 

developmental stages.For further explanation see text. 

(a)fromMcLaughlin(1977)and(b)fromYoonandMcLaughlin 

(1984), by copyright permission of the American Journalof 

Botany. 

homogeneous. Corner (1948) believed that the 

non-spherical shape of basidiospores was the 

result of differential setting of the wall material. 

This may well be true, but more recent studies 

have shown that the basidiospore wall also 

varies in thickness. Many basidiospores have 

smooth outer walls, but others have characteristic 

ornamentations, e.g. spines, folds or ridges. 

The ornamentations generally develop by extension 

of the outer wall layer of the basidiospore 

(Pegler & Young, 1971; Clémençon, 2004). In such 

spores, e.g. those of Lactarius and Russula, only 

the main body of the spore is ornamented, 

whereas the region of the adaxial face immediately 

above the hilar appendix is smooth. This 

region is termed the suprahilar plage, disc or 

depression (Pegler & Young, 1971, 1979). It plays 

an important part in the spore discharge 

mechanism (see below). 

Abscission of the basidiospore from its sterigma 

is preceded by the formation of a plug of 

material, the hilar plug which blocks the spore 

hilum, and a sterigmal plug of wall material 

immediately below the hilum. Between the two 

plugs a septum appears which represents the 

With the exception of the gasteromycetes (see 

Chapter 20), in most terrestrial basidiomycetes 

basidiospores are ballistospores, i.e. they are 

actively projected from basidia. Various suggestions 

have been made as to the mechanism of 

ballistospore discharge (see Webster & Chien, 

1990), but the one which we now accept is the 

surface tension catapult, originally suggested by 

Buller (1922) and Ingold (1939). Discussions of 

the various theories of basidiospore discharge 

have been written by Webster et al. (1988) and 

Money (1998). Shortly before discharge, dissolution 

of the abscission layer occurs, indicated by 

a slight wobble in the position of the spore. Then 

a spherical drop of liquid, Buller’s drop, forms at 

the hilar appendix and a shallower liquid 

deposit, the adaxial drop (adaxial blob), appears 

on the face of the spore above the hilar appendix 

(Fig. 18.7). Cinephotography has been used to 

illustrate these events (Webster & Hard, 1998b; 

Webster, 2006b). Both drops increase in size until 

they eventually coalesce, and spore discharge 

then immediately occurs (Pringle et al., 2005). 

Experimental investigations on the phenomenon 

of ballistospore discharge have focused 

on Itersonilia perplexans, an unusual heterobasidiomycete 

with large ballistospores. This fungus 

is a weak plant pathogen and is commonly 

associated with lesions caused by other pathogens 

such as rust and smut fungi. It also grows in 

basidiocarps of certain jelly fungi and can be 

readily isolated by allowing it to shoot off its 

ballistospores from the basidiocarps of Dacrymyces 

stillatus or Auricularia auricula-judae (Ingold, 1983a, 

1984a). In culture it forms a clamped dikaryotic 

mycelium, the tips of whose branches swell to 

form clamped sporogenous cells, each with a 

single ballistospore (Fig. 18.6a). The sporogenous 

cells do not fully match the definition of basidia 

because nuclear fusion and meiosis do not occur 

in them; instead the dikaryotic cell forms a


dikaryotic ballistospore directly. A discharged 

primary ballistospore may germinate by a germ 

tube or by repetition to form a secondary 

ballistospore (Fig. 18.6b). Yeast-like growth can 

also occur, especially on rich media. 

Working with Itersonilia, several observations 

were made which provided clues to the mechanism 

of discharge. (1) Ballistospores can be 

detached from their sterigmata with a micromanipulator 

needle and spores so detached still 

develop Buller’s drop. This shows that the liquid 

in the drops does not originate from liquid 

transported through sterigmata. (2) During 

normal discharge, although the volume of 

Buller’s drop may attain 60% of that of the 

spore, there is no decrease in the dimensions of 

the ballistospore, indicating that Buller’s drop 

does not come from within the spore. The same 

observation has been made on other basidiomycetes 

and has led to the suggestion that the 

liquid in Buller’s drop and also in the adaxial 

drop is formed by condensation of water vapour 

around a hygroscopic substance extruded from 

the hilar appendix and through the spore wall 

(Webster et al., 1984a,b, 1989). Washings from the 

spores of basidiomycetes belonging to several 

different taxonomic groups were analysed by 

gas liquid chromatography, and all gave a positive 

result for the presence of mannitol. Glucose 

was also sometimes detected. The presence of 

mannitol and hexose in liquid drawn off by 

a micropipette from Buller’s drops in Itersonilia 

was confirmed by microscope fluorimetry, and 

measurements of the solute concentrations in 

Buller’s drop corresponded closely to the calculated 

concentrations which would be necessary 

to drive the uptake of water from a saturated 

atmosphere at the rates observed (Webster et al., 

1995). 

The surface tension catapult mechanism 

postulates that, as Buller’s drop develops, the 

centre of mass of the spore plus drop moves 

towards the hilar appendix (Fig. 18.8b). The 

coalescence of Buller’s drop with the adaxial 

drop causes a rapid redistribution of mass away 

from the hilar appendix, resulting in a momentum 

which carries the spore plus drop away from 

the sterigma (Fig. 18.8c; Webster et al., 1988). 

Pringle et al. (2005) have suggested that an even 

Fig18.6 Itersonilia perplexans. (a) Basidium (sporogenous cell) 

bearing a single ballistospore. Note the clamp connection at 

the base of the basidium (arrow). (b) A primary ballistospore 

has germinated by repetition to form a secondary 

ballistospore. 

greater momentum may be generated by the 

fusion drop moving towards the basidiospore 

apex and coming to an abrupt halt upon reaching 

it. For this mechanism to be effective, a rigid 

sterigma is required, and it is likely that the 

turgor pressure of the vacuolated basidium 

contributes to the required rigidity (Money, 1998). 

The requirement of high humidity for effective 

operation of the mechanism is a likely 

explanation for observations that basidiospore 

concentrations in the air peak at night (Kramer, 

1982). High humidity develops in the space 

between agaric gills or inside the hymenial 

tubes of toadstools and bracket fungi. The 

presence of free water would, of course, prevent 

operation of the surface tension catapult, and 

this may be the reason why agaric basidiocarps 

are often umbrella-shaped. The impossibility of 

the surface tension catapult mechanism operating 

under water also explains why, although 

some basidiomycetes grow vegetatively in fresh

NUMBERS OF BASIDIOSPORES 

495 

Fig18.7 Itersonilia perplexans. Appearance of Buller’s drop and adaxial drop. a 1 

a 5 

show events immediately preceding and following 

the discharge of a secondary ballistospore. An adaxial drop is clearly seen. b 1 

b 5 

show drops developing on a primary ballistospore. 

Note that there is no decrease in the size of the ballistospore as the drops develop. c 1 

c 3 

illustrate failure of ballistospore discharge. 

Here coalescence of Buller’s drop and the adaxial drop is not accompanied by separation of the spore from its sterigma and the 

spore soon topples from its perch. Reprinted from Webster et al. (1984a), with permission from Elsevier. 

water or the sea, they do not produce ballistospores 

there. 

The spore of Itersonilia is subjected to considerable 

acceleration and moves away from the 

sterigma at a velocity of over 1 m s 1 . However, 

the large surface/mass ratio of a relatively small 

object like a ballistospore results in high wind 

resistance and therefore rapid deceleration and 

loss of momentum, so that the spore soon falls 

under the preponderant influence of gravitational 

force. The trajectories of ballistospores 

of most fungi follow a short horizontal path 

for a distance of about 0.1 0.3 mm and then 

turn through a right angle so that spores in still 

air drift downwards at a steady sedimentation 

velocity. This characteristic trajectory, termed a 

sporabola, ensures that basidiospores projected 

into the space between the gills or into the 

lumen of a pore turn vertically downwards 

before hitting the opposing hymenial surface. 

18.6 Numbers of basidiospores 

The number of basidiospores produced by a 

single basidiocarp can be extremely high. Buller 

(1909) estimated that the detached cap of the


mushroom Agaricus campestris produced 1.8 10 9 

spores over 2 days at an average rate of 

40 million h 1 . Estimates for some other basidiomycetes 

are given in Table 18.1. The mycelia of 

all these fungi are perennial and an individual 

mycelium may produce numerous basidiocarps 

over a period of many years. It is therefore clear 

that an individual basidiospore has an infinitesimal 

chance of successfully establishing a 

fruiting mycelium. 

Fig18.8 Representation of events associated 

with ballistospore discharge. (a) Ballistospore 

attached to its sterigma before drop 

formation.The closed circle within the spore 

indicates the centre of mass of the spore. 

(b) Buller’s drop appears at the hilar appendix. 

The adaxial drop emerges on the spore wall 

above it and extends downwards as it 

increases in size.The centre of mass of spore 

plus drop moves to a position nearer the hilar 

appendix. (c) Contact between the two drops 

is followed by immediate coalescence and the 

combined mass of liquid moves rapidly up the 

adaxial face of the spore away from the hilar 

appendix.The centre of mass moves very 

rapidly in the direction of the thin arrow and 

the spore drop system gains kinetic energy 

and momentum in the same direction, 

simultaneously exerting an opposite force F 

on the sterigma at the hilum (thick arrow). 

Some angular momentum is also exerted on 

the spore, related to the distance a between 

the hilum and the hilar appendix. Reprinted 

from Webster et al. (1988), with permission 

from Elsevier. 

18.7 Basidiospore germination and 

hyphal growth 

18.7.1 Germination 

Basidiospores may remain dormant and retain 

viability for several months or even for a few 

years if conditions are unsuitable for germination. 

Dormancy is frequently exogenous, i.e. the 

spores require some external chemical or physical 

stimulus before germination can occur. 

Germination may be direct by production of a 

germ tube, by repetition (i.e. the formation of a 

secondary ballistospore), or by the formation of 

conidia. Repetitious germination is common in 

certain jelly fungi (Tremellales) (see Figs. 18.6b, 

21.7b and 21.13d). Germination by the formation 

of conidia is illustrated for Dacrymyces stillatus 

(Fig. 21.4a), Auricularia auricula-judae (Fig. 21.6c) 

and by yeast-like budding in Tremella frondosa (Fig. 

21.13c). During direct germination, germ tubes 

usually emerge through a special germ pore at 

the hilum or, as in Coprinus, through a pore at 

the opposite end of the spore. 

18.7.2 Monokaryotic and dikaryotic 

hyphae 

Because the nuclear divisions involved in basidiospore 

formation are meiotic, basidiospores 

are haploid. Since the post-meiotic nuclear 

divisions are mitotic, if there are several nuclei 

in a single basidiospore these are usually 

genetically identical. They are said to be homokaryotic 

(Gr. homos ¼ equal, alike; karyon ¼ a nut, 

here meaning nucleus). At germination, repeated 

mitotic nuclear divisions occur and the early 

germ tubes may consequently be multinucleate 

and coenocytic. Transverse septa are laid down 

behind the growing hyphal tip and eventually 

divide the hypha into segments which contain 

only a single nucleus. The uninucleate segments 

and the hyphae which contain them are said to 

be monokaryotic. The terms homokaryon and 

monokaryon or primary mycelium have also 

been applied to such haploid mycelia. As part of 

the sexual cycle, monokaryotic hyphae of genetically 

distinct mating type undergo plasmogamy 

(somatogamy), i.e. they fuse together and initiate 

the formation of a mycelium made up of

497 

BASIDIOSPORE GERMINATION AND HYPHAL GROWTH 

Coprinus comatus 5.2 10 9 2days 2.610 9 

Table 18.1. Numbers of basidiospores produced from single basidiocarps of selected basidiomycetes. From 

Buller (1922). 

Species Totalnumber of spores Spore fallperiod Spores discharged perday 

Calvatia gigantea 7 10 12 

Ganoderma applanatum 5.5 10 12 6months 310 10 

Polyporus squamosus 5 10 10 14 days 3.5 10 9 

Agaricus campestris 1.6 10 10 6days 2.610 9 

segments, each of which contains two genetically 

distinct nuclei. Such mycelia are said to be 

dikaryotic and heterokaryotic. The term secondary 

mycelium is also used. 

18.7.3 Dolipore septa 

The transverse septa which divide both monokaryotic 

and dikaryotic hyphae into segments 

are incomplete; they contain a central pore 

which permits cytoplasmic continuity between 

adjacent segments. The septal pore is surrounded 

by a barrel-shaped flange of thickened wall 

material. Such septa, which are characteristic of 

basidiomycete mycelia, are known as dolipore 

septa (Lat. dolium ¼ large jar, cask). They are 

discernible by light microscopy, especially with 

ammoniacal Congo red staining, but interpretation 

of their structure is only possible in sections 

or freeze-fractured cells viewed by electron 

microscopy (Figs. 18.9 and 18.10). Septal development 

begins by centripetal ingrowth of a 

membrane on which wall material (glucan and 

chitin) is deposited at both faces from associated 

vesicles (for references see Moore, 1985). The 

thickening surrounding the pore results from 

more rapid deposition of wall material, but there 

is evidence that very thick pore rims may be 

an artefact associated with chemical fixation. 

The pore itself may be blocked by an occlusion 

shaped like two champagne corks attached end 

to end (Fig. 18.9), but blockage of the pore is not 

a permanent feature. In some cases there is a 

transverse central plate in the pore canal 

(Fig. 18.10b). 

Overarching the septal pore on each side of 

the septum is a specialized portion of endoplasmic 

reticulum known as the septal pore cap 

or parenthesome (parenthesis ¼ round bracket, 

Gr. soma ¼ body). In some cases a second parenthesome 

(outer cap) has been reported. In many 

basidiomycetes with holobasidia (i.e. Homobasidiomycetes), 

the parenthesomes are perforated 

(fenestrated), but in many Heterobasidiomycetes, 

e.g. Auricularia, there is only a single perforation 

or none (Lü & McLaughlin, 1991; Wells, 1994; 

Wells & Bandoni, 2001). Other variations in 

ultrastructure are known and can be characteristic 

of different groups of basidiomycetes, so 

that the dolipore/parenthesome complex is 

considered to be of taxonomic significance 

(Khan & Kimbrough, 1982; Moore, 1985, 1996; 

McLaughlin et al., 1995; Müller et al., 1998a). 

An important role of the dolipore/parenthesome 

complex is to secure the integrity of hyphal 

cells and to maintain intercellular communication 

and transport of some organelles. A variety 

of cytoplasmic structures has been reported from 

within the pores of Rhizoctonia solani. These 

include small tubular and filamentous structures, 

small vesicles, tubular endoplasmic reticulum 

and other plugging material. The movement 

of mitochondria through the septal pore cap 

has also been documented (Müller et al., 2000). 

Whilst the movement of most organelles 

through the septal pore is permitted, the passage 

of nuclei is not, and this is possibly a consequence 

of their larger size. The migration of 

nuclei following plasmogamy between two sexually 

compatible monokaryotic mycelia is associated 

with enzymatic dissolution of the dolipore 

(see below). Another important function of 

dolipores is the repair of hyphal damage, the 

septal pore being rapidly plugged by electrondense 

material in the compartment of a hypha


Fig18.9 Diagrammatic 

interpretation of a basidiomycete 

dolipore/parenthesome septum. 

Reprinted from Moore and 

Marchant (1972), by copyright 

permission of the National Research 

Council of Canada. 

adjacent to the damaged segment (Aylmore et al., 

1984; Markham, 1994). 

18.7.4 Plasmogamy, dikaryotization, 

clamp connections 

When two compatible monokaryotic mycelia 

make contact, the hyphal walls separating 

them break down and cytoplasmic continuity 

(i.e. plasmogamy) of the two monokaryons is 

established. In Coprinus cinereus and some other 

fungi, plasmogamy may also occur following 

fusion of an oidium of one mating type with 

a hyphal tip of a compatible monokaryon. 

Nuclear migration follows and is associated with 

the breakdown of the dolipore/parenthesome 

complex to permit transfer of a compatible 

nucleus from one compartment to another 

(Giesy & Day, 1965; Marchant & Wessels, 1974). 

The mycelium which develops after plasmogamy 

is dikaryotic and the process of conversion 

of a monokaryon to a dikaryon is termed 

dikaryotization. 

Nuclear fusion (i.e. karyogamy) is delayed 

until the basidia have formed, and is thus 

preceded by a prolonged dikaryotic state. As a 

result of nuclear migration, the tip of a dikaryon 

contains two nuclei which are of different 

mating types in heterothallic basidiomycetes. 

The speed of nuclear migration can be much 

higher than the hyphal growth rate. Nuclear 

migration rates have been measured in a 

number of fungi, e.g. Coprinus cinereus

BASIDIOSPORE GERMINATION AND HYPHAL GROWTH 

499 

Fig18.10 Longitudinal sections of the dolipore/parenthesome septum in two basidiomycetes as viewed by transmission electron 

microscopy. (a) Auriscalpium vulgare, a homobasidiomycete.The parenthesome is perforated. (b) Auricularia auricula-judae, 

a heterobasidiomycete.The parenthesome is imperforate. Photographs kindly provided by D. J. McLaughlin. 

(0.5 1.0 mm h 1 ), Coprinus congregatus (4 cm h 1 ) 

and Schizophyllum commune (1.5 5.4 mm h 1 ) 

(Snider, 1965, 1968; Raper, 1966; Ross, 1976). 

Microtubules are associated with migrating 

nuclei in S. commune (Raudaskoski, 1972) and in 

Trametes versicolor (Girbardt, 1968). In the tip cell 

and also in the subapical segments (Fig. 18.12) of 

a dikaryon, the two nuclei maintain a constant 

distance apart from each other, indicating that 

they are paired together by microtubules. They 

also move forward together at a fixed distance 

from the apex (Kamada et al., 1993; Torralba et al., 

2004). 

The two nuclei in a dikaryotic hyphal tip 

divide simultaneously, a process termed 

conjugate nuclear division. In most but not all 

basidiomycetes, division is accompanied by 

nuclear rearrangement involving the formation 

of clamp connections, visible as a lateral bulge 

in the hyphal wall adjacent to a transverse 

septum. The events connected with the development 

of a clamp connection are set out diagrammatically 

in Fig. 18.11. A clamp connection 

develops near the position of the pair of nuclei 

in the terminal segment of a dikaryotic hypha 

(Fig. 18.11b). A backwardly directed hyphal 

branch (hook) develops and one daughter 

nucleus migrates into it and divides there 

mitotically at the same time as mitotic nuclear 

division is taking place in the subterminal 

nucleus (Fig. 18.11c). A transverse septum develops 

in the main hypha between the two daughters 

of the subterminal nucleus and an oblique 

septum also forms at the base of the hook 

(Fig. 18.11d). The hook, containing a single 

daughter nucleus, grows round the transverse 

septum of the main hypha and its tip fuses with 

the wall of the subterminal cell. Plasmogamy 

occurs and the nucleus from the hook migrates 

into the subterminal cell (Fig. 18.11e). The two 

pairs of nuclei then move away from the 

transverse septum (Fig. 18.11f). The clamp connection 

is a device which ensures that each segment 

of a dikaryotic hypha contains two genetically 

distinct nuclei. In the absence of clamps or of 

some other mechanism for rearrangement of


Fig18.11 Diagrammatic representation of the 

sequence of events associated with the formation 

of a clamp connection in the dikaryotic hypha of a 

basidiomycete. (a) Terminal segment of a hypha 

with two genetically dissimilar nuclei. (b) A lateral 

bulge in the hypha appears near the paired nuclei. 

The leading nucleus moves into the bulge. (c) The 

two nuclei undergo conjugate (i.e. simultaneous) 

nuclear division. Mitosis of the leading nucleus 

occurs within the bulge. (d) The lateral bulge has 

developed into a backwardly directed branch or 

hook with one daughter of the leading nucleus at 

its tip. One of the daughter subterminal nuclei 

moves forward.Transverse septa have developed 

simultaneously in the main hypha and at the base of 

the hook. (e) The tip of the hook has fused with the 

wall of the main hypha. Its nucleus has moved into 

the main hypha and taken up position behind the 

daughter of the subterminal nucleus. (f) The pairs 

of nuclei move away from the transverse septum in 

the main hypha, the terminal pair moving nearer 

the hyphal tip and the subterminal pair distally. 

Note that both segments contain dissimilar nuclei 

but that their arrangement has been reversed. 

nuclei, there would be a tendency for dikaryotic 

mycelia to break down into homokaryotic 

segments. Whilst it is reasonable to infer that 

mycelia with clamps at the septa are dikaryotic, 

the converse is not true because there are 

numerous basidiomycetes in which the dikaryotic 

mycelium does not bear clamps, and this is 

especially true of hyphae making up basidiocarps. 

For a fuller discussion of dikaryon 

formation see Casselton and Economou (1985). 

18.7.5 Aggregates of vegetative hyphae 

Basidiomycete hyphae can aggregate to form 

complex vegetative structures such as hyphal 

strands, mycelial cords, mycelial sheets and 

rhizomorphs (Butler, 1966; Watkinson, 1979; 

Rayner et al., 1985). These often grow more 

rapidly than individual hyphae, connect food 

bases such as litter fragments in soil, fallen logs 

and tree stumps, and are capable of rapid twoway 

conduction of water and nutrients. 

Mycelial cords 

Mycelial cords have been defined by Boddy (1993) 

as aggregations of predominantly parallel, 

longitudinally aligned hyphae (see Fig. 1.13). 

They are especially common in wood-decaying 

basidiomycetes but are also involved in the 

underground spread of basidiomycetes forming 

ectomycorrhiza. Wood-decaying mycelial cord 

formers are a very successful ecological group, 

using their cords in a variety of strategies to 

secure resources, e.g. by displacing other fungi 

from food bases or exploring new resources in 

the soil. The cords show relatively little differentiation 

in structure and pigmentation. 

Examples of fungi with mycelial cords are the 

stinkhorn (Phallus impudicus) and the agaric 

Megacollybia platyphylla. Their white cords can 

extend for many metres in the soil and can be 

traced back from the fruit bodies to tree stumps 

or other food bases if highly motivated students 

and digging tools are available (Fig. 18.13a). 

Rhizomorphs 

The term rhizomorph refers to the root-like form 

of these mycelial aggregates which are more 

highly differentiated than mycelial cords and are 

often pigmented brown or black due to the 

presence of melanin in the walls of small,

ASEXUAL REPRODUCTION 

501 

Fig18.12 Subapical hypha of a dikaryon of Omphalotus olearius. (a) Interference contrast image showing the segments delimited by 

clamp connections (arrowheads). (b) DAPI fluorescence staining of the same hypha showing that each segment contains two paired 

nuclei (bright fluorescent objects). 

thick-walled cells making up the rind (Townsend, 

1954; Cairney, 1991). The best-known example of 

a rhizomorph is that of the honey fungus 

Armillaria mellea, a serious tree pathogen whose 

flat, black, bootlace-like strands often persist 

for long periods beneath the bark of trees killed 

by the fungus (see pp. 16 18 and Fig. 18.13b). 

Many ectomycorrhizal fungi especially in the 

boletoid clade form hyphal aggregates which 

show intermediate features between mycelial 

cords and rhizomorphs. 

Sclerotia 

Sclerotia, an adaptation to prolonged survival 

and propagation, develop in some basidiomycetes 

(see pp. 18 20). They vary in size from 

50 mm to several centimetres and in weight from 

10 mg to several kilogrammes. They also vary in 

organization from loose aggregations of dark 

hyphae to highly differentiated structures with a 

rind of smaller, dark thick-walled cells and a 

medulla of larger, colourless, thin-walled cells 

packed with food reserves (Willetts, 1971, 1972; 

Clémençon, 2004). Many of the sclerotial types 

described on pp. 18 20 are produced by 

Basidiomycota, e.g. the loose type (Rhizoctonia 

solani) and the strand type (Sclerotium rolfsii). Some 

sclerotia are massive, as in Polyporus mylittae 

where they may give rise to fruit bodies 

(carpogenic development; Figs. 18.13c,d). 

Basidiocarps of many common agarics such as 

Coprinus cinereus, Collybia tuberosa, Hygrophoropsis 

aurantiaca and Paxillus involutus may develop from 

smaller sclerotia, and these are also characteristic 

of the clavarioid fungus Typhula (Corner, 

1950). Sclerotial germination, especially of plant 

pathogenic fungi such as Rhizoctonia, is more 

usually by the outgrowth of mycelium (myceliogenic 

germination). 

Pseudosclerotia with a similar function to 

sclerotia, but consisting of a compacted mass of 

intermixed substratum, soil, stones, etc., support 

the fruiting of certain polypores such as Polyporus 

tuberaster (the stone fungus, tuckahoe), and 

Meripilus giganteus. 

18.8 Asexual reproduction 

Conidium formation is less commonly reported 

in the Basidiomycota than in the Ascomycota. 

Conidia may develop on monokaryotic or dikaryotic 

mycelia, sometimes on both. They may also 

form on basidiocarps. Conidia may have an 

asexual function in propagation and dispersal 

or may also fulfil a sexual role. We can only 

consider a few examples. In terms of structure 

and ontogeny, basidiomycete conidia are of three 

basic kinds which are summarized below (see 

Kendrick & Watling, 1979; Clémençon, 2004).


Fig18.13 Hyphal aggregates of basidiomycetes. (a) White mycelial cords of Megacollybia platyphylla interconnecting a decaying log of 

wood serving as food base (far left) with two basidiocarps, exposed by removing the surface leaf litter. (b) Rhizomorphs of Armillaria 

mellea in their typical location between the bark (which has been stripped) and the wood of a dead tree. (c,d) The giant 

subterranean sclerotium of Polyporus mylittae which has produced an above-ground fruit body (c).When cut open, the sclerotium 

consists of a dark rind enclosing a medulla with a texture resembling compacted boiled rice (d). (c,d) reprinted from Fuhrer (2005), 

with permission by Bloomings Books Pty Ltd; original images kindly provided by B. Fuhrer. 

18.8.1 Oidia (arthroconidia) 

The development of arthroconidia in many 

ways resembles that found in ascomycetes 

(see p. 235). They are often termed oidia. They 

may be dry and dispersed by air currents, or wet 

and accumulating in slimy masses from which 

they are dispersed by insects, in water films or by 

rain splash. An example of dry oidia is seen in 

the agaric Flammulina velutipes, which fruits 

on dead tree stumps and logs in winter (see 

Plate 9d). Oidia may develop on monokaryotic 

and on clamped, dikaryotic mycelia, but the 

oidia formed on dikaryons are monokaryotic. 

They are formed by a process of de-dikaryotization 

in which each oidium comes to contain a 

single nucleus (Brodie, 1936; Ingold, 1980). 

Vacuoles appear at intervals in aerial hyphae, 

separating cylindrical lengths of uninucleate 

cytoplasm around which cell walls develop. The 

wall of the parent hypha then dissolves so that 

an irregular fragmented chain of oidia is formed 

(Fig. 18.14a). Oidia germinate by germ tubes 

formed at either or both ends of the spore. Dry 

oidia are not uncommon in members of the 

euagarics and polyporoid clades. Wet oidia are 

seen in Coprinus cinereus on monokaryons as well 

as dikaryons. They are formed on short, erect, 

branched or unbranched conidiophores (oidiophores) 

(Fig. 18.14b), the tips of which fragment 

into uninucleate, smooth-walled, cylindrical


503 

Fig18.14 Arthroconidia in two 

Homobasidiomycetes. (a) Arthroconidia of 

Flammulina velutipes formed on a monokaryotic 

mycelium.When the chains of conidia 

disarticulate, the conidia remain dry and are 

dispersed by wind currents. (b) Arthroconidia 

(oidia) of Coprinus cinereus formed on a 

monokaryon.The sticky oidia accumulate in 

mucilage in globose heads and are dispersed by 

insects visiting the dung on which this fungus 

grows. (c) The homing reaction in C. cinereus as 

seen in an agar culture.The tips of lateral 

branches of monokaryotic hyphae have been 

stimulated chemotropically to grow or curve 

towards oidia of compatible mating type 

placed near them a few hours earlier. 

Plasmogamy between a hyphal tip and a 

compatible oidium is followed by transfer of a 

nucleus from the oidium into the monokaryon, 

converting it into a dikaryon. 

segments (Heinz & Niederpruem, 1970; Polak 

et al., 1997). The oidia collect in mucilaginous 

globules from which they are dispersed by 

insects. 

Oidia, whether wet or dry, can function as 

spermatizing agents. If an oidium is placed a 

little distance ahead of a monokaryotic hypha, 

the growing hypha changes direction, being 

attracted chemotropically towards the oidium. 

This phenomenon is termed the ‘homing reaction’ 

(Fig. 18.14c). The response has been detected 

over distances up to 75 mm. This is remarkable in 

view of the fact that the width of the approaching 

monokaryon hypha is about 2.5 mm and the 

growing zone of the hyphal tip is about 0.5 mm 

(Kemp, 1975a). The homing reaction is elicited 

not only between compatible oidium hypha 

combinations but also between incompatible 

associations. It may even be triggered by oidia 

of different species. Where the oidium and 

approaching hypha are compatible, plasmogamy, 

i.e. fusion of the hyphal tip and the 

oidium, takes place, followed by nuclear 

migration and the eventual establishment of a 

dikaryon. Plasmogamy may also occur between 

an oidium and an unrelated approaching hypha, 

i.e. one belonging to a different species. In this 

case the introduction of a nucleus from the 

oidium into a cell of the unrelated hypha results 

in a lethal response, involving the death of the 

receptor cell and possibly some adjacent cells. 

Kemp (1975a,b) has argued that the lethal 

response is important in maintaining interspecific 

barriers. 

18.8.2 Blastic conidia 

Blastic development involves the marked 

enlargement of a recognizable conidium initial 

before the conidium is delimited by a septum. 

This is usually achieved by a blowing-out of part 

of the conidiophore wall. There are many 

different ways in which blastic conidia can 

develop (Kendrick & Watling, 1979). For example, 

they may develop singly, synchronously in 

clusters, or in succession. The growth form


Auricularia auricula-judae, a parasite of elder 

(Sambucus nigra), develops successive blastic 

conidia from conidiophores on germinating 

basidiospores (Fig. 21.6c) or from monokaryotic 

hyphae. At discharge, each basidiospore is 

unicellular, but three transverse septa divide 

the basidiospore before germination and each of 

the resulting cells may form a short conidiophore 

which swells and curves at the tip to form 

a horseshoe-shaped (lunate) conidium, followed 

by further similar conidia. 

Sistotrema hamatum (anamorph Ingoldiella 

hamata) is a subtropical aquatic basidiomycete 

with large, septate, branched conidia (Fig. 25.17; 

Nawawi & Webster, 1982). They consist of a main 

axis over 400 mm long with two to three tapering 

laterals. The tips of the branches are recurved. 

Conidia are formed on dikaryotic and on 

monokaryotic mycelia. Dikaryotic conidia are 

distinguished by the presence of clamp 

connections at the septa (Figs. 25.17a,b) which 

are absent from the otherwise similar monokaryotic 

conidia (Fig. 25.17c). Other species 

with aquatic branched conidia are recognizable 

as basidiomycetes either by the presence of 

clamp connections or dolipore septa within 

their conidia and mycelia (Nawawi, 1985; 

Webster, 1992). 

Fig18.15 Spiniger state of Heterobasidion annosum. 

Conidiophores and conidia.Conidial development is blastic. 

adopted by many basidiomycetous yeasts is an 

example of blastic development (see p. 659). 

Heterobasidion annosum, a tree-pathogenic 

polypore, forms clusters of dry blastoconidia 

synchronously on the swollen tips of upright, 

club-shaped conidiophores (Fig. 18.15). Following 

detachment of the conidia, the surface of the 

swollen tip of the conidiophore bears spiny 

denticles. These conidiophores resemble the 

Oedocephalum type of conidia found in certain 

ascomycetes (see Fig. 14.4), but the anamorph 

name Spiniger has been given to them (Stalpers, 

1974). 

18.8.3 Chlamydospores 

The term chlamydospore is used here in a wide 

sense following the definition by Kirk et al. (2001) 

as ‘an asexual one-celled spore (primarily for 

perennation, not dissemination) originating 

endogenously and singly within part of a preexisting 

cell, by the contraction of the protoplast 

and possessing an inner secondary and often 

thickened hyaline or brown wall, usually impregnated 

with hydrophobic material.’ A common 

example of a basidiomycete forming chlamydospores 

is Laetiporus sulphureus, a yellowish-orange 

bracket fungus parasitic on a range of tree hosts 

such as oak, willow and yew. In culture they are 

mostly formed terminally on aerial branched 

conidiophores which develop from a mycelium 

lacking clamp connections (Fig. 18.16a). In the 

mycelium within the substrate, intercalary chlamydospores 

are also formed. Adjacent to the


505 

Fig18.16 Sporotrichum state of Laetiporus sulphureus. (a) Branched aerial conidiophores with terminal chlamydospores. 

(b) Intercalary chlamydospores. (c) Detached chlamydospores. (a) and (b) to same scale. 

Fig18.17 SEM image of a bulbil of Minimedusa polyspora 

produced in agar culture. 

swollen segment packed with cytoplasm which 

becomes the chlamydospore, there are empty 

mycelial segments (Fig. 18.16b). The collapse of 

these empty cells brings about release of the 

chlamydospore (Fig. 18.16c) so that release is 

rhexolytic, as already seen in certain ascomycete 

conidia (see p. 235). 

Fig18.18 Bulbillomyces farinosus.Fragment of a large 

multicellular, branched propagule made up of inflated cells 

with clamp connections at their base. Air is trapped between 

the cells. From Abdullah (1980), with permission. 

18.8.4 Bulbils 

Certain basidiomycetes develop multicellular, 

pseudoparenchymatous propagules composed 

of thin-walled, undifferentiated, homogeneous 

cells in the form of raspberry-like bulbils. A 

classical example is the terrestrial basidiomycete 

Minimedusa polyspora (Fig. 18.17; Weresub & 

LeClair, 1971). Another good example of a multicellar 

propagule is seen in the semi-aquatic


fungus Bulbillomyces farinosus (anamorph Aegerita 

candida). The anamorphic state (Fig. 18.18) 

appears on the surface of wet wood from freshwater 

streams as white clusters of clamped cells 

between which air is trapped, giving the propagule 

buoyancy. This is a typical feature of aeroaquatic 

fungi which form asexual propagules 

in air on the surface of leaves and branches of 

trees previously submerged in fresh water (see 

Section 25.3). 

18.9 Mating systems in 

basidiomycetes 

18.9.1 Homothallic systems 

About 10% of the Basidiomycota which have been 

tested are homothallic (Raper, 1966). Three types 

of homothallic behaviour may be distinguished, 

namely primary, secondary and unclassified 

homothallism. 

Primary homothallism 

In Coprinus sterquilinus a single basidiospore 

germinates to form a mycelium, which soon 

becomes organized into binucleate segments 

bearing clamp connections at the septa. There 

is no genetic distinction between the two nuclei 

in each cell, and this mycelium is capable of 

forming fruit bodies. 

Secondary homothallism 

(pseudohomothallism) 

In Coprinus ephemerus f. bisporus the basidia 

bear only two spores, but the spores are heterokaryotic. 

After meiosis two nuclei enter each 

spore and a mitotic division may follow. On 

germination, a single spore forms a dikaryotic 

mycelium with clamp connections, capable of 

fruiting. Occasional spores, on germination, give 

rise to non-clamped mycelia, and fruiting occurs 

only if these are paired in certain combinations, 

showing that the fungus is basically heterothallic. 

The cultivated mushroom, Agaricus bisporus, 

also has a mating system of this type. Although 

most basidia bear two spores, four-spored basidia 

do occur, and when monosporous cultures 

derived from basidiospores from four-spored 

basidia are crossed, they produce fruiting mycelia 

in certain combinations. It has been suggested 

that a simple bipolar system (see below) is 

operating (Miller, 1971; Raper et al., 1972). 

This situation occurs in a number of other twospored 

basidiomycetes and is closely paralleled 

by that found in certain four-spored ascomycetes 

such as Neurospora tetrasperma (Raper, 1966). 

Fungi showing both secondary homothallism 

and heterothallic behaviour are said to be 

amphithallic. 

Unclassified homothallism 

The four-spored wild mushroom, Agaricus campestris, 

is homothallic in the sense that a mycelium 

derived from a single spore is capable of fruiting. 

There is nuclear fusion in the basidium, followed 

by two nuclear divisions, presumably meiotic. 

However, paired nuclei, conjugate nuclear divisions 

and clamp connections have not been 

observed. 

18.9.2 Heterothallic systems 

Amongst the remaining 90% of the 

Basidiomycota reported to be heterothallic, we 

can distinguish bipolar and tetrapolar 

conditions. 

Bipolar 

In species such as Coprinus comatus (the shaggy 

ink-cap) and Piptoporus betulinus (the birch polypore), 

when mycelia obtained from single spores 

from any one fruit body are mated together, 

dikaryons are formed in half the crosses. This can 

be explained on the basis of a single gene 

(or factor) with two alleles. Because only a 

single factor is involved, the genetic basis for 

the bipolar condition is described as unifactorial. 

Segregation of the two alleles at meiosis ensures 

that a single spore carries only one allele. 

Dikaryons are only formed between monokaryons 

carrying different alleles at the mating 

type locus. In fact, it is known that there may 

be numerous mating type alleles in a population 

of fruit bodies collected over a wide area (see 

below). About 25% of Basidiomycota examined 

have been shown to be bipolar. Most members of 

the Uredinales and Ustilaginales have mating

MATING SYSTEMS IN BASIDIOMYCETES 

507 

systems of this type, although a few have more 

complex systems. 

Tetrapolar 

In the coprophilous ink-cap Coprinus cinereus or 

the wood-rotting Schizophyllum commune, fertile 

dikaryons result in one-quarter of the matings 

when primary mycelia derived from basidiospores 

from a single fruit body are intercrossed. 

The explanation originally proposed for this 

situation was that incompatibility is controlled 

by two genes (factors), with two alleles at each 

locus. Because two separate factors are involved, 

the genetic basis is termed bifactorial. Thus we 

can denote the two genes as A and B and their 

two alleles as A 1 , A 2 and B 1 , B 2 , respectively. 

Consider the cross of a monokaryon bearing A 1 B 1 

with another bearing A 2 B 2 . This would result in 

a fertile dikaryon (A 1 B 1 þ A 2 B 2 ). Such a dikaryon 

would form spores following meiosis and the 

spores would be of four kinds: A 1 B 1 , A 2 B 2 

(parentals), A 2 B 1 and A 1 B 2 (recombinants). In 

most cases studied, the proportions of the four 

kinds of spore are equal, showing that the A 

and B loci are unlinked, i.e. borne on different 

chromosomes. 

Fertile dikaryons are only formed when the 

alleles present at each locus in the opposing 

monokaryons differ e.g. in crosses of the type 

A 1 B 1 A 2 B 2 or A 2 B 1 A 1 B 2 . Where there is an 

identical allele at either or both loci the cross 

is unsuccessful. Thus the success of inbreeding 

within the spores of any one fruit body is only 

25% in tetrapolar species as compared with 50% 

in bipolar forms. 

A species with tetrapolar heterothallism 

whose life cycle is unusual and difficult to 

interpret is Armillaria mellea. Most of the cells of 

the mycelium are monokaryotic, and there is no 

evidence of clamp connections in the mycelium 

or the rhizomorphs. Fruit body primordia arise 

from the monokaryotic rhizomorphs, and the 

cells of the young primordia are also monokaryotic. 

However, cells making up the gill tissue 

are dikaryotic, and these dikaryotic hyphae are 

associated with clamp connections, whilst the 

monokaryotic cells formed in the remaining 

tissue of the stem and cap have no clamps. 

Estimations of nuclear volume in monokaryotic 

and dikaryotic cells suggest that the nuclei of 

monokaryotic cells are diploid, whilst those of 

dikaryotic cells are haploid. It is presumed that 

the diploid nuclei undergo haploidization by an 

unknown mechanism during the formation of 

gill initials. Within the basidia, nuclear fusion 

and meiosis occur, and a single meiotic product 

enters each basidiospore. In the spore, the 

nucleus divides mitotically, and one daughter 

nucleus from each spore migrates back into the 

body of the basidium and degenerates (Korhonen 

& Hintikka, 1974; Tommerup & Broadbent, 1974; 

Ullrich & Anderson, 1978; Anderson & Ullrich, 

1982). 

Variations in the life cycle of A. mellea have 

been reported. In a form designated as ‘Japanese 

A. mellea’, Ota et al. (1998) presented evidence that 

four haploid nuclei appear after meiotic division 

of the diploid nucleus in the young basidium. 

These haploid nuclei fuse in pairs, resulting in 

two diploid nuclei which migrate into two of 

the developing basidiospores where they divide 

mitotically. One nucleus from each basidiospore 

returns to the basidium, leaving the spore 

containing one diploid nucleus. Occasionally 

nuclear migration fails to occur and the 

spore remains binucleate. Spores with diploid 

nuclei can complete the life-cycle by forming 

a mycelium competent to fruit. Ota et al. (1998) 

therefore concluded that the ‘Japanese 

A. mellea’ illustrates a kind of secondary 

homothallism. 

18.9.3 Multiple alleles, complex loci 

Although a single spore from one fruit body of 

S. commune or C. cinereus is compatible with only 

one-quarter of its fellow spores, crosses between 

spores from fruit bodies of different origin often 

result in 100% mating success, i.e. a spore from 

one fruit body can mate successfully with 100% 

of the spores from a different fruit body. The 

explanation of this phenomenon is that a large 

number of alleles is present in a population 

representing the species as a whole, instead of 

the single pair of alleles at each locus present 

in any one dikaryotic mycelium. Suppose that a 

second fruit body had the composition (A 3 B 3 þ 

A 4 B 4 ), then all the four kinds of spore it produced,


A 3 B 3 , A 3 B 4 , A 4 B 3 and A 4 B 4 would be compatible 

with all the spores of the original fruit body, on 

the assumption that the essential requirement 

for fertility is that in any cross both alleles 

should differ at both loci. This high value for 

outbreeding success implies the existence of a 

large number of different mating type factors, 

and estimates based on isolates from worldwide 

collections of fruit bodies indicate that the 

number of mating type factors of certain species 

may be many thousands (Raper, 1966). 

Our understanding of the structure and 

function of the mating type factors is derived 

from studies of three species, namely the two 

Homobasidiomycetes S. commune and C. cinereus, 

and the maize smut fungus Ustilago maydis 

(Ustilaginomycetes). Extensive literature is available 

on general aspects of this topic (see Kües & 

Casselton, 1992; Kämper et al., 1994; Kothe, 1996; 

Kronstad & Staben, 1997; Brown & Casselton, 

2001; Casselton, 2002) and on the individual 

species C. cinereus (Kües, 2000), S. commune 

(Stankis et al., 1990; Ullrich et al., 1991; Kothe, 

1999) and U. maydis (Banuett, 1995). 

18.9.4 Functions of the A and B loci 

There is a close similarity between the functions 

and structure of the A and B mating type loci 

in S. commune and C. cinereus as described in 

Table 18.2. The fact that they influence 

many different functions indicates that their 

gene products are active as regulatory proteins. 

The A locus encodes two peptides which together 

make up a heterodimer transcription factor, 

i.e. the molecule is active only if its two halves 

are different from each other (see below and 

Fig. 23.8). The B locus of S. commune and C. cinereus 

directly encodes the peptide pheromone and a 

transmembrane receptor for pheromones of 

compatible strains. In this way it differs from 

the mating system of the ascomycete yeast 

S. cerevisiae in which the mating type loci 

encode regulatory genes whose products stimulate 

the transcription of pheromone and pheromone 

receptor genes located elsewhere in the 

genome (see Fig. 10.5). 

18.9.5 Structure of themating type factors 

The results of crossing experiments between 

compatible monokaryons indicate that recombination 

may occur within the A and B loci 

to give novel mating types. This implies that 

both loci are complex. For S. commune it has 

been proposed that the A locus contains two subloci, 

Aa and Ab. Similarly the B locus contains two 

sub-loci, Ba and Bb. For each sub-locus, pairing 

tests revealed a number of ‘alleles’: 9 Aa, 32Ab, 

9 Ba and 9Bb (Ullrich et al., 1991). Recombination 

between the Aa and Ab ‘alleles’ gives rise to 288 

(i.e. 9 32) different A specificities. When these 

are multiplied by the 81 B specificities, over 

20 000 possible mating types are generated. In 

C. cinereus there are an estimated 160 A specificities 

and 79 B specificities which together 

generate over 12 000 mating types (Casselton, 

2002). The actual number of Aa and Ab alleles is 

not known (Casselton & Olesnicky, 1998). 

Table18.2. Functions of the A and B loci in Schizophyllum commune and Coprinus cinereus. The functions operate 

only if there are different specificities at the A and B loci. 

Locus 

A-regulated 

B-regulated 

Function 

Pairing of nucleiin dikaryon 

Initiation of clamp cell formation 

Synchronized nuclear division 

Septation 

Nuclear exchange between monokaryons 

Septal dissolution and nuclear migration 

Peg formation and clamp cell fusion 

Pheromone production

MATING SYSTEMS IN BASIDIOMYCETES 

509 

In both S. commune and C. cinereus it has been 

possible to obtain details of the structure of the 

sub-loci at a finer level of resolution. For 

example, the Aa locus of C. cinereus contains one 

gene pair (designated a1 and a2) and the Ab locus 

two gene pairs (b1 and b2, d1 and d2), each with a 

number of alleles. In the field, many strains have 

lost one or more of their maximum complement 

of six A genes (Fig. 18.19). The gene products 

are the subunits of the heterodimer transcription 

factor. The two different subunits (1 and 2) 

are encoded by compatible alleles. For example, 

a functional heterodimer can be formed from 

the product of an a allele at the a1 position 

(e.g. a1 1) and a different one at the a2 position 

(e.g. a2 2, a2 3, etc., but not a2 1). Likewise, 

heterodimers can be formed between the 

products of two compatible b or two d alleles, 

but there is a great deal of functional redundancy 

in the system in the sense that it is 

sufficient if only one of six possible heterodimers 

is formed. In other words, compatibility between 

two strains at the A locus is ensured if compatible 

alleles are present at the a or b or d genes. 

Casselton and Olesnicky (1998) have calculated 

that only 5 6 alleles would be required at each 

gene pair (e.g. 5 6 6) to account for the 

estimated 160 unique A gene combinations in 

C. cinereus. 

The genetics of mating type behaviour in the 

maize smut fungus Ustilago maydis is, in many 

respects, similar to that described for C. cinereus 

and S. commune. This fungus is dimorphic, with 

a monokaryotic, saprotrophic yeast-like state 

which can be readily cultured, and a dikaryotic 

mycelial state which is parasitic on maize 

and requires living host cells for growth (see 

Fig. 23.1). Ustilago maydis is tetrapolar, unlike 

most smut fungi which are bipolar. Incompatibility 

is governed by two loci, designated 

a and b. Unfortunately the functions of the 

b mating type factor in U. maydis correspond to 

those of the A factor in C. cinereus and S. commune, 

and vice versa. There are two alleles at the a locus 

(a 1 and a 2 ) and about 25, possibly more, at the b 

locus. The a locus encodes a pheromone and a 

pheromone receptor; it controls the switch to 

filamentous growth but not pathogenicity. The b 

locus encodes the production of a heterodimeric 

DNA-binding protein involved in self/non-self 

recognition and also in pathogenicity; two 

different b alleles are required for pathogenic 

growth (see p. 643). 

Much lower numbers of alleles have been 

estimated for the bird’s nest fungi (Gasteromycetes; 

see p. 581). For instance, Cyathus striatus 

has 4 A and 5 B alleles, and Crucibulum vulgare 3 A 

and about 16 B alleles. It has been suggested that 

Fig18.19 The A loci of two different field strains of Coprinus cinereus. Neither strain has the complete set of six genes, but none the 

less four different functional heterodimers canbe formed from gene products of different (compatible) alleles at the a, b and d genes. 

Only one would be sufficient for overall compatibility at the A locus. Note that the position of the d genes is reversed relative to 

those of the a and b genes.Genetic recombination events are possible in homologous DNA regions (thick lines) but not within the 

regions covered by the gene pairs a, b or d. Redrawn and modified from Casselton and Olesnicky (1998).


the small number of incompatibility factors may 

be related to the specialized method of dispersal 

in which numerous basidiospores are packaged 

into a peridiole. 

The molecular basis of bipolar (unifactorial) 

mating systems may be quite similar if one 

considers that here the A and B loci are simply 

linked to each other in close proximity on the 

same chromosome (see p. 637). 

18.9.6 The Buller phenomenon 

Buller (1931) discovered that a monokaryon of 

C. cinereus paired with a dikaryon of the same 

fungus could be converted to the dikaryotic 

state. The same phenomenon has been reported 

in some other bipolar and tetrapolar fungi. 

Conversion, i.e. dikaryotization, is brought 

about by nuclear migration from the dikaryon 

into the monokaryon. Different kinds of combination 

(di mon matings) are possible (Raper, 

1966). 

There are two kinds of legitimate combinations. 

(1) In fully compatible combinations, a 

monokaryon is compatible with both nuclear 

components of the dikaryon, e.g. bipolar (A 1 þ 

A 2 ) A 3 or tetrapolar (A 1 B 1 þ A 2 B 2 ) A 3 B 3 . (2) In 

hemicompatible combinations, a monokaryon is 

compatible with only one of the nuclear components 

of the dikaryon, e.g. bipolar (A 1 þ A 2 ) A 2 

or tetrapolar (A 1 B 1 þ A 2 B 2 ) A 1 B 1 .Inillegitimate 

(incompatible) combinations, a monokaryon is 

compatible with neither nuclear component of 

the dikaryon, e.g. tetrapolar (A 1 B 1 þ A 2 B 2 ) A 1 B 2 

or A 2 B 1 . 

Surprising features were discovered in some 

such pairings. In compatible pairings using 

Schizophyllum it was found that the selection of 

a compatible nucleus from the dikaryon to 

dikaryotize the monokaryon was not a matter 

of chance. Consider the fully compatible di mon 

mating (A 1 B 1 þ A 2 B 2 ) A 3 B 3 . If conversion of 

the monokaryon by one of the nuclei from 

the dikaryon were entirely random, dikaryons 

(A 1 B 1 þ A 3 B 3 ) and (A 2 B 2 þ A 3 B 3 ) would be equally 

frequent. However, this is not the case; there is 

evidence of preferential selection of one mating 

type over the other, but the reasons for this 

selection are obscure. A second unexpected 

feature is the discovery that dikaryotization can 

occur in incompatible pairings. A possible reason 

for this phenomenon is that somatic recombination 

between the nuclei in the original dikaryon 

can occur to give rise to a nucleus compatible 

with that of the monokaryon (Raper, 1966). 

An unusal mating phenomenon which is the 

equivalent of the Buller phenomenon has been 

discovered in Armillaria mellea. The vegetative 

phase of this fungus is mainly diploid, not 

dikaryotic. Its mating system is bifactorial, i.e. 

tetrapolar, controlled by A and B loci. When 

diploid and haploid mycelia are paired in certain 

combinations, mating occurs, i.e. the diploid 

mycelium is capable of dikaryotizing the haploid 

monokaryon (Anderson & Ullrich, 1982). 

18.10 Fungal individualism: 

vegetative incompatibility 

between dikaryons 

When genetically distinct dikaryons belonging to 

the same species are paired together, they do not 

coalesce. Although their hyphae may fuse 

together, the cells of the resulting heteroplasmon 

die and often become darkly pigmented. 

This is the result of vegetative incompatibility. In 

contrast, when genetically identical dikaryons 

are paired, their mycelia intermingle. Vegetative 

incompatibility is readily demonstrated in 

culture (Fig. 18.20c) and is recognizable in the 

field as black bands of fungal cells at the interface 

between adjacent dikaryotic colonies in 

decaying tree stumps (Fig. 18.20a). The phenomenon 

was first discovered in the bracket fungus 

Trametes versicolor, the cause of white-rot in 

deciduous trees, but has since been found to be 

widespread amongst different ecological groups 

of basidiomycetes, including wood rotting, coprophilous, 

ectomycorrhizal and plant pathogenic 

species, and has led to the concept of fungal 

individualism (see Todd & Rayner, 1980; Rayner, 

1991a,b). Pairing tests between dikaryotic 

isolates facilitate the determination of the 

limits and extent of an individual mycelium 

of a basidiomycete. In T. versicolor, tree trunks

RELATIONSHIPS 

511 

colonized by this fungus show a number of decay 

columns which can be traced through a series of 

transverse slices of wood extending the length 

of the trunk. In stumps of birch (Betula) these 

columns can be matched genetically with different 

clusters of fruit bodies emerging at the 

surface of the stump. 

By making pairings of isolates from basidiocarps, 

decaying wood, and mycelial cords or 

rhizomorphs of Megacollybia platyphylla or Armillaria 

bulbosa, it has been shown that a single 

individual can extend over many hectares 

(Anderson et al., 1979; Thompson & Rayner, 

1982). Isolations from basidiocarps of the fairy 

ring fungus Marasmius oreades show that the 

same individual mycelium has spread in an 

annular fashion and estimates of the incremental 

growth rate indicate that the same individual 

may be several centuries old (Mallett & Harrison, 

1988; Dix & Webster, 1995). 

Vegetative incompatibility enables a fungus to 

distinguish between ‘self’ and ‘non-self’ and 

prevents the spread of genetic information in the 

form of nuclei and mitochondria and possibly also 

of fungal viruses from one mycelium to another 

of the same species. It thus helps to preserve the 

genetic integrity of an individual mycelium. 

18.11 Relationships 

Basidiomycota are related to Ascomycota. 

Evidence for this view is based on similarities 

in composition and construction of the hyphal 

wall (e.g. presence of chitin; see Section 1.2.2), 

the molecular basis of mating type control 

(see p. 266), the production of similar conidial 

states, and molecular sequence data (see Bruns 

et al., 1992; Tehler et al., 2003). It has been 

Fig18.20 Vegetative incompatibility inTrametes versicolor. (a) Section of a tree stump containing several different dikaryotic 

colonies. At the interfaces between adjacent colonies double black lines indicate the incompatibility reaction. (b,c). Interactions 

between dikaryotic colonies in culture. (b) Reaction when two genetically identical colonies are inoculated near each other. 

The two mycelia intermingle. (c) Incompatible reaction when two genetically distinct dikaryons are paired.


Fig18.21 Phylogenetic tree of the 

Basidiomycota based on small 

nuclear (18S) rDNA gene analyses. 

The various taxonomic groups and 

the chapters covering them are 

indicated. Redrawn and modified 

from Nishida and Sugiyama (1994), 

with permission from Mycoscience. 

postulated that, in evolutionary terms, basidiospores 

are the equivalent of ascospores whose 

development has become external instead of 

taking place endogenously. Clamp connections 

(Fig. 18.11), characteristic of dikaryotic hyphae 

of basidiomycetes, are seen as homologous to the 

croziers in ascogenous hyphae (see Fig. 8.10); 

both have the same function of re-distributing 

nuclei. Tehler et al. (2003) have indicated the 

strength of their belief that the two groups are 

closely related by classifying them together in 

the Dikaryomycota. They have suggested that 

this group is a sister group to the Glomeromycota 

(treated in this book within the Zygomycota 

as the order Glomales, see Section 7.6). Ascomycetes 

and basidiomycetes probably diverged from 

zygomycetes some 400 600 million years ago 

(Berbee & Taylor, 2001). 

Basidiomycetes have a long history. Fossil 

records show that the characteristic feature of 

basidiomycete hyphae, the clamp connection, 

already existed some 300 million years ago in 

the Carboniferous period (Dennis, 1970). Clearly 

recognizable mushroom basidiocarps have been 

preserved in amber about 90 94 million years 

old (Hibbett et al., 1997a). This also contained 

well-preserved basidiospores with prominent 

hilar appendices. 

18.12 Classification 

The classification which we have chosen follows 

that proposed by McLaughlin et al. (2001). They 

have divided the phylum Basidiomycota into 

four classes: 

1. Homobasidiomycetes. Fungi with holobasidia, 

e.g. agarics and polypores. 

2. Heterobasidiomycetes. Fungi with heterobasidia, 

i.e. jelly fungi and their allies. 

3. Urediniomycetes. Rust fungi. 

4. Ustilaginomycetes. Smut fungi.


513 

These taxonomic groups are broadly 

supported by phylogenetic analyses (Swann & 

Taylor, 1993). An example of the kind of arrangement 

currently proposed for the basidiomycetes 

is shown in Fig. 18.21. Because their basidia are 

arranged on a freely exposed hymenium, the 

Heterobasidiomycetes and Homobasidiomycetes 

are sometimes collectively termed Hymenomycetes. 

Various basidiomycetes in which the 

hymenium is not freely exposed and which do 

not discharge their basidiospores violently have 

adopted alternative methods of spore dispersal. 

They are related to a number of Homobasidiomycete 

groups, from which they have arisen in 

the course of evolution. Whilst recognizing that 

they do not form a natural group, they are here 

considered together as gasteromycetes because 

they share important biological features (see 

Chapter 20). Basidiomycetous yeasts are another 

artificial assemblage of fungi which have relationships 

with various taxonomic groups; these 

are also considered in a separate chapter 

(Chapter 24).

19 

Homobasidiomycetes 


Fungi included in the Homobasidiomycetes 

possess holobasidia, in contrast to the heterobasidia 

(phragmobasidia) of the 

Heterobasidiomycetes, rusts and smuts 

(see Chapters 21 23). The traditional classification 

of the Homobasidiomycetes, founded by the 

nineteenth century Swedish mycologist Elias 

Fries, was based on a number of different 

arrangements of the hymenium on the hymenophore. 

The most common types, shown in 

Fig. 19.1, are (A) agaricoid, i.e. gill-bearing 

(lamellate); (B) poroid, i.e. bearing pores instead 

of gills; (C) hydnoid, i.e. with a toothed or spiny 

hymenium; (D) clavate, with a club-shaped 

or coralloid fruit body, the outside of which 

is covered by the hymenium; (E) resupinate, 

i.e. with a flattened (corticioid) hymenium 

appressed to the underside of solid surfaces; 

and (F) epigeous or (G) hypogeous gasteroid or 

secotioid (non-ballistosporic) hymenophores 

(see Chapter 20). It has long been suspected 

that the different hymenial arrangements have 

evolved separately in unrelated fungal groups, 

i.e. that they represent examples of convergent 

evolution. They can be interpreted as different 

ways of maximizing the hymenial area for a 

given amount of fungal tissue (Pöder, 1983; 

Pöder & Kirchmair, 1995). Examples of similar 

hymenophore arrangements in unrelated fungi 

are seen in the tubular hymenia characteristic 

of Boletus (Fig. 19.21) and Trametes (Fig. 19.26) 

or the toothed hymenia found in the 

homobasidiomycete Hydnum (Fig. 19.1c) and the 

heterobasidiomycete Pseudohydnum (Fig. 21.9b). 

Quite possibly, only one or a few genes are 

involved in the morphogenetic events resulting 

in these various hymenial structures, as has been 

shown for the transition of gill-bearing fungi to 

gasteromycetes (see pp. 578 580). There is much 

other evidence, e.g. in fruit body construction, 

ultrastructure, chemical reactions of basidiocarps, 

basidium cytology, spore colour and 

morphology, and molecular sequence data to 

support the view that gross morphological 

characters of hymenophores are unsatisfactory 

criteria on which to base a natural classification 

system. 

Hibbett et al. (1997b) and Hibbett and Thorn 

(2001), in their preliminary attempts at a 

more natural classification, found the 

Homobasidiomycetes to be distributed amongst 

eight phylogenetic clades (Fig. 19.2), and this 

scheme has been confirmed and extended in 

subsequent work (e.g. Binder & Hibbett, 2002; 

Moncalvo et al., 2002). The eight clades may 

ultimately be given the status of orders, and 

although it is tempting to use some of the 

existing order names in synonymy, e.g. 

Agaricales for the euagarics clade, the necessary 

emendations of orders have not yet been 

carried out. Therefore, we shall use the clade 

system for the time being. One serious limitation 

of it is that all large-scale attempts at 

Homobasidiomycete phylogeny undertaken to 

date have been based on nuclear and mitochondrial 

ribosomal DNA, and confirmation by 

comparing other genes will be required before

INTRODUCTION 

515 

Fig19.1 Examples of hymenial surfaces in the Homobasidiomycetes. (a) Gill-bearing (lamelloid) surface of Agaricus silvaticus. 

(b) Tubular (poroid) hymenium of Boletus badius.(c)Spiny(hydnoid)surfaceofHydnumrepandum. (d) Club-shaped (clavate) fruit body 

of Clavariadelphus pistillaris.The hymenium lines the surface of the fruit body. (e) Flattened (corticioid) hymenium of Peniophora 

quercina forming a crust on the underside of an oak twig. (f) Enclosed (gasteroid) fruit body of Scleroderma citrinum. 

a more definitive taxonomic system can be put in 

place. 

The eight clades, shown in Fig. 19.2, are as 

follows: (1) the polyporoid clade, including most 

members of the former order Polyporales; (2) the 

euagarics clade containing many members of 

the old order Agaricales, together with fungi 

from diverse other groups; (3) the boletoid clade; 

(4) a thelephoroid clade; (5) the russuloid clade 

including a particularly wide range of fruit body 

types; (6) the hymenochaetoid clade; (7) the 

cantharelloid clade; and (8) a gomphoid phalloid 

clade. Table 19.1 indicates that each of these 

clades contains several of the hymenophore

Fig19.2 The eight-clade phylogenetic system of the Homobasidiomycetes based on both nuclear and mitochondrial small-subunit 

rDNA sequences.Gasteromycete genera are printed in bold. Redrawn from Hibbett et al.(1997b),withpermission. 

ß 1997 National Academy of Sciences, U.S.A.

STRUCTURE AND MORPHOGENESIS OF BASIDIOCARPS 

517 

Table 19.1. Distribution of fruit body morphotypes among the major clades of Homobasidiomycetes shown 

in Fig. 19.2. From Hibbett and Thorn (2001). 

Major clades 

Hymenophore type 

(A) 

Agaricoid 

(B) 

Poroid 

(C) 

Hydnoid 

(D) 

Clavate 

(E) 

Resupinate 

(F) 

Epigeous 

gasteroid 

secotioid 

(G) 

Hypogeous 

gasteroid 

(1) Polyporoid þ þ þ þ þ þ 

(2) Euagarics þ þ þ þ þ þ 

(3) Boletoid þ þ þ þ þ þ 

(4) Thelephoroid þ þ þ þ þ 

(5) Russuloid þ þ þ þ þ þ þ 

(6) Hymenochaetoid þ þ þ þ þ 

(7) Cantharelloid þ þ þ þ 

(8) Gomphoid phalloid þ þ þ þ þ þ 

morphotypes shown in Fig. 19.1. This finding 

is perhaps best explained by the assumption that 

the first Homobasidiomycetes had a morphologically 

simple fruit body form, probably the 

flattened (resupinate) type, from which more 

complex fruit bodies arose as numerous independent 

evolutionary events (Hibbett & Binder, 

2002). The class Gasteromycetes is an artificial 

taxon, comprising gasteroid and secotioid fruit 

body forms which have lost the capacity for 

violent basidiospore discharge and have adopted 

alternative mechanisms for spore dispersal 

(see Fig. 19.2). Because of unifying biological 

and morphological features, the gasteromycetes 

are described separately in Chapter 20, where 

we will refer to their affinity to the 

Homobasidiomycete clades. 

19.2 Structure and morphogenesis 

of basidiocarps 

The fleshy basidiocarps of many fungi belonging 

to groups 2 5, 7 and 8 in Fig. 19.2 (‘agarics’) 

differ from the tougher fruit bodies found in the 

polyporoid and hymenochaetoid clades 1 and 6 

(‘polypores’) in texture and construction. Agaric 

basidiocarps are often umbrella-shaped, with a 

centrally attached stalk (stipe) supporting the 

cap (pileus) beneath which are the gills or tubes 

lined by basidia. The polypores include bracket 

fungi with basidiocarps which often bear pores 

and are laterally attached to their substratum. 

These fruit bodies are usually firmer in texture, 

i.e. leathery, corky or woody. The differences in 

texture reflect fundamental principles of 

construction as shown by analysis of the 

hyphae composing the basidiocarp. There are 

also differences in development between agaricand 

polypore-type fruit bodies. 

19.2.1 Hyphal analysis 

Corner (1932a,b, 1953) dissected the basidiocarp 

tissues of various polypores and showed that 

they were constructed of three distinctive types 

of hyphae generative, binding and skeletal 

(see below). Later work by Corner and others has 

identified a further range of hyphal types 

making up basidiocarps (see Pegler, 1996; Kirk 

et al., 2001; Clémençon, 2004). This method of 

hyphal analysis provides valuable criteria which 

have greatly improved the taxonomy of the 

genera of agaric- and polypore-type fungi. 

However, it does not of itself provide the basis 

for a higher-level ‘natural classification’ of 

homobasidiomycetes.

518 HOMOBASIDIOMYCETES 

There are three main hyphal types. (1) 

Generative hyphae are thin-walled near the 

margin of a basidiocarp but often thickerwalled 

behind, with or without clamp connections, 

usually with cytoplasmic contents. This 

kind of hypha is universally present in all 

basidiocarps at some stage of development. 

The generative hyphae produce basidia and 

other types of cell making up the hymenium, 

and they also give rise to the other kinds 

of hyphae from which the basidiocarp is 

constructed (Fig. 19.3a). (2) Skeletal hyphae are 

unbranched or sparsely branched, thick-walled 

hyphae with a narrow lumen. They arise as 

lateral branches of generative hyphae and form 

a rigid framework (Fig. 19.3c). (3) Binding 

hyphae (sometimes termed ligative hyphae) are 

much-branched, narrow, thick-walled hyphae of 

limited growth. These hyphae weave themselves 

between the other hyphae and bind them 

together (Fig. 19.3b). 

Several other kinds of hypha have been 

described, some as intermediates between the 

above three principal systems. Sarco-hyphae 

are composed of long, greatly inflated, mostly 

unbranched cells 500 3000 10 30 mm 

with relatively narrow septa. They can be interpreted 

as skeletal, inflated generative hyphae. 

In Amauroderma rugosum (Ganodermataceae) 

skeleto-ligative hyphae resembling skeletal 

hyphae have thick-walled contorted branches 

and function in the same way as binding 

hyphae. Arboriform skeletal hyphae with terminal 

thick-walled branches are present in the 

basidiocarps of Ganoderma (see Figs. 19.23b,c). 

Gloeoplerous hyphae have dense oily contents 

(Fig. 19.27). The diverse hyphal types may be 

present in basidiocarps in different 

Fig19.3 Hyphal analysis of material dissected 

from the fruit body of a trimitic polypore, 

Trametes versicolor. (a) Generative hyphae 

characterized by thin walls, dense cytoplasmic 

contents and clamp connections. (b) Binding 

hyphae, branched, contorted and thick-walled. 

The arrow shows the origin from a generative 

hypha. (c) A skeletal hypha, unbranched and 

thick-walled, originating from a generative 

hypha (arrow).


519 

combinations according to the mitic system of 

description (Gr. mitos ¼ a thread of the warp). 

Monomitic basidiocarps are made up of 

generative hyphae only. Most agaric fruit bodies 

are of this type, containing inflated generative 

hyphae with or without clamps. However, 

various modified cell types may also be present, 

e.g. the lactifers (laticifers) containing latex in 

Lactarius (Fig. 19.4). In Lactarius and Russula 

(russuloid clade), the flesh contains rosettes 

of globose, thin-walled sphaerocysts or sphaerocytes 

(see Figs. 19.4 and 19.9c) which give it a 

brittle texture. Basidiocarps of the polypore 

Bjerkandera adusta are also monomitic, but 

here the walls of the generative hyphae thicken 

with age. Sarcomitic construction is seen in 

the polypore-type basidiocarps of Meripilus, made 

up of inflated sarco-hyphae which function as 

skeletal elements. 

Dimitic fruit bodies, produced by various 

members of the polyporoid and russuloid clades, 

may show several kinds of construction. Dimitic 

fruit bodies with binding hyphae (i.e. generative 

and binding hyphae) are found in 

the basidiocarp of Laetiporus sulphureus (see 

Plate 10b). The dissepiments (i.e. the blocks of 

flesh separating the tubes) are, however, monomitic. 

Dimitic fruit bodies with skeletal 

hyphae are found in Heterobasidion annosum 

(see Fig. 19.26b), whereas dimitic basidiocarps 

with skeleto-ligative hyphae are found in Lentinus 

and Ganoderma. 

Trimitic fruit bodies contain all three kinds 

of hypha shown in Fig. 19.3. A good example 

is Trametes versicolor, a common bracket fungus 

on hardwood stumps, trunks and branches 

(see Plate 10a). At the growing margin of 

the fruit body and in the dissepiments, construction 

is dimitic, composed of generative and 

skeletal hyphae. Binding hyphae develop in the 

adult flesh behind the growing margin. The term 

sarcotrimitic has been used to describe fruit 

body construction in Trogia where there are 

generative, binding and sarco-hyphae. 

19.2.2 Development of basidiocarps 

Basidiocarps begin their development from a 

hyphal knot, an aggregation of hyphae formed 

usually on the secondary (i.e. dikaryotic) mycelium. 

The surface of the hyphae forming the 

fruit body primordium is often non-wettable 

due to hydrophobin rodlets (Wessels, 1994, 2000). 

This property ensures that air-filled channels 

are present within basidiocarps, allowing efficient 

gas exchange to occur even under wet 

conditions (Lugones et al., 1999). The first-formed 

hyphae making up the young fruit body are 

little differentiated from normal vegetative 

hyphae and are termed protenchyma but, as 

differentiation proceeds, the hyphae of the 

Fig19.4 Lactariusrufus. Cells from the pileus, 

including thin-walled septate generative hyphae, 

a wider, thicker-walled laticiferous hypha which 

contains a milky latex, and clusters of globose 

sphaerocysts.


basidiocarp become interwoven and often tightly 

packed, making up the plectenchyma. If the 

hyphae are less tightly packed, the resulting 

tissue is known as pseudoparenchyma. Although 

a range of cell types can be distinguished in the 

mature basidiocarp, they all develop from 

generative hyphae. Enlargement and differentiation 

of basidiocarps is associated with inflation 

of segments of these hyphae. Details of the 

morphogenesis of basidiocarps will be described 

later for selected genera. 

Several kinds of development have been 

described, relating to whether or not the 

hymenophore is at all times exposed or is at 

first surrounded by other tissues. For example, 

young fruit bodies may be enveloped by a 

universal veil which is broken as the pileus 

expands, leaving a cup-like volva at the base of 

the stipe and broken scales on the cap as in 

Amanita. In some agarics the hymenophore is 

protected during development by a partial veil 

stretching from the edge of the cap to the stem. 

Where the partial veil is thin and cobweb-like as 

in Cortinarius it is termed the cortina, but where 

it is composed of firmer tissues it persists as a 

ring (annulus) on the stem. Agaric fruit bodies 

may thus have both universal and partial veils 

(Fig. 19.5), either, or neither. These different 

kinds of development have been distinguished by 

technical terms as follows (Reijnders, 1963, 1986; 

Moore, 1998). 

Gymnocarpic hymenophores are naked from 

the time of their first appearance and are never 

enclosed by tissue. The pileus develops at the 

tip of the stipe and the hymenophore differentiates 

on the lower side. Gymnocarpic development 

is found in several unrelated genera, e.g. 

Cantharellus, Boletus, Russula, Lactarius and Clitocybe 

(Fig. 19.6a). 

The angiocarpic hymenophore is enclosed by 

tissue during part of its development. There are 

two kinds of angiocarpic development. In primary 

angiocarpy, the pileus margin, hymenophore 

and sometimes also pileus and stipe 

differentiate beneath the surface of the primary 

tissue of the primordium (protenchyma). 

Stropharia semiglobata and Amanita rubescens are 

primarily angiocarpic (Figs. 19.6c,d). In a fruit 

body showing secondary angiocarpy, hyphae 

from an already differentiated surface grow out 

towards the exterior to enclose the primordium 

or part of it. The hyphae may extend from the 

margin of the pileus towards the stipe, or from 

the stipe to the pileus, or both. In Lentinus tigrinus 

hyphae from both the pileus margin and the 

stipe extend to enclose the developing gills 

(Fig. 19.6b). 

The tissue of the monomitic agaric-type 

basidiocarp is plectenchymatous or pseudoparenchymatous. 

The fruit body expands due to 

inflation of the cells. Although differentiation 

into skeletal or binding hyphae is limited 

Fig19.5 Schematic drawing of an 

agaric-type fruit body showing both 

the universal and partial veils. (a) The 

button stage. (b) Fully expanded fruit 

body. Remnants of the universal veil 

are seen as cap scales and the volva, 

whereasthepartialveilhasformeda 

ring (annulus) around the stipe.


521 

Fig19.6 Basidiocarp developmentin some Agaricales illustratedby longitudinal sections (after Reijnders,1963). (a) Clitocybeclavipes. 

Gymnocarpic development. (b) Lentinus tigrinus. Secondary angiocarpy resulting from extension of hyphae from pileus margin and 

stipe to enclose the previously differentiated hymenophore. (c) Stropharia semiglobata. Primary angiocarpy. Note the universal veil 

enclosing the upper part of the primordium. In mature fruit bodies this becomes gelatinous.The hymenophore is also enclosed by a 

partial veil. (d) Amanitarubescens.Tangential section. Note the break up of the universal veil to form scales on the surface of the 

pileus.The gill chamber is enclosed by a partial veil. 

or absent, specialized tissues or cells may arise 

(see Fig. 19.4). In a study of the fine structure of 

the sporophore of Agaricus campestris, Manocha 

(1965) has shown that the stipe contains two 

kinds of cells wide inflated cells and narrower 

thread-like cells. A similar differentiation is 

found in Coprinus cinereus (Moore, 1998). When 

portions of stipe tissue are placed on suitable


agar media, only the thinner hyphae seem to 

give rise to vegetative growth (Borriss, 1934). 

19.2.3 Types of lamellae 

The gills of most lamellate fruit bodies are 

wedge-shaped in longitudinal section and are of 

the aequi-hymenial (aequi-hymeniiferous) type. 

This term refers to the fact that the hymenium 

develops in an equal manner all over the surface 

of the gill, i.e. basidial development is not 

localized at any one point on the gill. The 

wedge-shaped section may be an adaptation to 

minimize wastage of spores should the fruit body 

be tilted from the vertical. Buller (1909) calculated 

for the field mushroom Agaricus campestris 

that a displacement of 2°30’ from the vertical 

would still allow all the spores to escape. 

Adjustments in the orientation of the stipe and, 

sometimes, of the gills themselves may further 

help to minimize wastage. The topic of gravitropism 

(gravimorphogenesis), i.e. the re-orientation 

by stipe bending or gill curvature in 

displaced basidiocarps to restore hymenia to a 

vertical position, is discussed on p. 546. 

Gills of the inaequi-hymenial (inaequihymeniiferous) 

type are characteristic of the 

ink-caps (Coprinus sensu lato) where the gills are 

not wedge-shaped in section, but parallel-sided, 

and often held apart by cystidia (see Fig. 19.7). 

The term inaequi-hymenial refers to the fact that 

the hymenium develops in an unequal manner, 

with basidia ripening in zones. In Coprinus a wave 

Fig19.7 Coprinus atramentarius.Vertical section of the parallel-sided gills showing basidia, interspersed by globose paraphyses 

and a cystidium extending across the space between adjacent gills to make contact with the surface of the opposing gill.The dashed 

arrow indicates the trajectory (sporabola) taken by a projected spore.


523 

Fig19.8 Modes of gill attachment to the stipe, and 

their terminology. 

of gill maturation begins at the cap margin and 

passes slowly upwards and inwards. After the 

basidia at the lower edge of the gill have discharged 

their spores, the gill tissue undergoes 

autolysis (deliquescence) into an inky black 

liquid which drips away from the cap. The gravitropic 

gill curvature characteristic of aequihymenial 

types is absent, but the stipe may still 

curve to bring the gills into an approximately 

vertical position. 

An important criterion for identification of 

gill-bearing agarics in the field is the way in 

which the lamellae are attached to the stipe 

(Fig. 19.8). Gills are said to be free if their blade 

does not touch the stipe. Adnate gills show 

attachment to the stipe with their entire base, 

whereas adnexed gills are attached only partially 

to the stipe. In sinuate gills, the gill margin 

shows an S-shaped curve near the point of 

junction with the stipe. Decurrent gills run 

down the surface of the stipe. 

19.2.4 The hymenophoral trama 

The hymenophore structures of some 

Homobasidiomycetes are shown in Fig. 19.9. In 

most hymenophores, there is a central group of 

hyphae running from the underside of the cap to 

the tip of the gill, pore or spine, and these 

hyphae are collectively called the hymenophoral 

trama. Various distinctive types have been 

recognized by Reijnders and Stalpers (1992), but 

these do not correlate well with the phylogeny of 

the Homobasidiomycetes as shown in Fig. 19.2. 

1. In the trametoid type (e.g. in Lentinus, 

Fistulina and Schizophyllum), development begins 

with a bundle of parallel hyphae from which 

branches grow out in various directions and may 

become interwoven. 

2. In the cantharelloid type, the developing 

hymenophore is at first smooth and covered by a 

palisade of hyphae which will form 

the hymenium. Later, locally increased 

activity in the subhymenium may result 

in irregular ridges (Serpula), more regular veins 

(Cantharellus, Craterellus) or gills (Hygrophoropsis). 

3. The boletoid type is shown by Boletus and 

relatives (Fig. 19.9a). The first stage is made up of 

divergent hyphae which form a narrow central 

layer (mediostratum), followed by swelling and 

differentiation of the cells to form a lateral 

stratum. The diverging hyphae of the lateral 

strata curve sharply outwards to form the 

hymenium, and the term divergent trama is 

therefore used to describe this type of hymenophore. 

A subhymenium made up of narrow 

interwoven hyphae is also present. 

4. The agaricoid type is by far the most 

common and includes the coprinoid, russuloid, 

agaricoid, pluteoid and amanitoid subtypes. In 

cross-section, gills usually appear differentiated 

into a central trama, a subhymenium and the 

hymenium (Fig. 19.9b). The hyphae in the trama 

often run parallel to each other, but in the 

pluteoid subtype (e.g. Volvariella and Pluteus), the 

wide hyphae making up the trama are arranged 

in a V-shaped pattern (Fig. 19.9d), and this is 

called the inverted trama. In the russuloid 

subtype (Russula and Lactarius), the mature 

trama is said to be intermixed because in 

addition to the narrow generative hyphae it 

contains swollen cells (sphaerocysts) of very 

different width (Fig. 19.9c). The amanitoid type 

shows a central mediostratum made up of 

narrow generative hyphae from which wider 

subhymenial elements diverge (Fig. 19.9e). This 

type of trama is described as bilateral.


Fig19.9 Different types of hymenophoral trama. (a) The boletoid type shown by Boletus edulis. L.S. immature pore showing the 

divergent trama. (b e) Vertical sections of gills of various agarics of the aequi-hymenial type showing different types of 

hymenophore. (b) The agaricoid type shown in Flammulina velutipes. (c) The russuloid subtype shown by Russula cyanoxantha.Note 

the globose sphaerocysts. (d) The pluteoid subtype shown by Pluteus cervinus. Note the converging (V-shaped) arrangement of the 

cells making up the trama (inverted trama) and the hooked cystidia. (e) The amanitoid subtype.Vertical section of gill of Amanita 

rubescens, showing the bilateral hymenophoral trama. (c) and (d) to same scale.

IMPORTANCE OF HOMOBASIDIOMYCETES 

525 

19.2.5 The hymenium 

The ends of the tramal hyphae turn outwards 

to form a distinct layer of shorter cells, the 

subhymenium, which lies immediately beneath 

the hymenium of a palisade-like layer of ripe 

basidia, developing basidia (basidioles) and sometimes 

other structures such as cystidioles, 

cystidia and paraphyses. All these represent the 

terminal cells of hyphae making up the fruit 

body and are therefore homologous with basidia. 

Cystidioles are thin-walled, sterile elements of 

the hymenium, about the same diameter as the 

basidia, and usually protruding only slightly 

from the hymenial surface. 

Cystidia are more varied. They are often 

enlarged conical or cylindrical cells which may 

arise in the hymenium along with the basidia 

(hymenial cystidia) or sometimes deeper, for 

example in the trama (tramal cystidia). Fusion 

of paired nuclei within cystidia has been 

reported and in some cases 2 4 basidiospores 

have been observed to develop on cystidia. In 

Coprinus and its allies, the cystidia on the face of 

the gill may stretch across the space between the 

gills (Fig. 19.7). The tip of a cystidium makes 

contact with a cell on the opposing hymenium, 

and this cell, termed a cystesium (from cystidium 

þ Lat. haerare ¼ to adhere), then differentiates 

by developing a granular, vacuolated 

cytoplasm and becomes cemented to the tip of 

the cystidium, so that the cystidium bridging the 

gill cavity becomes firmly attached to both 

hymenia (Horner & Moore, 1987; Moore, 1998). 

The role of the hymenial cystidia in Coprinus 

was initially thought to be that of buttresses 

helping to space the inaequi-hymenial gills 

apart. However, it is now believed that the 

cystidium cystesium pairs function as tension 

elements, balancing the stretching forces generated 

by expansion growth of the cap and helping 

to straighten out the thin lamellae which are 

folded during early development (Chiu & Moore, 

1990a). In Pluteus the tramal cystidia bear hooklike 

tips (Fig. 19.9d) whose function is not 

understood. The suggestion that they might 

deter animals such as slugs from eating the gill 

tissue is not supported by feeding experiments 

(Buller, 1924). In Volvariella bombycina, cystidia on 

the face of the gill have aqueous drops adhering 

to them and are thus believed to be secretory in 

function, releasing water vapour into the space 

surrounding the basidia (Chiu & Moore, 1990b). 

Various terms have been used to describe cystidia 

from different parts of the basidiocarp. Those on 

the gill face are termed facial cystidia or 

pleurocystidia, those on the gill margin cheilocystidia. 

Cystidia are not confined to the hymenium. 

Similar structures have been found on the 

surface of the pileus (pileocystidia) and the stipe 

(caulocystidia). We are still ignorant of the 

function of many of these structures. For a 

fuller discussion see Singer (1986) and 

Clémençon (2004). 

Paraphyses are present in the hymenium of 

Coprinus. They develop on branches from the 

same hyphae which produce basidia (Fig. 19.7), 

arising after the young basidia are committed to 

meiosis. The tips of the paraphyses force themselves 

into the hymenium between developing 

basidia, grow to about two-thirds of the height of 

a basidium, become spherical and enlarge, thus 

playing an important role in the expansion of 

the maturing basidiocarp (Rosin & Moore, 1985; 

Moore, 1998). 

19.3 Importance of 

homobasidiomycetes 

Homobasidiomycetes have a significant impact 

on our lives. The fruit bodies of thousands 

of species are potentially edible, although 

only some 40 species have been cultivated. 

According to worldwide production data for 

the year 1997 (Chang & Miles, 2004), the most 

popular cultivated mushrooms are Agaricus 

bisporus (2 000 000 t per annum), Lentinula edodes 

(1 500 000 t), Pleurotus spp. (875 600 t), Flammulina 

velutipes (284 000 t) and Volvariella volvacea 

(180 000 t). Mushroom production is expanding 

rapidly, especially in the Far East. However, 

some of the most prized edible mushrooms are 

mycorrhizal associates of trees which cannot yet 

be cultivated away from their host. Mycorrhizal 

associations involving Homobasidiomycetes are 

prominent in forest situations and are dealt 

with in more detail below and also on p. 581.


An equally important ecological role played by 

the Homobasidiomycetes in the global environment 

is that of saprotrophs involved in the 

decomposition of the two most abundant organic 

carbon sources, cellulose and lignin, thereby 

releasing nutrients locked up in wood and leaf 

litter. The degradation of wood is achieved in 

two different ways, white-rot and brown-rot, 

and these are described briefly on pp. 527 532. 

A few wood-rotting species are plant pathogens, 

e.g. Armillaria mellea, Phellinus noxius and Crinipellis 

perniciosa, whereas others, notably the dry rot 

fungus Serpula lacrymans, cause economic damage 

of timber built into houses. 

19.3.1 Ectomycorrhiza 

Many members of the Homobasidiomycetes 

(including gasteromycetes), as well as a few 

Ascomycota such as the truffles (Tuber spp.; see 

p. 423), form ectomycorrhizal associations with 

coniferous and broad-leaved trees. These are 

distinguished from the vesicular arbuscular 

mycorrhiza between herbaceous plants and 

Zygomycota (see p. 217) in several key features 

which have been reviewed by Smith and Read 

(1997) and Peterson et al. (2004). The most 

immediately obvious is that the bulk of the 

fungal biomass is located outside the plant root, 

hence the term ectomycorrhiza. The colonization 

of a tree root by an ectomycorrhizal fungus has 

reciprocal morphogenetic effects. Lateral roots 

show stunted growth accompanied by increased 

branching which is often dichotomous 

(Fig. 19.10a) in response to fungal colonization, 

and they are covered by a thick sheath of hyphae, 

the mantle (Fig. 19.10b). There is also a limited 

colonization of the root cortex in the shape of 

the Hartig net, a system of unusually richly 

branched intercellular hyphae (Fig. 19.10b). The 

sequence of colonization events probably starts 

with hyphae being initially attracted to root tips 

by their exudates or possibly those of microorganisms 

associated with the rhizosphere, such 

as fluorescent pseudomonads (Garbaye, 1994; 

Smith & Read, 1997). Following contact with a 

root hair, hyphae grow alongside it until they 

meet the surface of the main root (Thomson 

et al., 1989). There, morphogenetic changes are 

initiated, such as hyphal branching and anastomosis 

which lead to the establishment of the 

mantle (Massicotte et al., 1987). These changes 

may result from the specific recognition of wall 

surface molecules between the root and fungus 

hypha (Giollant et al., 1993; Lapeyrie & Mendgen, 

1993). Outside the mantle, the mycelium 

may extend into the soil by a few centimetres, 

or much further if the fungus is capable of 

forming mycelial cords (see p. 581). The roots of 

different plants in complex forest ecosystems 

may be linked by common ectomycorrhizal 

fungi, and there may be a net transfer of 

carbon from sunlit plants to those growing in 

the shade (Leake et al., 2004). Mineral nutrients, 

notably phosphate, as well as water are transported 

from the fungus to the plant. 

Carbohydrates travel the opposite way. Sucrose, 

the main transport carbohydrate in plants, 

is secreted into the apoplast and hydrolysed to 

give fructose and glucose. The latter is taken up 

by the fungus and converted to glycogen, trehalose 

or polyols (Smith & Read, 1997). Some 10% of 

the net photosynthetic assimilate may be allocated 

to mycorrhizal fungi which make up 

20 30% of the microbial biomass in forest soils 

(Leake et al., 2004). Fruit bodies are a major sink 

for translocated carbon. Colourless (achlorophyllous) 

plants may obtain their carbon by plugging 

into the mycorrhizal network, a strategy known 

as mycoheterotrophy (Smith & Read, 1997). 

Fossil records of ectomycorrhizal associations 

date back some 50 million years (LePage et al., 

1997), although they are more likely to be 

around 200 million years old (Cairney, 2000). 

Mycorrhizae of this kind are particularly prominent 

in nutrient-poor or dry soils. Many ectomycorrhizal 

fungi have retained the capacity 

to produce hydrolytic enzymes and are capable 

of solubilizing, for example, phosphorus and 

nitrogen from complex sources (Perez-Moreno & 

Read, 2000). They are therefore often associated 

with humus layers in which saprotrophic 

species also grow. Ectomycorrhizal fungi may 

show a greater or lesser degree of host specificity; 

for instance, Suillus grevillei is associated almost 

exclusively with larch (Larix spp.), whereas 

Amanita muscaria (fly agaric), Boletus edulis 

(cep or penny bun) or Cantharellus cibarius


527 

Fig19.10 Ectomycorrhiza on beech roots collected from humus. (a) General view. Note the stunted growth and dichotomous 

branching of the lateral roots which are entirely covered by the mantle. (b) Transverse section through such a mycorrhizal root tip. 

A mantle several hyphae thick has formed a sheath around the epidermis. Branching hyphae grow between the outer cortical cells 

(arrows) to form the Hartig net. (a) kindly provided by A.E. Ashford. 

(chanterelle) are found under both broad-leaved 

and coniferous trees. 

The latter two species together with 

Tricholoma matsutake are the three most valuable 

mycorrhizal Homobasidiomycetes in commercial 

terms, with a combined annual crop value of 

over US$ 2 billion (Hall et al., 2003). Considerable 

efforts have been made to develop methods for 

their cultivation, but success has been limited. 

Whilst it is possible to cultivate mycelium of 

these species in vitro on agar media and to 

inoculate seedlings of host trees, the crops of 

fruit bodies after outplanting have been disappointing 

or altogether absent (Wang & Hall, 

2004). The situation is more encouraging for the 

ectomycorrhizal ascomycete truffles Tuber melanosporum 

and T. magnatum (see p. 423), but even 

with these species the establishment of commercial 

plantations has failed to reverse the decline 

in overall harvests due to overcollection and 

destruction of natural habitats. 

Fortunately, there are several ectomycorrhizal 

species which, although inedible, can be 

used as reliable inoculum to promote the 

growth of trees in challenging environmental 

situations. Probably the most successful group 

is the gasteromycete genus Pisolothus, which is 

used extensively in afforestation programmes 

(see p. 581). 

19.3.2 Degradation of wood 

The complex architecture of wood is summarized 

in Fig. 19.11. The middle lamella separating 

adjacent cells consists of a-(1,4)-linked galacturonic 

acid polymers collectively called pectins, in 

which the carboxylic acid group may be derivatized 

by methylation or calcium salt formation. 

The primary wall consists chiefly of cellulose 

made up of b-(1,4)-linked glucose units. 

Hemicelluloses are also present; these comprise 

several heterogeneous polymers with a backbone 

of glucose, mannose or xylose in b-(1,4)-linkage,


Fig19.11 Carbon-containing polymers and their localization in woody tissue.Lignin consists of a complex polymer (modified from Adler,1977) of the three phenylpropanoid units shown, 

which may be linked in numerous different combinations.


529 

with various sugars or uronic acids added as side 

chains. Since pectin, cellulose and hemicelluloses 

are all polymerized by enzymes in a regular 

fashion, they can also be degraded by hydrolytic 

Fig19.12 Wood rot symptoms. (a) White-rot of beech caused 

byTrametes hirsuta (left). Note the bleached appearance of the 

branch interior at the broken surface. Beech wood attacked 

by a brown-rot is also shown for comparison (right). (b) Trunk 

segments of Picea abies attacked by Fomitopsis pinicola.The 

brown-rot had caused a hollowing of the standing tree prior 

to felling. (c) Log of Picea abies colonized by Fomitopsis pinicola, 

showing brown rot symptoms.The wood has cracked into 

cube-like fragments which are easily ground into a powder. 

enzymes, although accessibility problems may 

prevent this from happening in situ (see below). 

The architecture of secondary plant walls is 

radically different. Apart from hemicelluloses 

as a minor component, the principal building 

material is lignin, a polymer of aromatic 

alcohols which are cross-linked in a random 

fashion by free radical reactions. Lignin therefore 

has a complex, non-repetitive three-dimensional 

structure resistant to direct attack by 

enzymes. Only few basidiomycetes are able to 

mineralize lignin to H 2 O and CO 2 , and this is 

achieved by oxidative rather than hydrolytic 

enzymes. The result is that wood undergoes 

white-rot (see Plate 10a; Fig. 19.12a), i.e. it 

appears bleached because all its components 

are degraded more or less simultaneously, or 

lignin degradation precedes attack on cellulose. 

In contrast, many fungi which degrade cellulose 

leave behind the lignin component of wood 

which turns brown upon oxidation, and this type 

of decay is therefore called brown-rot. The 

removal of cellulose destroys the structural 

integrity of wood so that the lignin cracks into 

cubes (Fig. 19.12c) and ultimately breaks up into 

a powder which becomes incorporated into 

humus. Living trees may survive infection by 

brown-rot fungi if this is confined to the heartwood 

in the core of the trunk, leaving a 

sufficiently strong cylinder of sound wood 

(Fig. 19.12b). Prolonged or repeated attacks by 

such wood-rotting basidiomycetes are responsible 

for the hollowing of trunks observed in 

many historic trees. 

Brown-rot 

The hyphae of brown-rot fungi colonizing wood 

through its lignin-encased tubular cavities face 

the major problem of gaining access to degradable 

substrates. One point of attack is the middle 

lamella, which is exposed by simple or bordered 

pits in the secondary cell walls of adjacent cells, 

and polygalacturonases are indeed produced 

by many brown-rot fungi (Green & Clausen, 

1999, 2003). A typical feature of brown-rots is 

the production of oxalic acid, which may be 

important in chelating calcium ions released at 

potentially toxic concentrations by the degradation 

of calcium pectate. Calcium oxalate crystals


are common on the surfaces of many fungal 

hyphae. Oxalic acid may also chelate other ions 

such as Cu 2þ , which is used as a preservative for 

the treatment of wood. The oxalic acid concentration 

may bring about strongly acidic conditions, 

sometimes as low as pH 1.7, which would 

be sufficient for acid hydrolysis of pectin and 

even cellulose (Green et al., 1991). Both endoand 

exo-enzymes of the cellulase complex are 

generally produced by brown-rot fungi (Hegarty 

et al., 1987), and these may act in the usual 

synergistic way to convert cellulose to oligosaccharides 

and thence to glucose (Radford et al., 

1996). Hemicellulases are thought to act in a 

similar way. However, these enzymes may 

not gain access to their substrate where it is 

masked by the lignin-containing secondary wall. 

Although the detailed mechanism of brown-rot 

decay is still unknown, there is evidence that 

at least the initial attack on cellulose 

(and hemicellulose) is mediated by small molecules 

capable of penetrating the lignin layer. 

These may be the hydronium ion (H 3 O þ ) generated 

by oxalic acid in water, or another molecule 

such as the hydroxyl radical (HO) released from 

hydrogen peroxide (H 2 O 2 ) by the Fenton reaction 

(Fe 2þ þ H 2 O 2 ! Fe 3þ þ HO þ HO ). The 

mechanism of brown-rot decay is all the more 

mysterious because many brown-rot fungi do, 

in fact, produce enzymes capable of degrading 

lignin (Mtui & Nakamura, 2004), but these may 

have other functions, such as the detoxification 

of antimicrobial phenolics which are often 

present in wood at high concentrations 

(Rabinovich et al., 2004). 

White-rot 

The suite of enzymes required to break down 

lignin has been most thoroughly examined in 

the white-rot fungus Phanerochaete chrysosporium 

(see de Jong et al., 1994a; Heinzkill & Messner, 

1997). There are numerous conflicting ideas 

about the enzymology of lignin degradation, 

and we can only generalize here. Initial attack on 

lignin is mediated by lignin peroxidases (LiP) 

and/or manganese peroxidases (MnP) which do 

not themselves enter the lignin layer. Instead, 

small diffusible molecules probably act as redox 

charge carriers between the enzymes and their 

substrate. A possible reaction scheme for LiP is 

shown in Fig. 19.13 (Heinzkill & Messner, 1997; 

ten Have & Teunissen, 2001). The enzyme consists 

of a single polypeptide chain and a protoporphyrin 

IX (haem) group which is buried deep 

inside the enzyme, accessible to small diffusible 

molecules through a narrow pore. LiP loses two 

electrons when it reduces H 2 O 2 to water. This 

highly oxidized LiP I state is returned to the 

ground state in two steps, each associated with 

the one-electron oxidation of a reductant into 

its cation radical. Veratryl alcohol, produced 

in abundance by most white-rot fungi, is such 

a reductant. The two cation radicals leave the 

enzyme and either themselves attack the lignin 

structure, or pass on their charge to other small 

molecules. Either way, the extraction of one 

electron from an aromatic ring of lignin generates 

a structure reacting both as a cation and as a 

radical, leading to numerous possible degradation 

products. The conversion of LiP into LiP I 

requires H 2 O 2 which is generated by extracellular 

enzymes such as glucose oxidase or aryl 

alcohol oxidase. The latter uses organohalogens 

such as 3-chloroanisylalcohol as substrates, and 

these may accumulate in the environment 

colonized by white-rot fungi (de Jong et al., 

1994b), even though organohalogens have traditionally 

been regarded as man-made (anthropogenic) 

environmental pollutants. 

Manganese peroxidase (MnP) is closely related 

to LiP in its protein structure and its catalytic 

cycle, except that the co-factor is Mn 2þ instead of 

veratryl alcohol. The oxidized Mn 3þ may be 

stabilized by organic acids en route to the 

lignin substrate, where it catalyses a one-electron 

oxidation either directly or via charge transfer 

molecules, followed by recycling of Mn 2þ back to 

the MnP enzyme. Copper-containing laccases are 

a third group of enzymes attacking lignin, and 

these are produced by a range of fungi much 

wider than that causing white-rot. By reducing 

O 2 to H 2 O, laccases are capable of performing a 

four-electron oxidation either of a redox carrier 

or the final substrate itself. In this way, laccases 

may be able to degrade smaller lignin fragments, 

although they are probably incapable of a direct 

attack on intact lignin, due to steric problems. 

The precise role of laccases in lignin degradation


531 

Fig19.13 Reaction cycle of lignin peroxidase.The reduction of H 2 

O 2 

to H 2 

O withdraws two electrons from the ground-state 

enzyme (LiP), one from the ferric ion to give the ferryl ion (Fe4þ), and the other from the protoporphyrin group itself which is 

converted to the porphyrin cation radical.This results in the highly oxidized LiP I state which catalyses two separate one-electron 

oxidations of a reductant, e.g. veratryl alcohol (VA), becoming reduced via the LiP II state to the ground state.TheVA cation 

radical is regenerated when it withdraws one electron from lignin itself or from other molecules serving as redox charge carriers 

(not shown). H 2 

O 2 

can be generated by several means, including the oxidation of 3-chloro-anisylalcohol (CA alc) to give its 

corresponding aldehyde (CA ald). 

has not yet been fully characterized, although it 

is likely to be pivotal as most, if not all, white-rot 

fungi produce them, and in some white-rot 

species such as Pycnoporus cinnabarinus they may 

be the only kind of ligninolytic enzyme present 

(Eggert et al., 1997). All three lignin-attacking 

enzymes are usually secreted as multiple 

isoforms which differ in their pH optima or 

catalytic properties (Kirk & Cullen, 1998). It 

should be noted that lignin degradation is 

always co-metabolic, i.e. white-rot fungi cannot 

utilize lignin as the sole source of carbon or 

energy, and they probably remove it for the 

purpose of gaining access to more easily 

degraded substrates such as cellulose. Although 

white-rot fungi are generally considered to be 

more ‘efficient’ than brown-rots, the latter, in 

circumventing the effort of lignin degradation, 

probably obtain more glucose per unit metabolic 

effort. 

The attack on lignin by means of charge 

transfer molecules being a non-specific reaction 

mechanism, ligninolytic enzymes will also 

degrade other substances, including man-made 

recalcitrant environmental pollutants such 

as polycyclic aromatic hydrocarbons, organohalogens, 

or the explosive TNT (see Gadd, 2001). 

White-rot fungi are therefore being investigated 

extensively for their potential in the bioremediation 

of contaminated environments. Another


biotechnological application is the use of oxidative 

enzymes for the bleaching of wood pulp for 

paper production, or of textile dyes. 

There is a further twist to the tale. Many 

fungal metabolites, including veratryl alcohol 

and 3-chloro-anisylalcohol (see Fig. 19.13), contain 

methoxy groups or methyl esters, whose 

methyl groups are added late during biosynthesis. 

Various molecules may act as donors 

of methyl groups, including chloromethane 

(CH 3 Cl), a known greenhouse gas. A few woodrotting 

fungi, notably Phellinus spp., have 

gained notoriety because they produce vastly 

more chloromethane than they require for 

their biosynthetic machinery. Watling and 

Harper (1998) estimated that atmospheric chloromethane, 

which is mainly of natural origin, 

accounts for 15 20% of the chlorine-mediated 

ozone destruction in the stratosphere, and that 

86% of the total fungal chloromethane contribution 

can be attributed to the genus Phellinus. 

19.4 Euagarics clade 

As shown in Table 19.1 and Fig. 19.2, the 

euagarics clade includes not only forms with 

lamellate (i.e. agaricoid) basidiocarps formerly 

classified in the Agaricales, but also forms with 

other hymenial configurations. This means that 

there are few, if any, reliable gross morphological 

characters by which members of the euagarics 

clade can be recognized. It is probable that 

agaricoid basidiocarp types have evolved repeatedly 

(Hibbett et al., 1997b). Kirk et al. (2001) have 

recognized 26 families, 347 genera and about 

10 000 species, but cautioned that there are 

difficulties in defining these families at present. 

In the account of some common genera which 

follows, the estimated numbers of species have 

been taken from Kirk et al. (2001) unless otherwise 

indicated. 

19.4.1 Agaricaceae 

The Agaricaceae are one of the most diverse 

families of the Agaricales, estimated to contain 

over 50 genera and some 900 species. The spore 

print (i.e. the accumulation of spores projected 

from a basidiocarp) may be white or coloured. 

There are also variations in the structure of the 

hymenophoral trama and the surface of the 

pileus. Partial and/or universal veils are usually 

present. Despite these variations, molecular 

evidence supports the view that the core genera 

of this family, including Agaricus and Lepiota, are 

monophyletic (Moncalvo et al., 2000, 2002; 

Vellinga, 2004). 

Agaricus (c. 200 spp.) 

This is a large genus of fungi often synonymized 

with the term ‘mushrooms’, distributed mainly 

in temperate regions. Agaricus spp. are saprotrophs, 

growing in pastures and woodland litter. 

The mycelium is perennial and some species, e.g. 

A. arvensis (horse mushroom), A. xanthodermus 

(yellow stainer) and A. tabularis may fruit in rings. 

From measurements of the annual rate of 

increase in diameter, a ring of A. tabularis 60 m 

in diameter was estimated to be 250 years old. 

Agaricus basidiocarps are moderate to large in 

size, generally firm and white but sometimes 

changing colour upon bruising (e.g. in A. xanthodermus). 

There is a ring on the stem (two rings in 

A. bitorquis), but no volva. The gills are at first 

pink due to the colour of the cytoplasm of the 

spores, but, as the spores mature, their walls 

darken to a purple-brown, the colour of the spore 

print. Many species have edible basidiocarps 

and some are prized as food, e.g. A. campestris 

(field mushroom), A. arvensis, A. macrosporus and 

A. silvaticus. Agaricus bisporus (Fig. 19.14a), now 

sometimes called A. brunnescens, is the cultivated 

white button mushroom (see below) and is 

occasionally found in nature on manure heaps, 

garden waste and roadsides, and under Cupressus 

in coastal areas of California and France. The 

basidiocarps of A. xanthodermus may cause gastrointestinal 

upsets in some people, probably due 

to the presence of phenol which also gives the 

fruit bodies an unpleasant smell of carbolic acid 

(Gill & Strauch, 1984). 

Cultivation of Agaricus bisporus 

The white button mushroom has been cultivated 

for its edible fruit bodies for almost four 

centuries since collectors discovered that its 

spawn could be used to inoculate compost. The

EUAGARICS CLADE 

533 

Fig19.14 Basidiocarps in the euagarics clade (1). (a)The commercial mushroom, Agaricus bisporus. (b) The parasol mushroom, 

Macrolepiota procera. In mature specimens the ring is moveable. (c) Coprinus comatus, the shaggy inkcap or lawyer’s wig. (d) Coprinus 

cinereus fruiting in the laboratory on a dung/straw mixture. (e) Pleurotus ostreatus,theoystermushroom. 

widespread cultivars used in the mushroom 

industry originated in France, where it is called 

champignon de Paris or champignon de couche. 

There are probably about seven such ancestral 

lineages (Callac, 1995). Specimens growing in 

nature belong to two distinct groups, namely 

genetically diverse indigenous populations and 

more uniform ‘cultivar-like’ populations 

which probably represent escapes from cultivation 

(Xu et al., 1997). Mushroom cultivation is 

now an important industry in temperate countries, 

and technical details have been described 

by van Griensven (1988) and Chang and Miles 

(2004). In 1996 global production exceeded


2 million tonnes (Moore & Chiu, 2001). In areas 

with a warmer climate, e.g. in Southern Europe, 

A. bitorquis is also grown. 

Mushrooms were originally cultivated in 

caves, but today most are grown in specially 

constructed sheds. The basic substratum is a 

composted straw/manure mixture (Straatsma 

et al., 1995). The heap of compost is kept outdoors 

where it heats up naturally to 80°C over a period 

of 2 weeks, with occasional turning. The heat 

produced during composting selects for the 

growth of specialized thermophilic microbes, 

the most important of which for mushroom 

production is the anamorphic mould Scytalidium 

thermophilum (syn. Humicola insolens) (Straatsma & 

Samson, 1993). The yield of mushrooms from 

a compost inoculated with S. thermophilum is 

doubled as compared with pasteurized controls 

(Straatsma et al., 1994a,b) because the A. bisporus 

mycelium can grow partly on the residues 

associated with the activities of S. thermophilum 

and partly on its living mycelium and conidia 

(Bilay & Lelley, 1997). The heat produced during 

composting destroys many competing microbes, 

and further destruction is achieved by a pasteurization 

process in which the compost, now 

moved into a shed, is heated by steam to a 

temperature of 60°C for 8 h which minimizes 

diseases caused later by other fungi. 

After cooling, the compost is inoculated with 

mushroom spawn pre-grown on sterilized cereal 

grains. The inoculated compost is incubated at 

25°C for 2 weeks, and fruiting is induced by 

covering the colonized spawn with a 3 5cm 

deep layer of casing soil or a special mixture of 

moist peat and chalk. The mycelium grows up 

through the casing layer and forms anastomosing 

mycelial cords from which ‘pinheads’ 

develop at the surface, some of which expand 

to form mature basidiocarps. In addition to any 

physical or chemical effect associated with the 

casing layer, there is also a biological component. 

This is shown by the fact that sterilized 

casing soil is far less effective than natural soil in 

encouraging fruiting. Re-inoculation of bacteria 

isolated from casing soil into sterile casing has 

shown that Pseudomonas spp. and especially 

P. putida are effective in inducing fruiting 

(Hayes et al., 1969). The growth of P. putida, 

in turn, is selectively stimulated by volatile 

substances such as ethanol emanating from 

the mushroom compost. Bacteria accumulate 

around Agaricus hyphae in a zone sometimes 

termed the hyphosphere. 

Bacteria which are active in inducing basidiocarp 

formation might achieve their effect 

in two ways. Possibly, they induce starvation 

of A. bisporus hyphae in a manner similar to 

fungistasis in soil, where the depletion of 

nutrients by competing microbes inhibits 

fungal spore germination. An alternative idea 

is that bacteria in the casing layer 

absorb substances which retard the fruiting of 

A. bisporus. This idea is supported by observations 

that fruiting can be induced by replacing the 

casing layer with activated charcoal, believed to 

adsorb inhibitory substances (Long & Jacobs, 

1974; Flegg & Wood, 1985; Noble et al., 2003). 

The isolation of putative inhibitors is a difficult 

task, but one substance, 1-octen-3-ol, has been 

shown to inhibit primordium formation in plate 

culture. 

Two weeks after application of the casing 

layer, fruiting is stimulated by forced 

air ventilation which lowers the temperature 

to 20°C and the CO 2 concentration to 

300 1000 ppm. Cropping occurs after 10 days, 

followed by 2 3 more flushes at weekly 

intervals. The whole cycle from compost preparation 

to cropping is completed in 10 weeks. 

Morphogenesis of A. bisporus basidiocarps 

The pinheads which form at the surface of the 

casing soil attached to mycelial cords are 

basidiocarp primordia, consisting at first of 

loose aggregates of hyphae. Basidiocarp development 

has been followed by several workers 

(see Bonner et al., 1956; Umar & van Griensven, 

1997). The hyphal aggregates become compact 

and enlarge to form flattened ‘buttons’. When 

these are about 2 mm high, there are signs of 

reorientation of hyphae in the region of the gills, 

and a gap develops beneath the gill region as a 

result of programmed cell death (apoptosis) 

to form the hymenial chamber, enclosed below 

by the partial veil. At a height of about 5 mm 

the stipe becomes recognizable by the parallel 

arrangement of hyphae and, by the time the


535 

primordium has grown to a height of 10 mm, the 

orientation of the upper stalk region is complete. 

Subsequent increase in height of the stipe is 

almost entirely due to cell expansion, although 

some nuclear and cell division also occur, 

especially in the upper region of the stipe 

where cell elongation is most marked 

(Craig et al., 1977). The gills develop in radially 

arranged ridges made up of downward-growing 

hyphae terminating in a tightly packed palisade 

of cells which are the basidia. Although the 

hyphal segments making up the vegetative 

mycelium and the stipe are multinucleate, 

the number of nuclei in the basidia is reduced 

to two. As the pileus continues to expand, the 

partial veil is broken and persists as a ring 

attached to the stem (Fig. 19.14a). There is 

evidence that stipe elongation is promoted by 

a factor of unknown chemical identity, which is 

mainly produced by the ripening gills (Frazer, 

1996). Konishi (1967) partially purified a 

substance which enhanced stipe elongation. 

The promoting substance included a mixture of 

amino acids, and it is not known if they function 

as nutrients or growth factors. It has also been 

claimed that a compound found chiefly in gill 

tissue of mushrooms, 10-oxo-trans-8-decenoic acid 

(ODA), stimulates mycelial growth and enhances 

elongation of the upper stipe (Mau et al., 1992). 

Unfortunately, attempts to confirm these findings 

have been disappointing (Champavier et al., 

2000). 

Biochemical changes occur during basidiocarp 

development (Hammond, 1985; de Groot 

et al., 1998). Mannitol, glycogen and trehalose 

accumulate in basidiocarp primordia, lowering 

the water potential and thereby possibly causing 

uptake of water from the mycelium. This would 

lead to an increase in turgor pressure, causing 

cell enlargement and fruit body expansion 

(Hammond & Nichols, 1979). Rapid synthesis 

of chitin is correlated with stipe elongation 

(Craig et al., 1979). 

A hydrophobin-like protein is secreted by the 

vegetative mycelium of A. bisporus and an 

abundant hydrophobin (ABH1) forms hydrophobic 

rodlet layers on the surfaces of the cells in 

certain regions of the basidiocarp, especially 

those where there are air spaces, such as in the 

outer regions of the pileus and stipe, in the veil 

and in the core of the stipe, but not in the gills. 

The hydrophobic layer may be responsible for the 

non-wettability of the surface of the basidiocarp, 

preventing the inflow of water from the outside 

and possibly protecting against bacterial and 

fungal parasites (Lugones et al., 1996). 

Life cycle of Agaricus bisporus 

The life cycle of A. bisporus is unusual (Miller, 

1971). The majority of the spores formed on its 

two-spored basidia are at first binucleate but 

post-meiotic mitosis increases the number of 

nuclei to four. The spores are heterokaryotic for 

mating type, i.e. they contain non-sister nuclei 

with dissimilar A mating type idiomorphs 

(Evans, 1959; Elliott, 1985). The products of 

meiosis in the basidium are four haploid 

nuclei, two with mating type idiomorph A 1 and 

two with A 2 . Since two nuclei enter each 

basidiospore, the spores may be homokaryotic 

(A 1 þ A 1 or A 2 þ A 2 ) or heterokaryotic (A 1 þ A 2 ). 

Of the 12 possible pairings of the 4 haploid 

meiotic products, 4 are homokaryons and 8 are 

heterokaryons, i.e. in a ratio of 1 : 2. Evans (1959) 

has claimed that the disproportionately high 

ratio of heterokaryotic spores results from the 

alignment of the nuclear spindles during meiosis 

in the basidia. 

On germination the heterokaryotic spores 

give rise to a mycelium with multinucleate 

hyphal segments capable of forming basidiocarps. 

Mycelia from homokaryotic spores 

can only fruit following anastomosis with mycelia 

of opposite mating type. Basidia of normal 

cultivated A. bisporus may rarely bear three 

or four basidiospores, and most of these are 

initially uninucleate. Mycelium from such an 

aberrant spore will only fruit when mated with 

a mycelium of opposite mating type. Thus 

A. bisporus has two alternative kinds of mating 

behaviour, secondary homothallism or bipolar 

heterothallism. Such ambivalent behaviour is 

sometimes termed amphithallic (Lange, 1952) 

and is not confined to A. bisporus, being 

also found in some other basidiomycetes with 

two-spored basidia, e.g. certain species of Coprinus 

(euagarics clade) and the four-spored Stereum 

sanguinolentum (russuloid clade).


Breeding of Agaricus bisporus 

The development of new strains of A. bisporus 

with superior qualities such as more efficient 

substrate conversion rates, rapid fruiting, higher 

yield, resistance to disease, ease of picking, 

extended shelf-life, better appearance, flavour 

or consistency is actively pursued by the mushroom 

industry (see Raper, 1985; Sonnenberg, 

2000). This task is difficult but worthwhile in 

view of the high commercial value of the crop, 

and various techniques are being used: 

1. Selection of strains collected in the field 

and arising during cultivation. 

2. Hybridization. The small amount of variation 

in the gene pool of commercial stocks of 

A. bisporus creates little scope for recombination. 

However, a search for new genetic resources 

within wild Agaricus populations, the Agaricus 

Resource Program (ARP), has made available 

novel germ plasm which will prove useful in 

breeding (Kerrigan, 1996). Of particular interest 

is the discovery in the Sonoran desert (California) 

of tetrasporic populations, named A. bisporus var. 

burnettii, which are completely interfertile with 

commercial lines (Kerrigan et al., 1994; Kerrigan, 

1995). Agaricus bisporus var. eurotetrasporus, 

another four-spored variety, has been discovered 

in Europe. Whilst var. burnettii is amphithallic 

and predominantly heterothallic, var. eurotetrasporus 

is homothallic (Callac et al., 2003). 

3. Protoplast fusion. The fusion of protoplasts 

from different homokaryons is an alternative to 

the conventional hybridization technique involving 

the pairing of compatible homokaryotic 

mycelia. 

4. Transformation (genetic modification) 

using Agrobacterium as a vector for the transforming 

DNA is also possible, but genetically modified 

food products are unpopular with consumers 

and certain political parties. 

Macrolepiota (30 spp.) 

The best-known species of Macrolepiota are the 

parasol M. procera (Fig. 19.14b) and the shaggy 

parasol M. rhacodes, both of which grow in parks, 

pastures and woodland. They are saprotrophs. 

The pale brown fruit bodies are large and 

generally considered good to eat, although 

those of M. rhacodes may cause gastric upsets. 

A feature of both species is that the ring 

is detachable and is free to move up and 

down the stem. Macrolepiota procera and 

M. rhacodes have been separated from Lepiota, 

and Vellinga et al. (2003) have proposed that they 

should be separated from each other as well, 

with M. procera showing affinities with 

Leucoagaricus and Leucocoprinus, and M. rhacodes 

with Agaricus. 

There are concerns about the ability of 

M. procera to concentrate mercury absorbed 

from the soil into the basidiocarp tissues, with 

values in the caps as high as 13 mgg 1 reported 

from various sites in Poland. The mercury 

content of the caps and stalks was generally 

independent of the soil substrate concentration, 

suggesting a remarkable ability of the M. procera 

mycelium to bioconcentrate mercury (Gucia & 

Falandysz, 2003). 

Coprinus 

Molecular evidence indicates a relationship 

between lepiotoid fungi and two species of 

Coprinus, namely C. comatus and C. sterquilinus 

(Hopple & Vilgalys, 1999; Redhead et al., 2001). 

Although it is now possible, with hindsight, to 

recognize other features shared by these species 

and other Agaricaceae, e.g. the shaggy surface of 

the cap or the moveable annulus (Fig. 19.14c), we 

will discuss them in the context of the many 

biological features uniting them with their 

former allies (see below). 

19.4.2 Coprinaceae (now Psathyrellaceae) 

Molecular studies have shown that the genus 

Coprinus is not monophyletic (Hopple & Vilgalys, 

1999; Redhead, 2001; Redhead et al., 2001), 

implying that the coprinoid character of deliquescent 

gills has evolved more than once. 

This finding has caused a taxonomic nightmare 

because one of the two species found to 

be related more closely to Macrolepiota than 

to Coprinus happened to be the type-species 

C. comatus. Its move from the Coprinaceae to 

the Agaricaceae meant that those numerous 

species remaining in the Coprinaceae were 

given new names, namely Coprinopsis (e.g. C. 

atramentarius, C. cinereus, C. lagopus, C.


537 

psychromorbidus), Coprinellus (e.g. C. bisporus, C. 

domesticus, C. heptemerus, C. micaceus, C. plagioporus, 

C. sassii), and Parasola (e.g. C. plicatilis). Members of 

the genus Coprinopsis produce fruit bodies with 

hollow stipes and are closely related to 

Psathyrella, thereby presenting the opportunity 

to re-name Coprinaceae as Psathyrellaceae. 

However, because the old name Coprinus in a 

broad sense (sensu lato) continues to be used in 

most non-taxonomic studies, we follow that 

convention for the time being. It is also possible 

that there will eventually be an initiative to 

designate a new type-species of Coprinus, i.e. to 

change the name C. comatus rather than those of 

almost all the other species. 

Coprinus sensu lato (c. 350 spp.) 

This is the large group of ‘ink-caps’ with 

deliquescent inaequi-hymenial gills undergoing 

autodigestion at maturity (see Orton & Watling, 

1979). Representatives of Coprinus sensu lato 

are cosmopolitan, fruiting on a great variety of 

substrata including soil, dung and wood (Orton 

& Watling, 1979). Coprinus comatus (the shaggy 

ink-cap or lawyer’s wig; Fig. 19.14c) fruits on 

soil, especially on disturbed ground. It has a 

well-developed, moveable annulus. Another characteristic 

feature is the presence of an elastic 

strand of aggregated hyphae which extends 

through the lumen of the hollow stipe 

(Redhead, 2001). Basidiocarps of C. atramentarius 

(common ink-cap or pavement cracker) emerge 

at the soil surface from buried wood; those of 

C. micaceus (glistening ink-cap) are found in 

similar situations, or directly on broad-leaved 

tree stumps. Coprinus domesticus also fruits on 

dead wood of deciduous trees arising from a 

rust-coloured sporulating mat of mycelium, the 

Ozonium anamorphic state. 

There are many coprophilous species, the 

most studied being C. cinereus (earlier erroneously 

named C. lagopus) on cattle and horse manure 

heaps and manured straw (Fig. 19.14d). This 

species grows and fruits well in the laboratory 

and has been the subject of much research, 

ably reviewed by Kües (2000), on the genetics 

of mating systems (Pukkila & Casselton, 1991; 

Casselton & Riquelme, 2004), cytology (Raju & Lu, 

1970; L. Li et al., 1999), morphogenesis (Moore, 

1998), gravitropism (Moore et al., 1996), stipe 

elongation (Kamada, 1994), nuclear migration, 

clamp formation, physiology of fruiting and 

other phenomena. Whilst most Coprinus species 

are saprotrophic, C. psychromorbidus (¼ ‘diseased 

by cold’) belongs to a group of low-temperature 

basidiomycetes which are plant pathogens. It is 

the cause of snow mould disease of grasses and 

other plants in Canada and also causes a postharvest 

rot of apples in cold store. It can 

continue to grow actively under snow cover 

because it possesses special thermal hysteresis 

proteins with antifreeze properties (Sholberg & 

Gaudet, 1992; Hoshino et al., 2003). 

Basidiocarps of Coprinus have thin inaequihymenial 

gills with prominent pleurocystidia 

and cystesia (see p. 525). Basidiocarps range in 

size from a few millimetres in coprophilous 

forms to over 30 cm (C. comatus). Spore development 

and discharge occurs first at the base of the 

gill, followed by autodigestion of the discharged 

basidia and the hyphae which supported them. 

Chitinase and other hydrolytic enzymes play a 

major role in autodigestion (Iten & Matile, 1970; 

Miyake et al., 1980). The digested tissue drips 

away from the base of the gills as a black fluid 

which can be used as writing ink. Meanwhile an 

upward wave of basidiospore discharge 

continues above the digested tissues. In certain 

species, the gills do not deliquesce, or do so only 

partially. In C. curtus some limited autodigestion 

occurs at the edge of the gill and the gills open, 

as in C. plicatilis, by a V-shaped groove which 

widens from above (Buller, 1909, 1931). Buller 

(1924) has shown that in many species of Coprinus 

the basidia are dimorphic, with long and short 

forms present in the same gill. The short forms 

are fully functional, i.e. the basidia ripen at 

different levels of the hymenium. This arrangement 

makes it possible to crowd a larger number 

of basidia into a given area without interference 

in spore release. Trimorphic and tetramorphic 

basidia are present in some species. 

Sclerotia in Coprinus 

Sclerotia are formed by several species. Coprinus 

sterquilinus develops its sclerotia at the surface 

of cattle dung and, under suitable conditions, 

basidiocarps develop from them (Buller, 1924).


In culture, the sclerotia of C. cinereus form on 

monokaryons as well as dikaryons growing 

aerially or submerged (Waters et al., 1975a,b). 

They are quite small (100 1000 mm in diameter), 

dark brown to black and more or less spherical. 

These sclerotia do not develop basidiocarps. 

Three tissue layers are distinguishable in aerial 

sclerotia: an outer diffuse layer of apparently 

dead cells, a multi-layered rind of heavily 

pigmented, closely packed, thick-walled cells, 

and a medulla with predominantly thick-walled 

cells. These thick-walled cells at first accumulate 

rosettes of a glycogen-like polysaccharide in the 

cytoplasm, but this disappears as the cells 

mature, while a secondary cell wall layer 

increases in thickness. It is believed that the 

glycogen serves a temporary storage function but 

that the secondary wall represents the long-term 

storage compartment. 

Stipe elongation in Coprinus 

Shortly before spore discharge begins in Coprinus, 

the stipe undergoes rapid elongation, most of it 

taking place in its upper half. Although in 

C. cinereus the cells of the vegetative mycelium 

are dikaryotic, the cortical cells of the stipe 

undergo repeated nuclear division prior to rapid 

elongation so that they may contain between 

32 and 156 nuclei. Stipe elongation is largely 

brought about by turgor-driven cell expansion, 

not cell division. The cells increase in length, but 

not in width, by about eightfold in the final 15 h 

of fruit body expansion. During that period, the 

osmotic pressure is actively maintained as water 

enters the cells. The solutes contributing to the 

maintenance of osmotic pressure have not been 

identified. The increase in stipe length is 

mirrored by an increase in the chitin content. 

Helically coiled chitin microfibrils are present in 

the walls of cortical cells, and it is believed that 

newly synthesized microfibrils are inserted 

between pre-existing ones, a process termed 

diffuse extension growth to distinguish it from 

the usual apical extension growth of hyphal tips 

(Kamada, 1994). 

The force of the elongating stipe can be 

considerable. Buller (1931) placed weights on an 

expanding fruit body of C. sterquilinus which had 

a pileus height of 1.4 cm and diameter of 0.8 cm. 

This fruit body could lift a weight of 204 g. 

The cross-sectional area of the ring of tissue 

surrounding the hollow stipe was 29 mm 2 

and calculations of the upward pressure of the 

stipe gave a value of two-thirds of an atmosphere 

(0.7 10 4 Nm 2 ). This may explain why the 

expanding fruit bodies of C. atramentarius can 

crack asphalt and why other fungi can lift paving 

slabs. 

Mating behaviour in Coprinus 

Some Coprinus spp. are primarily homothallic, 

e.g. C. heptemerus. Species with two-spored basidia 

are often secondarily homothallic, e.g. C. bisporus 

(¼ C. ephemerus var. bisporus). Yet other species 

show bipolar (i.e. unifactorial) heterothallism 

(e.g. C. comatus and C. ephemerus), or tetrapolar 

(i.e. bifactorial) heterothallism (e.g. C. cinereus; 

see Section 18.9). M. Lange (1952) has proposed 

the term amphithallism (see p. 532) to describe 

the behaviour of species of Coprinus in which 

both homothallic and heterothallic mycelia can 

be raised from the same fruit body, giving as 

examples C. sassii, a bisporic species which is 

amphithallic-bipolar, and the amphithallictetrapolar 

C. plagioporus. 

In C. cinereus, as in many other species, 

monokaryotic (rarely dikaryotic) mycelia form 

globose mucilaginous heads containing numerous 

oidia dispersed by insects. Plasmogamy 

preceding dikaryotization may be achieved 

by fusion between compatible monokaryotic 

hyphae or by fusion between a monokaryotic 

hypha and a compatible oidium. Monokaryons 

may also be dikaryotized following hyphal fusion 

with dikaryons (the Buller phenomenon; see 

pp. 508 and 566). 

Edibility of Coprinus basidiocarps 

Some species of Coprinus have basidiocarps which 

are edible when young. Coprinus comatus is an 

example. The fruit bodies of C. atramentarius are 

edible and harmless except if consumed with 

alcohol, which results in unpleasant symptoms 

of nausea and palpitations. The substance associated 

with this effect has been identified as 

coprine (Fig. 19.15a), and this is similar in its 

effects to the drug disulfuram (antabuse) which


539 

Fig19.15 Secondary metabolites in the euagarics clade.Coprine (a) produced by Coprinus atramentarius is toxic only when consumed with alcohol. a-Amanitin (b) and phalloidin (c) are the 

toxic principles of death caps, especially Amanita phalloides and A. virosa.The alkaloids ibotenic acid (d) and its derivative muscimol (e) are found in the fly agaric, Amanitamuscaria.Theyare 

hallucinogenic, probably mimicking neurotransmitters. Similarly, the indole alkaloids psilocybin (f) and its derivative psilocin (g), produced by Psilocybe spp., are hallucinogenic.Their 

structure is similar to the neurotransmitter serotonin.The bipyridyl toxin orellanine (h) is the cause of poisoning by Cortinarius orellanus.


is used in attempts to wean alcoholics from their 

addiction, although it is different chemically. 

Interference competition involving Coprinus 

Many species of Coprinus are coprophilous, typically 

with their basidiocarps appearing relatively 

late in the succession of fungi on dung (Dix & 

Webster, 1995). Certain species are known to 

suppress the fruiting of other fungi. A good 

example of this phenomenon is C. heptemerus, 

which inhibits the fruiting of many species in 

nature on rabbit dung and in culture. Its effect 

on the sensitive ascomycete Ascobolus crenulatus 

was tracked down to the moment when the 

hyphae of the two fungi make contact. Within 

minutes, the hyphal segment of Ascobolus 

touched by a hyphal tip of Coprinus is killed. 

There is a rapid loss of turgor, shown by the 

bulging of the septa of adjacent cells into the 

affected cell, which also loses the ability to 

undergo plasmolysis, whilst adjacent cells readily 

plasmolyse when bathed in hypertonic fluid. 

This form of competition has been termed 

hyphal interference or interference competition. 

It occurs in a range of genera of coprophilous 

basidiomycetes, but is not confined to this ecological 

group, having been demonstrated to be 

effective also in lignicolous fungi (Ikediugwu & 

Webster, 1970a,b; Ikediugwu et al., 1970). 

Cell damage is very similar to the effects seen 

when self- and non-self hyphae of the same 

species confront each other. An oxidative burst is 

stimulated and hydrogen peroxide accumulates 

in cells of the sensitive partner. This is interpreted 

as a defence reaction (Silar, 2005). 

19.4.3 Amanitaceae 

Amanita (c. 500 spp.) 

This is a large and important genus whose 

species form sheathing mycorrhiza with trees. 

Amanita muscaria (‘fly agaric’; Plate 9a) is often 

associated with birch (Betula) but also grows in 

mycorrhizal association with Abies, Pinus, Picea, 

Quercus and other hosts. As is well known, 

the basidiocarps of some species are poisonous, 

especially those of A. phalloides (death cap), 

A. virosa (destroying angel), A. pantherina (panther 

cap) and A. verna, whilst those of A. muscaria are 

more hallucinogenic than poisonous. There are 

also species whose basidiocarps are excellent to 

eat, most notably A. caesarea (Caesar’s mushroom; 

Plate 9b), which has been hunted enthusiastically 

in Southern European countries since Roman 

times. Emperor Claudius was an early connoisseur 

of A. caesarea and may have paid for his 

mycophagy with his life, probably falling victim 

to a poisoned mushroom dish manipulated by 

his wife Agrippina in AD 54 (Ramsbottom, 1953). 

Other edible species are A. rubescens (blusher), 

A. vaginata (grisette) and A. fulva (tawny grisette). 

In view of the possible confusion between edible 

and poisonous species, it is obviously best to 

avoid eating basidiocarps of any whose identity 

is uncertain. 

The characteristic features of Amanita include 

a white spore print and the presence of a volva, 

i.e. the torn remnants of a universal veil. The 

volva persists as a cup at the base of the stipe and 

broken volva fragments may also adhere to the 

cap, as seen as the white scales on the red caps of 

A. muscaria (Plate 9a). Most species also have 

a ring (annulus) on the stem, the remnant of the 

partial veil which protected the gills during fruit 

body development, but there is no ring in 

some species formerly classified in Amanitopsis 

(e.g. A. vaginata and A. fulva). 

Amanita poisoning 

Symptoms after ingestion of fruit bodies of 

A. phalloides follow a characteristic time course 

over a period of 7 days (Faulstich & Zilker, 1994). 

After a mushroom meal and symptom-free 

interval (day 1), there is a period of emesis 

(vomiting), abdominal cramps and diarrhoea 

(day 2), followed by a period of remission (day 

3) which is treacherous because it lures many 

patients into believing that they have overcome 

the poisoning. Meanwhile, severe liver damage is 

ongoing and symptoms resume with a vengeance 

with gastrointestinal bleeding (day 4), hepatic 

encephalopathy (brain damage, day 5), kidney 

failure (day 6) and death (day 7). 

Amanita poisoning is caused by two toxins, 

namely the amatoxin a-amanitin and the 

phallotoxin phalloidin (Bresinsky & Besl, 1990; 

Wieland & Faulstich, 1991; Chilton, 1994, 

Wieland, 1996). Both are bicyclic oligopeptides


541 

(see Figs. 19.15b,c). Of these, the more damaging 

is a-amanitin which binds to hepatocytes (liver 

cells). It inhibits a nuclear polymerase responsible 

for transcribing DNA into mRNA, resulting 

in reduced protein synthesis at the ribosomes 

and ultimately the death of cells. Phalloidin acts 

by binding to G-actin in liver cells and brings 

about an efflux of potassium ions and lysosomal 

enzymes, which leads to cell destruction 

(Chilton, 1994). 

The treatment of patients suffering from 

A. phalloides poisoning includes forced vomiting 

and other means of evacuating the stomach, 

orally applied activated charcoal to adsorb the 

toxins, external dialysis, infusion with silybinin, 

an extract from the milkthistle Silybum marianum 

which competes with a-amanitin for adsorption 

on to hepatocytes, and liver transplantation 

(Faulstich & Zilker, 1994). 

The effects of ingesting basidiocarps of 

A. muscaria are less severe, being mainly hallucinogenic. 

Characteristic symptoms are drowsiness, 

followed by deep sleep in which vivid 

dreams occur. Recovery is generally complete, 

with no permanent or prolonged ill after-effects. 

The two toxins chiefly involved are the alkaloids 

ibotenic acid and muscimol (Figs. 19.15d,e; 

Michelot & Melendez-Howell, 2003), and the 

former is readily converted to the latter in the 

gut. The molecular structures of ibotenic acid 

and muscimol closely resemble those of two 

neurotransmitters, glutamic acid and g-aminobutyric 

acid (GABA), respectively. Certain ethnic 

groups (e.g. in Siberia) have taken advantage of 

the hallucinogenic properties of A. muscaria to 

experience euphoria. Its use has extended to 

semi-religious practices in which shamans have 

induced themselves into trances in which they 

claim to have powers of revelation. Within 1 h of 

ingestion, ibotenic acid and muscimol are 

detectable in the urine of humans and also 

reindeer, and this may account for the tradition 

of drinking such urine in order to obtain a 

‘second-hand kick’. Such practices have now been 

discontinued in favour of alcoholic beverages, 

although A. muscaria is still occasionally taken as 

a recreational drug. 

The name ‘fly agaric’ refers to the supposed 

insecticidal properties of A. muscaria caps. When 

soaked in milk the caps attract flies, possibly 

brought there in response to an attractant, 

diolein. The flies ingest the Amanita flesh, but it 

is likely that they are intoxicated rather than 

killed. 

Amanita muscaria, easily recognized by its red 

cap adorned by white volva scales, is the bestknown 

of all macro-fungi, featuring in countless 

illustrations, folk tales, religious and semireligious 

ceremonies. It has been considered as 

the ‘tree of life’ or ‘tree of knowledge’ (Wasson, 

1968). Michelot and Melendez-Howell (2003) have 

given an account of its chemistry, biology, 

toxicology and ethnomycology. It is widely 

distributed in Europe, North America and Asia, 

and has probably been introduced into other 

parts of the world as a mycorrhizal partner on 

the roots of imported trees. Molecular phylogeny 

studies suggest that it should be separated into 

at least three groups, corresponding to Eurasian, 

Eurasian subalpine and North American regions 

(Oda et al., 2004). 

19.4.4 Pluteaceae 

Pluteus (c. 300 spp.) 

Species of Pluteus are saprotrophs, growing 

mainly on rotting wood. Pluteus cervinus is 

common, fruiting on deciduous tree stumps, 

logs, fallen branches and on sawdust heaps. 

Characteristic features are the free gills and 

pink spore print. On the surface of the hymenium, 

tapering, thick-walled cystidia crowned by 

pointed prongs protrude (Fig. 19.9d). Their function 

is unknown. 

The Pluteaceae are related to the 

Amanitaceae, and these two families appear as 

sister groups in phylogenetic analyses (Moncalvo 

et al., 2002). 

19.4.5 Pleurotaceae 

This family includes only two genera, Pleurotus 

and Hohenbuehelia (Thorn et al., 2000; Moncalvo 

et al., 2002). 

Pleurotus (20 spp.) 

Pleurotus spp. (oyster mushrooms) have laterally 

attached, lamellate basidiocarps. Most cause 

white rot decay of wood. The basidiocarps are


edible and several species, e.g. P. ostreatus and 

P. sajor-caju, are widely cultivated. Ligno-cellulosic 

waste products from a range of agricultural 

crops (e.g. wheat, rice, maize straw, banana 

leaves and dried water hyacinth) and industrial 

extraction processes can be used as substratum 

and cultivation can be practised in factories as 

well as on a smaller scale, e.g. in large cylindrical 

plastic bags in the context of a ‘cottage industry’ 

which can provide a valuable food supplement 

in developing countries (Poppe, 2000; Sánchez, 

2004). Spent substratum can be used for 

further fungal fermentations or as animal 

feed. A problem with the cultivation of Pleurotus 

spp. is the massive amount of basidiospores 

released from an early developmental stage 

onwards, causing ‘mushroom worker’s lung’. 

In order to overcome this problem, sporeless 

mutants have been bred. 

Pleurotus ostreatus, one of the best-known 

species, forms clusters of fan-shaped, bluishgrey 

basidiocarps at the base of deciduous tree 

stumps (Fig. 19.14e), especially beech (Fagus 

sylvatica). The gills are decurrent (running down 

the base of the stipe). Development in P. ostreatus 

is gymnocarpic and construction monomitic, but 

in some other species, e.g. P. tuberregium, skeletal 

hyphae are present. Some species develop 

thallic arthric anamorphs, e.g. P. cystidiosus in 

which the conidiophores are synnematal. In 

addition to being able to decompose wood, 

P. ostreatus and some related species are nematophagous 

(Barron & Thorn, 1987; Hibbett & Thorn, 

1994; Thorn et al., 2000; see p. 679), and the 

nematode prey represents an important supplement 

of nitrogen which is often the growthlimiting 

nutrient in woody substrata. The 

ability to parasitize nematodes has been used 

as a criterion to support the classification of 

P. tuberregium, a tropical species whose basidiocarps 

arise from large subterranean sclerotia 

(Hibbett & Thorn, 1994). 

Hohenbuehelia (50 spp.) 

This genus includes terrestrial lignicolous 

species. The basidiocarps frequently contain 

gelatinized tissue. All species are nematophagous. 

Nematodes are trapped on hourglassshaped 

(i.e. constricted) knobs covered with a 

toxic secretion, formed either directly on the 

clamped mycelium or at the tips of bent, tapering 

conidia assigned to the anamorph genus 

Nematoctonus (Barron, 1977; Barron & Dierkes, 

1977; see Fig. 25.7). 

19.4.6 Schizophyllaceae 

Although the unique pattern of fruit body and 

gill morphogenesis seemed to set Schizophyllum 

clearly apart from the Agaricales (Donk, 1964), 

the euagarics clade is where we must now 

place it on the basis of DNA analyses (Moncalvo 

et al., 2002). More confusingly still, the two fungi 

apparently closest to Schizophyllum are the 

polypore Fistulina and the gill-bearing genus 

Volvariella. 

Schizophyllum 

Schizophyllum commune has a worldwide distribution 

but is more common in warmer regions. 

It grows saprotrophically or parasitically on a 

wide range of woody substrata forming beigecoloured, 

fan-shaped, laterally attached fruit 

bodies with a furry upper surface. Since 1990 it 

has become common in Western Europe on 

plastic-wrapped hay silage bales from which 

clusters of basidiocarps burst out (Fig. 19.16a; 

Brady et al., 2005). Its spores are wind-borne. 

James and Vilgalys (2001), working in the 

Caribbean, trapped spores sedimenting onto 

the surface of Petri dishes containing a pregrown 

homokaryon culture. A successful trapping 

event was detected by the appearance of 

dikaryotic growth (with clamp connections). 

Deposition rates of 18 spores m 2 h 1 indicate 

that there is ample inoculum to ensure the 

colonization of most available substrates as soon 

as they are available for decay. 

The name Schizophyllum refers to the longitudinally 

‘split gills’ which are a xeromorphic 

adaptation (Figs. 19.16b and 19.17). In dry 

weather the ‘gills’ curve inwards so that the 

hymenial surface is protected by a series of 

adjoining folds. The curvature is due to the 

shrinkage of thinner-walled hyphal layers on 

drying. Since the remaining tissue of the gill is 

composed of thick-walled clamped hyphae which 

do not shrink so readily, inward curvature 

follows. Dried basidiocarps can be stored for


543 

Fig19.16 Basidiocarps in the euagarics clade (2). (a,b) Schizophyllum commune. (a) Cluster of fruit bodies growing through the plastic 

covering of a silage bale. (b) Basidiocarp as seen from below. (c) Volvariella speciosa. Note the presence of a volva and the absence 

of a ring. (d) Volvariella surrecta, a mycoparasite fruiting on basidiocarps of Clitocybe nebularis.(e)Panaeolus sphinctrinus. 

years and revive when placed in a moist 

environment. Water uptake occurs especially 

through the hairy upper surface, and the gills 

straighten out as the hymenium expands 

within 2 3 h. Spore discharge commences after 

3 4 h, and basidia are readily seen in hand 

sections, rendering S. commune a suitable object 

for microscopic examination if classes have to be 

held out of season. 

Schizophyllum commune is a ‘model’ fungus 

with a very extensive literature. It has been 

studied in detail by workers interested in its 

mating system, which is tetrapolar with complex 

A and B loci, each composed of two sub-loci, 

a and b. Several alleles have been identified at 

each sub-locus, creating over 20 000 mating 

type specificities (see p. 506). Other aspects of 

its biology which have been studied in depth


Fig19.17 Schizophyllum commune. (a) V.S. portion of 

basidiocarp showing the divided inrolled ‘gills’. 

(b) High-power drawing of part of the‘gill’ in the 

region of the split (arrowed). Note that the hyphae 

in this region are thin-walled in contrast to the 

thicker-walled hyphae making up the rest of the 

flesh. 

include genetics (Raper & Hoffman, 1974), 

nuclear migration (Snider, 1965) and morphogenesis 

(Wessels, 1993b, 1994). Dikaryotic mycelia 

fruit readily in culture. Monokaryotic fruiting 

may also occur (for references see Moore, 1998). 

The early stages of basidiocarp development have 

been studied by Raudaskoski and Viitanen (1982) 

and Raudaskoski and Vauras (1982). A short 

exposure to light and good aeration are necessary 

to induce sporulation; elevated CO 2 concentrations 

are inhibitory. Under dark conditions, 

mycelial growth is depressed beneath the surface 

of the medium under a layer of slimy material. 

Within 3 h after transfer of 3 day old dark-grown 

cultures to continuous light, there is abundant 

growth of aerial hyphae at the margin of the 

culture. After 9 h the emergent aerial hyphae 

become aggregated into a horseshoe-shaped 

structure which is the ventral surface of the 

fruit body. After 15 h basidial initials form the 

beginnings of the hymenium which develops 

over the entire lower surface of the basidiocarp. 

The outside of the fruit body consists of vertical 

and horizontal hyphal strands, and its outermost 

layer is formed by parallel backward growth of 

numerous hyphal tips towards the developing 

hymenium. By more rapid growth on one side, 

the fruit body may become fan-shaped. The split 

gills arise by marginal proliferation, and their 

number is increased by downgrowths from the


545 

flesh of the fruit body. The cytology of basidial 

development shows no unusual features. 

Surface properties, especially the wettability 

of hyphal surfaces, play an important role in 

mycelial growth and fruit body development in 

Schizophyllum. Aerial hyphae, including those 

making up the basidiocarp, are strongly hydrophobic 

(i.e. non-wettable) because they are 

covered by parallel rodlets of special proteins, 

hydrophobins, which were first discovered 

during research with S. commune. Hydrophobins 

are amphipathic, i.e. they arrange themselves 

into sheets with one wettable (hydrophilic) 

face and a non-wettable (hydrophobic) face. 

At an air water interface or over the surface 

of a hypha, the hydrophilic face attaches to the 

meniscus or to the hyphal surface whilst the 

hydrophobic layer faces outwards, giving it its 

non-wettable properties (Wessels, 1997, 2000). 

Schizophyllum commune has at least four hydrophobin 

genes. The gene SC3 is active in both 

monokaryons and dikaryons, whereas SC1, SC4 

and SC6 are active in dikaryons only. When 

grown experimentally in liquid culture, the 

hyphae of S. commune secrete the monomers of 

SC3p which accumulate at the air liquid interface 

and also lower the surface tension of 

the culture liquid. This enables individual 

hyphae to penetrate the interface, and to grow 

into the air, simultaneously becoming coated 

with hydrophobin. The function of the product 

of the SC4 gene, the hydrophobin SC4p, has been 

clarified. It covers the surface of the hyphae 

lining the numerous air channels which traverse 

the basidiocarp, preventing them from being 

clogged by water and thus permitting gas 

exchange to continue during respiration. 

Volvariella 

There are about 50 species of Volvariella, and their 

taxonomic position is still unsettled but may 

be close to Schizophyllum (Moncalvo et al., 2002). 

The genus includes several species cultivated 

for their edible basidiocarps. The best known is 

V. volvacea, the paddy straw mushroom, widely 

grown in Asia on rice straw, cotton waste and 

other cellulose-rich agricultural waste products. 

In terms of world production it is one of 

the most important edible mushrooms. It is a 

warm-temperature fungus which can grow vegetatively 

at 32 34°C, with an optimum temperature 

for fruiting of 28 30°C. Under favourable 

conditions, the period between inoculation and 

harvest of fruit bodies is 8 10 d, the shortest in 

any cultivated fungus (Chang & Miles, 2004). 

The basidiocarps of Volvariella spp. are enclosed 

by a universal veil which persists as a prominent 

cup-like volva (Fig. 19.16c). There is no ring. 

The gills are free and the spore print is pink. 

Volvariella volvacea has an unusual life cycle 

(Chang & Yau, 1971; Chiu, 1993). It is homothallic 

and its mycelium is haploid, being made up of 

multinucleate segments. There are no clamp 

connections and it is reported that nuclei can 

pass through the transverse septa which separate 

adjacent hyphal segments. Brown, thick-walled, 

multinucleate chlamydospores are borne on 

specialized branches of the aerial mycelium. 

They serve as asexual propagules under adverse 

conditions, germinating by hyphal growth. 

Young basidia contain two haploid nuclei 

which fuse to form a diploid nucleus. Meiosis 

gives rise to four haploid nuclei, one entering 

each of the four basidiospores. Basidiospores are 

therefore normally uninucleate (occasionally 

binucleate). 

Volvariella bombycina, the silver silk straw 

mushroom, has a similar life cycle. It fruits 

readily in laboratory culture and its basidiocarp 

development has been studied by Chiu and 

Moore (1990b). Development is normally hemiangiocarpic, 

but angiocarpic (i.e. with the 

hymenium enclosed until a late stage) and 

gymnocarpic (hymenium exposed) development 

may also occur. Hemi-angiocarpic development 

has been arbitrarily divided into five 

phases: the bulb, button, egg, elongation and 

mature stages. During the button stage, a 

schizogenous cavity is formed, enclosed by the 

universal veil and basal bulb. The hymenophore 

develops within this cavity. Elongated cylindrical 

hyphae of uniform size develop on ridges, 

initiating the formation of the gills. These 

ridges do not extend to the future stipe, so the 

gills remain free. During the late egg stage, i.e. 

before rupture of the universal veil, local 

proliferation of the gills occurs, and at the 

site of proliferation the hymenophore is folded


in a sinuous or labyrinth-like pattern in contrast 

with the regular folding seen in the mature 

stage. During the elongation stage, expansion of 

the stipe and cap causes the universal veil to 

rupture. In addition to the primary gills which 

run along the entire radius of the cap, secondary 

or tertiary gills, extending for shorter distances, 

develop either by successive bifurcation of an 

older gill near its inner, free edge or by the 

formation of a new hymenial layer at or near the 

root of an old gill. The hymenium includes 

basidia and larger, skittle-shaped facial cystidia 

which may extend across to the opposite gill 

face. Droplets observed on the cystidia suggest 

that the cystidia may have a secretory role. 

Volvariella surrecta is mycoparasitic. Its 

basidiocarps grow on the caps of other agarics 

such as Clitocybe nebularis (Fig. 19.16d). 

19.4.7 Bolbitiaceae 

Panaeolus (25 spp.) 

Most members are coprophilous but some grow 

in pastures. Common examples are P. semi-ovatus 

(sometimes classified in a separate genus 

Anellaria) and P. sphinctrinus (Fig. 19.16e). Both 

species fruit on cattle dung. The gills are 

wedge-shaped in section and aequi-hymeniiferous. 

The spores are black. Panaeolus spp. are 

commonly called mottle-gills, and this refers to 

the fact that the basidia ripen in patches, not 

uniformly, so that areas in which the spores 

are ripe appear darker than those in which 

the spores are still immature (Buller, 1922). 

Basidiocarps of some Panaeolus spp. contain 

psilocybin and are hallucinogenic (see p. 553). 

19.4.8 Hygrophoraceae 

Members of the Hygrophoraceae are sometimes 

included in Tricholomataceae but have been 

resolved in recent phylogenetic studies as a 

separate family (Moncalvo et al., 2002). 

Representative genera are Hygrophorus (100 spp.) 

and Hygrocybe (150 spp.), also known as waxcaps 

because of the texture of their basidiocarps. 

Some species grow in woodland and may form 

ectomycorrhiza with trees, e.g. Hygrophorus 

eburneus from beech woods (Fagus sylvatica). 

However, the characteristic habitats of many 

waxcaps are impoverished, non-fertilized 

pastures. Their basidiocarps are often slimy or 

gelatinous and brightly coloured, e.g. the bloodred 

Hygrocybe coccinea (scarlet waxcap; Plate 9c) or 

the greenish-yellow Hygrocybe psittacina (parrot 

waxcap). The basidiocarps of Hygrocybe conica 

(blackening waxcap) turn black when bruised. 

19.4.9 Marasmiaceae 

Although the Marasmiaceae, like most families 

in the euagarics clade, may well become substantially 

rearranged in the future, the work by 

Moncalvo et al. (2000) lends some support for 

the grouping together of key genera such as 

Lentinula, Omphalotus, Marasmius, Crinipellis, 

Flammulina and Strobilurus. Most fungi formerly 

known as Collybia are now also accommodated 

in the Marasmiaceae, assigned to the genera 

Gymnopus and Rhodocollybia. Several members 

of the Marasmiaceae are known to produce 

antifungal substances in pure culture, and one 

group, the strobilurins, has been developed into 

fungicides currently enjoying worldwide application 

(Sauter et al., 1999; see p. 410). Some 

strobilurins and the related oudemansins have 

been shown to be secreted by their producers 

into colonized wood at concentrations which are 

toxic to potential competitors, thereby indicating 

their ecophysiological function as a means of 

resource capture and defence (Engler et al., 1998). 

Whereas most members of the Marasmiaceae are 

saprotrophs on wood and humus, some are 

necrotrophic or, rarely, biotrophic pathogens of 

trees. 

Marasmius (500 spp.) 

Species of Marasmius often have rather tough, 

leathery basidiocarps which shrivel on drying 

but rapidly revive on wetting. The best known 

species is M. oreades, the fairy ring fungus whose 

basidiocarps are edible and may be dried 

(Fig. 19.18a). The mycelium of the fungus 

grows outwards from a central point and, as 

the mycelial front progresses radially, the 

older, trailing mycelium dies. This results in a 

ring of active mycelium, visible as a circle of 

green grass in lawns and pastures (Fig. 19.18b). 

Measurements of the radial extension of growing


547 

Fig19.18 Basidiocarps in the euagarics clade (3): Marasmiaceae. (a) Marasmius oreades.(b)TwofairyringsofM. oreades approaching 

each other on a lawn.The centres of the rings are to the top and bottom of the picture. (c) Oudemansiella radicata which grows 

attached to tree stumps andburied wood andhas a long, tapering, undergroundbase to the stem (pseudorhiza). (d) Armillaria mellea. 

(e) Flower cushion of cocoa tree infected by the monokaryotic mycelium of Crinipellis perniciosa.Bothhealthyflowersandswollen 

infected shoots are visible. (f) Basidiocarps of C. perniciosa on a dead cocoa twig. (e) and (f) from Griffith et al.(2003),New Zealand 

Journal of Botany, by copyright permission of the Royal Society of New Zealand; original images kindly provided by R.N. Birch, J.N. 

Hedger and G.W.Griffith. 

rings show that they can extend outwards at a 

rate of about 1 3.5 cm per annum, and measurements 

of their diameter indicate that some, 

in permanent pastures, may be centuries old. 

The mycelium is intermingled with the grass 

roots usually near the soil surface at a depth of 

8 10 cm, but it may extend to a depth of 30 cm, 

depending on soil type. Closer inspection shows 

that there are three concentric rings at the soil 

surface: (1) an outer zone in which the grass is 

greener and taller than outside, and in which the 

fungus fruits; (2) a middle zone where the 

grass is dead and the ground bare, especially in 

dry seasons; and (3) an inner zone of stimulated


growth often occupied by other plants which 

have colonized the previously bare ground. 

The stimulated growth of grass in the outer 

ring zone is associated with more rapid decomposition 

of soil organic matter and the concomitant 

release of nutrients. The amount of soil 

organic carbon may be lowered by about 50% as 

compared with a non-invaded turf. The death of 

grass in the bare central ring zone is probably 

due to a combination of factors, including 

parasitic attack by the fungus, drought resulting 

from impeded water percolation, and toxins of 

fungal origin (e.g. cyanide, HCN) which damage 

the grass root tips (see Dix & Webster, 1995). 

Other common species of Marasmius include 

M. androsaceus with thin, black, horsehair-like 

rhizomorphs and small basidiocarps arising 

from pine needles, dead heather, etc., and 

M. ramealis which forms clusters of basidiocarps 

on dead twigs and herbaceous stems. Marasmius 

rotula grows in similar situations. Its gills are not 

attached directly to the stem but to a cylindrical 

collar. 

Oudemansiella (10 spp.) 

This is a genus containing temperate and 

tropical species. Some species, e.g. O. mucida 

(porcelain fungus), have a membranous ring 

on the stem, but in others, e.g. O. radicata, a 

ring is lacking. Oudemansiella mucida is parasitic 

on beech (Fagus sylvatica) and forms white 

basidiocarps with slimy caps on the branches of 

infected trees. Oudemansiella radicata is so called 

because the base of the stipe is prolonged into a 

tapering pseudorhiza which connects with 

buried woody branches extending for several 

cm beneath ground level (Fig. 19.18c; see also 

Buller, 1931). 

Flammulina (10 spp.) 

The best known species is F. velutipes, the velvet 

shank or winter fungus, which grows on deciduous 

tree stumps and branches and fruits in 

winter, forming golden yellow basidiocarps 

singly or in clusters (Plate 9d). Basidiocarps 

can survive being frozen and soon continue to 

discharge spores on thawing. In the past, most 

collections of Flammulina were named F. velutipes, 

but it is now believed that several taxa had 

been included under this name (see Hughes et al., 

1999). The Latin and trivial names refer to the 

brown velvety hairs at the base of the stipe. 

The distribution of the fungus is throughout 

temperate regions of the Northern Hemisphere. 

An anamorph is produced as chains of dry 

arthroconidia which have already been described 

(see Fig. 18.14a). The basidiocarps of F. velutipes 

are edible and the fungus is cultivated for food in 

Japan as enoki-take (Chang & Miles, 2004). Spawn 

of the fungus develops on sawdust in plastic bags 

or on logs incubated at 21 24°C for 14 18 d and 

then subjected to a cold shock (4 10°C) for 3 5d 

to induce fruiting, which follows within 5 8dat 

a temperature of 10 16°C. Light is required for 

fruiting. 

Graviperception and gravitropism 

in Flammulina 

When normally erect basidiocarps of F. velutipes 

are displaced into a horizontal position, they 

respond within about 3 h by bending upwards to 

restore their original orientation (Fig. 19.19). 

Experimental studies, some conducted in orbit 

in a space laboratory, have helped elucidate the 

mechanism (Moore et al., 1996; Kern et al., 1998; 

Kern, 1999). Bending occurs by curvature of 

the stipe in a transitional zone (2 3 mm long) 

immediately beneath the cap, where the hyphae 

making up the stipe and cap intertwine. 

Although basidiocarps which develop on Earth 

are erect, those formed in space were randomly 

orientated, growing out in all directions from 

their substrate. Despite this, normal caps, basidia 

and spores were produced. This shows that 

gravitational force is needed for stipe orientation 

but not for other aspects of fruit body development. 

Two responses operate to control fruit 

body development, namely negative hydrotropism 

causing basidiocarps to grow away from 

their moist substrate into drier air, and negative 

gravitropism. Bending is caused by greater 

enlargement of the cells making up the lower 

flank of the stipe as compared with those of the 

upper flank. The cells of the lower flank are more 

vacuolate than those of the upper. In green 

plants with gravitropic responses, graviperception 

is correlated with the sedimentation of 

denser cytoplasmic particles, statoliths, which


549 

Fig19.19 Gravitropism of basidiocarps in 

Flammulina velutipes growing on a branch of 

gorse (Ulex europaeus).The branch was turned 

clockwise by 90° 4 h earlier, and the upper 

stipe regions are undergoing curvature 

(arrows) to bring the pilei back into the 

horizontal position. 

congregate and are more abundant in the lower 

sides of cells in horizontally displaced organs. In 

Flammulina, Monzer (1996) considered that only 

the nuclei, with a density of 1.22 g cm 3 , were 

valid candidates for gravity-related sedimentation 

to enable them to function as statoliths. 

In the transition zone there may be up to 10 

nuclei per hyphal segment. These nuclei are 

enmeshed in filaments of F-actin, and Monzer 

(1995) has suggested that tension of the actin 

filaments associated with sedimentation of 

nuclei is transmitted to the plasma membrane 

and provides the trigger to initiate cellular 

changes involved in the gravitational response. 

Evidence supporting the involvement of actin 

filaments is that the gravitropic response 

is affected by the actin-depolymerizing drug 

cytochalasin D, but not by treatment with 

microtubule-inhibiting drugs. 

Within 30 min of displacement of a basidiocarp 

from a vertical to a horizontal position, 

differences may be noted between the upper and 

lower flank cells. Microvesicles, most likely 

derived from the endoplasmic reticulum and 

Golgi cisternae, are more abundant in the lower 

flank cells. They fuse with the vacuoles, thereby 

contributing to the volume increase and turgordriven 

enlargement of these cells. Vesicles 

containing wall precursor materials and 

enzymes also develop, providing for enlargement 

and stretching of the walls of lower flank cells. 

There are some 1.2 million hyphae present in the 

cross-section of a Flammulina stipe. They remain 

strictly parallel to each other but do not show 

anastomosis or direct contact with each other. 

It is believed that each separate hypha in the 

transition zone responds to the gravitational 

stimulus. Possibly a growth factor which inhibits 

the growth of upper flank cells is involved, but 

no such substance has yet been demonstrated or 

identified. 

Detailed studies of gravitropism have also 

been made using stipes of the coprophilous inkcap 

Coprinus cinereus (Kher et al., 1992). Although 

there are similarities to Flammulina, there are 

also differences. For example, the response 

time of Coprinus is much shorter than that 

of Flammulina, and curvature extends along the 

entire stipe rather than being restricted to 

the transition zone. These differences reflect 

the varied growth conditions of the two fungi 

(Moore et al., 1996). Flammulina velutipes is 

lignicolous and its basidiocarps are relatively 

long-lived whilst C. cinereus is coprophilous and 

its basidiocarps are evanescent. 

Armillaria (42 spp.) 

Most species are root pathogens, especially of 

woody plants, and there is an extensive literature 

on their biology and pathogenicity (see Shaw & 

Kile, 1991; Holliday, 1998; Fox, 2000). In the past, 

most collections were identified as A. mellea 

(the ‘honey fungus’), but this is now regarded 

as an aggregate of about 5 10 species, A. mellea


agg. (Fig. 19.18d). Pegler (2000) has given a key to 

the European species. Basidiocarps may occur 

singly, but often grow in clumps of dozens or 

even hundreds on the stumps of dead trees. The 

fruit bodies are reported to cause gastro-intestinal 

upsets if eaten raw, but are edible if they are 

cooked and the cooking water is discarded. Most 

species are annulate (i.e. with a ring on the stem), 

but in A. tabescens a ring is lacking. Serious 

pathogens include A. luteobubalina and A. mellea 

sensu stricto on a very broad range of hosts, and 

A. ostoyae on conifers (Larix, Pinus, Pseudotsuga, 

Picea) and birch (Betula). Armillaria cepistipes and 

A. lutea are mainly saprotrophic. 

In infected trees, sheets of white mycelium 

grow between the wood and bark, destroying the 

phloem and cambium. In plantations, infections 

arise when air-borne basidiospores colonize the 

cut ends of thinning stumps. Spread of infections 

is by root-to-root contact from diseased to 

healthy trees and by means of bootlace-like 

rhizomorphs (see and Fig. 18.13b). In this way 

adjacent trees in plantations become infected, 

resulting in group dying. A considerable area of 

forest may be affected by Armillaria, with an 

individual clone of A. bulbosa shown to extend 

over several hectares (Smith et al., 1992). The 

mycelium of Armillaria continues to grow saprotrophically 

after the death of an infected tree, 

and the zone of infected wood within the tree 

may be surrounded by dark, melanized, pseudosclerotial 

plates. Rhizomorphs may survive there 

for up to 40 years and continue to support 

fruiting over several years. Infected wood is 

often bioluminescent. Survival of the mycelium 

and its protection by pseudosclerotial plates 

makes the control of diseases caused by 

Armillaria difficult and expensive, although 

fungicidal treatment has been attempted (West, 

2000). Alternative biological control measures 

using fungal antagonists such as Trichoderma spp. 

also hold promise. Integrated control based on a 

combination of fungicidal treatments and biological 

antagonists (fungi and nematodes) has 

had a limited measure of success (Raziq, 2000). 

Although A. mellea agg. is generally regarded 

as a pathogen, it forms endotrophic mycorrhiza 

with several genera of chlorophyllous 

orchids in the tropics, and also with the 

colourless (achlorophyllous) orchid Gastrodia 

elata. As in other orchids (see p. 597) the seedlings 

of Gastrodia only become established following 

infection by the haploid basidiomycete 

Rhizoctonia. However, the Rhizoctonia infection is 

only a primary phase of limited duration, and 

secondary infection by Armillaria is essential 

for successful further growth of the orchid 

protocorm. The Armillaria mycelium within the 

protocorm is connected to mycelium growing 

parasitically on adjacent trees (Smith & Read, 

1997). 

Crinipellis (75 spp.) 

Crinipellis perniciosa is the cause of a severe 

witches’ broom disease of cocoa (Theobroma 

cacao) especially in South America (Purdy & 

Schmidt, 1996; Griffith et al., 2003). Young 

shoots are induced to proliferate and become 

swollen (Fig. 19.18e). There is considerable 

reduction in the yield of cocoa pods, and crop 

losses of up to 80% have been reported. Crinipellis 

perniciosa is hemibiotrophic; its monokaryotic 

mycelium is biotrophic but its dikaryotic mycelium 

is necrotrophic. It forms groups of small 

(pileus diameter: 5 15 mm) crimson to pink 

basidiocarps on dead cocoa twigs (Fig. 19.18f). 

Infection is by air-borne basidiospores which 

germinate under conditions of high humidity 

(e.g. dew) on meristematic tissues such as 

flowering cushions, young leaves and shoots. 

Germ tubes penetrating stomata or wounded 

tissue establish a monokaryotic mycelium which 

pervades the proliferating hypertrophied shoots. 

Infection is not systemic. The monokaryotic 

phase does not grow in agar culture, but 

growth can be induced in cocoa or potato 

callus tissue cultures. There are several biotypes 

of C. perniciosa infecting different host plants. 

The C (cacao) biotype is primarily homothallic. 

Infected host twigs and pods eventually become 

necrotic and death of host tissues is associated 

with a change in the nuclear condition of the 

mycelium to the dikaryotic state. Basidiocarps 

develop on the dikaryon in the dead twigs. The 

dikaryotic mycelium can be grown in culture, 

and fruit body development is also possible on 

agar or on a bran vermiculite medium covered 

with a peat-based casing soil.


551 

Control of witches’ broom disease is difficult 

but crop losses can be reduced by sanitation, 

i.e. the regular removal of brooms and diseased 

pods. Other measures involve the use of 

Trichoderma isolates as agents of biological 

control. Some are antagonistic, but T. stromaticum 

is mycoparasitic on mycelium and basidiocarps 

(Samuels et al., 2000; Sanogo et al., 2002). 

Systemic fungicides are also used. Further, 

there is an ongoing search for hosts resistant to 

the pathogen which could be used for breeding 

purposes. The origin of the cocoa pathogen is 

thought to be native (wild) species of Theobroma 

growing in the forests, but other C. perniciosa 

strains attack members of the Solanaceae, Bixa 

spp., lianas (climbers) and woody debris on the 

forest floor. 

A closely related fungus, C. roreri 

(Myceliophthora roreri), causes the damaging 

frosty pod rot disease of cacao. Infected pods 

are covered by white powdery masses of winddispersed 

spores, originally regarded as conidia. 

These spores are borne on a dikaryotic mycelium 

which can be grown in culture. Dikaryotic 

hyphae swell and branch to form sporophore 

initials. The nuclei in the dikaryon fuse and septa 

are laid down, resulting in chains of diploid cells 

which have been interpreted as the equivalent of 

probasidia. The diploid cells develop thick walls 

to become spores and their nuclei undergo 

meiosis, but division may be arrested at a 

binucleate state (after the first meiotic division) 

or proceed to the formation of nuclear tetrads. 

On germination, there are indications that a 

four-celled metabasidium may be produced, with 

sterigmata which function as infective hyphae. 

As in C. perniciosa, this monokaryophase is biotrophic 

and can only be grown on living cocoa 

tissue. The life cycle of C. roreri is thus considerably 

modified, and a recognizable mushroomlike 

basidiocarp stage probably does not occur 

(Evans et al., 2002, 2003; Griffith et al., 2003). 

19.4.10 Mycenaceae 

Mycena (about 150 spp.) 

This is a large polyphyletic genus of fungi, with 

most species clustering in phylogenetic analyses 

around the type-species, Mycena galericulata. This 

group has been called Mycenaceae by Moncalvo 

et al. (2002). Mycena spp. produce rather small, 

delicate basidiocarps which have long slender 

stipes and conical or bell-shaped caps. Fruit 

bodies may emerge singly or in clusters from 

wood, leaf litter and other debris such as twigs, 

pine cones and bracken petioles in woodland and 

pastures. Some species exude latex when the 

stipe is broken, e.g. M. sanguinolenta with blood 

red latex and M. galopus which produces a 

milk white exudate. Much is known about the 

autecology of M. galopus, which has a perennial 

mycelium when growing in coniferous litter and 

also fruits on a wide range of twiggy debris but 

does not grow in bulky wood masses, possibly 

because of restricted aeration there (Frankland, 

1984; Dix & Webster, 1995). It is capable of 

growing on most of the constituents of leaf litter 

and its ability to break down lignin and cellulose 

enables it to function as a typical white-rot decay 

fungus. Mycena galopus is a key decomposer of 

oak leaves and, within two years of leaf fall, 

its mycelium may be present on 80% of fallen 

leaves. This species is regarded as a secondary 

colonizer, growing on plant material which is 

already well-colonized by other fungi. In this 

context, it is worth mentioning that many 

Mycena spp. produce antifungal metabolites, 

including strobilurins, and these may aid in the 

displacement of other wood-rotting fungi. 

Despite this, moribund fruit bodies of various 

Mycena spp., including strobilurin producers, 

may be parasitized by the zygomycete Spinellus 

fusiger (Plate 3e). 

Basidiocarp development in M. stylobates 

growing on beech leaves has been described 

and well-illustrated by Walther et al. (2001). 

An irregular arrangement of interwoven 

hyphae within the leaf bursts through to form 

an ovoid structure at the surface, composed 

mainly of vertically arranged hyphae. Cells at the 

margin increase in diameter and enclose the 

early stages of the primordium entirely. 

Separation of this large-celled wrapping tissue 

from internal hyphae results in the formation of 

a ring-like groove at the base of the primordium 

and a layer of protective hyphae covering a 

central bulb. The cells of the outer layer of 

vertically arranged hyphae increase in diameter


to form the stipe. Simultaneously, hyphae at the 

apex of the bulb form horizontal outgrowths, 

giving rise to the pileus. The development of the 

hymenophore starts with the formation of small 

alveoli on the lower surface of the pileus, near its 

margin. 

19.4.11 Tricholomataceae 

This family has not yet been clearly separated 

from related groups in recent phylogenetic 

analyses. Genera currently placed here include 

Tricholoma, Lepista, Clitocybe, Termitomyces and 

Lyophyllum. A few Collybia spp. (C. tuberosa, 

C. cirrhata, C. cookei) are also grouped here, 

whereas most of the genus Collybia sensu lato 

seems to belong to the Marasmiaceae (see p. 546). 

It is probable that many other genera included 

in the Tricholomataceae are also polyphyletic 

(Moncalvo et al., 2000, 2002). 

Clitocybe 

This is a large genus with about 60 species in 

Britain. The basidiocarps are funnel-shaped with 

decurrent gills (Fig. 19.20a) and can be large, up 

to 20 cm in diameter in C. geotropa. Clitocybe 

nebularis may form fairy rings many metres in 

diameter in deciduous and coniferous woods. 

The fruit bodies of several species are edible and 

those of C. odora have a fragrant, aniseed-like 

flavour. Clitocybe spp. are non-mycorrhizal. 

Lepista (50 spp.) 

The basidiocarps of Lepista are generally known 

as ‘blewits’ and include several good edible 

species such as L. nuda and L. saeva. The gills 

are attached to the stem in a sinuate manner, 

i.e. with an S-shaped point of attachment 

(see Fig. 19.8). Lepista is distinguished from 

Tricholoma in having a pale pink spore print 

(white in Tricholoma). Lepista spp. are nonmycorrhizal, 

growing mainly among humus 

and leaf litter. 

Tricholoma (200 spp.) 

This genus of mostly ectomycorrhizal species is 

mainly North-temperate in distribution in woodlands 

and pastures. The basidiocarps have sinuate 

gills and produce a white spore-print. 

The most important edible species is the matsutake 

mushroom, T. matsutake, which is highly 

valued, especially in the Far East. Unfortunately, 

basidiocarps still have to be collected from 

woodlands because all attempts at cultivating it 

for commercial production have failed (see Wang 

& Hall, 2004). However, Guerin-Languette et al. 

(2005) have succeeded in infecting mature pine 

roots with T. matsutake in the laboratory, and 

this may have laid the foundations for an 

inoculation protocol for forest trees in future. 

An edible European species is St George’s mushroom 

(T. gambosum or Calocybe gambosa) which 

grows in pastures, often under trees, and fruits 

in spring around St George’s Day (23 April). 

Tricholoma sulphureum is a common woodland 

species whose basidiocarps are readily recognized 

by their sulphureous colour and unpleasant 

smell. 

19.4.12 Laccaria 

The relatively small basidiocarps of Laccaria 

(25 spp.) are known as ‘deceivers’ because of the 

change of colour intensity of the cap surface 

between wet (intensely coloured) and dry (pale) 

conditions. Laccaria spp. are important ectomycorrhizal 

associates of forest trees and are used 

for artificial inoculation of trees to be planted 

out into challenging situations. They are usually 

among the early-stage colonizers of tree 

roots, being replaced by others as the succession 

proceeds (Last et al., 1983, 1987; Kropp & Mueller, 

1999). Among the best known species are 

L. laccata, growing with Pinus and a range of 

other hosts, L. bicolor which grows with Abies, 

Pseudotsuga, Pinus and Picea, and L. amethystina 

(amethyst deceiver), an associate of oak (Quercus) 

and beech (Fagus). All species of Laccaria have 

edible basidiocarps. The relationships of Laccaria 

are poorly resolved, and family assignment is 

uncertain at present. 

Bertaux et al. (2003) have reported the 

presence of a bacterium (Paenibacillus sp.) within 

the hyphae of L. bicolor. Bacterial cells were 

visualized by fluorescence microscopy, and 

the escape of these bacteria in liquid culture 

conditions was shown to account for the sporadic 

bacterial ‘contamination’ of fermenter


553 

Fig19.20 Basidiocarps in the euagarics clade (4). (a) Clitocybe nebularis.(b)Stropharia semiglobata.(c)Psilocybe semilanceata,the 

magic mushroom. (d) Hypholoma sublateritium.(e)Cortinarius purpureus. Note the fibrillose cortina on the stipe of the young 

specimens (centre and right). 

cultures. Intrahyphal bacteria appear to be 

rare in higher fungi, but they have been reported 

in certain Zygomycota, notably Geosiphon (p. 221) 

and Rhizopus (p. 184). 

19.4.13 Strophariaceae 

Against all expectations, species included among 

the Strophariaceae do seem to group together, 

albeit with weak statistical support, in recent


phylogenetic analyses (Moncalvo et al., 2002). 

Two groups of Psilocybe fall outside the core of 

the Strophariaceae, with the hallucinogenic 

species clustering separately from other 

Psilocybe spp. 

Stropharia 

Species of Stropharia fruit on soil, dung or wood. 

The developing gills are protected by a membranous 

veil which may persist as a solid annulus or 

a loose weft of fibrils. The spores are purplishbrown 

to black. Stropharia semiglobata, extremely 

common on several kinds of herbivore dung, has 

a viscid, yellowish, hemispherical cap and a ring 

of dark fibrils on the stem (Fig. 19.20b). Stropharia 

aeruginosa (verdigris agaric) has an attractive 

bluish-green viscid cap flecked with white 

scales and grows in woodland while S. aurantiaca, 

with bright orange caps, fruits on sawdust and 

on wood chippings. 

Psilocybe (c. 300 spp.) 

The basidiocarps of Psilocybe (Fig. 19.20c) are 

generally small and campanulate (bell-shaped), 

with attached gills and purple-brown spores. 

Some species have a fibrillose veil whilst others 

have a distinct annulus. The genus includes 

several species whose basidiocarps are hallucinogenic 

and are used as recreational drugs. Psilocybe 

mexicana (sacred mushroom, teonanácatl) has 

been used for centuries by Mexican Indians in 

religious ceremonies (Heim & Wasson, 1958), 

and P. cubensis (golden top or giggle mushroom) 

is cultivated to obtain hallucinogenic basidiocarps. 

In Europe, P. semilanceata (magic mushroom, 

liberty cap) fruits in late summer and 

autumn on the ground in sheep pasture and 

well-manured grassland. It is saprotrophic, its 

mycelium being associated with decaying grass 

roots. Fruit bodies are picked and dried, 

although their sale is illegal in many European 

countries. The main hallucinogens of Psilocybe 

are the alkaloids psilocybin and psilocin 

(Figs. 19.15f,g), which are N-methylated tryptamines. 

They operate on serotonergic systems of 

the brain and are similar in their effects to 

mescaline and LSD (Lincoff & Mitchel, 1977; 

Bresinsky & Besl, 1990). Psilocin is less stable 

than psilocybin, and when oxidized shows a blue 

discoloration. This may be the reason why 

the flesh of many of the hallucinogenic Psilocybe 

spp. turns blue when bruised or broken. 

A readable account of the discovery of LSD 

and the elucidation of hallucinogenic principles 

in magic mushrooms has been written by 

the discoverer of both, Albert Hofmann. English 

translations of the original German text 

(Hofmann, 1979) are readily available. 

Hypholoma 

The best-known species are H. fasciculare (sulphur 

tuft) and H. sublateritium (Fig. 19.20d), both 

growing on wood. They are sometimes classified 

in the genus Naematoloma. Hypholoma fasciculare 

is very common, forming clusters of yellow 

basidiocarps on many kinds of deciduous and 

coniferous tree stumps, whilst H. sublateritium 

fruits on deciduous tree stumps and has brickred 

caps. There is a cottony veil on the stem and 

the spores are purplish-brown. Hypholoma fasciculare 

basidiocarps are inedible and bitter to 

taste. They cause gastro-intestinal irritation and 

there are occasional reports of death following 

ingestion (Lincoff & Mitchel, 1977). Hypholoma 

fasciculare is highly competitive against other 

wood-rotting fungi. It is capable of extending 

from a woody food base through the soil by 

means of mycelial cords in search of further 

woody substrata. It can also utilize leaf litter. As 

a wood-decaying fungus its strategy is secondary 

resource capture, i.e. the displacement of 

other fungi which have earlier colonized wood, 

killing their mycelia. It therefore tends to fruit 

late in succession (Rayner & Boddy, 1988; Boddy, 

1993). 

Pholiota (c. 150 spp.) 

Most species of Pholiota grow on wood. Pholiota 

squarrosa is associated with soft, pale brown-rot 

(butt rot) of living trees of ash (Fraxinus), beech 

(Fagus) and poplar (Populus). Dense clusters of 

scaly brown basidiocarps are formed at the base 

of the trunk (Plate 9e). There is a prominent ring 

on the stem and the spores are smooth and 

rusty brown. It is best to avoid eating the 

basidiocarps of Pholiota spp. because serious 

ill-effects may follow, especially if they are 

consumed with alcohol. However, the nameko

BOLETOID CLADE 

555 

fungus (P. nameko) is cultivated commercially on 

sawdust-based substrate in Far Eastern countries 

for its edible basidiocarps (Chang & Miles, 2004). 

It is a moisture-loving fungus, growing in nature 

on dead trunks and stumps of deciduous 

trees at high altitudes in Japan and Taiwan. Its 

mating system is bipolar. Arthroconida develop 

on monokaryotic and on dikaryotic mycelia. 

Similarly, basidiocarps develop on monokaryons 

and on dikaryons. 

19.4.14 Cortinariaceae 

Cortinarius (c. 2000 spp.) 

Because of its large number of species, this genus 

provides one of the toughest challenges to fungal 

taxonomists as well as field mycologists. In 

Britain alone, 230 species have been listed. The 

genus has been divided into several subgenera 

(e.g. Cortinarius, Dermocybe, Leprocybe, Phlegmacium, 

Myxacium, Telamonia). Species in the subgenus 

Myxacium have slimy caps and stems derived 

from a glutinous universal veil, whilst in the 

subgenus Phlegmacium only the cap is sticky 

whereas the stem is dry. The genus is distributed 

in temperate regions of the Northern 

Hemisphere. All species are mycorrhizal with 

trees, so that they fruit in woodlands and 

woodland margins. The fruit bodies are small 

to large, buff, clay-coloured, orange-brown or 

sometimes very colourful, e.g. violet in C. violaceus 

or blood-red in C. sanguineus, C. purpureus and 

related species. Young fruit bodies are enveloped 

in a filamentous or glutinous veil and developing 

gills are protected by a fibrillose cortina which 

may be evanescent or may persist, attached to 

the stem (Fig. 19.20e). The spores are mostly 

warty, and the spore print is cinnamon to rustbrown. 

It is unwise to attempt to eat Cortinarius 

basidiocarps because the edibility of many 

species is unknown and some are deadly poisonous. 

The most notorious among them is 

C. orellanus, which contains the bipyridyl toxin 

orellanine (Fig. 19.15h), the cause of delayed 

renal failure. Other toxins are cortinarins, which 

are cyclic peptides. The long delay of 2 20 days 

between ingestion of the mushroom and the 

onset of symptoms (nausea, vomiting, diarrhoea, 

gastric upset and abdominal pain) are 

characteristic features of Cortinarius poisoning. 

Death may ensue 2 6 months later (Bresinsky & 

Besl, 1990; Michelot & Tebbett, 1990). 

19.5 Boletoid clade 

This clade includes not only the Boletales, but 

some other groups with basidiocarps which are 

dissimilar in appearance. Traditionally, the 

Boletales, typified by the genus Boletus, have 

included forms with fleshy, mushroom-like basidiocarps 

with tubular hymenophores. Later, 

based on morphological and chemical criteria, 

the concept was expanded to include gill-bearing 

forms such as Paxillus and Hygrophoropsis. 

Relationships were also suggested between 

poroid boletes and resupinate forms such as 

Coniophora or Serpula, and gasteroid genera such 

as Scleroderma or Rhizopogon. Molecular phylogenetic 

techniques have confirmed these relationships 

and a boletoid clade has been recognized to 

embrace this wider concept (Bruns et al., 1998; 

Hibbett & Thorn, 2001). We shall study representatives 

of a gill-bearing group (Paxillaceae), 

poroid groups (Boletaceae, Suillaceae) and resupinate 

forms (Coniophoraceae). 

19.5.1 Paxillaceae 

Paxillus (15 spp.) 

Most species of Paxillus are ectomycorrhizal 

(Wallander & Söderström, 1999), but P. atrotomentosus 

fruits on conifer stumps. The basidiocarps 

are soft and fleshy. A characteristic feature 

is that the hymenial tissue separates readily 

from the flesh of the cap. The roll-rim Paxillus 

involutus (Fig. 19.21a) has a brown, funnel-shaped 

cap with an inrolled margin, decurrent gills and 

brown spores. Upon bruising, an intense brown 

colour develops due to the accumulation of 

the pigment involutin (Fig. 19.22a), a member 

of the shikimic acid-derived pulvinic acid 

family typical of Boletales. Considering that it 

is a mycorrhizal species, P. involutus has an 

unusually wide host range, with 23 different 

tree species listed by Wallander and Söderström 

(1999). It is most commonly associated with birch 

(Betula) and oak (Quercus) in acid woodlands.


Fig19.21 Basidiocarps in the boletoid clade. (a) Paxillus involutus. Note the inrolled cap margin and decurrent gills.The fruit 

bodies shown here have been attacked by the parasitic mould Sepedonium chrysospermum (white patches). (b) Boletus (Xerocomus) 

chrysenteron.(c)Boletus edulis, the cep or penny bun. (d) Suillusgrevillei, an ectomycorrhizal associate of Larix.Notethering 

on the stem. (e,f) Serpula lacrymans, the dry rot fungus. (e) Beam supporting the roof of a church showing the typical 

cracking transverse to the grain of the wood which also shows shrinkage. (f) Resupinate fruit body on a ceiling showing the 

shallow pores. 

Spread through the soil to fresh young roots is 

by an effuse mycelium or by rhizomorphs. 

The fungus may survive in the soil by means of 

sclerotia. Some isolates are capable of saprotrophic 

growth and can fruit in the absence of a 

mycorrhizal host. Affinity with the Boletales has 

long been suspected because basidiocarps of P. 

involutus are commonly attacked by the bright 

yellow conidial state (Sepedonium chrysospermum) 

of the mycoparasitic ascomycete Apiocrea chrysosperma, 

which also attacks different boleti and 

gasteromycetes believed to be related to them 

(Fig. 19.21a; Plate 9h; p. 581). 

The basidiocarps of P. involutus, although traditionally 

considered edible, are, in fact, poisonous. 

There are two symptoms. A heat-labile substance


557 

consumption. The toxic principle(s) appear to be 

unknown as yet. 

Fig19.22 Pulvinic acid-type pigments typical of members 

of the boletoid clade. (a) Involutin, a brown pigment produced 

by Paxillus involutus. (b) Variegatic acid, a yellow pigment. 

(c) The dark blue oxidation product of variegatic acid upon 

bruising the fruit bodies of Boletus erythropus and certain 

other Boletus spp. (d) Grevillin B produced by a range of 

Suillus spp. 

seems to be responsible for gastric upsets within 

a few hours of consuming raw or undercooked 

specimens, whereas haemolysis due to an 

allergic reaction can cause delayed liver 

failure and kidney damage only after repeated 

19.5.2 Boletaceae 

Boletus (300 spp.) 

Formerly comprising a broad range of porebearing 

fungi, the genus Boletus has been divided 

into a number of groups, often now recognized 

as separate genera. Species of Boletus are ectomycorrhizal. 

They have medium-sized, large or 

very large fleshy basidiocarps with a tubular 

hymenophore. The pores marking the openings 

of the hymenial tubes may be of the same 

yellowish-green colour as the tubes or may be 

coloured orange to blood-red as in B. erythropus 

(Plate 9f) and B. satanas. The pigments in Boletus 

are of the pulvinic acid group (Gill & Steglich, 

1987), with variegatic acid (Fig. 19.22b) being the 

most common. Within seconds of bruising or 

cutting the basidiocarps of certain species such 

as B. erythropus, their flesh and pores become 

discoloured blue or bluish-black due to the 

enzyme-mediated oxidation of variegatic acid 

(Fig. 19.22c) and xerocomic acid. 

One of the most common species, B. chrysenteron 

(Fig. 19.24b), sometimes classified in the 

separate genus Xerocomus, is easily recognized by 

the exposure of yellow or red flesh when the 

cap surface skin cracks. It is associated with 

broad-leaved trees. The stem of some species 

may be punctate, i.e. dotted with tiny warts (e.g. 

B. erythropus; Plate 9f), or veined (e.g. B. edulis). 

There are several species with delicious edible 

basidiocarps; amongst the best-known are B. 

edulis (cep or penny bun; Fig. 19.21c), B. badius 

(bay bolete; Plate 9h) and B. appendiculatus. 

Although it is possible to grow mycelium of B. 

edulis in pure culture, it is as yet impossible to 

induce it to form basidiocarps, and therefore this 

much-prized edible species continues to be 

collected in forests (Wang & Hall, 2004). Some 

Boletus spp. are safe to eat only after cooking, 

e.g. B. luridus and B. erythropus, whereas others 

have poisonous basidiocarps, notably B. satanas 

(devil’s bolete) and B. satanoides. 

Boletus parasiticus forms fruit bodies attached 

to the basidiocarps of the earth ball Scleroderma. 

Doubts have been expressed as to whether this


fungus is actually parasitic, and quite possibly it 

is merely stimulated to fruit by the presence of 

the earth ball. 

Leccinum (75 spp.) 

Like Boletus spp., the genus Leccinum has large 

fleshy basidiocarps. A characteristic feature is 

that the stem is covered with scales composed of 

cystidia. Leccinum scabrum (brown birch bolete) 

and L. versipelle (orange birch bolete) are common 

ectomycorrhizal associates of birch (Betula). 

Basidiocarps of Leccinum are generally edible. 

19.5.3 Suillaceae 

Suillus (90 100 spp.) 

Suillus species have medium-sized fleshy basidiocarps 

forming ectomycorrhizal associations with 

conifers. Their fruit bodies are usually of yellowish 

colours due to the abundance of pigments 

derived from the shikimic acid pathway, especially 

grevillins (Fig. 19.22d; Besl & Bresinsky, 

1997). The cap may be dry and scaly but is more 

usually viscid or slimy. There are species with a 

ring on the stem (Fig. 19.21d), e.g. S. grevillei 

(larch bolete) and S. luteus (slippery jack), whilst 

in many others (e.g. S. bovinus, S. granulatus) there 

is no ring (Plate 9g). The spores are smooth 

and elongate, and pale brown to brown. The 

presence of bundles of cystidia in the hymenium 

is a feature which distinguishes this genus 

from other boletes, and the classification into a 

separate family is supported by phylogenetic 

studies (e.g. Grubisha et al., 2001). Also included 

in the Suillaceae are the gasteromycete genus 

Rhizopogon (see p. 581) and the gill-bearing 

Gomphidius. 

The distribution of species mirrors that of 

their mycorrhizal hosts, coniferous trees which 

are largely confined to North-temperate regions, 

only extending to other areas where introduced. 

There is a fairly high degree of host specificity. 

For example, in nature S. grevillei (Fig. 19.21d) is 

almost exclusively associated with Larix spp. 

(larch) whilst S. bovinus and S. luteus are associated 

with Pinus spp. This ecological specificity is 

probably associated with the effects of competition 

because in the laboratory, under aseptic 

conditions, a wider range of hosts has been 

infected experimentally. Many species of 

Suillus have edible basidiocarps and some areas 

of planted pine (P. radiata) forests in South 

America are devoted to production of S. luteus, 

with astonishing annual productivity values of 

up to 1 t dry weight ha 1 reported (Dahlberg & 

Finlay, 1999). Suillus bovinus and S. variegatus are 

common in Swedish pine plantations. Whereas 

S. bovinus is an early-stage mycorrhizal fungus, 

S. variegatus is often found in older stands. 

In open communities dominated by seedling 

pines, S. bovinus first develops a large number of 

genets (genetically defined mycelial individuals) 

derived from basidiospores. Once established, 

a colony extends by mycelial spread and by 

rhizomorphs to nearby host roots. The extent of a 

genet can be estimated by evidence of somatic 

incompatibility between mycelial isolates made 

from basidiocarps. As the original genets expand, 

they compete with each other. The number of 

genets decreases, but as the genets increase in 

size they may fragment so that parts of the same 

genet may become separated. The maximum 

rate of mycelial extension has been estimated to 

be about 20 cm per annum and the age of the 

largest genet to be about 75 years (Dahlberg & 

Stenlid, 1990, 1994; Dahlberg, 1997). 

19.5.4 Coniophoraceae 

This group includes wood-rotting fungi such 

as Serpula and Coniophora which form 

spreading, crust-like resupinate fructifications. 

Morphological characteristics suggested that the 

Coniophoraceae have an affinity with Boletales 

(Pegler, 1991), and Hibbett and Thorn (2001) 

have included them in their bolete clade. This is 

supported by the presence of pulvinic acids in 

both Serpula and Coniophora (Gill & Steglich, 

1987). Here we shall consider only Serpula. 

Serpula 

Serpula lacrymans (Figs. 19.21e,f) causes dry rot 

and is one of the most serious agents of timber 

decay in buildings. There is a very extensive 

literature (see Rayner & Boddy, 1988; Jennings & 

Bravery, 1991). Both hardwoods and softwoods 

are attacked but, because softwoods are more 

commonly used in building construction, it is on


559 

such timbers that the fungus is most frequently 

reported. There is evidence that S. lacrymans 

has become adapted to man-made habitats. 

In the wild, S. lacrymans has been collected 

on spruce logs in the Himalayas at an altitude 

of 8000 10 000 ft (Bagchee, 1954; Singh et al., 

1993), and it has also been reported from 

Northern Europe, Northern California and 

Siberia. It can continue to grow vegetatively at 

2°C, and the optimum (23°C) and maximum 

(26°C) temperatures for growth are rather low. 

Strains of S. lacrymans associated with houses 

are considered to belong to S. lacrymans var. 

domesticus and may have been spread by human 

activities in recent times. The Himalayas are 

often mentioned as a likely centre of origin, 

although Kauserud et al. (2004) put forward an 

alternative hypothesis featuring North America. 

Either way, possible vehicles for the dispersal 

of S. lacrymans var. domesticus may have been 

wooden sailing ships. Ramsbottom (1938), 

in his fascinating review of a wealth of original 

literature sources, concluded that wooden 

vessels were frequently infested by S. lacrymans, 

often being unsound even before being launched 

due to the careless use of non-seasoned 

timber combined with poor ventilation of the 

ship holds. Typical symptoms were described by 

a Commission of Inquiry, reporting to King 

James I in 1609 on the state of battleships in 

the Royal Navy (taken from Ramsbottom, 1938): 

In buylding and repaireing Shippes with greene 

Tymber, Planck and Trennels it is apparent both by 

demonstration to the Shippes danger and by heate of 

the Houlde meeting with the greenesse and sappines 

thereof doth immediately putrefie the same and 

drawes that Shippe to the Dock agayne for 

reparation within the space of six or seven yeares 

that would last twentie if it were seasoned as it 

ought and in all other partes of the world is 

accustomed. Adde hereunto experience at this day 

that many Shippes thus brought in to be repaired, 

subject to miscareinge upon employment, and 

besides they breed infection among the men that 

serve in them. 

Only wood with a moisture content above about 

20 25% of the oven-dry weight is susceptible to 

attack by the fungus. Well-dried and seasoned 

timber has a moisture content of 15 18%, and 

in a properly ventilated house this soon falls to 

12 14% or lower. If woodwork becomes wet 

through contact with the soil, damp masonry, 

faulty construction or inadequate ventilation, 

then infection from air-borne basidiospores is 

likely to follow. Basidiospores germinate in the 

presence of free water on moist wood surfaces. 

The mycelium within the wood develops chiefly 

at the expense of the cellulose; lignin is not 

attacked, and the type of decay is a brown-rot. 

Well-rotted timber is shrunken with transverse 

cracks and has a dry crumbly texture. 

Water produced by the breakdown of cellulose 

(sometimes termed the water of metabolism) 

may be sufficient for further growth even if the 

air humidity is lowered below the point at which 

new basidiospore infections could arise. Up to 

55.6% of the cellulose consumed may be available 

as metabolic water (see Bravery, 1991). As in 

many brown-rot fungi (see p. 527), oxalic acid is 

released into the environment, lowering the pH 

of the wood and mortar over which S. lacrymans 

is growing. 

The epithet lacrymans (weeping) refers to the 

beads of moisture sometimes found on decaying 

timber, at the tips of hyphae and on mycelial 

cords. Sheets of mycelium may extend over the 

timber and adjacent brickwork, and the fungus 

is also capable of spreading several metres by 

means of mycelial cords up to 5 mm in diameter. 

The internal hyphae of the mycelial cords 

are exceptionally wide (up to 60 mm) and are 

modified for rapid conduction, enabling water 

and nutrients to be transported (Nuss et al., 1991). 

Transport is by pressure-driven hydraulic flow 

(Jennings, 1987, 1991). Carbohydrate is transported 

mainly in the form of trehalose. 

The strands can penetrate mortar and stonework 

between walls and can spread throughout a 

building provided that there is enough wood as 

a food base. Strands remaining after removal 

of affected timber may still be able to initiate 

fresh infections. 

Reproduction in Serpula lacrymans 

This fungus is heterothallic and tetrapolar. 

Globally there are probably no more than four 

A and five B alleles (Schmidt & Moreth-Kebernik, 

1991). Arthroconidia are formed on


monokaryons but not on dikaryons. Basidiocarps 

develop from dikaryons as flat, fleshy resupinate 

structures (Nuss et al., 1991). They may grow 

undetected under floorboards and in roof spaces 

for long periods and may reach a diameter of 

1 2 m. The lower side is brown and corrugated 

into shallow pores supporting the hymenium 

(Fig. 19.21f). The folding of the hymenophore is 

the result of continuous thickening of the 

hymenium. The construction is at first monomitic, 

but becomes dimitic with the development 

of skeletal hyphae. Sporulation is 

continuous and it has been estimated that a 

basidiocarp measuring 100 cm 2 can produce 

300 million spores h 1 . The immense numbers 

of rusty-brown basidiospores may form deposits 

visible to the naked eye on cobwebs, shelves, etc. 

In the basements of buildings containing fruit 

bodies, spore concentrations of around 

80 000 m 3 air have been detected (see Hegarty, 

1991), raising concern over respiratory allergy 

which may already have been referred to in the 

report to King James I (see above). 

Control of dry rot 

The economic consequences of failing to eradicate 

and control dry rot in a building can be 

severe. Modern methods aim to render the 

indoor environment hostile to S. lacrymans by 

eliminating all routes by which water could gain 

access to timber, accompanied by constantly 

high ventilation (Bravery, 1991; Palfreyman & 

White, 2003). A more traditional method is the 

removal of all infected timber and surrounding 

sound wood, and the treatment of any timber 

left in place with a recommended and approved 

fungicide. Replacement timbers should be 

selected for their durability properties and 

can be treated with pressure-impregnated fungicides 

such as copper/chromium/arsenic preservatives. 

Plaster can be treated with zinc 

oxychloride. Given the low temperature maximum 

of S. lacrymans, it is also sometimes possible 

to encase an entire building with a tent and 

subject it to thermal treatment (50°C). Since 

S. lacrymans is susceptible to attack by Trichoderma 

spp., biological control has been proposed but 

not yet put into practice (Palfreyman et al., 1995). 

The most important control measure, however, is 

proper construction to ensure that the moisture 

level of the timber remains below the point at 

which infection can be initiated. 

19.6 Polyporoid clade 

Included in this clade are certain members of 

the Polyporales (¼ Aphyllophorales), a group 

comprising hymenomycetes in which (with a 

few exceptions) the hymenium is not borne on 

the surface of gills. It included bracket fungi 

(polypores), tooth fungi, coralloid fungi and 

forms with flattened or crust-like basidiocarps. 

However, morphological, anatomical and chemical 

studies have indicated that this was not a 

natural grouping, and molecular phylogenetic 

investigations have amply confirmed this view, 

with Hibbett and Thorn (2001) showing that the 

aphyllophoroid condition occurs in all eight 

clades of Homobasidiomycetes. Most aphyllophoralean 

fungi outside the polyporoid clade 

are now considered to belong to the russuloid 

clade (see Section 19.7). The taxonomic hierarchy 

within the polyporoid clade is too tentative to be 

adopted at present, and therefore we have 

desisted from using family names here. 

Economically important wood-rotting bracket 

fungi are found in the polyporoid clade. As 

described in detail on pp. 519 522, two main 

types of wood decay caused by basidiomycetes 

have been recognized, namely brown-rot in 

which cellulose is destroyed whereas lignin is 

left essentially unchanged, and white-rot in 

which both lignin and cellulose are attacked. 

Both types of rot can be caused by members of 

the polyporoid clade, e.g. brown-rot by Piptoporus 

betulinus (Fig. 19.23d) and white-rot by Trametes 

versicolor (Plate 10a). However, both rots can also 

be caused by other groups of basidiomycetes. 

The mycelium of members of the polyporoid 

clade is often perennial in large tree trunks and 

may give rise to a fresh crop of basidiocarps 

annually. In some species, e.g. Fomes fomentarius 

or Ganoderma applanatum (Figs. 19.23b,c), the 

fruit body itself may be perennial and new 

layers of hymenial tubes develop annually on 

the lower side of the basidiocarp. Typically

POLYPOROID CLADE 

561 

Fig19.23 Basidiocarps in the polyporoid clade. (a) Ganoderma lucidum. Basidiocarps formed in culture from sawdust contained 

in plastic bags. (b,c) Ganoderma applanatum. (b) Two sporophores attached to a living beech tree. (c) Detached sporophore split 

vertically to show two layers of hymenial tubes. (d) Piptoporus betulinus on a dead birch trunk. (e) Polyporus squamosus, basidiocarp 

attached to a living sycamore tree. (f) Polyporus brumalis growing from a dead beech twig. (g) Sparassis crispa fruiting at the base of 

a living pine tree. a kindly provided byY.-J.Yao. 

polypore fruit bodies develop as fan-shaped 

brackets lacking stipes, but there are forms 

with lateral (eccentric) stipes, such as Polyporus 

squamosus (dryad’s saddle; Fig. 19.23e), or even 

with centrally stalked fruit bodies, e.g. the 

winter polypore Polyporus brumalis (Fig. 19.23f). 

When the fruit bodies of polypores and other 

wood-rotting fungi develop on the underside of


logs, they may be appressed to the surface of the 

wood and are then described as resupinate. 

The hyphal construction (hyphal analysis) 

of polypore basidiocarps varies (see p. 517 519) 

and is useful in identification. In some, 

e.g. Bjerkandera adusta, construction is monomitic; 

the basidiocarps are composed entirely of 

generative hyphae. The basidiocarps of Laetiporus 

sulphureus (chicken of the woods; Plate 10b) are 

dimitic, whereas Trametes versicolor has trimitic 

basidiocarps. The distinction between the different 

kinds of construction is best appreciated 

by attempting to tear the fruit bodies of these 

fungi apart. Trametes versicolor basidiocarps tear 

with difficulty, in contrast to the cheese-like 

consistency of L. sulphureus. Various modifications 

to the different hyphal systems may 

occur with age. For example, in L. sulphureus 

the generative hyphae may become inflated. 

In Polyporus squamosus the binding hyphae arise 

relatively late following inflation of the generative 

hyphae, converting the sappy flesh of the 

fully grown fruit body to a drier and firmer 

texture. In Piptoporus betulinus, too, binding 

hyphae arise very late but ultimately replace 

the generative hyphae. The dissepiments (tissues 

between the pores) show a different construction, 

being dimitic with skeletal hyphae. 

The polyporoid clade is a large group, 

probably containing about 70 genera and over 

600 species. There is a very extensive literature. 

Notes on interesting features of some common 

polypores are given below. 

Trametes 

Trametes (Coriolus) versicolor (Plate 10a), colloquially 

called ‘turkey tail’, is a common saprotroph 

on various hardwood stumps and logs, causing 

white-rot. Both the mycelium and the fruit 

bodies are tolerant of desiccation. The annual 

fruit bodies have a zoned, multicoloured, velvety 

upper surface which readily absorbs rain. Details 

of the anatomy of the fruit body are shown in 

Fig. 19.24. 

Basidiocarps of T. versicolor may come in a 

range of colours and shapes, and if such 

variations in fruit body appearance occur on a 

single log, they can be traced to distinct columns 

of decayed wood when the log is serially 

sectioned. Dark brown ‘zone lines’ separate the 

columns. All isolations from within a column 

yield an identical dikaryon, and the zone lines 

mark intraspecific antagonism between distinct 

dikaryons (see Fig. 18.20a). Therefore, within a 

log of wood the fungus does not behave as 

a single ‘unit mycelium’ but as a series of 

discrete individuals (Rayner & Todd, 1977, 

1979). When monokaryons are inoculated experimentally 

into logs in the field, they quickly 

become converted into dikaryons by anastomosis 

with compatible monokaryotic colonies derived 

from air-borne basidiospores (Williams et al., 

1981). The individual dikaryotic colonies, once 

established, may persist and retain their integrity 

over several years, continuing to produce 

fresh crops of basidiocarps of the same genetic 

constitution each year. Antagonism, i.e. vegetative 

incompatibility between different dikaryons, 

can also be readily demonstrated in pure culture 

as shown in Fig. 18.20c. Monokaryotic mycelia 

form arthroconidia. This species is tetrapolar 

with multiple alleles. 

Because of its prolific production of 

peroxidase-type enzymes, T. versicolor is used 

industrially in such processes as the bioremediation 

of textile dyes or the wood preservative 

pentachlorophenol (PCP), and in delignification 

and decolorization of Kraft woodpulp. Some 

T. versicolor strains used in industry are thermotolerant. 

In addition to enzymes, T. versicolor also 

produces polysaccharopeptides, and these are 

of commercial interest in anti-cancer therapy 

(reviewed by Cui & Chisti, 2003). A range of these 

substances are produced by different strains of 

the fungus. Their exact chemical composition 

is variable, with a branched sugar backbone 

consisting of b-(1,3) and a-(1,4) linkages and a 

protein content of about 30%. Polysaccharopeptides 

are extracted from mycelium grown in 

fermenters, purified, and administered orally. 

Although it is unclear how these large molecules 

can be taken up intact by the gut and how 

exactly they act to achieve the claimed results, 

several effects on the human body are suspected, 

with a general enhancement of the immune 

system being the most common. They are therefore 

considered useful as a complemention of 

other, more aggressive anti-cancer treatments.


563 

Fig19.24 Trametes versicolor. (a) Vertical section through a basidiocarp. (b) Group of hyphae teased from the growing margin.Only 

generative and skeletal hyphae are present here. In the adult flesh, binding hyphae are also present (see Fig.19.3). (c) Transverse 

section across a pore showing the hymenium. (d) Longitudinal section of part of a dissepiment.The tissue contains only generative 

and skeletal hyphae. (b d) to same scale. 

Piptoporus 

Piptoporus betulinus basidiocarps are a common 

sight on dead and dying birch trees (Fig. 19.23d). 

The fungus is probably a wound parasite, its 

basidiospores entering and germinating where 

branches have broken off. Infected trees show 

a brown-rot of the heart wood which first 

undergoes cubical cracking and later disintegrates 

as a powder. Although the brown-rot 

indicates cellulose decay, there is also evidence


of peroxidase activity which suggests limited 

lignin breakdown. The fungus is bipolar with 

about 30 alleles at the mating type locus. 

Multiple infections of single birch trunks are 

comparatively rare, but where they do occur, 

transverse sections of trunks with multiple 

infections show a characteristic pattern of 

black ‘zone lines’ marking the interface between 

antagonistic dikaryons (Adams et al., 1981). The 

dikaryons retain their integrity and persist over 

several years. A fresh crop of basidiocarps is 

produced annually on standing trees or on fallen 

trunks. The birch polypore was formerly known 

as the razor strop fungus in the days when the 

basidiocarps were used to hone ‘cut throat’ 

razors. 

Laetiporus 

The poroid Laetiporus and Phaeolus, together with 

Sparassis which produces lobed, cauliflower-like 

fruit bodies (Fig. 19.23g), form one of the few 

well-resolved branches within the polyporoid 

clade (Wang et al., 2004). Biological features 

uniting these genera are that they cause wood 

decay of the brown-rot type often in living 

trees, and that their mating system is bipolar. 

The former species L. sulphureus sensu lato has now 

been subdivided into several new taxa which 

show a certain degree of host specificity (Burdsall 

& Banik, 2001). Infection is typically through 

wounds of living trees, causing an intense 

brown-rot in the heartwood of standing trees. 

The mycelium is clearly long-lived, with fresh 

crops of basidiocarps (Plate 10b) produced 

annually for several years in the living tree, 

and later from the dead trunk. Laetiporus is 

considered to be one of the main causes for the 

hollowing of old oak trees in parks. Fruit trees 

(especially apple) are also affected. In the Alps, 

broad-leaved trees are attacked at altitudes 

below 3000 ft whereas coniferous species are 

infected higher up in the mountains. In addition 

to basidiospores, L. sulphureus also produces a 

chlamydosporic conidial state called Sporotrichum 

(see Fig. 18.16). 

Laetiporus sulphureus sensu lato has traditionally 

been considered an edible species, as its 

common name ‘chicken of the woods’ indicates. 

However, consumption has been associated with 

gastrointestinal upsets ( Jordan, 1995). 

Polyporus 

Polyporus squamosus (Fig. 19.23e) is a wound 

parasite of deciduous trees such as elm (Ulmus), 

beech (Fagus) and sycamore (Acer pseudoplatanus), 

producing an intensive white-rot. The mycelium 

persists on dead trunks, stumps and logs, and 

forms successive annual crops of basidiocarps 

during the early summer. The large, fan-shaped 

fruit bodies are creamy yellow, with brown 

scales. They are edible. Their texture is distinctly 

fleshy due to a dimitic structure with binding 

hyphae. 

Ganoderma 

There are more than 250 species of Ganoderma. 

They are white-rot fungi causing root and 

stem rots of hardwood and softwood hosts. 

A distinguishing feature is that the spore appears 

double-walled, with a dark-coloured inner layer 

bearing an ornamentation which pierces the 

hyaline outer one, so that the spore appears to 

have a spiny surface (Fig. 19.25). Mims and 

Seabury (1989) have interpreted the basidiospore 

wall of Ganoderma lucidum as comprising three 

Fig19.25 Ganoderma applanatum. Basidiospore.The truncate 

portion is the apex of the spore. Spiny extensions of the 

darker inner spore wall penetrate the hyaline outer wall.


565 

distinct components, an outermost primary 

wall, inter-wall pillars surrounded by electrontransparent 

regions, and an innermost secondary 

wall. Wall pillars, which initially develop 

immediately adjacent to the spore plasma 

membrane, eventually appear to fuse with both 

the primary and secondary walls. 

Ganoderma applanatum and G. adspersum are 

two species with similar basidiocarps which 

are confused with each other but can be 

distinguished by their basidiospores which are 

larger in G. adspersum. Both are wound parasites 

of deciduous trees, producing large (up to 1 m), 

perennial, brown, woody brackets (conks) which 

form a fresh layer of hymenial tubes annually 

(Figs. 19.23b,c). Recently formed hymenial tubes 

of G. applanatum are chocolate-brown in colour 

in contrast to the paler appearance of older 

layers formed earlier. The older layers are 

less dense and have a lower nitrogen content 

than the current year’s growth, suggesting 

that nitrogen is translocated from older, 

spore-depleted strata to the newly formed 

layers (Setliff, 1988). Nitrogen is often in 

limited supply in woody substrates, and its 

conservation is therefore important for wooddecaying 

fungi. 

Ganoderma applanatum is less common than 

G. adspersum and is usually found on old trunks 

of beech (Fagus sylvatica), where it causes a white 

heart rot. The hyphal structure of the fruit body 

is trimitic. A characteristic feature is that the 

skeletal hyphae are of two types, namely arboriform, 

i.e. showing an unbranched basal part 

with a branched tapering end, and aciculiform, 

i.e. unbranched and usually with a sharp tip 

(Hansen, 1958; Furtado, 1965). The hymenial 

tubes of G. applanatum may be up to 2 cm in 

length and about 0.1 mm in diameter, i.e. 200 

times as long as broad. The fall of the spores 

down this tube raises problems. The hard, rigid 

construction of the sporophore minimizes 

lateral disturbance to the vertical alignment of 

the tubes. Gregory (1957) has shown that the 

majority of the spores carry a positive electrostatic 

charge, but whether this charge has any 

relevance to the positioning of the spores during 

their fall by causing them to be repelled from the 

tube wall seems doubtful. It has been calculated 

that a large specimen may release as many as 

20 million spores min 1 during the 5 or 6 months 

from May to September (Buller, 1922). Spore 

discharge can continue even during periods of 

drought, doubtless associated with uptake of 

water from the tree host (Ingold, 1954b, 1957). 

In addition to wind dispersal, basidiospores of 

G. applanatum have been shown to be dispersed 

by specialized mycophagous flies visiting the 

basidiocarps (Tuno, 1999). Basidiocarps of 

G. applanatum are parasitized by larvae of the 

mycophagous fly Agathomyia wankowiczii. The 

trama is stimulated to proliferate into conical 

or cylindrical gall-like outgrowths on the underside 

of the basidiocarp. When the larva has 

completed its development, it bores an exit hole 

through the tip of the gall and drops to the forest 

floor for pupation (Eisfelder & Herschel, 1966). 

Gall-forming insects rarely attack fungi, and 

even other Ganoderma spp. do not seem to be 

attacked by A. wankowiczii. 

Spores placed on media suitable for germination 

may take 6 12 months to develop germ 

tubes. Pairings between monosporous mycelia 

show that the fungus is tetrapolar, with multiple 

alleles. The large output of spores may be related 

to the low probability of compatible spores 

infecting the same tree trunk. 

As discussed above for Trametes, Ganoderma 

spp. have also been credited with having 

medicinal value against a wide range of 

ailments. Ganoderma lucidum (Fig. 19.23a), distinguished 

by its stalked, shiny (lacquered) basidiocarps, 

grows on the roots of deciduous trees. 

It is cultivated in China on sawdust in 

plastic bags for its basidiocarps from which 

polysaccharides and other pharmacologically 

active substances are extracted (Chang & Miles, 

2004). 

Phanerochaete 

There are about 100 species to this genus of 

saprotrophic fungi forming resupinate, crust-like 

basidiocarps with smooth, wrinkled or spiny 

but non-poroid hymenial surfaces. By far the 

best-known species is P. chrysosporium, which 

has become a ‘model’ organism for the examination 

of lignin-degrading enzymes (see Fig. 19.13)


and their potential biotechnological applications. 

There is a conidial state called 

Sporotrichum pulverulentum (Burdsall, 1981). Little 

is known about the ecological role of P. chrysosporium 

because this species is rarely found in 

nature. 

19.7 Russuloid clade 

The russuloid clade is probably the most confusing 

group in the eight-clade system of Hibbett 

and Thorn (2001), containing the complete range 

of hymenophore types shown in Table 19.1 and 

Fig. 19.1. The phylogeny within this clade has 

been examined in detail by Larsson and Larsson 

(2003), who found that the main character uniting 

all members is the presence of gloeocystidia, 

i.e. cystidia filled with light-refractile (lipidrich) 

contents (Fig. 19.29b). In Stereum, these are 

modified as laticiferous hyphae (Fig. 19.27). Other 

characters commonly used to identify russuloid 

fungi are diagnostic only at lower taxonomic 

ranks, e.g. the ornamented walls of basidiospores 

and their starch-positive (amyloid) staining 

with Melzer’s iodine. We shall study representatives 

of agaricoid basidiocarps (Russulaceae), 

polyporoid fruit bodies (Heterobasidion), the 

spine-bearing Auriscalpium and corticioid forms 

(Stereaceae). The family arrangement is still 

tentative, and we give family names only where 

these have a fair chance of survival in future 

classification schemes. 

19.7.1 Russulaceae 

There are two important genera, Lactarius and 

Russula, and they share many features such 

as being ectomycorrhizal species, and having 

a characteristically brittle texture to the gills 

and general fruit bodies due to the presence 

of sphaerocysts embedded in the tissue (see 

Fig. 19.4). Basidiospores are typically amyloid 

and ornamented with warts or ridges. 

Russula (c. 750 spp.) 

The genus Russula presents a similar taxonomic 

nightmare to Cortinarius, and it is unlikely that 

this genus is monophyletic. Species are widely 

distributed and ectomycorrhizal. The basidiocarps 

(Fig. 19.26a) are moderate to large, often 

with a brightly coloured upper cap surface 

(white, yellow, green, red, purple or black). The 

gills are straight, arranged in a crowded but 

regular pattern, and vary from white to strawcoloured. 

The spores are ornamented with a 

network of branched ridges or plates. Some 

common species are R. ochroleuca (edible), 

R. fellea (bitter to the taste and inedible) and the 

sickener, R. emetica (poisonous). Russula ochroleuca 

fruits under coniferous and deciduous trees, 

R. fellea under beech (Fagus sylvatica) and R. emetica 

under pines. 

Lactarius (c. 400 spp.) 

The common name for Lactarius is milk cap, 

referring to the milky juice which exudes when 

the flesh of the cap is broken. The juice varies in 

colour from white to yellow, orange or violet 

and may change after exposure to the air. For 

example, the juice of L. deliciosus (saffron milk 

cap; Plate 10c) is carrot-coloured at first, but 

turns bright green upon prolonged exposure to 

air. The juice also varies in taste, being mild to 

faintly bitter in L. quietus, hot and acrid in 

L. pyrogalus, or first mild and then acrid in L. 

rufus. The juice is contained within broad 

laticiferous hyphae (see Fig. 19.4). As in Russula, 

the flesh also contains clusters of sphaerocysts. 

The gills are generally decurrent and the spores 

are ornamented like those of Russula. Some 

species of Lactarius have a narrow range of 

mycorrhizal partners, e.g. L. torminosus (woolly 

milk cap) and L. turpis (ugly milk cap) are 

associated with birch (Betula), and L. deliciosus 

and L. deterrimus with Pinus and Picea. There 

are several species with edible basidiocarps, 

but some are poisonous or their edibility is 

unknown. Fruit bodies of L. deliciosus are especially 

valued, and it is possible to produce them 

in plantations of artificially inoculated 

host trees. 

19.7.2 Bondarzewiaceae 

Heterobasidion, a seemingly typical polyporoid 

wood-degrading bracket fungus, has been 

placed in the russuloid clade in several phylogenetic 

analyses. Some authors have assigned it to

RUSSULOID CLADE 

567 

Fig19.26 Basidiocarps in the russuloid clade. (a) Russula atropurpurea.(b)Heterobasidion annosum, the cause of butt rot of conifers. 

(c) Stereum hirsutum basidiocarps growing on an oak branch viewed from above. Note the white-rot at the broken end of the 

wood. (d) As (c) but viewed from below to show the smooth hymenium. (e) Auriscalpium vulgare basidiocarps growing from a 

buried pine cone.The hymenium is borne on spines on the lower side of the cap. 

the family Bondarzewiaceae (Larsson & Larsson, 

2003). 

Biology of Heterobasidion 

Heterobasidion annosum (Fig. 19.26b) is the cause of 

heart rot or butt rot of managed conifer 

plantations, and occasionally of deciduous trees 

such as birch in North-temperate regions 

(Korhonen & Stenlid, 1998; Asiegbu et al., 2005). 

It is the most important pathogen of conifers 

in these areas. The disease is especially common 

on alkaline soils. The fungus is a necrotrophic 

parasite whose mycelium extends downwards 

into the root system and upwards into the stem, 

causing a stringy heart rot which damages the 

strength and affects the saleability of the wood. 

Root decay is often followed by wind throw. The 

fungus may survive in the root system, especially 

if it is resinous, for over 60 years. In Europe, three 

somatic incompatibility groups have been distinguished, 

an ‘S’ group (S for spruce) confined to 

Norway spruce (Picea abies), a ‘P’ group which


Fig19.27 Stereum rugosum. 

Section of hymenium.The 

thick-walled hyphae with dense 

contents are sanguinolentous 

hyphae which exude a red fluid 

when damaged, causing the 

hymenium to ‘bleed’. 

grows on pine, spruce, birch and other hosts, 

and an ‘F’ group growing on fir trees (Abies 

spp.) in Southern Europe. These groups, originally 

considered as infra-specific populations 

of H. annosum, have since been recognized as 

separate species (Niemelä & Korhonen, 1998). 

The name H. annosum is retained, but in 

a restricted sense for the ‘P’ group. The ‘S’ type 

is now named H. parviporum and the ‘F’ type 

H. abietinum. The first two groups also occur in 

North America. 

The fruit bodies are perennial, at first thin 

and leathery, later hard and woody (the epithet 

annosum means aged). They are formed at the 

base of dead trees, stumps or beneath fallen logs 

and are readily identified whilst still actively 

growing by their orange-brown colour with a 

white margin. They are dimitic with skeletals. 

Several successive layers of hymenial tubes are 

formed on old basidiocarps, and basidiospores 

are produced throughout the year. The mating 

system is unifactorial (i.e. bipolar) with 

multiple alleles, probably over 100 (Korhonen & 

Stenlid, 1998). Basidiospores germinate to 

form a homokaryotic primary mycelium with 

multinucleate segments. Anastomosis with 

a compatible homokaryon results in the formation 

of a heterokaryotic secondary mycelium 

also with multinucleate segments and 

clamp connections at some, but not all, septa. 

The conidial state (Fig. 18.15) has been assigned 

to the anamorph genus Spiniger. Conidiophores 

can develop on primary and secondary mycelium 

and the conidia may be uninucleate or 

multinucleate. 

Freshly cut stump surfaces are hot-spots for 

infection by H. annosum, and the disease foci in 

plantations are often from thinning stumps 

which have become infected from air-borne 

spores. Insects are also possible vectors of 

conidia. Colonization of the roots of the stump 

is followed by spread to adjacent healthy trees by 

root-to-root contact and possibly by root-to-root 

graft because the fungus does not grow freely 

in the soil. Spread in this way may result in the 

development of genets (clones) many metres in 

diameter, in which several adjacent trees are 

infected by a secondary mycelium (heterokaryon) 

of identical genotype (Swedjemark & Stenlid, 

1993). The pathogenic effect of H. annosum 

may be correlated with the secretion of fungal 

toxins, of which several have been described,


569 

predominantly benzofuran derivatives (Asiegbu 

et al., 1998). 

Control of Heterobasidion annosum 

Earlier methods of control were aimed at 

preventing stump infection by treatment with 

biocides such as creosote, sodium nitrite, urea, 

and boron-containing chemicals. The last two are 

still in use (Pratt et al., 1998; Asiegbu et al., 2005). 

An interesting alternative treatment, using 

biological control, is to inoculate freshly cut 

stumps with the conidia of the saprotrophic 

basidiomycete Phlebiopsis gigantea (¼ Peniophora 

gigantea; polyporoid clade) which competes 

with the parasite in the stumps and prevents 

its colonization, killing the cells of Heterobasidion 

by hyphal interference (Rishbeth, 1952, 1961; 

Ikediugwu et al., 1970). Conidial suspensions of 

P. gigantea are available commercially for use in 

biological control or, in conjunction with urea, 

in integrated control of stump infection in 

Picea plantations (Vasiliauskas et al., 2004, 2005). 

Trichoderma harzianum is another effective 

biological control agent (Holdenrieder & Greig, 

1998). 

19.7.3 Stereaceae 

In this family the fruit body is flattened, 

appressed or resupinate, with a smooth (untextured) 

hymenium on the lower surface. 

Construction may be monomitic or dimitic 

with skeletals. Basidiospores are commonly 

smooth-walled and amyloid. Most members are 

lignicolous and saprotrophic but some are 

pathogens of trees. Hibbett and Thorn (2001) 

have placed the family in the russuloid 

clade, and Larsson and Larsson (2003) found 

that there are several groups of Stereum-like fungi 

in the russuloid clade. Forms with Stereum-like 

basidiocarps also occur in several other clades of 

basidiomycetes (Yoon et al., 2003). 

Stereum sensu stricto 

Basidiocarps of Stereum are common on decaying 

stumps and on attached and fallen tree branches. 

Stereum hirsutum (Figs. 19.26c,d) forms clusters 

of yellowish, fan-shaped leathery brackets with a 

hairy upper surface and a smooth hymenial 

surface on various angiospermous woody hosts, 

especially oak. It is a saprotrophic species 

and important as a cause of decay of sapwood 

of oak logs after felling. Stereum gausapatum is 

another common fungus on oak, which can grow 

parasitically on living trees, causing long narrow 

decay columns (‘pipe rot’) of the heartwood. 

When the hymenium is bruised it exudes a 

red latex. The same phenomenon is found in 

S. rugosum, common on coppice poles of hazel 

(Corylus avellana) and trunks of alder (Alnus 

glutinosa), and in S. sanguinolentum, a wound 

parasite or saprotroph on conifers. In most 

Stereum spp. there are specialized laticiferous 

(sanguinolentous) hyphae which extend through 

the flesh into the hymenium (Clémençon, 2004). 

These hyphae (Fig. 19.27) are thick-walled and are 

interpreted as modified skeletals homologous to 

the gloeocystidia of other members of the 

russuloid clade. 

Mating in Stereum 

The mating behaviour of Stereum spp. presents 

some unusual features. Germinating basidiospores 

form a multinucleate primary mycelium, 

often with whorls (verticils) of clamp connections 

at the septa, a condition described as 

holocoenocytic (Boidin, 1971). This feature led 

to the erroneous conclusion that S. hirsutum 

is homothallic, but in fact it shows unifactorial 

(i.e. bipolar) multi-allelic heterothallism (Coates 

et al., 1981). The mating type factor has been 

termed the ‘C’ factor. Compatible homokaryotic 

primary mycelia conjugate to form a heterokaryotic 

secondary mycelium which also produces 

whorled clamps. However, secondary mycelia can 

be distinguished by their yellowish pigmentation 

and often leathery surface, in contrast to the 

more delicate white primary mycelium. Some 

species of Stereum (S. hirsutum, S. sanguinolentum) 

include outcrossing and non-outcrossing populations 

(Ainsworth, 1987), whereas in others (e.g. 

S. gausapatum and S. rugosum) only outcrossing 

populations have been detected. In S. hirsutum, 

a feature of non-outcrossing homokaryons is 

their inability to accept non-self donor nuclei 

whilst they themselves can transfer nuclei to 

outcrossing strains (Ainsworth & Rayner, 1989; 

Ainsworth et al., 1990). In the short term,


non-outcrossing strains may have the selective 

advantage in being able to exploit a particular 

habitat. They are also resistant to potential 

takeover or conversion to unfit or unstable 

genomic combinations. 

Like many wood-rotting basidiomycetes, 

Stereum spp. show antagonistic reactions in the 

form of discoloured barrage zones where different 

strains confront each other, as seen in 

transverse sections of tree branches which 

contain more than one heterokaryon (Rayner & 

Boddy, 1988). Similar zones also develop on 

culture plates when dissimilar heterokaryons 

meet. Confrontations between heterokaryotic 

(secondary) and homokaryotic (primary) mycelia, 

equivalent to ‘di mon’ mating in Coprinus 

cinereus and Schizophyllum commune (see p. 508), 

have been studied in S. hirsutum in search of 

evidence of the ‘Buller phenomenon’ (Coates & 

Rayner, 1985a). Such confrontations may be fully 

compatible, where both types of nuclei from the 

heterokaryon are potentially competent in bringing 

about dikaryotization of the homokaryon, or 

hemi-compatible, where only one kind of 

nucleus is competent. The Buller phenomenon 

does occur in S. hirsutum, with either one or two 

new heterokaryons formed per interaction. The 

genotypes of the new heterokaryons can be 

classified as composite (acceptor homokaryon 

plus heterokaryon component), parental (identical 

with the donor heterokaryon) and novel 

(different from all three parental and composite 

combinations). There is preferential selection of 

a non-sib-related component of the donor heterokaryon, 

i.e. a nucleus from an unrelated strain, 

not derived from the same fruit body as the 

recipient homokaryon. 

The bow-tie reaction 

Because S. hirsutum is bipolar, 50% of sib-matings 

(i.e. matings between primary mycelia from 

basidiospores of the same basidiocarp) are 

compatible, whilst non-sib matings are uniformly 

compatible because of multiple alleles 

at the mating type locus. In about one-third of 

incompatible sib-related matings a distinctive 

pattern of mycelial interaction occurs in agar 

cultures termed the ‘bow-tie’ reaction (see 

Fig. 19.28a; Coates et al., 1981). A band of 

appressed sparse mycelium, shaped like a bowtie 

in being widest at the edges, develops 

between the two homokaryons, and is bounded 

by narrow regions with exude watery droplets. 

Hyphae within the bow-tie band often burst, 

have granular contents and produce abundant 

irregular lateral branches (Figs. 19.28b,c). It is 

believed that the bow-tie region of a culture 

is occupied by a weakly growing heterokaryon. 

The bow-tie region often expands and may 

replace the mycelium of one of the component 

monokaryons. In some cases, a darkened zone 

of mutual antagonism develops between them. 

The development of bow-ties is controlled by 

a multi-allelic genetic factor, the B-factor, 

unlinked to the mating type C-factor. 

Heterozygosity of the B-factor results in bowtie 

formation which is only visible between 

incompatible homokaryons. The bow-tie 

phenomenon, although discovered in S. hirsutum, 

is not a feature peculiar to this fungus. Similar 

behaviour has been found in mating type 

compatible pairings of some other basidiomycetes, 

e.g. S. gausapatum, Phanerochaete velutina, 

Mycena galopus and Coniophora puteana (Coates & 

Rayner, 1985b). 

Mating in Stereum sanguinolentum 

The mating behaviour of S. sanguinolentum is also 

unusual (Calderoni et al., 2003). Karyogamy, 

meiosis and post-meiotic mitosis may occur in 

the four-spored basidia or spore primordia. 

Most basidiospores contain two nuclei and are 

heterokaryotic, producing a mycelium capable 

of fruiting. Stereum sanguinolentum therefore 

shows secondary homothallism or pseudohomothallism. 

Pairings between single-basidiospore 

isolates from the same basidiocarp (intrabasidiome 

pairings) are somatically compatible 

but virtually all pairings between isolates from 

different basidiocarps (inter-basidiome pairings) 

are somatically incompatible, with demarcation 

lines developing between them. This indicates 

that in S. sanguinolentum there are numerous 

vegetative incompatibility groups (Calderoni 

et al. 2003).


571 

Fig19.28 The bow-tie reaction between incompatible monospore isolates of Stereum hirsutum. (a) General appearance during 

early development; w, watery exudation; b, bow-tie region. (b,c) Abnormal branching of hyphae in the bow-tie region.From 

Coates et al. (1981), with permission from Elsevier. Photograph kindly provided by A.D.M. Rayner. 

Chondrostereum purpureum 

There are several species superficially resembling 

Stereum but falling outside the core group 

currently placed in the russuloid clade. One 

such fungus is Chondrostereum purpureum 

(formerly known as Stereum purpureum), with 

purplish leathery bracket-like or resupinate 

basidiocarps (Plate 10d). Its exact placement in 

the Homobasidiomycetes remains to be determined. 

It is a wound pathogen of numerous 

genera of deciduous trees but especially of 

members of Rosaceae, including plum and 

cherry trees in which it causes ‘silver leaf’ 

disease. The silver sheen on the leaves is due to 

the separation of the epidermis from the 

mesophyll induced by secretions of toxic secondary 

metabolites (Strunz et al., 1997) and/or 

cellulase- and pectinase-type enzymes (Simpson 

et al., 2001) from mycelium in the branches 

below the leaves. Although C. purpureum is 

of considerable economic importance as a 

pathogen of fruit trees, it has been proposed as 

a biocontrol agent in forest situations where 

coniferous trees are to be grown and broadleaved 

trees, such as alder or birch, occur as 

weeds (Shamoun, 2000). 

Amylostereum 

There are several species of Amylostereum related 

to each other, but of uncertain placement within 

the Homobasidiomycetes (Slippers et al., 2003). 

They are necrotrophic wood-rotting wound 

pathogens of Pinus spp. and have entered a 

species-specific relationship with wood wasps 

of the genus Sirex, which distribute conidial 

(arthrosporic) inoculum in their internal glands 

and deposit it with mucilage surrounding 

their eggs, thereby providing the fungus with a 

suitable entry route into host trees. 

Decomposition of the wood by Amylostereum 

spp. facilitates feeding by the Sirex larvae, 

which take up inoculum prior to pupation


(Talbot, 1977). Severe infections of pine plantations 

are thought to be due to a synergism 

between the fungus and its insect vector, 

and are particularly common in the Southern 

Hemisphere. 

19.7.4 Auriscalpium 

The fruit bodies of Auriscalpium have a toothed 

hymenium, but molecular sequence studies have 

shown that the genus is related to the gillbearing 

Lentinellus and the clavarioid fungus 

Clavicorona (Pine et al., 1999), both included in 

the russuloid clade (Fig. 19.2). Auriscalpium 

vulgare, the earpick fungus, is distributed in the 

Northern Hemisphere. It grows on buried pine 

cones, forming stalked, one-sided, brown, hairy 

fruit bodies during autumn and winter 

(Fig. 19.26e). The hyphal construction is dimitic 

with skeletals. The hymenium is formed on 

vertical, finger-like downgrowths from the 

underside of the pileus. Interspersed amongst 

the basidia are irregularly enlarged, thin-walled 

hyphal tips with highly refractile contents, 

gloeocystidia (Fig. 19.29). Basidiocarps show 

rapid gravitropic readjustment to the vertical 

position if displaced laterally. The mating 

system of Auriscalpium is bifactorial, i.e. 

tetrapolar (Petersen & Wu, 1992; Petersen & 

Cifuentes, 1994). 

19.8 Thelephoroid clade 

This includes the order Thelephorales, a small 

group of predominantly ectomycorrhizal fungi 

with variable basidiocarps. The most important 

genus is Thelephora (c. 50 spp.). The earth fan 

T. terrestris (Plate 10e) produces clusters of fanshaped 

basidiocarps which are chocolate-brown 

in colour with a paler margin. They are 

often formed around the stem of young trees, 

seemingly ‘choking’ them. Basidiocarps of 

T. terrestris superficially resemble those 

of Stereum but are monomitic, composed of 

clamped generative hyphae only. The basidiospores 

are brown and warty. Thelephora terrestris 

fruits in association with coniferous trees 

growing on light sandy soils and heaths. It is 

Fig19.29 Auriscalpium vulgare. 

(a) Spine from the underside of the 

basidiocarp cap. (b) Portion of the 

hymenophore showing skeletal 

hyphae, gloeocystidia and basidia.

HYMENOCHAETOID CLADE 

573 

one of a group of early-stage ectomycorrhizal 

associates of a variety of trees and also forms 

mycorrhiza with Arbutus menziesii, a member of 

the Ericaceae (Zak, 1976). According to Molina 

and Trappe (1984), T. terrestris represents the most 

abundant naturally present mycorrhizal fungus 

in bare-root nurseries. 

19.9 Hymenochaetoid clade 

One feature that distinguishes the five 

Homobasidiomycete clades considered in the 

previous sections from the remaining three 

clades is the structure of the parenthesome, i.e. 

the membranous structure overarching the 

septal pore (see Fig. 18.10). In the five clades 

already described, the typical homobasidiomycete 

dolipore with a perforated parenthesome is 

found, whereas in the hymenochaetoid, cantharelloid 

and gomphoid phalloid clades shown in 

Fig. 19.2, the parenthesome is generally imperforate 

(Hibbett & Thorn, 2001). Imperforate 

parenthesomes are also found in certain 

Heterobasidiomycetes, namely Dacrymycetales 

(Section 21.3) and Auriculariales (Section 21.4). 

This character has been discussed as being of 

phylogenetic significance, supporting the eightclade 

system shown in Fig. 19.2. Hibbett and 

Thorn (2001) have estimated that the hymenochaetoid 

clade comprises about 630 spp. 

recruited from three families, namely the 

entire Hymenochaetaceae and parts of 

Corticiaceae and Polyporaceae. 

19.9.1 Hymenochaetaceae 

Most members of the hymenochaetoid clade are 

wood-decomposing fungi, exemplified by the 

white-rots Inonotus and Phellinus which often 

fruit on old living trees and continue to do so 

after the death of the host. In general terms, the 

basidiocarps are monomitic and annual in 

Inonotus but dimitic, hard and perennial in 

Phellinus. Generative hyphae typically lack 

clamp connections in both genera. Fruit body 

morphology is variable, with resupinate and 

bracket-like forms most commonly produced; 

the hymenium is usually poroid. There are 

transitional forms between the genera Inonotus 

and Phellinus, and both have now been split up 

into several smaller units (Wagner & Fischer, 

2001). Here we shall focus on Phellinus sensu lato. 

Phellinus sensu lato (c. 180 spp.) 

This genus is widespread and cosmopolitan, 

affecting both coniferous and broad-leaved 

trees. An interesting example is P. weirii, of 

which Hansen and Goheen (2000) have given 

a superb account. This species causes laminated 

root rot in native coniferous trees in the 

West Coast forests of North America, affecting 

especially Douglas fir (Pseudotsuga menziesii). 

Mycelium is able to penetrate intact roots and 

then spreads to adjacent trees by root-to-root 

contact. Trees of all ages are affected and 

are killed when extensive rot of the root 

system renders them unstable to storms, often 

several years or decades after initiation of 

infection. In this way, large genets of P. weirii 

slowly spread through the native forest, 

profoundly influencing the host population 

dynamics and shaping the forest landscape 

en route. Mycelium can also survive for decades 

in fallen logs. Phellinus weirii has a bipolar 

(unifactorial) mating-system although, according 

to Hansen and Goheen (2000), basidiospores 

are not an important part of the life cycle which 

relies mainly on clonal spread. 

Phellinus noxius is the cause of root rot in 

numerous tree species in Central America and 

the Far East, Taiwan being particularly severely 

affected. Disease progression is unusually rapid 

for this group of pathogens, with infected trees 

sometimes dying within one growing season 

(Ann et al., 2002). This pathogen may remain 

viable in dead colonized roots for several years if 

the soil is relatively dry, and the flooding of 

affected areas, where practicable, is an efficient 

control method. 

There are also several species encountered in 

gardens, parks and forests in temperate climates, 

colonizing the trunks especially of mature and 

declining trees. Basidiocarps may be located 

several metres above ground. For example, 

P. igniarius (Plate 10f) forms basidiocarps predominantly 

on willow (Salix) and apple (Malus) trees,


P. pomaceus on plum trees (Prunus), and P. robustus 

on oak (Quercus). 

Phellinus pomaceus has been extensively 

examined for the mechanism by which it 

produces the greenhouse gas chloromethane. 

This activity is indirectly associated with its 

lignin degradation system (see p. 527). 

19.10 Cantharelloid clade 

This is a further group of Homobasidiomycetes 

with a wide range of morphologically different 

basidiocarps. Species likely to be encountered 

during forays belong to the Cantharellaceae, 

Hydnaceae and Clavulinaceae. Pine et al. (1999) 

have provided evidence of the relationship 

between these groups. Hibbett and Thorn (2001) 

have suggested that Tulasnella might be included 

in this group, but since members of this genus 

produce heterobasidia, we regard them as 

belonging to the Heterobasidiomycetes (see 

Fig. 21.1b). 

19.10.1 Cantharellaceae 

The genera Cantharellus and Craterellus belong to 

the most sought-after edible species. Cantharellus 

and related species are known as the chanterelles, 

with C. cibarius being the most readily 

recognized (Plate 10g). Another abundant, 

although less well-known, edible species is 

C. tubaeformis (Fig. 19.30a). The fruit bodies of 

most Cantharellus spp. appear in vibrant yellow or 

red colours due to carotenoid pigments, including 

canthaxanthin in the case of C. cinnabarinus. 

The fruit bodies are funnel-shaped, and the 

hymenium consists of shallow branching ridges 

which are strongly decurrent. The number of 

sterigmata and basidiospores on the basidium 

of C. cibarius seems to vary in the range of 4 7. 

In Craterellus cornucopioides, the horn of plenty 

or death’s trumpet, the hymenium is smooth, 

and the fruit bodies are trumpet-shaped with a 

hollow stipe. 

Members of this group are ectomycorrhizal 

with coniferous (Picea, Pinus) and broad-leaved 

(Fagus) trees, and it has been possible to 

grow C. cibarius on agar-based media and to 

Fig19.30 Basidiocarps in the cantharelloid clade. 

(a) Cantharellus tubaeformis.(b)Hydnumrufescens, the hedgehog 

fungus. (c) Clavulina cristata. 

generate mycorrhizal associations under laboratory 

conditions (Danell, 1994). There is hope 

that a method may ultimately be developed 

towards commercial production of fruit

GOMPHOID PHALLOID CLADE 

575 

bodies under controlled conditions (Wang & 

Hall, 2004). 

19.10.2 Hydnaceae 

Hydnum 

The fruit bodies of the hedgehog fungi Hydnum 

repandum (see Fig. 19.1c) and H. rufescens 

(Fig. 19.30b) grow in deciduous and coniferous 

woodlands where they are ectomycorrhizal. They 

are more or less mushroom-shaped, with a cap 

and a central or lateral stipe. Hydnum spp. are 

good to eat and H. repandum is often collected for 

sale in mainland Europe. The basidiocarp 

construction is monomitic, with generative 

hyphae which become inflated, giving the fruit 

body a fleshy texture. The hymenium covers the 

tapering spines which develop from the lower 

side of the cap. 

19.10.3 Clavulinaceae 

Although the spindle-shaped fruit bodies of 

Clavulina are morphologically very similar to 

those of Clavaria, both genera have been placed 

in different clades. Clavulina spp. are saprotrophic 

fungi growing in the humus layer in 

forests and on lawns where they form coral- or 

spindle-shaped basidiocarps which are white, 

grey or pale yellow in colour. A common 

representative is C. cristata, which is a variable 

fungus with highly branched fructifications 

(Fig. 19.30c). A characteristic feature of the 

genus Clavulina is that the basidia are twospored, 

narrowly cylindrical, and often undergo 

septation after spore discharge. The hymenium 

thickens with age. The fruit body construction 

is monomitic, with clamped inflated hyphae 

(Fig. 19.31). 

19.11 Gomphoid phalloid clade 

There are about 350 species in this group which 

has given rise to the most fascinating array of 

gasteromycetes, including the cannonball 

fungus, earth stars and stinkhorns. These are 

described in detail in Section 20.4. There are 

also some genera of actively spore-discharging 

basidiomycetes in the gomphoid phalloid 

clade, especially with club-shaped and coralloid 

basidiocarps. These are grouped in the 

Clavariaceae which are briefly described below. 

19.11.1 Clavariaceae 

Hymenomycetes with smooth, branched or 

unbranched cylindrical or clavate fructifications 

were previously aggregated into this family, but 

microscopical and molecular phylogenetic analysis 

show that such an arrangement groups 

together unrelated forms, and it is clear that 

the clavarioid type of fructification has evolved 

Fig19.31 Clavulinarugosa.Portionof 

the flesh and hymenium. Note the 

clamped hyphae and the narrow 

two-spored basidia.


independently in several unrelated basidiomycete 

groups (Pine et al., 1999). For example, 

Clavulina is now included in the cantharelloid 

clade (p. 575). Corner (1950) has monographed 

the clavarioid fungi and Petersen (1973) has 

given keys to genera. 

Clavaria and its allies 

This is a large genus of pasture and woodland 

fungi with cylindrical or club-shaped branched 

or unbranched fructifications. The flesh of 

Clavaria is made up of thin-walled hyphae 

which lack clamp connections and may become 

inflated and develop secondary septa. The hymenium 

which covers the whole surface of the 

fruit body usually consists of four-spored basidia 

with or without basal clamps, bearing colourless 

spores. A typical species is C. vermicularis 

which fruits in grassland, forming tufts of 

whitish, unbranched spindle-shaped basidiocarps. 

Clavaria argillacea forms yellow clubshaped 

fructifications on moors, heaths and 

peat bogs. In North America fructifications are 

consistently associated with ericaceous plants, 

including cultivated blueberries (Vaccinium angustifolium 

and V. myrtilloides), Azalea and Erica 

(Englander & Hull, 1980). In Australia a similar 

species is associated with cultivated Azalea 

indica (Seviour et al., 1973). The close association 

suggests a mycorrhizal relationship, and 

although it has not been possible to synthesize 

mycorrhiza by inoculating aseptically grown 

ericaceous seedlings with mycelial cultures of 

Clavaria, evidence in support of a mycorrhizal 

partnership has been obtained by the demonstration 

of a two-way transfer of radioactive carbon 

and phosphorus between Clavaria and ericaceous 

plants, and by immunofluorescence studies in 

which hyphal coils were stained within root 

epidermal cells with conjugated antibodies 

raised against Clavaria basidiocarps (Mueller 

et al., 1986). It is therefore likely that ericoid 

mycorrhizae develop following root infection by 

basidiomycetes as well as by ascomycetes such as 

Hymenoscyphus ericae (see p. 442), and both groups 

of fungi may infect the same root. 

There are numerous other common representatives 

of the Clavariaceae. Clavariadelphus pistillaris 

(giant club) forms exceptionally large clubshaped 

fruit bodies (7 30 2 6 cm) in beech 

woods on chalk (see Fig. 19.1d). The construction 

is monomitic, with clamps at the septa. As the 

fruit body matures, the hymenium becomes 

thicker by the development of further layers of 

basidia. Some of the more richly branched fairy 

clubs are placed in the genus Ramaria, distinguished 

by tougher flesh and pink, yellow or 

brown-coloured basidiospores, which are often 

rough. A particularly striking example is 

R. botrytis (Plate 10h). Most Ramaria spp. are 

ectomycorrhizal (Nouhra et al., 2005); R. stricta is 

exceptional in growing on rotten wood.

20 

Homobasidiomycetes: gasteromycetes 


Gasteromycetes are an unnatural assemblage of 

basidiomycetes sharing the common negative 

character that the basidiospores are not 

discharged violently from their basidia. Instead 

of the ballistosporic basidiospores of other 

basidiomycetes which are asymmetric in side 

view (see Fig. 18.5), those of the gasteromycetes 

are usually symmetrically poised on their sterigmata 

or are sessile. Dring (1973) has termed 

such basidiospores statismospores. Commonly 

the basidia open into cavities within a fruit body, 

and the basidiospores are released into these 

cavities as the tissue between them breaks down 

or dries out. A recognizable fertile layer (hymenium) 

may be present or absent (see Reijnders, 

2000). The internal production of basidiospores 

has given the gasteromycetes their name (Gr. 

gaster ¼ stomach). The gasteromycete fruit body 

is termed the gasterocarp, and the spore mass 

enclosed by the gasterocarp wall (peridium) 

is the gleba. Sometimes, as in Lycoperdon 

or Geastrum, the gasterocarp opens by a pore 

through which the spores escape, but in forms 

with subterranean (hypogeous) fruit bodies there 

is no special opening, and it is possible that the 

spores are dispersed by rodents and other 

burrowing animals (Colgan & Claridge, 2002). 

In Phallus and its allies, the basidiospores are 

exhibited in a sticky mass attractive to insects, 

whilst in Cyathus and Sphaerobolus the spores are 

enclosed in separate glebal masses or peridioles 

which are dispersed as units. In spite of these 

variations in gasterocarp morphology, the life 

cycles of most gasteromycetes follow the 

general Homobasidiomycete pattern outlined 

in Fig. 18.4. Most species for which details are 

known appear to be heterothallic, with a basidiospore 

germinating to give a monokaryotic 

primary mycelium. Following fusion of compatible 

primary mycelia, a dikaryotic secondary 

mycelium is established, and this produces 

gasterocarps in which karyogamy and meiosis 

occur, and haploid basidiospores are formed. 

Dikaryotic asexual propagules are also known in 

some gasteromycetes. 

Most members of the group are saprotrophic 

and grow on soil, rotting wood and other 

vegetation, or dung. Mycelial cords or rhizomorphs 

are often formed. Rhizopogon which 

produces hypogeous gasterocarps, and 

Scleroderma and Pisolithus with epigeous fruit 

bodies, are important ectomycorrhizal associates 

of forest trees. There are also two genera of 

aquatic gasteromycetes. Nia vibrissa grows on 

driftwood in the sea, forming globose, yellowish 

gasterocarps a few millimetres in diameter. Its 

basidiospores bear 4 5 radiating appendages 

(Jones & Jones, 1993). Such appendages are a 

typical adaptation to the aquatic habitat (see 

Section 25.2). Limnoperdon forms small, floating 

fruit bodies in freshwater swamps and marshes 

(Escobar et al., 1976). 

Because of the conspicuous shape and appearance 

of their gasterocarps, gasteromycetes have 

long attracted the attention of mycologists, and 

several keys and descriptions are available, 

including the books by Miller and Miller (1988),

578 HOMOBASIDIOMYCETES: GASTEROMYCETES 

Ellis and Ellis (1990) and Pegler et al. (1995). 

Species with hypogeous gasterocarps (‘false 

truffles’) have been described by Pegler et al. 

(1993). 

20.2 Evolution and phylogeny of 

gasteromycetes 

In theory, the evolution of a gasteromycete 

from a hymenomycete ancestor requires only 

two morphogenetic changes, i.e. the production 

of a closed fruit body accompanied by the loss 

of the active spore discharge mechanism. 

The coincidence of these two features is shown 

by several examples of secotioid fruit bodies, 

i.e. basidiocarps in which the margin of the 

pileus fails to become detached from the stipe 

(Thiers, 1984). Watling (1971) described such 

aberrant development in the agaric Psilocybe 

merdaria growing in culture, where the failure 

of the fruit body to expose its hymenium 

coincided with morphological changes to the 

gills and basidia. Chiu et al. (1989) reported a 

similar case in Volvariella bombycina, and Hibbett 

et al. (1994) demonstrated that a naturally 

occurring recessive allele in a single gene is 

responsible for converting the lamellate fruit 

body of Lentinus tigrinus into a secotioid one. 

Except for the L. tigrinus mutant in which an 

existing hymenium is belatedly overgrown by a 

veil (see Fig. 19.6b), most secotioid forms seem to 

arise as a developmental defect causing incomplete 

differentiation of an agaric- or bolete-type 

basidiocarp (Thiers, 1984; Hibbett et al., 1997b). 

Several species pairs are known in nature in 

which a secotioid form is closely related to 

a mushroom-type species, e.g. Montagnea and 

Podaxis (Fig. 20.1) related to Coprinus comatus 

(Fig. 19.14c), Gastroboletus related to Boletus, 

Gastrosuillus related to Suillus, Hydnangium related 

to Laccaria, orThaxterogaster related to Cortinarius 

(Thiers, 1984; Mueller & Pine, 1994; Hopple & 

Vilgalys, 1999). Such evolutionary trends 

towards ‘gasteromycetation’ may be ongoing, 

and e.g. Gastrosuillus laricinus is thought to 

have arisen from Suillus grevillei as recently as 

Fig 20.1 Fruit bodies of the secotioid 

mushroom Podaxis pistillaris, a close relative of 

the ink cap Coprinus comatus (see Fig.19.14c). 

(a) Young fruit body. (b) Mature disintegrating 

fruit body.Original photographs kindly 

provided by A.E. Ashford.

EVOLUTION AND PHYLOGENY OF GASTEROMYCETES 

579 

70 years ago (Baura et al., 1992). In contrast, the 

most ancient fossil gasteromycete found so far, 

an earth star resembling Geastrum, dates back to 

the Cretaceous period some 65 70 million years 

ago (Krassilov & Makulbekov, 2003). 

One selective environmental pressure towards 

the secotioid and ultimately gasteromycete habit 

might be drought, since the very nature of the 

active basidiospore discharge mechanism by 

drop fusion (see p. 493) precludes its function at 

low humidity. It is perhaps no coincidence that 

secotioid fungi are particularly common in arid 

regions (Thiers, 1984). Secotioid fruit bodies are 

generally assumed to be the first step towards 

typical gasteromycete forms such as earth balls, 

puffballs and false truffles (Reijnders, 2000). 

However, mycologists are still at a loss to explain 

how the fantastically complicated fruit bodies, 

e.g. of the stinkhorns or bird’s nest fungi, could 

have evolved from there. 

Given the ease with which secotioid fruit 

bodies can arise, it is hardly surprising that 

gasteromycetes have evolved several times independently 

from hymenomycete ancestors, as 

indicated by numerous phylogenetic studies 

(see Fig. 19.2; Hibbett et al., 1997b; Hibbett & 

Thorn, 2001). In subsequent sections of this 

chapter we shall consider the three most 

important groupings which are as follows (see 

Table 20.1): 

1. Members of the euagarics clade (Section 

19.4). The puffballs (Lycoperdaceae) and bird’s 

nest fungi (Nidulariaceae) as well as a few 

smaller groups of gasteromycetes belong to this 

group. The Lycoperdaceae are close to 

Macrolepiota (Krüger et al., 2001), whereas the 

Nidulariaceae cannot be placed accurately as yet 

but are likely to have arisen on a separate 

occasion. A further independent evolutionary 

event was that leading to the marine gasteromycete 

Nia vibrissa (Binder et al., 2001). 

2. Members of the boletoid clade (Section 

19.5). Several gasteromycetes have their origin 

in the boletoid clade (Binder & Bresinsky, 2002). 

The most important group is the family 

Sclerodermataceae, i.e. the earth balls and their 

relatives (Scleroderma, Pisolithus, Astraeus) which 

are closely related to Gyrodon. Another example 

is Rhizopogon which is close to Suillus. Like their 

actively spore-discharging relatives, these boletoid 

gasteromycetes are important ectomycorrhizal 

associates of trees. 

3. The gomphoid phalloid clade. This 

group contains the coral fungi and similar 

basidiomycetes with exposed hymenia and 

active basidiospore discharge (Ramaria, 

Clavariadelphus, Gomphus; see p. 575), as well as 

several important groups of gasteromycetes, 

namely the earth stars (Geastrum spp.), the 

cannonball fungus (Sphaerobolus), and the stinkhorns 

and their allies. The phylogeny of this 

grouping has been discussed by Humpert et al. 

(2001). 

Although the artificial nature of the gasteromycetes 

as a taxonomic group has been known 

or suspected for many decades, it still comes as a 

shock to most mycologists to realize just how 

strongly convergent the evolution of these fungi 

has been. For instance, the implications from the 

results of phylogenetic studies (see Table 20.1) 

are that the earth stars (Geastrum spp.) have 

arisen independently of the barometer earth star 

(Astraeus), that the raindrop-mediated bellows 

mechanism of basidiospore release through 

an apical pore in puffballs and earth stars has 

evolved at least three times, and that the 

peridioles in the bird’s nest fungi (Cyathus, 

Crucibulum), in Sphaerobolus and in Pisolithus are 

analogous rather than homologous structures. 

Referring to these and other findings made by 

molecular phylogeneticists, Reijnders (2000) concluded 

that ‘if this key denotes real affinities, 

morphologists must be ashamed of their wrong 

conclusions’. 

Ingold (1971) regarded the gasteromycetes 

as a biological group which, having lost the 

active spore discharge mechanism of their 

hymenomycete ancestors, have attempted a 

remarkable series of experiments in spore 

liberation. In order to explore this aspect of 

gasteromycete biology, we shall consider these 

fungi together in the present chapter, but 

drawing on the taxonomic framework as set 

out in Chapter 19.


Table 20.1. Taxonomic affinities and spore release mechanisms of selected gasteromycetes. 

Hymenomycete 

grouping 

Gasteromycete 

genus 

Gasterocarp 

type 

Propagule Dispersal Ecology 

Euagarics clade Bovista,Calvatia Puffball 

(epigeous) 

Lycoperdon Puffball 

(epigeous) 

Crucibulum, Bird’s nest 

Cyathus (epigeous) 

Nia 

Gelatinous 

(epigeous) 

Boletoid clade Rhizopogon False truffle 

(hypogeous) 

Melanogaster False truffle 

(hypogeous) 

Pisolithus Earth ball 

(epigeous) 

Scleroderma Earth ball 

(epigeous) 

Astraeus Earth star 

(epigeous) 

Calostoma Puffball 

(epigeous) 

Gomphoid 

phalloid clade 

Geastrum 

Anthurus, 

Clathrus, 

Phallus, 

Mutinus 

Sphaerobolus 

Earth star 

(epigeous) 

Stinkhorn, etc. 

(epigeous) 

Cannonball 

(epigeous) 

Basidiospore A Saprotrophic 

Basidiospore B Saprotrophic 

Peridiole C Saprotrophic 

Basidiospore D Saprotrophic 

Basidiospore E Ectomycorrhizal 

Basidiospore E Ectomycorrhizal 

Peridiole or A Ectomycorrhizal 

basidiospore 

Basidiospore A Ectomycorrhizal 

Basidiospore B Ectomycorrhizal 



Basidiospore F Saprotrophic 

Peridiole G Saprotrophic 

Dispersal mechanisms of propagules are as follows: 

A.Disintegration of gasterocarp followed by release of propagules by wind or animal trampling. 

B.Puffing through a pore after a raindrop hits the endoperidium (‘bellows mechanism’). 

C. Splash cup dispersal following impact by a raindrop. 

D. Passive release into water. 

E.Distribution by burrowing animals and/or passive release into the soil following disintegration of the 

gasterocarp. 

F.Insectdispersal following olfactory and visual attraction. 

G. Active discharge of peridiole by tension-snap mechanism.

GASTEROMYCETES IN THE EUAGARICS CLADE 

581 

20.3 Gasteromycetes in the 

euagarics clade 

The euagarics clade contains some 10 000 fungi 

in 26 families (Hibbett & Thorn, 2001; Kirk et al., 

2001). Hymenia may be produced on the gills, 

pores and ridges of mushrooms and on the 

surface of coral-shaped fruit bodies, or basidia 

may be enclosed in gasterocarps. Among the 

gasteromycetes found within the euagarics, 

the two most important families are the 

Lycoperdaceae comprising puffballs and related 

forms, and the Nidulariaceae (bird’s nest fungi). 

20.3.1 Lycoperdaceae: puffballs 

Puffballs such as Lycoperdon, Vascellum and 

Calvatia form a phylogenetically well-defined 

group which seems to be closely related to the 

genus Macrolepiota both on the basis of DNA 

sequence analyses (Krüger et al., 2001) and 

because of similarities in the ontogeny and 

architecture of rhizomorphs (Agerer, 2002). The 

current family Lycoperdaceae contains 18 genera 

and 158 species of gasteromycetes with epigeous 

fruit bodies. The mature gasterocarp is thinwalled 

and either forms an apical pore 

(in Lycoperdon) or disintegrates from the apex 

downwards (e.g. in Calvatia, Vascellum, Bovista). 

Basidiospores are brown in colour and have 

warty or spiny walls, with the distal part of the 

basidial sterigma often remaining attached to 

mature spores (Portman et al., 1997). Most species 

are saprotrophic on soil and humus. 

Lycoperdon 

About 50 species are known, producing fruit 

bodies which are pear-shaped or top-shaped. 

Most species grow on the ground. Lycoperdon 

pyriforme (Fig. 20.3) is unusual in growing directly 

on old stumps, rotting wood and sawdust heaps. 

It is not closely related to other Lycoperdon spp. 

and is now called Morganella by some authors. 

Gasterocarps of Lycoperdon spp. commonly arise 

on mycelial cords. The individual cells of the 

mycelium usually contain paired nuclei, but 

clamp connections are absent (Dowding & 

Bulmer, 1964). A longitudinal section of a 

young gasterocarp of L. pyriforme (Figs. 20.3a,b) 

shows that it is surrounded by a two-layered 

peridium, but as the fruit body expands the 

pseudoparenchymatous exoperidium may slough 

off or crack into numerous scales or warts 

(Fig. 20.2a) whilst the tougher endoperidium 

made up of both thick-walled and thin-walled 

hyphae remains unbroken, apart from a pore at 

the apex of the fruit body. The tissue within the 

peridium is differentiated into a non-sporing 

region or sub-gleba at the base of the gasterocarp, 

which extends as a columella into the 

sporulating region (gleba) in the upper part of 

the fruit body. The glebal tissue is sponge-like, 

containing numerous small cavities, and in the 

upper fertile part the cavities are lined by the 

hymenium. The tissue separating the hymenial 

chambers is made up of thick- and thin-walled 

hyphae. The thin-walled hyphae break down as 

the gasterocarp ripens, but the thick-walled 

hyphae persist to form the capillitium threads 

between which the spores are contained. The 

basidia lining the cavities of the gleba are 

rounded and bear one to four basidiospores 

symmetrically arranged on sterigmata of varying 

length (Fig. 20.3c). Young basidia are binucleate, 

and nuclear fusion and meiosis occur in the 

usual way. One nucleus migrates into each spore, 

and if fewer than four spores are produced, 

the spare nuclei degenerate in the basidium 

(Dowding & Bulmer, 1964). The basidiospores are 

not violently projected from the sterigmata. As 

the glebal tissue breaks down and dries, the 

spores are left as a brown dusty mass inside the 

fruit body. An apical pore develops by controlled 

lysis of the endoperidium (Fig. 20.2b). The thin 

upper layer of the endoperidium is elastic and 

acts as a bellows, and when rain drops impinge 

on this layer, small clouds of spores are puffed 

out (Gregory, 1949). Little is known of the mating 

behaviour of Lycoperdon. 

Calvatia 

Gasterocarps about the size of a rugby football 

are produced by Calvatia (Langermannia) gigantea 

(Fig. 20.2c) growing on grassland and on 

disturbed ground. There is no definite pore; the 

peridium breaks away to expose a brown spore 

mass. Buller (1909) estimated that the output of


Fig 20.2 Gasteromycetes in the euagarics clade. (a,b) Lycoperdon perlatum.Young gasterocarps (a) are ornamented by warts formed 

from the exoperidium. In older gasterocarps (b), the warts have sloughed off and the endoperidium has formed the apical pore. 

(c) Calvatia gigantea.Young fruit bodies growing with Urtica dioica.The coin is 2.5 cm in diameter. (d) Cyathus stercoreus.Gasterocarps 

(about 5 mm diameter) opening up to reveal the peridioles. 

a specimen measuring 40 28 20 cm was 

7 10 12 spores (see Table 18.1), and much larger 

specimens have been recorded. The spores are 

spherical with scattered warts. A more 

commonly encountered species is C. excipuliformis, 

which fruits on humus (Plate 11a). 

When attempts are made to germinate 

the spores of this and other puffballs in 

the laboratory, the percentage of germination is 

extremely low, often less than 0.1%. Germination 

takes several weeks and is stimulated by the 

growth of yeasts (Bulmer, 1964; Wilson & Beneke, 

1966). 

20.3.2 Nidulariaceae: bird’s nest fungi 

Here the gasterocarps are funnel-shaped, and 

the gleba is differentiated into lens-shaped 

peridioles (glebal masses) which contain the 

basidiospores. Some 50 species in 4 genera are 

known, of which the most common examples 

are Cyathus and Crucibulum. Detailed and highly 

readable accounts of the biology of bird’s nest 

fungi have been given by Brodie (1975, 1984). 

Members of this family are saprotrophic and 

are capable of degrading lignin (Wicklow et al., 

1984). 

Cyathus 

The fruit bodies of C. olla can be found in autumn 

growing amongst cereal stubble. Cyathus striatus, 

recognized by the furrowed inner wall of its 

cups, grows on old stumps and twigs whilst 

C. stercoreus grows on old dung patches. This last 

species can be made to fruit readily if mycelium

GASTEROMYCETES IN THE EUAGARICS CLADE 

583 

Fig 20.3 Lycoperdon pyriforme. (a) L.S. gasterocarp. (b) Portion of peridium and gleba. Note the pseudoparenchymatous 

exoperidium and the fibrous endoperidium. (c) Portion of gleba showing basidia, thin-walled hyphae and capillitium threads. 

grown on a mixture of cow dung and straw 

is covered with a thin layer of casing soil and 

then left at room temperature for a few weeks 

(Fig. 20.2d; Webster & Weber, 1997). The fungus 

can also fruit on agar media (Lu, 1973). Light is 

essential for fruit body formation. Since the 

peridioles retain viability for many years if 

frozen, C. stercoreus provides a convenient example 

to study. 

The first sign of fruit body development is the 

appearance of brown mycelial cords at the soil 

surface, on which knots of hyphae differentiate. 

In young gasterocarps, the mouth of the funnel 

is closed over by a thin papery epiphragm 

(Figs. 20.2d, 20.4a) which ruptures as the fruit 

body expands. Within the funnel, the peridioles 

develop. They are lens-shaped, slate-blue in 

colour and attached to the peridium by a 

complex funiculus. In earlier stages of development 

in this and other species of Cyathus, the 

peridioles are separated by thin-walled hyphae 

which disappear at maturity (Walker, 1920). The 

peridiole wall consists of an outermost layer 

(tunica) made up of loosely interwoven hyphae, 

a dark cortex, and an inner layer of thick-walled 

but hyaline cells (Fig. 20.4g). The fertile centre of 

the peridiole is made up of thin-walled hyphae 

(‘nurse hyphae’) between which basidia develop. 

The basidia form 4 8 basidiospores and disappear 

soon afterwards, but the spores continue to 

enlarge and become thick-walled (Fig. 20.4g). 

Most of the nurse hyphae also break down, 

possibly providing nutrients for the enlarging 

spores.


Fig 20.4 Cyathus stercoreus. (a) Section of immature gasterocarp showing peridioles. (b) Gasterocarp cut open and pinned back to 

show the attachment of the peridioles. (c e) Details of structure of funiculus. (c) Condition of funiculus before stretching. 

(d) Stretched funiculus.Note the funicular cord within the purse. (e) Funicular cord extended after rupture of the purse.The base of 

the funicular cord is frayed out to form the hapteron. (f) Portion of funicular cord. Note the spirally coiled hyphae.The thickenings 

are modified clamp connections. (g) Detail of peridiole wall and contents (b, basidiospore; c, cortex; e, epiphragm; em, 

emplacement;f,funiculus;f.c.,funicularcord;h,hapteron;m.c.,mylialcords;m.p.,middlepiece;p,peridiole;pu,purse;s,sheath; 

t, tunica). 

The gasterocarps of Cyathus and Crucibulum 

have been aptly termed splash cups because the 

peridioles are splashed out by the action of rain 

drops to distances of over 1 m. The key to 

understanding the mechanism of discharge lies 

in the structure of the funiculus. In Cyathus 

(Figs. 20.4d,e), the funiculus is made up of several 

characteristic structures (see Brodie, 1975). 

The sheath is a tubular network of hyphae 

attached to the inner surface of the gasterocarp. 

It terminates in the middle piece where the 

innermost hyphae of the sheath unite to form a 

short cord. The middle piece flares out at its top 

where its hyphae are attached to a cylindrical sac, 

the purse, which is firmly attached to the 

peridiole at a small depression. Folded up 

within the purse is a long strand of spirally 

coiled hyphae, the funicular cord (Fig. 20.4f). The 

free end of the funicular cord is composed of a 

tangled mass of adhesive hyphae, the hapteron. 

Rain drops, which may be as much as 4 mm in 

diameter and have a terminal velocity of about 

8ms 1 , fall into the cup. Drops of this size 

are most likely to drip from the woodland 

canopy (Savile & Hayhoe, 1978). The force creates 

a strong upward thrust which tears open the

GASTEROMYCETES IN THE BOLETOID CLADE 

585 

purse. The funicular cord, spirally coiled up 

within the purse, swells explosively, stretching to 

a length of about 2 3mm in C. stercoreus, whilst 

in C. striatus it may be as long as 4 12 cm. As the 

peridiole is flicked away, the sticky hapteron 

at the base of the funicular cord helps to 

attach the peridiole to surrounding vegetation, 

and the momentum of the peridiole may cause 

the funicular cord to wrap around objects. 

Peridioles of C. stercoreus are presumably eaten 

by herbivorous animals and it is known that the 

basidiospores on release from the peridiole are 

stimulated to germinate by incubation around 

37°C. Whether animals play a significant role 

in the dispersal of other bird’s nest fungi is 

uncertain. The funiculus of Crucibulum is different 

from that of Cyathus, with a longer middle 

piece, a very short purse, and a funicular cord 

which is composed of relatively few hyphae only 

slightly coiled. 

Both Cyathus and Crucibulum show tetrapolar 

heterothallism with relatively few alleles 

(generally not more than 15) at each locus, and 

this is the most usual condition within the 

Nidulariaceae (Burnett & Boulter, 1963; Lu, 1964). 


boletoid clade 

The boletoid clade, as defined by molecular 

phylogeny (Hibbett & Thorn, 2001), contains 

fungi with a wide range of fruit body types, 

including lamellate (e.g. Paxillus), boletoid 

(e.g. Boletus, Leccinum, Suillus, Xerocomus) and 

resupinate forms (e.g. Coniophora, Serpula). These 

have been described previously (Section 19.5). 

Gasteromycete fungi have arisen from boletoid 

ancestors on several occasions, with the family 

Sclerodermataceae having an affinity with 

Gyroporus in a ‘boletoid’ branch, and the 

Rhizopogonaceae with Suillus (‘suilloid’ branch; 

Grubisha et al., 2001; Binder & Bresinsky, 2002). 

Both families contain mainly ectomycorrhizal 

fungi (see Table 20.1). 

Features of their association with tree roots 

are typical of members of the boletoid clade in 

that there is a large amount of fungal biomass 

extending from the mantle into the soil by 

means of mycelial cords or rhizomorphs which 

may be several metres long. This type of 

ectomycorrhiza appears to be particularly effective 

in exploiting a large volume of soil for 

nutrients, and it is also credited with improving 

the water status and thus the performance of the 

tree host under conditions of drought (Smith & 

Read, 1997; Agerer, 2001). The ability to form an 

extensive rhizomorph system may explain why 

mycorrhizal gasteromycetes belonging to the 

boletoid clade are particularly prominent in dry 

habitats. It is probable that long-distance transport 

processes in rhizomorphs are facilitated by 

peristaltic movement through a system of tubular 

vacuoles (Fig. 1.9; Ashford & Allaway, 

2002). Certain ectomycorrhizal fungi such as 

Rhizopogon, Scleroderma and Pisolithus can be 

grown in pure culture, and basidiospore inoculum 

from their relatively large fruit bodies is also 

easily collected and stored. Hence, these species 

are suitable for laboratory-based research as well 

as inoculation of trees prior to outplanting into 

forestry situations. 

In addition to the morphology of ectomycorrhiza, 

there are several further features betraying 

an affinity of the Sclerodermataceae and 

Rhizopogonaceae with the boletoid clade. For 

instance, pulvinic acid-type pigments typical of 

Boletus, Suillus and Xerocomus (see Fig. 19.22) are 

also found in their gasteromycete relatives, 

either in a pure form (e.g. variegatic acid, 

xerocomic acid) or as derivatives (Gill & 

Watling, 1986; Gill & Steglich, 1987; Winner 

et al., 2004). Further, the mycoparasitic mould 

Apiocrea chrysosperma (anamorph Sepedonium 

chrysospermum), which frequently forms a 

golden yellow conidial crust on fruit bodies of 

Boletus, Suillus, Xerocomus and Paxillus (Plate 9h), 

also infects gasteromycetes such as Scleroderma 

and Rhizopogon (see Gill & Watling, 1986). 

Pathogens may be competent taxonomists! 

20.4.1 Sclerodermataceae: earth balls and 

relatives 

This family comprises some 50 species in 

7 genera (Kirk et al., 2001), including the earth 

ball Scleroderma, the stalked puffball Calostoma,


the dye ball Pisolithus, and the barometer 

earth star Astraeus. Binder and Bresinsky (2002) 

have examined the phylogeny of the group 

and have recommended its partitioning into 

several families. All members seem to be ectomycorrhizal 

with trees. Here we shall consider 

the two most important genera, Pisolithus and 

Scleroderma. 

Pisolithus 

The best-known species is P. tinctorius (¼ 

P. arhizus), which is so called because its 

immature gasterocarps, when injured, produce 

an intense black dye (see Plate 11b). Because of 

the variability of gasterocarp appearance, the 

taxonomy of Pisolithus has been problematic, and 

initially P. tinctorius was thought to be of panglobal 

distribution, capable of associating with 

almost any ectomycorrhiza-forming tree species 

(Marx, 1977). Pisolithus is now known to consist of 

more than 10 species (Cairney, 2002; Martin et al., 

2002), with P. tinctorius distributed throughout 

the Northern Hemisphere and associated mainly 

with Pinus and Quercus. The centre of evolution of 

the genus is probably Australia, and P. marmoratus 

associated with Eucalyptus is regarded as the 

Southern Hemisphere equivalent of P. tinctorius. 

This and other species have been spread to South 

America, South East Asia and Africa, together 

with their host trees (Eucalyptus, Acacia) which are 

used in intensive forestry and in reforestation 

programmes (Dell et al., 2002; Martin et al., 

2002). In addition to this anthropogenic dispersal, 

there is also evidence that Pisolithus can travel 

long distances as air-borne basidiospores, e.g. 

from Australia to New Zealand (Moyersoen et al., 

2003). 

Pisolithus spp. may be displaced by other 

ectomycorrhizal fungi in cool, wet situations 

(McAfee & Fortin, 1986) but are prominent in 

extreme environments, e.g. dry habitats with 

sandy soil, or areas polluted with heavy metals 

(Walker et al., 1989; Smith & Read, 1997). In such 

situations, the growth of mycorrhizal trees can 

be increased several-fold relative to uninoculated 

controls. Benefits of Pisolithus infections to the 

host tree include enhanced provision of nutrients 

and water, detoxification of heavy 

metals, and protection against soil-borne plant 

pathogens. The considerable promise of Pisolithus 

is reflected by an immense body of literature 

which has been summarized admirably by 

Cairney and Chambers (1997) and Chambers 

and Cairney (1999). 

Pisolithus has a tetrapolar mating system 

(Kope & Fortin, 1990), and although monokaryons 

can infect tree roots, a full-scale ectomycorrhizal 

association requires a dikaryotic 

mycelium. The establishment of a mycorrhiza 

proceeds in several steps. Chemotropic growth of 

Pisolithus hyphae towards host root tips is 

followed by the secretion of glycoprotein fibrils 

by the fungus during initial contact (Lei et al., 

1990). Dead or moribund cells in the root cap 

region are infected first; the mantle is then 

established within 48 h, and a Hartig net formed 

subsequently (Horan et al., 1988; Lei et al., 1990). 

Only root material grown after initial contact is 

colonized. Rhizomorphs radiate outwards for 

several metres, and these may partly account 

for the success of the Pisolithus mycorrhiza, 

especially in dry habitats. Another factor may 

be the formation of sclerotia which enable the 

fungus to survive adverse conditions in the soil 

(Grenville et al., 1985). Eventually, fruit body 

initials are formed in the soil, with the maturing 

gasterocarps pushing through the surface. 

Basidiospores are produced inside numerous 

peridioles which disintegrate to release their 

spores passively (Plate 11b). The formation and 

maturation of peridioles proceeds from the tip 

to the base of the gasterocarp which gradually 

breaks up in the process. Gasterocarps can be 

sizeable, up to 20 cm tall. 

Studies on Pisolithus mycelia in Australian 

eucalypt forests have revealed that genetically 

distinguishable individuals (genets) may be 

variable in size, ranging from less than 2 m 2 to 

50 m 2 or more. Since these are interspersed, 

the smaller genets are interpreted as the result 

of recent re-colonization events from winddispersed 

basidiospore inoculum (Anderson 

et al., 1998, 2001). 

Scleroderma 

There are about 25 species of Scleroderma (Sims 

et al., 1995), three common temperate examples 

being S. bovista, S. citrinum (Fig. 20.5) and

GASTEROMYCETES IN THE BOLETOID CLADE 

587 

Fig 20.5 Scleroderma citrinum. (a) Maturing gasterocarps, about 3 6 cm in diameter.One has been cut open to reveal the gleba 

containing purplish-black basidiospores. (b) Old gasterocarps.The peridium has cracked open, permitting passive dispersal of the 

black basidiospore mass. 

In mature gasterocarps, the peridium is 

apparently a single, fairly thick layer. Although 

the glebal mass may be traversed by a system 

of sterile veins, there is no columella and 

no capillitium. The basidiospores are sessile 

(Fig. 20.6). When the gasterocarp is ripe, it 

cracks open irregularly and the dry spores 

escape (Fig. 20.5b). There is no well-developed 

bellows mechanism as in Lycoperdon (p. 579) or 

Geastrum (p. 588). 

Fig 20.6 Scleroderma verrucosum. Basidia and basidiospores. 

Note that the spores are almost sessile. 

S. verrucosum (Pegler et al., 1995). Earth balls are 

found in the autumn in acid woodlands and 

heaths under such trees as Pinus, Betula, Quercus 

and Fagus with which they form ectomycorrhizal 

associations. Mycorrhizal infection is easily 

reproduced under laboratory conditions, using 

aqueous spore suspensions (Parladé et al., 

1996). General aspects of mycorrhiza involving 

Scleroderma have been reviewed by Jeffries (1999). 

20.4.2 Rhizopogonaceae: beard truffles 

This family comprises some 150 species in 

4 genera. By far the most important genus is 

Rhizopogon, which is mycorrhizal mostly 

with coniferous trees. It originates from the 

Northern Hemisphere, with an unusually high 

diversity of species encountered in the Pacific 

Northwest where several host trees are native 

(Martín, 1996; Molina et al., 1999). Rhizopogon is 

related to Suillus in the boletoid clade (Grubisha 

et al., 2001). 

Rhizopogon 

Members of this genus form gasterocarps which 

resemble those of Scleroderma but are hypogeous, 

arising from mycelial cords (Plate 11c). 

The gasterocarps may be eaten by burrowing


mammals, and basidiospores pass through their 

digestive tracts unharmed (Colgan & Claridge, 

2002). Rhizopogon luteolus and R. roseolus are 

common and cosmopolitan under Pinus spp., 

whereas R. vinicolor and others are specific 

associates of Douglas fir (Pseudotsuga menziesii). 

Reviews of the genus have been written 

by Molina and Trappe (1994) and Molina 

et al. (1999). 

Rhizopogon spp. provide similar benefits to 

their hosts as Pisolithus and are the subject of 

research and development activities in forestry. 

Inoculation is readily achieved by dusting seeds 

with basidiospores or immersing the roots of 

seedlings in spore suspensions (Parladé et al., 

1996). Although Rhizopogon spp. can be grown in 

pure culture, inoculation of host tree seedlings 

with mycelium is not generally efficient with 

this and related fungi, unless the hyphae are 

protected from mechanical damage, for example, 

by being grown inside porous or gel-like beads 

(see Smith & Read, 1997). 


gomphoid phalloid clade 

The gomphoid phalloid clade contains some 

350 species of morphologically diverse fungi 

(Hibbett & Thorn, 2001). Most of the species 

with active basidiospore discharge form coral- or 

club-shaped basidiocarps, e.g. Ramaria (see Plate 

10h), Clavariadelphus and Gomphus. Several groups 

of well-known gasteromycetes also belong here 

(Hibbett et al., 1997b; Humpert et al., 2001), and 

these show the most spectacular spore dispersal 

mechanisms of all gasteromycetes, including 

the bellows mechanism, insect dispersal, and 

active discharge of peridioles. Details of the 

phylogeny or evolutionary history of these 

gasteromycetes still appear to be unknown, 

although some groups such as earth stars may 

be ancient (Krassilov & Makulbekov, 2003). 

Members of the gomphoid phalloid clade are 

mostly saprotrophic on wood, other plant debris 

and humus, extending to the soil by means of 

mycelial cords. 

20.5.1 Geastraceae: earth stars 

There are some 50 species of earth stars. 

Descriptions of the common species may be 

found in the keys by Ellis and Ellis (1990) and 

Pegler et al. (1995). One of the most frequent and 

widespread species in temperate and subtropical 

forests is Geastrum triplex (Fig. 20.7a) which grows 

in the leaf litter of beech, sycamore and pine. The 

young fruit body is onion-shaped and develops at 

or just below the soil surface. The exoperidium is 

complex, consisting of a brown outer layer made 

of narrow hyphae mostly running longitudinally, 

and a paler pseudoparenchymatous inner 

layer. As the fruit body ripens, the whole of the 

exoperidium splits open from the tip in a stellate 

fashion and, due to swelling of the pseudoparenchyma 

cells of the exoperidium, the triangular 

flaps curve outwards and make contact with the 

soil, lifting the inner part of the fruit body into 

the air (Fig. 20.7a). The thin, papery endoperidium 

opens by an apical pore. Spores are puffed 

out by the bellows mechanism when rain drops 

strike the endoperidium (Ingold, 1971). The 

gleba contains a columella (sometimes termed 

a pseudocolumella) and capillitium, much as in 

the puffball Lycoperdon (Fig. 20.3) with which 

Geastrum is not related. Basidial development can 

only be observed in young unexpanded gasterocarps. 

The basidia are pear-shaped, with 4 6 

(sometimes up to 8) spores borne on a knob-like 

extension of the pointed end. 

20.5.2 Sphaerobolus 

Sphaerobolus is unique among gasteromycetes in 

that it has developed an active discharge 

mechanism of peridioles (glebal masses), thereby 

reversing the loss of active basidiospore liberation. 

The precise taxonomic position of 

Sphaerobolus is still unclear at present; formerly 

grouped together with the bird’s nest fungi 

(p. 578), it is now known to belong to the 

gomphoid phalloid clade. Kirk et al. (2001) have 

included it in the Geastraceae. 

Sphaerobolus stellatus forms globose orange 

gasterocarps about 2 mm in diameter. They are 

attached to rotten wood, rotting herbaceous 

stems, sacking and weathered dung of herbivores 

such as cow and sheep. Ripe fruit bodies open

GASTEROMYCETES IN THE GOMPHOID PHALLOID CLADE 

589 

Fig 20.7 Gasteromycetes belonging to the gomphoid phalloid clade. (a) The earth star Geastrum triplex.(b)Sphaerobolus stellatus. 

Stages of maturation can be seen from left (immature gasterocarp) through the centre (two opened gasterocarps exhibiting glebal 

masses) to right (discharged gasterocarp with everted inner cup). (c) The veiled stinkhorn, Phallus indusiatus.This beautiful species is 

called ‘queen of mushrooms’ (kinoko no joou) in Japan. (d) The dog’s stinkhorn, Mutinus caninus. (b) reproduced from Webster and 

Weber (1999), with permission from Elsevier.Original print of (c) kindly provided by N.Tuno. 

to form a star-like arrangement of two cups 

fitting inside each other, attached only by the 

triangular tips of their teeth (Fig. 20.7b). Within 

the inner cup is a single brown peridiole or 

glebal mass about 1 mm in diameter. By sudden 

eversion of the inner cup, the peridiole is 

projected for a considerable distance. Buller 

(1933) has given a detailed account of peridiole 

discharge. He showed that the peridiole could be 

projected vertically for more than 2 m, and 

horizontally for over 4 m, with the record 

currently standing at 5.7 m (Ingold, 1971, 1972). 

The fungus can be cultivated if a peridiole is 

placed in a plate of oatmeal agar, and gasterocarps 

are produced after a few weeks’ incubation 

in daylight on this medium or on chopped 

straw saturated with a nutrient solution (Flegler, 

1984; Webster & Weber, 1999). 

A section through an almost mature, but 

unopened, gasterocarp is shown in Fig. 20.8a. The 

peridiole is surrounded by a peridium in which 

six layers can be distinguished. Three of these 

layers form the structure of the outer cup. The 

three layers making up the inner cup consist of 

an outer layer of tangentially arranged interwoven 

hyphae, a central layer of radially elongated 

cells forming a kind of palisade, and a thin 

innermost layer of pseudoparenchyma whose 

cells undergo deliquescence before glebal 

discharge to form a liquid which bathes the 

gleba and lies in the bottom on the inner cup. 

Before the gasterocarp opens up, the cells of the 

palisade layer are rich in glycogen, but this is 

converted to glucose during ripening (Engel & 

Schneider, 1963). Intracellular accumulation of 

glucose causes the osmotic concentration of 

the cells to rise so that they absorb water and 

become more turgid. The swelling of the palisade 

layer is restrained by the tangentially arranged 

hyphae, and this sets up strains within the 

tissues of the inner cup which are only released 

by its turning inside out. 

Light is necessary for development, and the 

opening of the fruit body is phototropic,


Fig 20.8 Sphaerobolus stellatus. (a) V.S. of nearly ripe gasterocarp showing the central glebal mass (peridiole) surrounded by a 

six-layered peridium. (b) Details of the peridial layers:1, outermost layer composed of interwoven hyphae; 2, layer in which the 

hyphae are separated by extensive mucilage; 3, pseudoparenchymatous layer; 4, fibrous layer; 5, palisade layer; 6, layer of lubricating 

cells; gl, outer layers of glebal mass. (c) Enlarged portion of layers 4 6 and portion of the glebal mass: c, cystidia; g, gemmae; 

b, basidiospores. (d) Clusters of basidia from unripe gasterocarps.There are usually 4 6 basidiospores. (e) Gemmae. 

(f) Basidiospores. (c, e) and (f) to same scale. 

ensuring that the glebal mass is projected 

towards the light (Alasoadura, 1963). Peridiole 

discharge follows a diurnal rhythm, with 

release occurring during the light phase. In 

continuous light rhythmic discharge ceases, but 

in continuous darkness a culture previously 

exposed to alternating periods of 12 h of light 

and darkness continues to discharge peridioles 

rhythmically at times corresponding to the 

previous light periods, indicating an endogenous 

circadian rhythm. 

The spherical peridiole (glebal mass) is 

surrounded by a dark brown sticky coat derived 

from the breakdown of the cells of the innermost 

peridial layer. Immediately within the brown 

outer coat of the glebal mass are layers of rounded 

cells sometimes termed cystidia (Fig. 20.8c). 

Apparently these cells are incapable of germination 

and their function is not known. The rest of 

the glebal mass consists of oval thick-walled 

haploid basidiospores and thinner-walled dikaryotic 

gemmae. About 4 8 basidiospores develop 

on the basidia some 2 days before discharge (Fig. 

20.8d), but the basidia disappear as the glebal 

mass ripens. Gemmae arise either terminally or in 

an intercalary position on hyphae within the 

glebal mass. Oil-rich cells are also present. The 

sticky peridiole adheres readily to objects on 

which it is impacted, and after drying it is very 

difficult to dislodge even by a jet of water. 

Peridioles are viable for several years. Projectiles 

adhering to herbage may be eaten by animals, and 

this may explain the presence of fruit bodies on 

dung. 

On germination the peridioles give rise to 

clamped hyphae which usually arise directly from 

the gemmae and not from the basidiospores. Most 

basidiospores, if they germinate, give rise to 

mycelia with simple septa. Pairings of monosporous 

mycelia have indicated that the fungus is 

usually heterothallic, although details of the 

mating system still appear unclear at present. 

20.5.3 Phallaceae: stinkhorns 

An original solution to the problem posed by the 

loss of active basidiospore discharge has been 

developed also by members of the Phallaceae 

which attract insects, especially cadaverfeeding 

flies such as bluebottles, to visit their 

gasterocarps. Attraction may be by the emission

GASTEROMYCETES IN THE GOMPHOID PHALLOID CLADE 

591 

of a cadaverous smell or by colour, with gasterocarps 

of species like Clathrus ruber (Plate 11e) and 

C. archeri (Plate 11f) appearing dark red due to the 

accumulation of carotenoids, chiefly lycopene 

(Fiasson & Petersen, 1973; Gill & Steglich, 1987). 

There may be a synergism of attractions because 

species with brightly coloured gasterocarps tend 

to emit less evil smells than dull-coloured ones. 

Common temperate examples of Phallaceae 

are the graphically named stinkhorn Phallus 

impudicus (Lat. impudicus ¼ shameless; Plate 11d) 

and the dog’s stinkhorn Mutinus caninus 

(Fig. 20.7d). 

Phallus 

In late summer and autumn, stinkhorns can 

be detected readily by their smell. They can be a 

common or even dominant component of the 

population of basidiocarps on the forest floor, as 

shown by Shorrocks and Charlesworth (1982) who 

estimated some 50 000 70 000 gasterocarps km 2 

per season in a woodland. In such situations, 

stinkhorns and their primordia, the ‘eggs’, 

provide a major breeding ground for mycophagous 

flies. Eggs of P. impudicus are about 5 cm in 

diameter and develop from an extensive system of 

white mycelial cords which can be traced underground 

to a buried tree stump (see Fig. 1.12b; 

Grainger, 1962). A longitudinal section of an egg 

(Fig. 20.9a) shows a thin papery outer and inner 

peridium and a wider mass of jelly making up the 

middle peridium. The central part of the gasterocarp 

is differentiated into a cylindrical hollow 

stipe and a folded honeycomb-like receptacle 

which bears the fertile part of the gleba. Within 

the young gleba are cavities lined by basidia 

bearing up to nine spores (Fig. 20.9b), but as the 

glebal mass ripens the basidia disintegrate. 

Gasterocarps expand very rapidly: within a few 

hours the stipe may elongate from about 5 cm to a 

length of 15 cm or more, leaving behind the 

peridial remains as a volva at its base. 

A demonstration of gasterocarp erection in the 

laboratory by incubation of freshly collected ripe 

eggs in a moist chamber rarely fails to impress. 

The sudden expansion is probably at the expense 

of water stored within the jelly of the middle 

peridium. The mean weight of expanded stipes is 

more than twice that of unexpanded ones (Ingold, 

1959). Expansion of the stipe of P. impudicus is 

accompanied by breakdown of glycogen and its 

conversion to sugar (Buller, 1933). A similar 

conversion has been reported in P. indusiatus 

(Fig. 20.7c) in which cells of the unexpanded 

stipe are folded but expand to almost 12 times 

their original volume during stipe elongation 

(Kinugawa, 1965). 

At about the same time as the stipe of 

P. impudicus is elongating, the fertile glebal mass 

begins to release strong-smelling volatile 

substances which are attractive to flies, especially 

bluebottles (Plate 11d). Depending on the analytical 

methods used, the smell has been attributed 

to a range of substances including methylmercaptan 

and hydrogen sulphide (List & Freund, 

1968) or dimethyl disulphide (see Fig. 15.4) and 

dimethyl trisulphide (Borg-Karlson et al., 1994). 

Once a fly has located a gasterocarp, it is 

presented with the dark green glebal 

mass of basidiospores embedded in a liquid 

which contains sugars and also sweet-smelling 

substances such as phenylacetaldehyde and 

phenylethanol. Flies feed on the spore mass 

which is removed within a few hours, leaving 

behind the pale receptacle. The ingested basidiospores 

are defaecated, apparently unharmed, 

onto surrounding vegetation and the soil, often 

within a short time of ingestion. Tuno (1998) 

found that the gut of fruitflies (Drosophila spp.) 

feeding on P. indusiatus and P. duplicatus contained 

up to 240 000 basidiospores, and that of the larger 

muscid flies up to 1.7 million. Basidiospore 

germination was unaffected by passage through 

the gut. However, it is unknown how the 

mycelium from germinating basidiospores 

succeeds in reaching fresh tree stumps, and 

clonal spread by mycelial cords may be an 

important additional mode of reproduction. 

There have been few studies of the nutrition 

and physiology of Phallus, but P. ravenelii has 

been shown to make good vegetative growth on 

a wide range of carbohydrates, and to require 

thiamine (Howard & Bigelow, 1969). The veiled 

stinkhorns P. indusiatus (Fig. 20.7c) and P. duplicatus 

are grown in China as a culinary 

speciality. Expanded fruit bodies are produced 

commercially from inoculated wood both in 

woodlands and indoors, and are marketed in a


Fig 20.9 Phallus impudicus. (a) L.S.‘egg’ showing the 

unexpanded stipe. (b) Basidia. 

dried form; sensibly, the volva and glebal mass are 

removed prior to marketing (Chang & Miles, 

2004). Apparently, the egg stage is also eaten 

after it has been boiled. These species were 

formerly thought to belong to a separate genus, 

Dictyophora, on the basis of the presence of a veil. 

However, this character is no longer considered 

useful because even the common stinkhorn may 

occasionally produce a short veil and is then 

called P. impudicus var. togatus (see Kibby & 

Bingham, 2004). 

Other genera 

The general form of Mutinus, the dog’s stinkhorn, 

is similar to Phallus, but the gasterocarps are 

smaller (Fig. 20.7d). The upper part of the stipe is 

orange in colour, and the smell is less overpowering. 

The receptacle bearing the glebal mass 

is not reticulate. 

Clathrus ruber (Plate 11e) forms conspicuous, 

red cage-like gasterocarps in warm, dry 

habitats in the Mediterranean, occasionally 

extending to temperate climates. Other Clathrus 

spp. are tropical. Clathrus archeri, the squid 

fungus, was probably introduced to Europe 

from Australia some 100 years ago 

(Ramsbottom, 1953) and is now established 

in many localities. An even more bizarre 

Australian species is Aseroe rubra, the starfish 

fungus (Plate 11f).

21 

Heterobasidiomycetes 


The class Heterobasidiomycetes is approximately 

synonymous with the terms ‘Phragmobasidiomycetes’ 

or ‘jelly fungi’ and contains fungi with 

the following characteristics. 

1. The dolipore septum is complex, i.e. it is 

surrounded by a parenthesome. Parenthesomes 

are also found in the Homobasidiomycetes (Chapters 

19 and 20), but not in the Urediniomycetes 

(Chapter 22) and Ustilaginomycetes (Chapter 23). 

2. The basidia of Heterobasidiomycetes may 

be strongly lobed and often divided by transverse, 

oblique or longitudinal septa. Such basidia are 

loosely termed heterobasidia, especially if they 

arise directly from hyphae instead of teliospores 

as in most Urediniomycetes and Ustilaginomycetes. 

If the basidia are septate, they are also 

called phragmobasidia. The sterigma of the 

heterobasidium is unusually prominent and is 

often termed epibasidium (Martin, 1945). In 

contrast, the basidia of Homobasidiomycetes 

are club-shaped and always single-celled. 

3. The fruit bodies of most Heterobasidiomycetes 

are simpler in architecture than those of 

Homobasidiomycetes, and the hymenium is not 

normally protected by a roof- or shelf-like architecture. 

In compensation, these simple fruit 

bodies are generally able to survive drying and 

rehydration, with fresh crops of basidiospores 

produced after each rehydration event. Fully 

hydrated basidiocarps are typically greatly 

swollen and gelatinous, hence the term ‘jelly 

fungi’ for the Heterobasidiomycetes. 

4. The basidiospores of most species are 

capable of producing secondary spores which 

may be ballistoconidia, passively released conidia 

or yeast cells. 

Species included in this class show considerable 

morphological diversity, and taxonomic 

concepts have been in a state of flux. The first 

workers to emphasize the importance of basidial 

morphology were Patouillard (1887) and 

Brefeld (1888). Most orders currently included 

were placed here by Martin (1945) and Bandoni 

(1984), and these are listed in Table 21.1. 

The inclusion of these groups is supported 

by DNA-based phylogenetic studies (Weiss & 

Oberwinkler, 2001). The life cycles of Heterobasidiomycetes, 

as far as they are known, show 

an alternation of monokaryotic and dikaryotic 

stages. The two broad subclasses, Heterobasidiomycetidae 

and Tremellomycetidae, can be distinguished 

by their monokaryotic phase being 

mycelial or yeast-like, respectively. All heterobasidiomycete 

yeasts discussed in Chapter 24 

seem to belong to the Tremellomycetidae 

(Wells & Bandoni, 2001). Thorough and authoritative 

circumscriptions of the Heterobasidiomycetes 

have been written by Wells (1994) and Wells 

and Bandoni (2001). 

Ecologically, Heterobasidiomycetes are associated 

with wood and other decaying plant 

matter, either as saprotrophs or as mycoparasites 

of saprotrophic fungi. Some species, especially 

in the Ceratobasidiales (Section. 21.2), play dual 

roles as necrotrophic pathogens of various plants 

and mycorrhizal associates of orchids. Heterobasidiomycetes 

are mainly terrestrial.

594 HETEROBASIDIOMYCETES 

Table 21.1. Orders and selected genera currently 

included in the Heterobasidiomycetes. After Wells 

and Bandoni (2001). 

Subclass Heterobasidiomycetidae 

1. Ceratobasidiales (see below) 

Ceratobasidium (anam. Rhizoctonia ¼ Ceratorhiza). 

Thanatephorus (anam. Rhizoctonia ¼ Moniliopsis). 

2. Tulasnellales (see Fig. 21.1b) 

Tulasnella (anam. Rhizoctonia) 

3. Dacrymycetales (p. 598) 

Calocera 

Dacrymyces 

Ditiola 

4. Auriculariales (p. 601) 

Auricularia 

Exidia 

Pseudohydnum 

Sebacina 

SubclassTremellomycetidae 

1. Tremellales (p. 60 4) 

Cryptococcus and Bullera (yeast forms;Table 24.1) 

Filobasidiella neoformans (see p.660) 

Tremella 

2. Christianseniales 

3. Filobasidiales (yeast forms; seeTable 24.1) 

4. Cystofilobasidiales (seeTable 24.1) 

Itersonilia (see p.493) 

Phaffia, Xanthophyllomyces (see p.665) 

5. Trichosporonales (yeastforms; seeTable 24.1) 

21.2 Ceratobasidiales 

The most important members of this family 

belong to the anamorph genus Rhizoctonia which 

we shall consider in detail. Sneh et al. (1996) 

and Roberts (1999) have compiled important 

reference works on this group. The secondary 

hyphae of Rhizoctonia have conspicuous dolipore 

septa which are visible even with the light 

microscope (Tu et al., 1977). Electron microscopy 

studies have revealed the parenthesomes to be 

perforated by several large pores (Müller et al., 

1998b). Clamp connections are not found in 

Rhizoctonia but may be present in other members 

of the order. The hyphae of Rhizoctonia are highly 

characteristic. Branches typically arise at a right 

angle to the leading hypha, with the branch 

point slightly constricted and a septum located a 

little way into the branch (Fig. 21.2a). Depending 

on the species, the compartments of vegetative 

hyphae are binucleate or multinucleate; uninucleate 

hyphae are uncommon. Teleomorphic 

states are rare and conidia are not produced, 

but sclerotia of the loose type (see Fig. 1.16a) are 

frequently seen. The form-genus Rhizoctonia has 

now been broken up into several taxa which 

correlate with different teleomorphs (Moore, 

1987; Andersen & Stalpers, 1994). For instance, 

Moniliopsis has multinucleate hyphae and is 

referred to the teleomorph genus Thanatephorus 

whereas the hyphae of Ceratorhiza (teleomorph 

Ceratobasidium) are binucleate (Tu et al., 1977; 

Vilgalys & Cubeta, 1994). Fungi resembling 

Rhizoctonia transgress the boundaries of 

orders, with some teleomorphs referable to the 

Tulasnellales. Indeed, a few Rhizoctonia-like fungi 

have even been assigned to the Ascomycota. 

Whereas hyphae of Rhizoctonia are readily 

recognized as such, they offer few microscopic 

features for species identification, and a system 

based on anastomosis groups, i.e. the ability of 

a given isolate to undergo plasmogamy with 

hyphae of defined tester strains, has been 

developed (Sneh et al., 1991). Such pairings may 

yield three different responses, with intermediate 

reactions also possible. (1) In genetically 

identical or closely related strains, anastomosis 

leads to perfect fusion. (2) In less closely related 

members of the same anastomosis group, anastomosis 

is followed by death of the fusion cell due 

to vegetative incompatibility. (3) No anastomosis 

occurs between members of different anastomosis 

groups. The best-studied taxon, R. solani, 

contains about a dozen anastomosis groups, 

some of which have been further divided into 

subgroups according to biochemical or other 

criteria. Although the individual anastomosis 

groups within R. solani and other taxa (e.g. 

Ceratorhiza) correlate with phylogenetic clusters 

obtained by DNA-based phylogeny (Kuninaga 

et al., 1997; Gonzalez et al., 2001) and also to 

a certain extent with the range of plant hosts

CERATOBASIDIALES 

595 

affected (Sneh et al., 1991), the question of the 

boundaries of biological species remains unanswerable 

at present. 

The basidiocarps of Ceratobasidiales are thin, 

gelatinous and often resupinate. Their formation 

can sometimes be induced by covering an agar 

culture with soil (Warcup & Talbot, 1966). Hyphal 

tips due to develop into a probasidium are 

generally binucleate, and karyogamy is followed 

swiftly by meiosis. During the later stages of 

meiosis, four prominent sterigmata referred to 

as epibasidia are formed (Wells & Bandoni, 2001), 

but septa are not laid down, even in the mature 

basidium (Fig. 21.1a). The basidiospores are uninucleate 

and frequently germinate by repetition 

to produce uninucleate ballistoconidia. Eventually, 

hyphal germination occurs. Mating systems 

in the Ceratobasidiales are not well understood, 

and several species may be homothallic. 

The basidium of the Tulasnellales differs in 

that the four epibasidia become separated from 

the metabasidium by septation after meiosis. 

Maturation of the four epibasidia may occur at 

different times (Fig. 21.1b). 

21.2.1 Rhizoctonia in agriculture 

The most important taxon is R. (Moniliopsis) solani 

(teleomorph Thanatephorus cucumeris), which causes 

a wide array of soil-borne necrotrophic diseases 

especially of herbaceous plants including all 

kinds of vegetables, rice, turfgrasses, and less 

frequently also woody tree hosts (Adam, 1988; 

Agrios, 2005). The most common disease is 

damping off of seedlings in which the infected 

hypocotyl region becomes water-soaked and no 

longer provides structural integrity (see p. 95), 

leading to pre- or post-emergence death of 

the seedling. In older plants, infection may not 

immediately cover the entire circumference of 

the plant stem, so that cankers and girdling of the 

stem may result. Roots are also frequently 

infected, as are aerial plant organs in contact 

with the soil or exposed to watersplash from the 

soil surface. The fungus can survive in the soil 

for several years as small sclerotia about 1 3mm 

in diameter. These are often associated with 

the debris of host plants killed by the fungus. 

Sclerotia are occasionally seen as black scurf on 

the surface of potato tubers because they are not 

easily removed, even by assiduous washing. 

Rhizoctonia diseases are typically most severe 

at cool temperatures, presumably because the 

seedling stage of host plants is prolonged due 

to their slow growth. The infection process 

is similar to that of Gaeumannomyces graminis, 

i.e. hyphae branch and build up a cushion-like 

compound appressorium on the host plant 

surface, from which penetration is achieved. 

Fig 21.1 (a) Basidium of Thanatephorus cucumeris 

(Ceratobasidiales). Note the four prominent 

epibasidia and the lack of septation within the 

basidium. (b) Basidium of Gloeotulasnella cystidiophora 

(Tulasnellales) showing various stages of maturity. 

The epibasidia are separated from the metabasidium 

by septation.Three epibasidia have already 

discharged their basidiospore, with one about to 

produce it. (a) redrawn from Warcup and Talbot 

(1962) with permission from Elsevier, (b) redrawn 

from Wells and Bandoni (2001) with kind permission 

of Springer Science and Business Media.


Simple appressoria may also be formed. Several 

lytic enzymes including cellulases, pectinases 

and cutinases are involved in colonizing and 

degrading plant tissue. 

Another pathogenic species is Rhizoctonia 

cerealis (¼ Ceratorhiza cerealis, C. ramicola; teleomorph 

Ceratobasidium cornigerum ¼ C. cereale), 

which causes sharp eyespot of cereals. As in 

R. solani, infection is favoured by cool conditions, 

and the disease is more common on winter 

cereals than spring-sown varieties. The fungus 

overwinters on stubble as mycelium and sclerotia, 

and infections give rise to spindle-shaped 

eyespot lesions on stems and leaves. These differ 

from true eyespot caused by Tapesia yallundae 

(p. 439) in being more sharply demarcated, with a 

reddish-brown margin enclosing an inner greyish 

region. Crop losses in cereals due to R. cerealis are 

not generally severe so that chemical control is 

not practised specifically against sharp eyespot 

(Parry, 1990). Rhizoctonia cerealis also causes yellow 

or brown patches in swards of turfgrass, as well 

as root and foliar infections in a range of other 

crop plants (Kataria & Hoffman, 1988). 

Whereas chemical control of Rhizoctonia spp., 

like that of many other soil-borne pathogens, is 

difficult, biological control shows some promise. 

Several biocontrol organisms are effective under 

controlled laboratory and greenhouse conditions, 

including species of Bacillus, Serratia and 

Streptomyces, as well as 2,4-diacetylphloroglucinolproducing 

Pseudomonas spp. (see p. 385). The high 

efficacy of Trichoderma spp. against Rhizoctonia has 

been partially correlated with their secretion of 

cell wall-degrading enzymes, notably chitinases 

and b-(1,3)-glucanases (Innocenti et al., 2003; 

Markovich & Kononova, 2003). As in the case of 

the cereal take-all pathogen Gaeumannomyces 

graminis, certain soils can acquire the capacity 

to suppress Rhizoctonia after several consecutive 

cultivation cycles with the same crop (Henis et al., 

1979; Mazzola, 2002), and this has been attributed 

to the build-up of biocontrol organisms, especially 

Trichoderma and Pseudomonas spp. 

21.2.2 Rhizoctonia and orchid mycorrhiza 

Stimulating accounts of this topic have been 

written by Arditti (1992), Smith and Read (1997), 

Peterson et al. (1998) and Rasmussen (2002). 

All members of the plant family Orchidaceae 

(about 17 500 species) appear to be associated 

with mycorrhizal fungi at all stages of their life 

cycle in nature. In contrast to other types of 

mycorrhiza, there is a net flow of sugars from the 

fungal partner to the plant at least during the 

establishment of the orchid seedling. All colourless 

(non-photosynthetic) orchids continue to rely 

on this external supply throughout their lives, 

and even green orchids do not seem to share 

their photosynthetic products with the fungus 

(Alexander & Hadley, 1985). In orchid mycorrhiza, 

therefore, the plant parasitizes the fungus, 

and it is a curious fact that many of the fungi 

thus exploited are themselves serious plant 

pathogens, especially Rhizoctonia spp. (Roberts, 

1999). Indeed, the very Rhizoctonia strains isolated 

as pathogens of other plants (e.g. R. solani, 

R. cerealis) can support the germination of orchid 

seeds (Figs. 21.2b f). These as well as other 

species (e.g. R. goodyerae-repentis, R. repens) can 

also be isolated from mature orchid roots. Orchid 

mycorrhizal symbiosis therefore seems to be less 

specific than other forms of mycorrhiza 

(Masuhara et al., 1993). 

Orchid seeds are tiny and lack differentiated 

embryos or food reserves. In the absence of soluble 

external carbohydrates, they show only 

limited germination to form an intermediate 

stage called a protocorm. This may emit a few 

epidermal hairs before growth stalls (Fig. 21.2b). 

Further development of the protocorm (Fig. 21.2c) 

occurs only if a suitable soluble carbon source is 

added, or if a mycorrhizal fungus such as 

Rhizoctonia is allowed to grow from a food base 

(e.g. starch or cellulose) to the protocorm. Growth 

ensues even if the fungus is made to cross a 

barrier between the food base and the protocorms, 

thereby demonstrating net carbon translocation 

(Smith, 1966). This experiment is easily 

set up in the laboratory (Fig. 21.2d; Weber & 

Webster, 2001b). The main transport compound 

seems to be trehalose, and this may be hydrolysed 

to glucose and converted to sucrose by the plant 

(Smith, 1967; Smith & Read, 1997). 

Infection of the orchid protocorm is initiated 

through the epidermal hairs (Fig. 21.2e) or 

through the suspensor tissue at the base of

CERATOBASIDIALES 

597 

Fig 21.2 Rhizoctonia cerealis and its mycorrhiza with the heath spotted orchid (Dactylorhiza maculata ssp. ericetorum)inthe 

laboratory. (a) Vegetative hypha showing typical branching and dolipore septa (arrowheads). (b) Seeds of D. maculata on agar after 

ten weeks without Rhizoctonia. Protocorms with a few epidermal hairs have formed. (c) Seeds after ten weeks but with R. cerealis 

spreading from a food base.The protocorms have grown and are differentiating shoot tips (arrows). Same scale as (b). (d) The 

split-plate experiment. Rhizoctonia cerealis has been inoculated onto a food base (tissue paper, top half) which is separated from 

the orchid seeds by a partition.The fungus has overgrown this barrier, and the orchid protocorms are using the translocated sugars 

derived from the degraded cellulose; 13 weeks after inoculation. (e) Penetration of an epidermal hair by R. cerealis. (f) Penetration of 

R. cerealis hyphae through an epidermal hair into the cortex of a protocorm where pelotons have formed. (b) and (d f) reprinted 

from Weber and Webster (2001b), with permission from Elsevier. 

the seedling. Penetration of the wall of a cell 

in the protocorm cortex invaginates the plasmalemma 

and results in the formation of a peloton, 

i.e. a dense mass of coiled hyphae (Fig. 21.2f). 

Initially, each hypha is ensheathed by the host 

plasmalemma, which is called the perifungal 

membrane and is functionally modified from the 

plasmalemma of uninfected regions (Peterson & 

Currah, 1990; Peterson et al., 1996). An interfacial 

matrix of unknown composition is located 

between the perifungal membrane and the 

fungal cell wall. Within 24 h of formation, a 

peloton may begin to be degraded and is ultimately 

left behind as an amorphous clump 

of lysed hyphae surrounded by one continuous 

perifungal membrane (Hadley & Williamson, 

1971; Peterson & Currah, 1990). Any one 

orchid cell can become repeately re-infected


(Uetake et al., 1992), and the same protocorm, 

mature root or even individual cell can be 

colonized simultaneously by different fungi. 

The unstable nature of the orchid mycorrhiza 

is indicated by the quick and repeated cycle of 

peloton formation and degradation, and the 

several different outcomes of the orchid fungus 

interaction observed under laboratory conditions 

(Fig. 21.2d). A balanced mycorrhizal symbiosis 

will develop only in a proportion of 

protocorms, whereas other seeds of the same 

orchid species may be parasitized and killed by 

the fungus, or simply resist infection and stall in 

their development (Hadley, 1970; Smreciu & 

Currah, 1989; Beyrle et al., 1995). There is also 

vevidence of a succession of mycorrhizal fungi 

during the development of an orchid in nature, 

and the mycorrhizal fungi isolated from adult 

plants may not support protocorm growth and 

vice versa (Xu & Mu, 1990; Zelmer et al., 1996). 

Mature orchids may be associated with 

Rhizoctonia spp. and/or a range of other Basidiomycota, 

including saprotrophic (e.g. Mycena), 

necrotrophic (e.g. Armillaria; see p. 546) or 

ectomycorrhizal species related to Russula and 

Thelephora (Rasmussen, 2002). Ectomycorrhizal 

fungi transport carbohydrates from their tree 

host to the orchid, thus allowing green orchids 

to grow even in densely shaded woodland 

conditions (Taylor & Bruns, 1997; McKendrick 

et al., 2000; Bidartondo et al., 2004). Interestingly, 

these fungi form typical ectomycorrhiza with 

their tree hosts but pelotons in infected orchid 

roots (Zelmer & Currah, 1995). The orchid therefore 

calls the shots in its symbiosis with 

basidiomycetes, and peloton formation and 

degradation is traditionally interpreted as a 

balanced defence reaction of the orchid against 

invasion attempts by the fungus. 

21.3 Dacrymycetales 

This order is characterized by forked (furcate) 

basidia (Figs. 21.4 and 21.5), which are found in 

all species except Dacrymyces unisporus. The fruit 

bodies are coloured yellow or orange due to the 

presence of a wide range of carotenoids (for 

references, see Gill & Steglich, 1987). Fruit bodies 

are gelatinous and show a striking diversity of 

forms as exemplified by the cushion-like basidiocarps 

of Dacrymyces stillatus (Fig. 21.3) and the 

clavarioid ones of Calocera viscosa (Plate 11g). 

Not much is known about the life cycle of 

the Dacrymycetales, but it is presumed that 

the usual basidiomycete pattern of alternating 

mono- and dikaryotic stages operates. There are 

no clamp connections. The dolipore-type septa 

Fig 21.3 Fruit bodies of Dacrymycetales. (a) Basidial 

cushions of Dacrymyces stillatus on rotting wood. 

(b) Basidiocarps of Calocera cornea.

DACRYMYCETALES 

599 

Fig 21.4 Dacrymyces stillatus. (a) Basidiospores showing germination by germ tubes or formation of conidia (bottom). (b) Basidia. 

Note that the attached basidiospores are unicellular.They become three-septate on germination. (c) Arthrospores from a conidial 

pustule. 

are surrounded by parenthesomes without 

perforations (Wells, 1994). The probasidium 

arises from a dikaryotic hypha and is initially 

club-shaped. At this stage karyogamy occurs and 

is immediately followed by meiosis. Meanwhile 

the two epibasidia develop. Each of the two 

basidiospores seems to receive one nucleus, and 

the remaining two nuclei degenerate in the 

epibasidia (see Wells & Bandoni, 2001). Before 

the basidiospore germinates, it lays down one or 

more septa. Each spore segment can produce a 

haploid monokaryotic hypha or may give rise to 

conidia which in turn germinate by means of 

monokaryotic germ tubes (Ingold, 1983b). It is 

unclear in many species how and where dikaryotization 

occurs, but it is probably by fusion 

of monokaryotic hyphae. Mating systems, where 

known, are bifactorial (tetrapolar), i.e. with two 

mating type loci A and B. 

Members of the Dacrymycetales are saprotrophic 

on wood and cause brown-rots, although 

some lignin degradation has also been observed 

(Seifert, 1983; Worrall et al., 1997). The fruit 

bodies are common on decaying wood, including 

wood built into outdoor structures such as park 

benches or fences. There are about 70 species, 

and the order is monophyletic (Oberwinkler, 

1993). Reid (1974) has given keys and descriptions 

of the common British and European species. 

The seminal features of the order have been 

summarized by Wells (1994) and Wells and 

Bandoni (2001).


21.3.1 Dacrymyces 

Orange gelatinous cushions about 1 5mm in 

diameter, so common on damp rotting wood, 

are the fructifications of D. stillatus (Fig. 21.3a). 

Close inspection with a hand lens reveals that 

the fruit bodies are of two kinds: soft, bright 

orange, hemispherical cushions and firmer, pale 

yellow, flatter structures. The bright orange 

cushions are conidial pustules which consist of 

hyphae whose tips are branched and fragment 

into numerous dikaryotic arthroconidia (Fig. 

21.4c). The cells are packed with oil globules 

containing carotenoids. Such conidia are readily 

dispersed by rainsplash and are obviously similar 

in function to the splash-dispersed conidia of 

Nectria cinnabarina (see Plate 5d). The yellow 

flatter structures are basidial cushions which 

are attached centrally to the woody substratum. 

The surface layer is composed of clusters of 

forked basidia (Fig. 21.4b) which arise from 

dikaryotic hyphae. Each basidium forms two 

haploid basidiospores. After discharge, a basidiospore 

undergoes nuclear division and 

septation to give four cells. Depending on environmental 

conditions, each cell germinates by 

means of a monokaryotic haploid germ tube 

or by a short conidiophore (denticle). Conidia 

may also arise on older hyphae. They germinate 

to give monokaryotic hyphae. Dikaryotization 

occurs when two compatible monokaryotic 

hyphae fuse. Mossebo and Amougou (2001) have 

shown that the parenthesome and dolipore 

complex dissolve in order to facilitate passage 

of nuclei through the septum in the course of 

dikaryotization. Dacrymyces stillatus is heterothallic 

with a bifactorial (tetrapolar) mating system. 

Cells of the secondary mycelium are usually but 

not unfailingly dikaryotic (Mossebo, 1998). 

21.3.2 Calocera 

At first sight the ubiquitous cylindrical orange 

outgrowths of C. viscosa from coniferous logs 

(Plate 11g), or the smaller C. cornea from hardwood 

logs (Fig. 21.3b), could be mistaken for 

species of Clavaria. However, the gelatinous 

texture and the characteristically forked basidia 

(Fig. 21.5) place them in the Dacrymycetales, and 

this placement has been confirmed by molecular 

phylogenetic studies (Weiss & Oberwinkler, 2001). 

Ingold (1983b) has carefully observed the fate 

Fig 21.5 Calocera viscosa. (a) T.S. through hymenium with furcate basidia at different stages of development. (b) Freshly discharged 

basidiospores which are aseptate.The clear area in each spore shows the displacement of cytoplasmic contents by the single 

nucleus. (c) Two 24-hour-old basidiospores on tap-water agar. Each spore has produced two conidiophores bearing microconidia 

on denticles. (d) Direct germination of a basidiospore has given rise to monokaryotic hyphae which are forming microconidia. 

The septum dividing the spore into two is clearly visible. (b d) to same scale.

AURICULARIALES 

601 

of basidiospores in C. viscosa. Freshly discharged 

basidiospores are aseptate (Fig. 21.5b) but they 

soon develop one septum. Further development is 

by direct germination or formation of globose 

microconidia from basidiospore segments and 

from haploid monokaryotic hyphae (Figs. 21.5c,d), 

as described above for D. stillatus. 

21.4 Auriculariales 

The order Auriculariales has been subject to 

numerous taxonomic rearrangements. As currently 

understood, its members produce both 

mono- and dikaryotic mycelia with dolipores 

and parenthesomes lacking perforations (see Fig. 

18.10b). Basidia are septate (Wells, 1994; Wells & 

Bandoni, 2001). The Auriculariales are distinguishable 

from the Tremellales (Section 21.5) 

which have yeast-like monokaryotic stages, and 

from the Ceratobasidiales and Dacrymycetales 

which have aseptate basidia. Although taxonomic 

adjustments continue to be made, there is now 

little doubt that the order Auriculariales should 

contain both Auricularia with its transversely 

septate basidia, and Exidia and Pseudohydnum, 

which have basidia with longitudinal septa, 

the so-called tremelloid basidia (Weiss & 

Oberwinkler, 2001). 

There are great variations in fruit body size 

and shape. Clamp connections may be present 

or absent, depending on species. Most species 

have a bifactorial mating system with multiple 

alleles at both loci (Wells, 1987, 1994; Wong & 

Wells, 1987; Wong, 1993). Depending on environmental 

conditions, basidiospores are typically 

able to germinate in several different ways, 

e.g. by repetition (ballistospore formation), as 

hyphae, or by forming sickle-shaped (lunate) 

microconidia. Members of the Auriculariales 

are saprotrophic on wood, causing intensive 

white-rots (Worrall et al., 1997). 

21.4.1 Auricularia 

The Jew’s ear fungus A. auricula-judae forms 

rubbery, ear-shaped fruit-bodies on branches of 

elder (Sambucus) (Plate 11h) and is a weak 

pathogen, growing on the wood and pith of 

living branches and on dead wood. A wide range 

of other hosts has been reported, on which 

A. auricula-judae causes a rapid white-rot similar 

to that produced by members of the polyporoid 

clade (see Plate 10a; Worrall et al., 1997). 

A section through the flesh of a fruit body 

shows a hairy upper surface, a central gelatinous 

layer containing narrow clamped hyphae, and 

a broad hymenium on the lower side (Fig. 21.6a). 

Details of basidiocarp anatomy are useful in 

classification (Lowy, 1952). The fruit body can dry 

to a hard brittle mass, but on wetting it quickly 

absorbs moisture and discharges spores within 

a few hours. The basidia are cylindrical and 

become divided into four cells by three transverse 

septa (Fig. 21.6b). Each cell of the basidium 

develops a long cylindrical epibasidium which 

extends to the surface of the hymenium and 

terminates in a conical sterigma bearing a 

basidiospore which is monokaryotic. At 20 mm 

or more in length, the Auricularia basidiospore 

is one of the largest objects propelled by the 

surface tension catapult mechanism (see Pringle 

et al., 2005), and ballistospore discharge is easily 

observed with thin slices of basidiocarp material 

placed sideways on water agar (see Webster & 

Hard, 1998b). Auricularia auricula-judae is heterothallic 

with a bifactorial (tetrapolar) mating 

system, and there are indications of multiple 

alleles (see Wong, 1993). 

Germination of the basidiospore can proceed 

in several different ways (Fig. 21.6c), and such a 

variability is common in the Auriculariales 

(Ingold, 1982a, 1984b). Washings from the hymenial 

surface of fruit bodies contain basidiospores 

undergoing repetitious germination by means 

of a sterigma which produces another ballistospore. 

Ingold (1982a) interpreted this as a second 

chance for the spore to get away from the fruit 

body. Basidiospores alighting on a nutrient-poor 

surface such as tap water agar lay down three 

transverse septa, and each of the resulting four 

cells may emit one or more extensions (denticles) 

which produce a cluster of lunate microconidia. 

Alternatively or additionally, germination may 

occur directly by means of a germ tube, and 

this mode of germination is found especially 

on slightly richer media such as cornmeal agar. 

Septa are laid down, the first one bulging


Fig 21.6 Auricularia auricula-judae. 

(a) Section of fruit body.The 

hymenium is on the lower side. 

(b) Squash preparation of the 

hymenium showing basidia. Note the 

transverse segmentation and the 

long epibasidia.The basidia are 

associated with branched hyphae. 

(c) Basidiospores.Two are 

ungerminated; one has developed 

a septum and is germinating directly 

by means of a germ tube; and 

two basidiospores have become 

three-septate and are producing 

lunate conidia from short 

conidiophores (denticles). 

(d) A basidiospore which had fallen 

back onto the hymenial surface and is 

germinating repetitiously to form a 

ballistoconidium. (b d) to same scale. 

backwards from the protoplast-containing 

germ tube towards the empty basidiospore. 

Such septa are interpreted as retraction septa 

(Ingold, 1982a). A richly branched monokaryotic 

mycelium of very fine hyphae develops, and after 

a while these hyphae form lateral or terminal 

denticles which produce clusters of lunate 

microconidia. 

The lunate conidia are a feature found in 

many species of Auriculariales, but their significance 

in the life cycle is uncertain. Like basidiospores 

and the repetitious ballistoconidia 

produced from them, they are capable of germination 

to form monokaryotic hyphae, but they 

might also function directly as spermatia. The 

putative life cycle of A. auricula-judae is shown in 

Fig. 21.7. 

Another common species is A. mesenterica, 

which forms thicker, hairy, fan-shaped fruit 

bodies on old stumps and logs of elm (Ulmus) 

and other trees. It, too, causes active wood 

decay and may occasionally be weakly 

pathogenic. 

Auricularia as a cultivated mushroom 

Although devoid of any distinctive taste, the 

fruit bodies of Auricularia are highly nutritious 

and possess a chewy, rubbery texture which 

renders them attractive ingredients for Far 

Eastern soups and stir fries. The main species 

cultivated for food is A. polytricha (‘Mu-Erh’). 

The history of cultivation dates back to AD 600 

in China (Cheng & Tu, 1978; Chang & Miles, 

2004), making Auricularia the first cultivated 

mushroom for which we have historical 

records. Some 465 000 t of fresh fruit bodies are 

currently produced per annum (Pegler, 2001). 

Very conveniently, the fruit bodies can be 

stored dry for several months, and rehydrated 

when needed. Cultivation is traditionally performed 

by inoculating logs of suitable broadleaved 

trees with mycelial spawn. Infected logs 

can produce good crops for several years. The 

fungus is now also often cultivated in plastic 

bags filled with a mixture of sawdust and rice 

bran, allowing the fruit bodies to emerge 

through holes in the plastic.

AURICULARIALES 

603 

Fig 21.7 Life cycle of Auricularia auricula-judae. Depending on the substrate, a basidiospore has various options by which to 

germinate; these are equivalent for both mating types, but for clarity we show them here for only one of them (white nuclei). 

Basidiospores falling onto the fruit body hymenium may germinate by repetition to form another ballistospore. Depending on the 

nutrient status, basidiospores may germinate by formation of a monokaryotic mycelium or by producing lunate microconidia.The 

latter may also be produced by monokaryotic hyphae.Conjugation leads to the establishment of a dikaryotic mycelium which may 

form basidiocarps. Key events in the life cycle are plasmogamy (P), karyogamy (K) and meiosis (M). Haploid nuclei are drawn as 

empty or filled circles; the diploid nucleus is drawn larger and half-filled. 

21.4.2 Other members of the 

Auriculariales 

Exidia 

Exidia glandulosa, sometimes called ‘witches’ 

butter’, forms black rubbery fructifications on 

decaying branches of various woody hosts, especially 

lime (Tilia) and oak (Quercus) (Fig. 21.9a). 

The hymenium is borne on the lower side of the 

fruit body and in this species is studded with 

small black warty outgrowths. The basidia are 

formed deep within the hymenium and produce 

long epibasidia. They are divided by longitudinal 

instead of transverse septa (Fig. 21.8). 

Basidiospores of E. glandulosa show germination 

patterns identical to those described above 

for A. auricula-judae, and Ingold (1982b) found 

that the only clear microscopic difference 

between these two species is the arrangement 

of septa in the basidium. Phylogenetic studies 

have confirmed the close relationship between 

Auricularia and Exidia (Weiss & Oberwinkler, 2001). 

Pseudohydnum gelatinosum 

This species grows on dead stumps and branches 

of coniferous trees. The fruit body is jelly-like in 

consistency and has a short eccentric stalk. 

The hymenium is on the lower side of the 

pileus and is arranged into numerous conical 

teeth (Fig. 21.9b) resembling those of Hydnum. 

The basidia are similar to those of Exidia in 

being longitudinally septate. As in Exidia and 

Auricularia, basidiospores failing to escape from


the hymenium may germinate by repetition or, 

in other situations, by means of a germ tube, but 

lunate or other microconidia have not been 

observed (Ingold, 1985). 

21.5 Tremellales 

Fig 21.8 Exidiaglandulosa.Sectionofhymeniumshowing 

longitudinally divided basidia with long epibasidia extending to 

the surface. 

Formerly understood as a broad taxon which 

included genera such as Exidia and Pseudohydnum 

(see p. 603), the order Tremellales is now 

restricted to fungi which possess a yeast-like 

haploid state, basidia divided by longitudinal 

septa (tremelloid basidia), and dikaryotic hyphae 

with a dolipore septum and a parenthesome 

which is sacculate, i.e. invaginated towards the 

septal pore (Fig. 21.10a; Berbee & Wells, 1988). 

Dikaryotic hyphae usually have clamp connections. 

The monokaryotic yeast state resembles 

heterobasidiomycete yeasts such as Filobasidiella 

neoformans, Phaffia rhodozyma and species of 

Bullera and Cryptococcus, all of which belong to 

the Tremellales and related orders within the 

Tremellomycetidae (Fell et al., 2001). Heterobasidiomycetes 

growing predominantly in the 

yeast state are discussed in Chapter 24 (p. 660). 

In the life cycle of the filamentous Tremellales 

considered here, the dikaryotic condition is the 

dominant phase and is re-established by 

Fig 21.9 Fruit bodies of Auriculariales. (a) Exidiaglandulosa.Fruit bodies on lime (Tilia).The hymenial surface bears black warts and 

is on one face of the fruit body. (b) Pseudohydnum gelatinosum.Fruit bodies seen from above (right) and below (left).The hymenium 

covers the surface of the spines.

TREMELLALES 

605 

conjugation of compatible yeast cells. The mating 

system has been described as ‘modified tetrapolar’ 

(Bandoni, 1963) because there are only two 

alleles at the A locus but multiple alleles at B. 

This system is uncommon in the Basidiomycota, 

which usually have multiple alleles at both loci, 

aiding outbreeding (see p. 507). The modified 

tetrapolar system of Tremella is, however, also 

found in Ustilago maydis, and the designation 

of loci is equivalent (p. 643). Thus, the A locus 

controls conjugation and the B locus growth of 

the resulting dikaryon. Both A alleles of Tremella 

encode peptide-type hormones (Sakagami et al., 

1981; Ishibashi et al., 1984) and receptors for 

the hormone of the opposite mating type. In 

T. mesenterica, these hormones are linear peptides 

called tremerogen A-10 (12 amino acids) and 

tremerogen a-13 with 13 amino acids. Both 

peptides are derivatized with a farnesyl unit. 

Mating occurs by formation of conjugation tubes 

which requires the presence of the hormone 

of the opposite mating type; each hormone 

is produced constitutively, irrespective of the 

presence or absence of a compatible mating 

partner (Bandoni, 1965). Yeast cells with opposite 

alleles at A but like B alleles will conjugate but 

fail to initiate dikaryotic hyphal growth. 

The fruit bodies of Tremellales are usually 

formed on wood, often in association with those 

of other fungi (Asco- and Basidiomycota) or 

with lichen thalli, which may be parasitized 

(Diederich, 1996; Chen, 1998). Parasitism is by 

intimate hyphal contact via haustorial branches 

(Figs. 21.10b,c; see below). The fruit bodies of 

Tremellales are highly variable in size, ranging 

from a limited hymenium on the mycelium of 

putative hosts to large structures (several centimetres) 

surrounding host basidiocarps or growing 

near them. Although often considered as 

saprotrophs, no special capacity to degrade wood 

seems to have been recorded. 

Accounts of the Tremellales have been written 

by Bandoni (1987), Bandoni and Boekhout 

(1998) and Chen (1998). 

21.5.1 Tremella 

This is a large genus of some 80 species. Detailed 

descriptions of representatives of all species 

groups have been given by Chen (1998). One of 

the commonest and most thoroughly examined 

species is T. mesenterica, whose yellow or orange 

gelatinous fruit bodies are readily seen on 

various woody hosts such as oak, willow, gorse 

and beech (Plate 11i). Variations in the intensity 

of fruit body coloration could be due to a 

stimulation of carotenoid synthesis by high 

light intensity because fruit bodies exposed to 

sunlight are often more deeply coloured than 

those in the shade (Wong et al., 1985). The fruit 

bodies of T. mesenterica are usually associated 

with those of Peniophora in the field, and 

Zugmaier et al. (1994) have shown that hyphae 

of Peniophora spp. are parasitized in vivo and in 

vitro. Several Tremella spp. are more obviously 

mycoparasitic than T. mesenterica. For instance, 

T. globospora produces its fruit bodies within the 

perithecia of Diaporthe, and T. encephala overgrows 

the fructifications of its host, Stereum, which 

remain as a firm core in the Tremella basidiocarp. 

There are also several other genera within the 

Tremellales which parasitize other fungi (Bauer, 

2004; Figs. 21.10b,c). 

Parasitism is mediated by modified hyphae 

which Olive (1947) called ‘haustorial branches’. 

They consist of a swollen binucleate hyphal 

segment, delimited at its base by a clamp 

connection which puts forward one or several 

long thin filaments (Fig. 21.11a). The association 

of the swollen segment with the term ‘haustorium’ 

is unfortunate because the haustorial 

branch is formed outside the host cell. Where 

‘haustorial filaments’ of Tremella or related 

fungi contact the hypha of a suitable host, the 

host wall is dissolved and a micropore is formed 

which establishes direct cytoplasmic contact 

between the filament and the host, apparently 

by fusion of the two plasma membranes 

(Figs. 21.10b,c). 

The life cycle of T. mesenterica is complex and 

not yet fully understood (Fig. 21.12). Haploid 

basidiospores are discharged from long epibasidia 

by the surface tension catapult mechanism. 

Basidiospores failing to escape from the hymenium 

can germinate by repetition to form 

ballistoconidia (Ingold, 1982b). When landing on 

a suitable substrate, the basidiospore germinates 

by forming several buds which remain attached


Fig 21.10 Ultrastructure of Tremellales. (a) Cupulate parenthesome and dolipore septum of T. globospora.(b,c)Tipofthe 

haustorial filament of Trimorphomyces papilionaceus (top) which has made contact with a hypha of its host, Arthrinium 

sphaerospermum (bottom). Membrane continuity has been established in the micropore region (c).Original prints kindly provided 

by M.L.Berbee (a) and R.Bauer (b,c). a reprinted from Berbee and Wells (1988), with permission from Mycologia. ßThe Mycological 

Society of America. 

Fig 21.11 Tremella mesenterica. (a) Haustorial branch. 

The swollen dikaryotic branch arises from a clamp 

connection and emits filaments which may contact 

host hyphae. (b) Dikaryotic clamped hypha from the 

hymenium of a fruit body. One branch has produced 

a basidium whereas the other has formed dikaryotic 

conidia. Redrawn from Wells and Bandoni (2001) with 

kind permission of Springer Science and Business 

Media. 

to the basidiospore. These buds act as conidiogenous 

cells by producing numerous minute 

blastoconidia, which in turn germinate by swelling 

and budding to give rise to the haploid yeast 

state. Fusion between compatible yeast cells 

re-establishes the dikaryotic mycelial phase. 

In addition to producing basidia, hyphae in the 

fruit body may also form a dikaryotic conidial

TREMELLALES 

607 

Fig 21.12 Life cycle of Tremellamesenterica.The monokaryotic part of the cycle is shown only for one of the two mating types 

(white nuclei).Basidiospores failing to leave the fruitbody maygain a second chance byrepetitious germination to form a 

ballistoconidium.On other substrates, basidiospores germinate by way ofblastoconidia which give rise toyeastcells.Conjugation 

of two compatibleyeastcells givesrise to the dikaryotic mycelial stagewhich forms fruitbodiesproducing dikaryotic conidia, haploid 

yeastcells by de-dikaryotization (not shown), andhaploidbasidiosporesby meiosis.Key eventsin thelife cycle areplasmogamy (P), 

karyogamy (K) andmeiosis (M).Haploid nuclei are drawn as empty or filled circles; the diploid nucleus is drawn larger andhalf-filled. 

state (Fig. 21.11b) with an uncertain role in the life 

cycle. Additionally, de-dikaryotization to give 

yeast cells has been observed in the fruit bodies 

of T. mesenterica. 

Another common species is T. foliacea (sometimes 

synonymized with T. frondosa) with its fleshcoloured 

to pale brown, lobed or contorted fruit 

bodies on oak and beech stumps. In this species, 

basidiospores germinate on suitable substrates 

by giving rise directly to budding yeast cells 

(Fig. 21.13). This has also been observed in 

T. encephala (Ingold, 1985). There are no dikaryotic 

conidia in these two species. Most Tremella spp. are 

heterothallic with a modified tetrapolar mating 

system, but in T. fuciformis both homothallic 

and heterothallic strains have been observed 

(Fox & Wong, 1990). 

Cultivation of Tremella 

The ‘silver ear’ fungus, T. fuciformis, has been 

cultivated in China on wood and sawdust for 

about 200 years (Chang & Miles, 2004). Although 

almost always associated with Hypoxylon spp. 

in nature (Chen, 1998), mycoparasitism does 

not seem to be obligate because cultivation is 

possible in monoculture. However, yields are 

greatly stimulated in the presence of a ‘friend of 

the mycelium’, i.e. the substrate is co-inoculated 

with T. fuciformis and Hypoxylon archeri or another 

suitable host species (Chang & Miles, 2004).


Fig 21.13 Tremella frondosa. (a) Basidia showing epibasidia with various stages of spore development. (b) Freshly discharged 

basidiospore. (c) Basidiospore germinating on malt extract agar by budding to form yeast-like cells which also undergo budding. 

(d) Basidiospores germinating in water by repetition, i.e. by producing ballistospores. (e) Immature basidia seen from above, showing 

the division of the basidium into four cells by longitudinal septa. 

The fruit bodies of T. fuciformis are consumed in a 

stewed form, especially as a dessert, and this 

species has traditionally also been viewed as a 

medicinal mushroom in the Far East. Lifeprolonging, 

vitalizing and anti-cancer properties 

have been ascribed to T. fuciformis, and these 

effects seem to be due mainly to a stimulation of 

the immune system (Wasser, 2002). The biochemical 

basis is thought to be due to the production 

of exopolysaccharides by this and other Tremella 

spp., including T. mesenterica (Reshetnikov et al., 

2000). However, it is as yet unclear how such 

polysaccharides are assimilated by the human 

digestive system, and how they interact with 

human cells. Many Homobasidiomycetes produce 

exopolysaccharides that are said to possess 

similar medicinal properties, and these molecules 

are mainly b-(1,3)-glucans substituted with 

various sugar moieties. In contrast, in Tremella 

the biologically active molecules have a b-(1,3)- 

mannan backbone substituted with xylose and 

glucuronic acid (de Baets & Vandamme, 2001; 

Vinogradov et al., 2004). A multitude of such 

mannans differing mainly in their substitution 

pattern is produced by the fruit bodies on 

solid substrata and by yeast cells in liquid 

culture. Yeast cells are encapsulated by these 

polysaccharides, as revealed by staining with 

Indian ink (see Fig. 24.1b). Structurally similar 

xyloglucuronomannans make up the capsule 

of the human pathogen Cryptococcus neoformans 

(see p. 661).

22 

Urediniomycetes: Uredinales (rust fungi) 

22.1 Urediniomycetes 

Following extensive re-arrangements, the class 

Urediniomycetes (about 8000 species) is now 

considered to be monophyletic, although the 

naming of orders and families is still proving 

difficult (Swann & Taylor, 1995; Kirk et al., 2001; 

Swann et al., 2001). The order Uredinales (rust 

fungi) is by far the largest (about 7000 species) 

and the most important. The order Microbotryales, 

although taxonomically part of the Urediniomycetes, 

is a group of fungi causing smut 

diseases and will be discussed in Chapter 23. 

Many Urediniomycetes belonging to several 

orders occur predominantly in the yeast state. 

An important group, the Sporidiales, contains 

the red yeasts Sporidiobolus and Rhodosporidium 

(anamorphs Sporobolomyces and Rhodotorula, respectively), 

and this order is considered in more 

detail on pp. 666 670. 

General information on the groups included 

in the Urediniomycetes has been given by Swann 

et al. (2001). They have defined Urediniomycetes 

as fungi in which the processes of karyogamy 

and meiosis occur in distinct parts of the basidium, 

i.e. the probasidium and metabasidium, 

respectively. The metabasidium is typically transversely 

septate, with basidiospores produced 

laterally (see Fig. 22.2d). Another useful character 

is the structure of septa viewed by 

transmission electron microscopy. Urediniomycete 

septa are simple with a single pore which 

may be open or plugged, but they typically 

lack the dolipore arrangement found in other 

basidiomycetes (see Fig. 18.9). Clamp connections 

are absent. 

22.2 Uredinales: the rust fungi 

Rust fungi (Uredinales) are a fascinating group of 

organisms. The life cycle of a typical rust species 

is among the most complex found anywhere in 

nature, consisting of five different spore stages 

on two plant hosts which are taxonomically 

entirely unrelated to each other. These pathogens 

infect most groups of vascular plants, 

including Pteridophytes (ferns), Gymnosperms, 

and Angiosperms (both monocots and dicots). 

Numerous fundamental questions about rust 

fungi remain to be answered, e.g. how a biotrophic 

organism manages to infect and parasitize 

two unrelated hosts using different 

mechanisms on either; how the five spore 

stages with their numerous different dispersal 

mechanisms could have evolved; how easily one 

or more of them can become aborted in derived 

(reduced) life cycles; how rust fungi survive in 

situations where one of their two hosts is 

unavailable; and how quickly new rust species 

or races spread to new habitats and then come to 

an equilibrium with their host plants. A protocol 

to generate stable transformants of rust fungi 

would greatly facilitate experimental work on 

them, but unfortunately this is not yet available. 

The species concept in rust fungi is also 

challenging. Morphological species are readily 

recognized, but these can show considerable

610 UREDINIOMYCETES: UREDINALES (RUST FUNGI) 

genetic adaptability by fragmenting into several 

forms which infect non-overlapping spectra of 

host species and thereby become reproductively 

isolated. Because of the identity of the host 

family as an additional taxonomic feature, species 

of rust fungi are relatively easily grouped 

into genera which are often monophyletic. At the 

higher taxonomic level, two large groups can be 

resolved weakly by phylogenetic analyses (Maier 

et al., 2003; Wingfield et al., 2004). They coincide 

with the Pucciniaceae and Melampsoraceae of 

earlier concepts (Dietel, 1928) in which these two 

families were distinguished by their teliospore 

or probasidium being stalked (Pucciniaceae) or 

unstalked (Melampsoraceae). Another point of 

distinction is that a particular spore-producing 

structure, the aecial stage (see below), is produced 

on angiosperm hosts by Pucciniaceae but 

on gymnosperms by Melampsoraceae (Wingfield 

et al., 2004). Dietel’s two broad groups are usually 

split up into about 13 14 smaller families 

(Kirk et al., 2001; Cummins & Hiratsuka, 2003), 

but since the boundary lines are still being 

re-drawn from time to time, we prefer to adhere 

to the original concept for the purposes of this 

book. 

The popular name ‘rust fungi’ refers to the 

reddish-brown colour of some of the spores 

which are produced in dense pustules on crop 

plants, giving them a ‘rusted’ appearance. This 

is especially true of the rusts on cereals, which 

have probably caused crop losses since the beginning 

of agriculture. Archaeological excavations 

have uncovered rusted cereal remains dating 

back to the Bronze Age (Kislev, 1982), and it is 

well known that the ancient Romans held a 

special festival, the Robigalia, to appease their 

rust gods. This took place on 25 April, i.e. at a 

time when the crop was particularly vulnerable 

to attack (Large, 1940). The Robigalia may be the 

origin of Rogation Sunday, a day of blessing of 

the crops which is still observed by some 

Christian churches every year in late April 

(Schuman, 1991). 

Rusts can also cause serious economic damage 

on non-cereal crops, and examples are given in 

later sections of this chapter. Because of the 

immense economic importance of rust fungi, 

an enormous body of literature has been written, 

and the wheat Puccinia graminis system is probably 

the most thoroughly examined of all 

host pathogen interactions involving fungi. 

None the less, no substantial integrated treatment 

of the rust fungi has appeared in the past 

two decades, the two-volume set on cereal rusts 

(Bushnell & Roelfs, 1984; Roelfs & Bushnell, 1985) 

having been the last major effort. However, good 

keys and species descriptions are available, e.g. 

in Grove (1913), Gäumann (1959), Wilson and 

Henderson (1966) and Cummins and Hiratsuka 

(2003). 

22.2.1 The basic life cycle of rusts 

The classical example of a rust fungus, Puccinia 

graminis, is the cause of black stem rust on wheat 

and other cereals (Fig. 22.1), which is described 

more fully in Section 22.3. The life cycle of rusts 

is homologous with that of the Homobasidiomycetes 

(Fig. 18.4) in being divided into stages of 

primary (homo- and mono-karyotic) and secondary 

(hetero- and di-karyotic) mycelium. The 

heterokaryotic phase is the main period in the 

life cycle of rusts and it is the only one in which 

some rusts can survive indefinitely under suitable 

conditions. The host plant species on which 

this stage is produced is therefore termed the 

principal host, with that bearing the homokaryotic 

mycelium called the alternate host. 

On leaves of the principal host, P. graminis 

produces urediniospores in pustules called 

uredinia, and they rapidly spread the infection 

because they are capable of re-infecting the same 

host species. Urediniospores are produced on 

stalks from which they break off at maturity, 

being released and distributed passively by wind. 

Urediniospores of rust fungi have a relatively 

thick wall which is often pigmented and typically 

spiny. They are capable of surviving airborne 

for several weeks or months, which accounts for 

their long-distance dispersal sometimes over 

hundreds or even thousands of miles. Each 

urediniospore is binucleate, with the two nuclei 

being of opposite mating type. In temperate 

climates, uredinia of many rusts are gradually 

replaced by telia in autumn, especially on leaf 

sheaths and stems. Teliospores (¼ probasidia) 

of Puccinia are two-celled and thick-walled.

UREDINALES: THE RUST FUNGI 

611 

Fig 22.1 The life cycle of Puccinia graminis, with its heterokaryotic phase on cereals and the homokaryotic stage on barberry 

(Berberis).The different ways in which the five spore stages are released and dispersed are indicated.Teliospores overwinter after 

nuclear fusion, i.e. as diploid cells. During basidiosporogenesis, meiosis is followed by a mitotic division so that each basidiospore is 

a homokaryon containing two nuclei of the same mating type.Open and closed circles represent haploid nuclei of opposite mating 

type; diploid nuclei are larger and half-filled. Key events in the life cycle are plasmogamy (P), karyogamy (K) and meiosis (M). 

Each cell contains two haploid nuclei of opposite 

mating-type which fuse to form a diploid nucleus 

(see Fig. 22.2c). The teliospore overwinters in the 

diploid state, firmly attached to the plant tissue 

on which it was produced. In spring, meiosis 

occurs while each teliospore cell emits a germ 

tube which becomes transversely septate and 

forms the promycelium or metabasidium. Each 

compartment of the metabasidium produces one 

basidiospore which initially contains one haploid 

nucleus. This commonly divides so that the 

mature basidiospore often contains two genetically 

identical haploid nuclei and is thus a 

dikaryotic homokaryon (Anikster, 1983). Basidiospores 

are actively liberated by the surface 

tension catapult mechanism involving Buller’s 

drop as described before for other basidiomycetes 

(Section 18.5). 

The basidiospores of P. graminis are unable to 

infect the cereal host but will infect the alternate 

host, barberry (Berberis vulgaris). The resulting 

primary mycelium is haploid, homo- and monokaryotic. 

At the upper (adaxial) surface of the 

host leaf, the primary mycelium forms a flaskshaped 

fructification known as a spermogonium. 

Within the mesophyll, knots of hyphae 

form a proto-aecium but do not develop further 

at this stage. Minute uninucleate spermatia 

are produced from annellide-like structures 

(Littlefield & Heath, 1979) within the main body 

of the spermogonium, and they aggregate within 

a rim of hairs (periphyses) at the spermogonial


Fig 22.2 Examples of spore stages in rust fungi. (a) Uredinium of Puccinia obscura on its principal host, the wood-rush 

Luzula campestris. Note the spiny urediniospores. (b) Development of a telium within an old uredinium of P. obscura.Some 

urediniospores are still seen on top of the smooth-walled teliospores pushing through. (c) Karyogamy in a teliospore of Puccinia 

lagenophorae, a demicyclic rust on Seneciovulgaris.The terminal cell still contains two paired nuclei (arrowheads) whereas in the basal 

cell the two nuclei have already fused to give one larger (diploid) nucleus. (d) Production of a promycelium (metabasidium) by Puccinia 

graminis.Four sterigmata have formed, each about to produce one basidiospore. (e) Spermogonium of P. obscura on its 

alternate host, Bellis perennis. Note the flask-shaped body and the ring of stiff periphyses which protrude beyond the upper host 

epidermis. (f) Aecia of P. lagenophorae on Senecio vulgaris. 

ostiole in a sugary liquid which attracts insects. 

These carry spermatia around, and fertilization 

occurs if a spermatium makes contact with 

a modified periphysis called receptive hypha 

of a spermogonium of opposite mating type. 

Spermatia are incapable of independent 

germination to establish new infections but 

perform solely a sexual role in fertilization. 

Most rust fungi are heterothallic with a bipolar 

mating system, although Narisawa et al. (1994) 

have claimed that P. coronata has a tetrapolar 

mating system with two mating type loci.


613 

Homothallic species are also known, and these 

generally do not produce spermogonia. A generalized 

account of rust life cycles has been given 

by Buller (1950). 

Following fertilization, the nucleus from 

the donor spermatium divides repeatedly and 

migrates down the receptive hypha into the 

receiving primary mycelium which thereby 

undergoes dikaryotization. When compatible 

nuclei reach the proto-aecium, this becomes 

converted into an aecium which breaches the 

lower epidermis. Heterokaryotic aeciospores 

develop and are released by a sudden roundingoff 

of the flattened wall separating adjacent 

spores, thus flicking the spores into the air. 

Aeciospores are relatively thin-walled and bear 

warty rather than spiny surface ornamentations. 

They are often brightly coloured due to the 

abundance of carotenoids accumulating in lipid 

droplets (Plate 12a). Aeciospores of P. graminis 

are unable to re-infect Berberis, but are infective 

on the principal grass host. The resulting secondary 

mycelium produces urediniospores, thus 

completing the life cycle. 

Examples of the different spore types and 

the pustules (sori) producing them are shown in 

Fig. 22.2. Spores and sori have been given various 

names, and we follow the naming used in the 

Dictionary of Fungi (Kirk et al., 2001). It is customary 

to assign Roman numerals 0, I, II, III or IV 

to the distinct spore types, and these numbers 

provide a convenient shorthand for describing 

the range of spores found in a given rust. 

The most important terms are summarized in 

Table 22.1. 

The various spore stages of rust fungi differ 

greatly in their length of survival. Although 

details are dependent on species and conditions 

of storage (temperature, state of hydration, 

light), it may be generalized that the maximum 

survival period in the field is in the order 

of days (spermatia and basidiospores), weeks 

(aeciospores), a few months (urediniospores) 

and several months to more than a year 

(teliospores). 

22.2.2 Derived life cycles and Tranzschel’s 

Law 

Rust fungi which must alternate between two 

different host plants in order to complete their 

life cycle are called heteroecious. In contrast, 

autoecious species are confined to one host 

plant. Species whose life cycle contains all five 

possible spore stages are called macrocyclic. In 

this terminology, P. graminis is a macrocyclic 

heteroecious rust whereas P. menthae, which 

produces all five spore stages on one host 

(mint), is macrocyclic but autoecious. Many 

rusts have derived life cycles in which one or 

more spore stages have been omitted. One 

common variation is the absence of uredinia in 

heterocyclic rusts. For instance, Gymnosporangium 

fuscum (see p. 629) produces spermogonia and 

aecia on the leaves of pear trees and has Juniperus 

spp. as its principal host for production of telia. 

Such rusts which lack uredinia are called 

demicyclic or -opsis forms. 

An autoecious version of the demicyclic theme 

is presented by P. lagenophorae which produces 

spermogonia, aecia and telia on Senecio spp. 

(see Figs. 22.2c f). In functional terms, the aecia 

could be considered uredinia because the aeciospores 

infect the same host species on which they 

were produced, and because in old aecia the 

Table 22.1. Generally accepted terminology of the sori and spore states of rust fungi. 

0 I II III IV 

Sorus Spermogonium Aecium Uredinium Telium Basidium 

Pycnium Aecidiosorus Uredosorus Teleutosorus Metabasidium 

Aecidium Uredium Promycelium 

Spore Spermatium Aeciospore Urediniospore Teliospore Basidiospore 

Pycniospore Aecidiospore Uredospore Teleutospore Sporidium 

Urediospore


aeciospores can be displaced by teliospores. Such 

aecia are sometimes termed aecidioid uredinia. 

Another common variation is the microcyclic 

one in which both aecia and uredinia are 

lacking. Such rusts are, of course, autoecious. 

Many microcyclic rusts do not undergo sexual 

reproduction in the sense of sexual recombination, 

i.e. spermogonia are absent and the only 

reproductive unit is the teliospore with or 

without basidiospores. Such species are either 

homothallic or asexual. The wide array of 

possible nuclear cycles has been summarized by 

Ono (2002). 

An example of a microcyclic rust fungus is 

P. mesnieriana, which produces telia on Rhamnus 

catharticus (buckthorn). The teliospores germinate 

to produce metabasidia, but only two basidiospores 

are formed per basidium (Anikster & Wahl, 

1985). This species is homothallic because a single 

basidiospore can infect R. catharticus, giving rise to 

a telium-producing infection. The teliospores are 

highly characteristic because they carry a ‘crown’ 

of spiny outgrowths. Very similar teliospores (see 

Fig. 22.13a) are produced by the macrocyclic 

‘crown rust’, Puccinia coronata, which also colonizes 

Rhamnus and related plants as alternate 

hosts, but infects grasses and cereals, especially 

oat (Avena), as the principal (i.e. uredinial and 

telial) host. Working in the late nineteenth and 

early twentieth century when the elucidation of 

rust life cycles was very much in vogue, the 

Russian mycologist Vladimir Tranzschel generalized 

that an unknown aecial stage of a macrocyclic 

uredinial/telial rust should be sought on 

plant species infected by microcyclic rusts with 

morphologically similar teliospores. This rule, 

known as Tranzschel’s Law, has been applied 

several times, and DNA-based studies have 

confirmed the close relationship, for example 

between P. mesnieriana and P. coronata (Zambino & 

Szabo, 1993; Shattock & Preece, 2000). In other 

words, the telia of the microcyclic species mimic 

the aecia of the macrocyclic ancestor. These 

two species are then said to be correlated. The 

specialization of a recently evolved microcyclic 

rust onto the alternate host of the ancestor rust 

species may have something to do with the 

observation that the alternate hosts are almost 

always perennial, whereas principal hosts may 

be annual (Shattock & Preece, 2000). Examples of 

the reverse case, i.e. the evolution of the microcyclic 

species on the principal host of the 

macrocyclic ancestral species, do not seem to be 

known. 

22.2.3 The infection process 

Concise reviews of this vast topic have been 

written by Heath and Skalamera (1997), Mendgen 

(1997) and Hahn (2000). One of the differences 

between germ tubes arising from basidiospores 

and those arising from heterokaryotic spores 

(aeciospores or urediniospores) is that the former 

usually penetrate the cuticle directly without an 

appressorium, whereas the latter usually form 

an appressorium and preferentially penetrate 

through stomata (Figs. 22.4b, 22.5; Mendgen, 

1997). An exception to this generalization is 

presented by germinating urediniospores of 

Phakopsora spp., which show appressoriummediated 

direct penetration of the cuticle 

(Adendorff & Rijkenberg, 2000). There are also 

differences in the carbohydrate polymers making 

up the walls of monokaryotic and dikaryotic 

stages of the same species of rust fungus, and at 

different steps of the infection process (Freytag & 

Mendgen, 1991). Relatively little is known about 

infection from basidiospores, not least because 

these are difficult to obtain in the quantity 

required for experiments (see Gold & Mendgen, 

1991). We shall therefore focus on the infection 

process arising from germinating urediniospores, 

since these are the most thoroughly 

researched system and have a major impact on 

agriculture as carriers of the repeated infection 

cycle. 

Before urediniospores can germinate, germination 

autoinhibitors such as methyl-cis-3, 

4-dimethoxycinnamate (e.g. in Uromyces appendiculatus) 

must be diluted out or degraded. This 

substance is active at concentrations in the 

10 11 M range (Macko et al., 1970; Staples, 2000), 

i.e. at a similarly low concentration as the sex 

hormones of Achlya (see p. 86). This makes it one 

of the most potent biological molecules. Wolf 

(1982) has suggested that the autoinhibitor acts 

by blocking the lysis of the germ pore. Lysis must


615 

Fig 22.3 Attachment of a hydrated urediniospore of 

Uromyces viciae-fabae to the surface of a broad-bean leaf1h 

after contact. (a) Spore removed with sticky tape.The germ 

pore has partially lysed. (b) The adhesion pad on the leaf from 

which the spore was removed. Some of the germ pore 

material has become incorporated into the pad which has 

made firm contact with the host cuticle.From Clement et al. 

(1997), with permission from Elsevier.Original image kindly 

provided by J. A.Clement. 

occur before the germ tube can emerge (see 

Fig. 22.3). 

Attachment of urediniospores to surfaces is 

a multi-step process. Initial attachment is probably 

purely physical and based on hydrophobic 

interactions since it is stronger on hydrophobic 

than hydrophilic surfaces (Terhune & Hoch, 

1993). As soon as the urediniospore becomes 

fully hydrated upon contact with water, there is 

evidence of the formation of an adhesion pad 

of unknown composition (Fig. 22.3; Clement 

et al., 1997). Further, cutinases and other esterases 

are released, and their activity is thought 

to modify the surface properties of the host 

cuticle, cementing the attachment pad to the 

host surface (Deising et al., 1992). The germ tube 

is also tightly attached to the host surface by 

means of a glue which probably consists of 

glucans and proteins (Epstein et al., 1985; 

Chaubal et al., 1991). 

The process of appressorium differentiation by 

dikaryotic stages of rusts may be unique among 

fungi in being triggered by thigmotropism. A 

ridge about 0.5 mm high is required and sufficient 

to induce appressorium differentiation even on 

chemically inert surfaces (Fig. 22.4a; Hoch et al., 

1987; Allen et al., 1991). In nature, the relevant 

topographic feature is the stomatal lip, i.e. the 

point where the cuticle broke during the developmental 

expansion and opening of the stoma 

(Terhune et al., 1991). Firm attachment of the 

germ tube to the surface is required for the 

perception of the signal for appressorium induction 

in urediniospore germ tubes of U. appendiculatus, 

and there is evidence that the reception 

of the physical signal involves microtubules and 

integrin-like molecules (Corrêa et al., 1996) and 

is transmitted via stretch-activated Ca 2þ channels 

(Zhou et al., 1991). We have already come across 

stretch-activated Ca 2þ channels and integrin as 

possible regulators of the rate of hyphal tip 

extension (see p. 8). Once the signal has been 

perceived, an appressorium differentiates in as 

little as 60 min. 

Following the differentiation of an appressorium 

over a stoma, a thin penetration hypha 

develops which swells beneath the guard cells 

to form the substomatal vesicle (Fig. 22.5). 

From this, intercellular hyphae grow and form 

appressorium-like structures called haustorial 

mother cells on the surface of leaf mesophyll 

cells. The haustorial mother cell co-ordinates 

penetration of the plant cell, leading to the 

formation of a haustorium. Morphologically 

recognizable haustoria are not normally formed 

by monokaryotic rust stages; instead, the 

hyphae appear to grow through mesophyll cells 

whose plasmalemma invaginates around them


Fig 22.4 Appressorium formation by urediniospore germ tubes. (a) The runner bean rust Uromyces appendiculatus.Urediniospores 

inoculated onto a polystyrene surface with artificial ridges (0.5 mm high) have germinated and differentiated appressoria upon 

reaching the ridge. (b) The broad bean rust Uromyces viciae-fabae.The germ tube has followed topographical features of the host 

surface until it has reached a stoma, over which an appressorium has formed. (a) Reprinted from Allen et al. (1991) with permission 

by APS Press.Original print kindly provided by H.C. Hoch. (b) reprinted from Mendgen (1997), with kind permission of Springer 

Science and Business Media.Original print kindly provided by K. Mendgen. Both images approximately to same scale. 

Fig 22.5 Schematic comparison of infection processes in Uromyces. (a) Germinating basidiospore.The monokaryotic germ tube 

infects directly through the epidermal wall without forming a pronounced appressorium.Growth is both inter- and intracellular. 

Differentiated haustoria are not formed, and intracellular hyphae are regarded as M-haustoria. (b) Germinating urediniospore. 

The dikaryotic germ tube forms an appressorium above a stoma and infects through the stomatal opening.Growth in planta is 

mainly intercellular. Stalked globose haustoria (D-haustoria) arising from haustorial mother cells are the only intracellular organs 

of note. Both M-haustoria and D-haustoria are surrounded by a matrix (not drawn). Based on Mendgen (1997) and Mendgen and 

Hahn (2002). 

(Gold & Mendgen, 1991). These are sometimes 

called M-haustoria. In contrast, differentiated 

haustoria are formed by dikaryotic hyphae 

(D-haustoria), and valuable physiological work 

has been performed on them. This is summarized 

in the following section. 

22.2.4 Thephysiologyofbiotrophyin 

rust fungi 

The dikaryotic haustorium of rust fungi 

(Fig. 22.7) is functionally very similar to that of 

the Erysiphales (see Fig. 13.5). The haustorial 

mother cell emits a narrow penetration tube


617 

Fig 22.6 Cryo SEM of freeze-fractured haustoria 

of Uromyces viciae-fabae.(a)Intacthaustorium 

(Hau) connected to the intercellular haustorial 

mother cell (HMC) by a thin penetration tube.The 

neck-band (NB) is visible in the penetration tube. 

The vacuole (Vac) of the infected plant cell is also 

obvious. (b) Fracture through a haustorium, 

revealing one of its two nuclei (HN).The nucleus 

of the infected plant cell (PN) is closely associated 

with the haustorium, a feature frequently 

observed in rust infections.The host cell wall 

(CW), vacuole (Vac) and a Golgi stack (G) are also 

visible. Both images to same scale. Previously 

unpublished images very kindly provided by 

E. Kemen and K. Mendgen. 

which swells inside the host cell to form the 

haustorial body. This contains a full complement 

of organelles, including two nuclei. In some 

rusts, especially the cereal-infecting species, 

these two nuclei sometimes fuse into one diploid 

nucleus (Harder & Chong, 1984). From the inside 

outwards, the haustorial cytoplasm is surrounded 

by the haustorial membrane, the 

haustorial wall, the extrahaustorial matrix and 

the extrahaustorial membrane (i.e. the modified 

plant plasmalemma). The haustorial matrix is 

sealed against the apoplast outside the infected 

plant cell by means of a neckband (Fig. 22.6a). 

The host nucleus is often closely associated with 

the extrahaustorial membrane (Fig. 22.6b). 

As in the Erysiphales (see p. 398), the extrahaustorial 

membrane surrounding D-haustoria 

seems to lack ATPase activity (Baka et al., 1995), 

thus indicating that the infected plant cell has no 

effective means to restrict the efflux of metabolites 

into the haustorial matrix. In contrast, 

ATPase activity in the fungal haustorial 

membrane may actually be increased relative to 

normal hyphae (Struck et al., 1996). Not surprisingly, 

proton-driven hexose and amino acid 

uptake appears to occur from the matrix across 

the haustorial membrane into the haustorium 

(Fig. 22.7; Voegele & Mendgen, 2003). The uptake 

mechanism is thus equivalent to the uptake of 

solutes into growing hyphae (see Fig. 1.11). 

Whereas powdery mildews appear to rely on the 

host plant for the hydrolysis of the transport 

disaccharide sucrose into the hexoses fructose 

and glucose prior to uptake into the haustorium 

(p. 398), Voegele and Mendgen (2003) have 

suggested that the rust haustorium secretes


Fig 22.7 Diagram showing nutrient uptake mechanisms in a D-haustorium. Enzymatic reactions and proton-driven pumping 

are indicated by solid arrows; dotted arrows indicate diffusion or translocation processes. Sucrose (Sucr.) is hydrolysed to fructose 

(Fruct.) and glucose (Gluc.) by invertase (Inv.) secreted into the extrahaustorial matrix.These monosaccharides as well as amino 

acids (AA) are taken up across the haustorial membrane by specialized porter proteins fuelled by a transmembrane H þ gradient. 

Fructose is converted to the fungal transport compound mannitol (Mann.) by alcohol dehydrogenase within the haustorium. 

Modified and redrawn fromVoegele and Mendgen (2003). 

invertase into the matrix to perform the necessary 

hydrolysis (Fig. 22.7). 

All rusts are obligately biotrophic in nature, 

i.e. they need to parasitize living host plants in 

order to complete their life cycle. The fact that 

many of them can now be cultivated on agar 

media in the laboratory does not alter their 

status as obligate biotrophs in nature (P. G. 

Williams, 1984). The initial report of the cultivation 

of P. graminis on a simple medium (Williams 

et al., 1966) raised high hopes for a breakthrough 

in research on rusts, but interest has waned in 

recent years. Excellent accounts recalling the 

excitement of discovery have been written by 

Maclean (1982) and P. G. Williams (1984). It is 

now possible to cultivate rust fungi on relatively 

simple agar media based on minerals (e.g. 

Czapek-Dox agar) with sucrose or glucose as 

carbon source and yeast extract, peptone or 

certain amino acids as a nitrogen source. 

22.2.5 Host resistance 

Resistance against rust infections can manifest 

itself at different stages of the infection process. 

Most commonly it becomes evident as a hypersensitive 

response when the infectious hypha 

attempts to breach the first host cell wall (Heath 

& Skalamera, 1997). With monokaryotic stages of 

rust fungi, this is the direct penetration through 

the wall of the epidermal cell, whereas the 

resistance response to an incompatible dikaryotic 

strain occurs later, during or after the


619 

formation of the first haustorium (Heath, 1982, 

2002). Either way, the hypersensitive response 

triggers biochemical events involved in local and 

systemic defence against the pathogen (Heath, 

2000). One point of difference between penetration 

by rust fungi and powdery mildews is that 

the host plant mounts some resistance response 

against the latter even if the interaction ultimately 

turns out to be compatible, whereas no 

such recognition occurs if a compatible rust 

germ tube penetrates (Heath, 2002). The ultrastructural 

consequence is that powdery mildew 

haustoria commonly have a callose ring around 

their neck, whereas this is absent or reduced in 

the case of rust haustoria (Heath & Skalamera, 

1997). 

The gene-for-gene concept was proposed to 

explain the specific interactions between the 

rust Melampsora lini and its host, Linum usitatissimum 

(flax). It postulates that for every resistance 

gene of the host plant there is a matching 

virulence gene in the pathogen (see Flor, 1971). 

Resistance is usually dominant (R) whereas 

virulence is recessive (a). An incompatible interaction 

results if a rust fungus with an avirulence 

allele (A) attempts to infect a host carrying the 

matching resistance (R) allele. The identity of 

most molecules interacting in recognition is 

still unknown. However, Catanzariti et al. (2006) 

have demonstrated that the protein products of 

several avirulence genes are secreted by developing 

haustoria of M. lini, and that these seem to 

enter the cytoplasm of infected host cells where 

recognition leading to hypersensitivity occurs. 

The localization of proteins of haustorial origin 

in host cells, including the host nucleus, was also 

demonstrated by Kemen et al. (2005) for Uromyces 

spp. on broad bean (Vicia faba). These authors 

suggested that fungal avirulence genes might 

encode transcription factors involved in manipulating 

the host’s metabolism during the 

biotrophic interaction. In this theory, avirulence 

would result if the host cell managed to detect 

the fungal transcription factor as foreign. It is 

not yet known how the avirulence proteins are 

translocated into the plant cell. The molecular 

basis of gene-for-gene interactions involving 

rust fungi is therefore fundamentally 

different from that, for example, in 

Cladosporium fulvum infecting tomato, where 

recognition events occur at the host plasma 

membrane (see p. 482). 

Rusts, like most other fungi, possess an 

uncanny ability to overcome major gene resistance 

based on gene-for-gene interactions, especially 

if a single resistance gene is involved. 

Genetic variation is enhanced by the ability to 

reproduce sexually in the field if the alternate 

host is available. Even in the absence of the 

alternate host, however, rust fungi can still 

undergo genetic recombination by anastomosis 

and nuclear exchange in various other ways (see 

p. 625). Different races of a given pathogen can 

be distinguished by their ability to infect any 

host in a set of cultivars containing defined 

resistance genes alone or in combination. Such 

tests are routinely employed by plant pathologists 

for the identification of races, and for 

monitoring their spread (see p. 626). 

Major gene resistance against rust fungi was 

recognized early in the twentieth century by 

Biffen (1905) and others, and extensive breeding 

programmes were initiated. Typically a new 

cultivar produces excellent results for a few 

cropping seasons until resistant races develop 

and spread in the field, thereby rendering the 

breeders’ efforts futile. This is the ‘boom-andbust’ 

cycle. The ‘bust’ of a cultivar can be delayed 

if it contains a ‘pyramid’ of several resistance 

genes which the pathogen may be unable to 

overcome. Sometimes the breeding for resistance 

against one pathogen can lead to susceptibility 

to another, as in the case of the Victoria oat 

cultivar which showed good resistance against 

P. coronata f. sp. avenae but was devastated by 

Cochliobolus victoriae (see p. 471). In addition 

to major gene resistance which is commonly 

associated with the hypersensitive response, 

there are other types of resistance. Some plant 

genes do not afford total resistance but give 

a moderate degree of resistance. If a combination 

of several genes is involved, the resistance 

may well be more durable in the field than 

single-gene resistance. An example of such ‘field’ 

or ‘partial’ resistance is the reduced formation 

of appressoria over stomata of grasses covered 

by a particularly thick wax layer, which seems 

to mask the topographic features of the


stomatal surface acting as the thigmotropic 

signal (Rubiales & Niks, 1996). There is also 

adult-plant resistance, usually an interaction 

between various genes which retard the progress 

of infection to such a degree that the losses are 

reduced to economically acceptable levels. 

22.3 Puccinia graminis, the cause of 

black stem rust 

A connection between the barberry bush (Berberis 

vulgaris) and rust disease on wheat and other 

cereals had been suspected for centuries by 

farmers who noticed the frequent occurrence of 

crop damage around or downwind from barberry 

bushes. Further, an altogether different-looking 

fungus known as Aecidium berberidis was known 

to infect barberry leaves. The formal proof that 

the barberry and wheat pathogens were different 

stages of the same species was made by Anton de 

Bary who, in 1865, performed cross-inoculation 

experiments to show that basidiospores derived 

from germinating teliospores from wheat were 

able to cause spermogonial and aecial infections 

on the barberry. This story has been recounted 

many times, but nobody has told it better than 

Large (1940). 

Black stem rust affects especially wheat but 

also most other cereals and a range of wild 

grasses. Crop losses can be severe as a reduction 

in quantity as well as quality of the grain yield. 

The host epidermis can become ruptured over 

much of its surface in severe infections, thereby 

debilitating the plants (see Fig. 22.8d). Serious 

epidemics have occurred in the past, e.g. in the 

USA in 1904 and especially during the war year 

1916. In fact, losses were so severe (up to 50% in 

the Great Plains; Eversmeyer & Kramer, 2000) 

that P. graminis was seriously considered and 

developed as a biological weapon by the US 

Government during the 1960s (Line & Griffith, 

2001). On susceptible wheat cultivars and without 

chemical protection, P. graminis can cause 

total crop failure. 

Although it is an ecologically obligate 

biotroph, Puccinia graminis is able to infect an 

astonishingly wide range of grass and cereal 

hosts. Gäumann (1959) listed 365 host species in 

Fig 22.8 Puccinia graminis. (a) Spermogonial pustules on the upper surface of a leaf of Berberis vulgaris.Notethedropsofnectar. 

(b) Aecia on the underside of a Berberis leaf.The outer frilly layer is the white peridium, within which is a mass of orange-coloured 

aeciospores. (c) Wheat leaf showing uredinia which appear as reddish-brown powdery masses. (d) Wheat straw showing telia as 

black raised pustules.

PUCCINIA GRAMINIS, THE CAUSE OF BLACK STEM RUST 

621 

54 genera, and this list is still expanding. 

However, no single isolate of P. graminis is able 

to infect all these host species. Instead, the 

species P. graminis can be separated into several 

specialized forms which have become adapted to 

one or a few principal host species. These are 

termed formae speciales (sing. forma specialis, 

abbreviated as ‘f. sp.’) because they cannot be 

distinguished reliably from each other on morphological 

criteria. A morphologically distinct 

form of the same species which can be clearly 

identified by microscopy or other means would 

be called varietas (abbreviated as ‘var.’). 

The most important formae speciales are 

P. graminis f. sp. tritici (on wheat), f. sp. avenae 

(on oat) and f. sp. secalis (on rye). In addition, there 

are several forms on wild grasses, e.g. f. sp. phleipratensis, 

f. sp. lolii and f. sp. agrostidis (Wilson & 

Henderson, 1966; Anikster, 1984). It is possible to 

produce hybrids between some of these formae 

speciales, e.g. between f. sp. tritici and f. sp. secalis 

(Green, 1971). The hybrid aeciospores are not very 

virulent on either principal host, and Green 

(1971) has argued that the hybrids resemble a 

more primitive form of Puccinia graminis with low 

virulence and a wide host range, and that evolution 

in stem rust of cereals is progressing from 

low virulence and a wide host range to high 

virulence and a narrowed host range. 

Each forma specialis on cereals in turn forms 

hundreds of races distinguished by the infection 

responses of differential host cultivars, with 

new races continually evolving (see p. 626). This 

feature highlights the remarkable genetic and 

physiological flexibility of rust fungi. 

22.3.1 Puccinia graminis on barberry 

The basidiospores are released in spring from 

overwintered cereal stubble at about the time 

when fresh barberry leaves unfold. Basidiospores 

are able to germinate by repetition if they do not 

land on a suitable host surface (Fig. 22.10e). 

Infection gives rise to a haploid monokaryotic 

mycelium which shows inter- and intra-cellular 

growth and colonizes the host tissue extensively. 

Generally, monokaryotic stages of rust fungi 

show more widespread colonization of host 

tissue than their dikaryotic counterparts. 

Viewed from the surface, the colonized barberry 

leaf area appears as a yellowish circular lesion. 

On the upper surface of this lesion, several 

flask-shaped spermogonia develop whose necks 

protrude beyond the epidermal layer. Among 

the orange-coloured tapering periphyses surrounding 

the opening of each spermogonium 

are several thinner, hyaline branched hyphae, 

the flexuous (or receptive) hyphae. Lining the 

inside surface of the spermogonium are tapering 

annellides which give rise to small uninucleate 

spermatia. These ooze out through the mouth 

of the spermogonium and are held by the periphyses 

in a drop of sticky sweet-smelling liquid 

(Figs. 22.8a, 22.9a). Within the mesophyll of the 

barberry leaf, the haploid mycelium gives rise 

to several spherical structures called proto-aecia. 

These are mostly made up of large-celled pseudoparenchyma, 

but in the upper region is a cap 

of smaller, denser cells (Fig. 22.9b). 

Single haploid lesions are incapable of 

further development unless cross-fertilization 

occurs. The sweet-smelling spermatial exudate 

contains fructose and several volatile substances 

(see p. 629) which attract insects feeding on the 

nectar and carrying the spermatia around by 

visiting several distinct pustules. The haploid 

pustules are of either of the two mating types, 

(þ) or( ), and if a (þ) spermatium is brought 

close to a flexuous hypha of opposite mating 

type, it produces a short germ tube which 

anastomoses with the flexuous hypha (Craigie, 

1927; Buller, 1950). Nuclear transfer is followed 

by repeated division and migration of the 

introduced nucleus towards the proto-aecium 

(Craigie & Green, 1962). This results in the 

dikaryotization of the haploid mycelium until 

binucleate cells become visible in the cap region 

of the proto-aecium after about 3 days. The 

binucleate cells now start to give rise to chains 

of alternating long and short cells which are also 

binucleate. The longer cells enlarge and become 

aeciospores, but the shorter cells disintegrate as 

the spore chains develop (Fig. 22.9c). During the 

development of the spore chains, the large 

pseudoparenchymatous cells of the protoaecium 

are also crushed and pushed aside. 

Surrounding the chains of spores is a specially 

differentiated layer of cells homologous with the


Fig 22.9 Puccinia graminis. (a) T.S. spermogonium on a leaf of Berberis vulgaris.The spermogonium has penetrated the upper 

epidermis.The wall of the spermogonium is lined by tapering annellides which give rise to spermatia. (b) T.S. leaf of B. vulgaris 

showing a spermogonium and a proto-aecium. (c) T.S. leaf of B. vulgaris showing an aecium in section.The aecium has burst through 

the lower epidermis of the host leaf. Note the columns consisting of alternating large and small cells.The large cells are the 

aeciospores. 

spore chains, whose outer walls are thick and 

fibrous. This layer forms a clearly defined border 

or peridium surrounding the spores. Eventually 

the peridium and spore chains burst through the 

lower epidermis. The peridium ruptures and 

aeciospores are now visible as orange-coloured 

cells enclosed by the white cup-like peridium 

(Fig. 22.8b). Since the aecia are commonly seen 

clustered together beneath a spermogonial 

lesion, this stage is popularly known as the 

cluster-cup stage. In a section through the centre 

of a group of young aecia, it is usually possible to 

find the spermogonia penetrating the upper 

epidermis and the aecia penetrating the lower. 

The aeciospores are violently projected from the 

end of the spore chain by rounding off of the 

flattened interface between adjacent spores 

(Ingold, 1971). Aeciospores are unable to reinfect 

barberry but readily infect wheat or 

other grasses. 

It is relatively easy to establish and maintain 

P. graminis in garden situations by planting 

B. vulgaris and allowing Agropyron repens to grow 

underneath (Webster et al., 1999). The form most 

likely to grow is P. graminis f. sp. secalis which 

readily alternates between Berberis and grasses 

in Britain (Wilson & Henderson, 1966). In other 

countries the connection between Berberis and 

P. graminis f. sp. tritici is strong, and the first 

barberry eradication laws were implemented 

long before de Bary had formally proven the 

connection. The first recorded cases of such laws 

were in Rouen in 1660 and Massachusetts in 1755. 

The greatest effort by far was the barberry 

eradication campaign undertaken as a consequence 

of the 1916 epidemic in the United States. 

Widespread eradication of susceptible Berberis 

spp. started in 1918 and continued on a massive 

scale well into the 1930s, and locally for several 

decades afterwards. Overall, this campaign is 

considered to have been successful, with wheat 

rust epidemics much reduced in severity, especially 

on a local scale. Because aeciospores are not 

particularly long-lived and are not produced in 

vast numbers, the direct impact of barberry 

bushes on wheat crops is limited to less than 

2 miles. Perhaps more importantly, barberry 

eradication also retarded the evolution of new 

races of P. graminis due to the reduced ability of 

the pathogen to reproduce sexually. Campbell 

and Long (2001) have provided a highly readable 

account of the eradication campaign in the USA.


623 

22.3.2 Puccinia graminis on cereals 

A symptom of infection on wheat leaves and 

stems is the appearance of brick-red pustules 

(uredinia) between the veins. Uredinia contain 

stalked, one-celled dikaryotic urediniospores 

which burst through the epidermis (Figs. 22.8c 

and 22.10a,b). These have a spiny wall which has 

four thinner areas (germ pores) near the middle 

of the spore. The urediniospores are detached by 

wind and blown to fresh wheat leaves upon 

which they germinate by extruding a germ tube 

from one of the germ pores. Germination 

requires free water (e.g. night-time dew) and 

proceeds optimally at about 20°C. Infection 

Fig 22.10 Puccinia graminis f. sp. secalis. (a) T.S. stem through a uredinium.The stalked unicellular urediniospores are protruding 

through the ruptured host epidermis. A teliospore (t) has also been formed. (b) Higher-power detail of urediniospores. Note the 

germ pores (g) and the haustoria (h) in the host cells. (c) Germination of urediniospores on host leaf. Note the directional growth 

of the germ tubes perpendicular to the long axes of the epidermal cells, towards the stomata. (d) T.S. leaf sheath through a telium. 

The stalked teliospores are projecting through the ruptured epidermis.Drawing to same scale as (a). (e) Germination of teliospores 

to form metabasidia bearing sterigmata and basidiospores.One basidiospore is giving rise to a secondary spore.


follows the usual pattern for dikaryotic propagules, 

i.e. via an appressorium through a stoma 

as shown in Fig. 22.5b. Within about 7 21 days 

of infection, a new crop of urediniospores is 

formed so that inoculum can build up rapidly 

within a crop. A single uredinium may produce 

between 50 000 to 400 000 spores, and there may 

be 4 5 generations of urediniospores in the 

growing period of a wheat crop. Disease development 

occurs best at daytime temperatures 

around 30°C. This may explain why stem rust 

of wheat is particularly prevalent in areas with 

a continental climate, whereas it is not a serious 

disease, for example, in Britain. 

Puccinia graminis f. sp. tritici can survive the 

winter in the mild climates, e.g. of Mexico and the 

Southern USA (see Fig. 22.11) as uredinial infections 

on its principal host, i.e. wheat crops and 

volunteer plants. Despite the almost complete 

elimination of the barberry, infections with 

P. graminis f. sp. tritici still occur every year in 

North America from uredinial lesions overwintering 

in the South. Urediniospores are longer-lived 

than aeciospores, and waves of inoculum can 

move northwards with the prevailing southerly 

winds. The track taken is called the ‘Puccinia 

pathway’ (Agrios, 2005). Using small aeroplanes, 

urediniospores have been detected at altitudes 

as high as 5000 feet. The total distance travelled 

each year from the Southern USA to Canada 

can be in excess of 2000 miles (Stakman & 

Christensen, 1946), but in most cases migration 

occurs in several shorter intervals, with new crops 

of uredinia being produced en route (Eversmeyer & 

Kramer, 2000). Consequently, infections start 

at successively later dates the further north 

the epidemic moves (Fig. 22.11). Attempts have 

been made to interrupt this migration by planting 

cultivars with different resistance genes in 

different regions of the Puccinia pathway (Frey 

et al., 1973). Towards the end of the season there 

may be a reversal of the flow of air, so that wheat 

Fig 22.11 The‘Puccinia pathway’ in North America, with dates indicating the average annual arrival of P. graminis f. sp. tritici in 

the wheat fields.The fungus regularly overwinters in the uredinial state south of 30° Northern latitude, and occasionally as far north 

as 34°. Redrawn from Roelfs (1986) and several other sources.


625 

in Texas and Mexico may be infected from 

urediniospores derived from the northern areas 

(Pady & Johnston, 1955). Similar long-distance 

transport of urediniospores has been reported 

from Europe and India (Nagarajan & Singh, 1990). 

Late in the season, uredinial lesions gradually 

turn to producing teliospores instead of urediniospores. 

Telial pustules appear as black raised 

streaks along leaf-sheaths and stems of infected 

plants (Fig. 22.8d). Teliospores are initially 

binucleate, but soon the two nuclei fuse and 

the spores survive the winter in the diploid 

state. A period of maturation corresponding to 

winter dormancy is required before teliospores 

are competent to germinate. When they do 

germinate, each of the two cells emits a fourcelled 

promycelium or metabasidium. Meiosis 

gives rise to four nuclei which migrate into 

the four basidiospores and then perform one 

further mitotic division. Each cell of the metabasidium 

bears one basidiospore containing two 

nuclei of the same mating type. The basidiospores 

are short-lived and do not travel far, and the 

teliospore state is of no significance in an 

agricultural context if no barberry bushes are in 

the vicinity. 

22.3.3 Resistance breeding and 

physiological races of P. graminis 

f. sp. tritici 

If the spores of a given isolate of P. graminis 

f. sp. tritici are inoculated onto a range of wheat 

cultivars, these hosts will differ in their response. 

Some may prove to be resistant, others highly 

susceptible, whilst yet others may be intermediate 

in their reaction. Spores from a second 

source may give an entirely different pattern 

of response. Using the reactions of different 

wheat cultivars, it has proven possible to classify 

P. graminis f. sp. tritici into over 300 physiological 

races. The existence of such a large number of 

races may be due to several factors. 

1. Sexual recombination. New races of rust 

are often found adjacent to barberry bushes. 

Further, following inoculation with a single race, 

a number of variants may be found among the 

aeciospore progeny. 

2. Anastomosis on the principal host. If two 

uredinial mycelia growing on the same host leaf 

come into hyphal contact, anastomosis may 

result. This can lead to the exchange of genetic 

material known as somatic hybridization. The 

simplest way is the exchange of entire nuclei 

which will lead to the formation of new heterokaryons 

and their dissemination as urediniospores 

(Ellingboe, 1961). However, when two 

different races of P. graminis were inoculated 

simultaneously onto a susceptible wheat cultivar, 

at least 15 different races were identified 

among the urediniospore progeny, which is more 

than would be expected from simple nuclear rearrangement 

(Watson & Luig, 1958; Bridgmon, 

1959). Puccinia graminis contains a haploid set of 

18 chromosomes (Boehm et al., 1992), and the 

exchange of any of them in the dikaryotic 

mycelium during synchronous nuclear division 

is conceivable (Hartley & Williams, 1971). 

Additionally, parasexual recombination between 

chromosomes could occur. Park et al. (1999) have 

provided evidence of the occurrence of somatic 

hybridization in P. triticina in the field. 

3. New races may arise by mutation, as shown 

by Park et al. (1995) for the brown leaf rust of 

wheat, P. triticina. 

The existence of this large range of rust races 

complicates the task of the plant breeder, but 

fortunately all these races are not prevalent in an 

area at any one time. Therefore the breeding of 

resistant cultivars remains practicable and profitable 

(Johnson, 1953; Dyck & Kerber, 1985). The 

frequency of different rust races varies over the 

years, reflecting the changes in the wheat 

cultivars planted (Fig. 22.12). A new race may 

suddenly build up in frequency, as shown by the 

appearance of Race 15 (actually a sub-race or 

biotype referred to as Race 15B) in Canada. The 

appearance of new races presents a problem to 

plant breeders, and it is clear that the breeding 

and release of resistant cultivars has to be 

carefully co-ordinated. 

The original scheme for using host differentials 

was devised by Stakman and Levine (1922) 

who used 12 different wheat cultivars (‘standard 

differentials’) to discriminate between the physiological 

races (‘standard races’). The standard 

differentials frequently failed to reveal important


Fig 22.12 Diagrammatic representation of the distribution in 

Canada of eight physiological races of wheat stem rust during 

the period 1919 1951 (after Johnson,1953). 

changes in the virulence of the rust population, 

and this led to the use of supplementary 

differentials to differentiate between further 

physiological races. Gradually the nomenclature 

for numbering rust races became quite 

complicated. In the wake of the acceptance of 

the gene-for-gene concept (see Flor, 1971), a 

more rational way of identifying the 

physiological races was to base their classification 

on the resistance genes of the host plant. Using 

the wheat cultivar Marquis, several ‘single gene 

lines’, i.e. wheat cultivars carrying single resistance 

genes, have been generated. The resistance 

genes were given the symbols Sr1, Sr2, etc. 

(Sr for ‘stem rust’). Some 40 resistance genes 

are known (Roelfs, 1985). Efforts at characterizing 

pathogen races are now standardized by 

means of an international nomenclatural system 

(Roelfs & Martens, 1988). An authoritative 

account of the history and importance of rust

OTHER CEREAL RUSTS 

627 

race characterization has been written by Roelfs 

(1984). 

The serious race 15B epidemics of the early 

1950s (see Fig. 22.12) resulted in the replacement 

of the then prevalent cultivars by others such as 

‘Selkirk’, which carried several resistance genes 

and remained resistant to P. graminis f. sp. tritici 

in North America for several decades (Roelfs, 

1985). Several wheat varieties more recently 

released have also retained their resistance for 

many years in the field (Roelfs, 1984; Dyck & 

Kerber, 1985), so that no major stem rust 

epidemic has occurred in the USA during the 

past 50 years. This success is probably due to two 

main reasons, namely the combination of several 

resistance genes in one cultivar which the rust 

fungus is apparently unable to overcome, and 

the stabilization of rust races by the elimination 

of sexual reproduction as a consequence of the 

barberry eradication campaign. 

22.4 Other cereal rusts 

Although potentially the most damaging cereal 

rust, P. graminis has lost much of its menace 

for reasons discussed in the preceding section. 

Several other rust species now cause more 

serious crop losses than P. graminis. These are 

briefly discussed below. Cereal rusts are primarily 

controlled by breeding of resistant cereal 

cultivars, and this is an ongoing battle against 

new races which, once arisen, are capable of 

spreading rapidly and on a global scale (Chen, 

2005; Kolmer, 2005). Chemical control by the 

application of fungicides is practised to protect 

crops grown for seed production, and to control 

severe outbreaks of rust if resistance fails. Fungicides 

used include the systemic strobilurin-type 

compounds and the ergosterol biosynthesisinhibiting 

triazoles (see Fig. 13.15), as well as 

various protectant compounds. 

22.4.1 Puccinia triticina (brown leaf 

rust of wheat) 

Puccinia triticina was formerly named P. recondita 

f. sp. tritici, but Zambino and Szabo (1993) and 

Anikster et al. (1997) have shown that it is not 

closely related to P. recondita, which infects rye 

but is only of minor significance. Puccinia triticina 

has displaced P. graminis as the economically 

most important rust of wheat especially in North 

America and Eastern Europe (Samborski, 1985). 

This species is macrocyclic, with Thalictrum speciosissimum 

(¼ T. flavum; Ranunculaceae) serving as 

the alternate host, although it seems to survive 

mainly in the uredinial state. Its epidemiology is 

therefore similar to that of P. graminis f. sp. tritici 

(Eversmeyer & Kramer, 2000). The temperature 

optima for urediniospore germination and infection 

(about 18°C) and sporulation (25°C) are 

lower than those of P. graminis (Singh et al., 

2002). Teliospores are not readily formed, and 

the disease symptoms are easily recognized by 

the chocolate-brown uredinial lesions on wheat 

leaves. There is no infection of the stem, in contrast 

to P. graminis. Triticale, a hybrid between 

wheat (Triticum) and rye (Secale), is also affected. 

About 50 Lr (‘leaf rust’) resistance genes are 

known, and wheat leaf rust is currently controlled 

mainly by using cultivars containing 

a pyramid of several of these Lr genes. 

22.4.2 Puccinia striiformis (stripe rust or 

yellow rust on wheat and barley) 

The alternate host of this rust species has not 

yet been found, and it may no longer have one. 

Therefore, its life cycle is probably confined to 

the grass or cereal hosts on which uredinia and 

telia are produced. This rust can be distinguished 

from P. triticina by its yellow uredinia which are 

arranged in stripe-like rows following the leaf 

veins. There are several formae speciales, but their 

host ranges overlap to a greater extent than 

in the other cereal rusts and they are therefore 

less clearly delimited. The most important 

forms are those on wheat (f. sp. tritici) and 

barley (f. sp. hordei). The temperature optima of 

P. striiformis are the lowest of any of the common 

cereal rusts, with urediniospore germination 

and penetration around 10°C, and urediniospore 

production at 12 15°C (Singh et al., 2002). This 

species overwinters by using winter crops and 

volunteers as a ‘green bridge’, and can cause 

early epidemics in spring. Zadoks and Bouwman 

(1985) have estimated that a single uredinium


per hectare is sufficient to spark an epidemic. 

Even if no lesions are seen on winter wheat, the 

rust may still be present, surviving as latent 

infections. Crop losses can be severe in the cooler 

climates of North-Western Europe and North 

America where winter cereals, especially winter 

wheat, are widely grown (Stubbs, 1985). Like 

most other rusts, P. striiformis is controlled 

mainly by resistance breeding (Line, 2002). Chen 

(2005) has given a detailed account of recent 

epidemics and migrations of P. striiformis. 

22.4.3 Puccinia hordei (barley leaf rust or 

‘dwarf rust’) 

This macrocyclic rust alternates between 

Ornithogalum spp. (Hyacinthaceae) as the alternate 

host and cultivated and wild barley (Hordeum) 

species as principal host. Clifford (1985) considered 

this species to be the most important rust on 

barley. The uredinial lesions are brownish in 

colour and are smaller than those of other rusts, 

hence the name ‘dwarf rust’. In agricultural 

situations, the alternate host is probably of little 

importance as the fungus can overwinter in the 

uredinial state on volunteer plants or winter 

barley. Its optimum temperatures for infection 

(15°C) and sporulation (10 20°C) are almost as 

low as those for P. striiformis. In Europe in the 

1970s, P. hordei caused major crop losses because 

the cultivars sown were highly susceptible. 

However, the situation seems to have improved 

in recent years, and several cultivars showing 

good partial resistance have been bred (Niks et al., 

2000). 

22.4.4 Puccinia coronata (crown rust of oats 

and forage grasses) 

This rust is so named because of the spiny 

extensions at the apex of its teliospore (see 

Fig. 22.13a). It is the most damaging disease on 

oats and has probably been a pathogen since oats 

were first cultivated (Simons, 1985). In addition to 

oats, numerous other grasses are infected, including 

important forage grasses such as the perennial 

ryegrass, Lolium perenne, for which separate 

resistance breeding programmes have been 

initiated (Kimbeng, 1999). Heavily infected 

meadows can acquire a distinctly orange hue 

due to the urediniospores being produced in 

great abundance. There are no formae speciales 

other than f. sp. avenae on oats because the 

delimitation between strains on different grasses 

is not clear cut. Puccinia coronata is macrocyclic, 

alternating with Rhamnus (buckthorn) shrubs. 

As with P. graminis and P. triticina, a standardized 

nomenclature for identifying races of P. coronata 

f. sp. avenae has been proposed. This is based on 

a differential comprising 16 oat cultivars carrying 

single resistance (Pc) genes (Chong et al., 2000). 

In total, about 100 resistance genes are known, 

and resistance breeding is the main strategy to 

control oat rust. Heavy infections of susceptible 

cultivars can result in total crop failure. 

Even well-known rust species can harbour 

surprises upon close inspection, and one of these 

was the description of a form of P. coronata 

infecting Bromus inermis as its principal host. 

Anikster et al. (2003) described that germinating 

teliospores of this form produced only two 

basidiospores, each of which had four instead 

of the usual two nuclei and was self-fertile, i.e. 

infection on Rhamnus cathartica gave rise to aecia 

without spermogonia. This fungus is therefore 

homothallic, like the correlated microcyclic 

P. mesnieriana (Anikster & Wahl, 1985) and probably 

the barley form of P. coronata. In contrast, 

P. coronata f. sp. avenae is heterothallic with a 

tetrapolar mating system, i.e. two mating type 

loci with two alleles each, instead of the usual 

bipolar system (Narisawa et al., 1994). 

22.4.5 The origin of cereal rusts 

It is generally assumed that the cereal rusts 

evolved at the centre of origin of the wild grasses 

which were the progeny of cultivated cereals. 

The argument is strengthened if the alternate 

host is native to the same area. This topic has 

been discussed extensively by Anikster and Wahl 

(1979) and Wahl et al. (1984). Puccinia graminis is 

thought to have evolved with Berberis vulgaris, 

which is of Asian origin, moving westwards to 

an area from Transcaucasia to the Western 

Mediterranean, which is the centre of origin of 

wheat and rye. Westward migration must have 

occurred early in the history of agriculture 

because 3300-year-old P. graminis-infected cereal

PUCCINIA AND UROMYCES 

629 

Fig 22.13 Teliospores of rust fungi belonging to the Pucciniaceae sensu Dietel. (a) Puccinia coronata.Notethe‘crown’ofspine-like 

wall extensions at the teliospore apex. (b) Uromyces appendiculatus.The teliospore is one-celled. (c,d) Phragmidium mucronatum. 

(c) Teliospore freshly mounted in water. (d) Spore after about15 min in water.The base of the pedicel has broken, exuding a 

large amount of mucilage which has been made visible by replacing the water with dilute Indian ink. (e) Triphragmium ulmariae. 

The teliospore is three-celled. (f) Gymnosporangiumfuscum. Note the long teliospore stalk. (a,b,e) to same scale; (c,d) to same scale. 

remains have been found in Israel (Kislev, 1982). 

The centre of origin of P. triticina and its aecial 

host, Thalictrum, is probably also in the Western 

Mediterranean, as is that of Puccinia striiformis. 

Rhamnus and wild oats are common in Israel, 

as is P. mesnieriana, suggesting that this is where 

P. coronata may have its origin. Wild barley 

species, especially Hordeum spontaneum, are also 

very common in Israel and adjacent countries 

where barley has been cultivated since the 

dawn of agriculture. Since the alternate host of 

P. hordei, Ornithogalum, is also found there and is 

profusely infected, this region may be where 

P. hordei evolved. 

22.5 Puccinia and Uromyces 

The genus Puccinia is by far the largest among 

the Uredinales, comprising about 4000 species 

(Kirk et al., 2001). The most readily recognized 

characteristic is the teliospore which usually 

contains two darkly pigmented cells borne on 

a thin hyaline stalk. Puccinia spp. are pathogenic 

mainly on Angiosperms, and especially on 

grasses as principal hosts. The genus Uromyces 

(about 800 spp.) is similar in appearance to 

Puccinia, differing mainly in its teliospore, which 

is commonly one-celled (Fig. 22.13b). Several 

Puccinia spp. also produce a certain proportion 

of one-celled teliospores (called mesospores) in 

their telia, and it is therefore easy to imagine how 

the one-celled teliospore of Uromyces could have 

evolved. DNA sequencing data support a close 

relationship between the genera Puccinia and 

Uromyces (Maier et al., 2003). 

22.5.1 Other common Puccinia spp. 

Puccinia sorghi was so named because Schweinitz, 

when he first described it, erroneously believed


that he was dealing with infected Sorghum 

material. It is, however, a pathogen of maize 

and can be encountered wherever that crop is 

grown. Since maize is native to Central America, 

the pathogen probably also originated there. 

In Europe, crop losses are not generally sufficiently 

severe to warrant control measures 

(Smith et al., 1988), but elsewhere breeding programmes 

are in operation and fungicides are 

also occasionally used (Hooker, 1985). The fungus 

produces numerous chocolate-brown uredinia 

on the leaves of grain and fodder maize. It is 

macrocyclic and heteroecious, alternating with 

Oxalis spp. 

Several macrocyclic Puccinia spp. not causing 

agriculturally significant disease are frequently 

encountered in the field. An example is P. caricina 

which has sedges (Carex spp.) as its principal host 

and produces spermogonia and aecia on 

Urtica (stinging nettle). The latter are associated 

with growth deformations (Plate 12b). Another 

ubiquitous species is P. poarum, with grasses of 

the genus Poa as principal and Tussilago farfara 

(coltsfoot) as alternate hosts. This species is 

unusual in completing two life cycles per 

growing season, with aecia appearing in May 

and August (Wilson & Henderson, 1966). Mint 

rust (P. menthae) is autoecious and macrocyclic. 

All the above species are abundant in Europe and 

on most other continents. 

Puccinia punctiformis is a systemic autoecious 

rust attacking Cirsium arvense (creeping 

thistle). In spring, infected plants are clearly 

distinguishable by their yellowish appearance 

and appressed leaves, and by the strong sweet 

smell associated with numerous spermogonia 

which develop all over the infected shoots. 

These aromatic substances include common 

fragrance molecules such as benzaldehyde, 

2-phenylethanol, indole and phenylacetaldehyde 

(Connick & French, 1991), and it is possible to 

smell infected thistles from a distance of several 

metres. All these substances are produced by 

a wide range of fungi and, with the exception 

of indole, also by the host plant during 

flowering. The infections develop from a dikaryotic 

mycelium overwintering systemically in 

the rootstock. The haploid condition of the 

spermogonial tissue is probably established by 

de-dikaryotization as new shoots are infected in 

spring. Transfer of spermatia to compatible 

flexuous hyphae results in dikaryotization, and 

the next structures to form resemble uredinia 

with chocolate-brown spores. They are sometimes 

called uredinoid aecia. The urediniospores 

can infect healthy thistles and normal uredinia 

develop on these. Later in the season, teliospores 

develop (Buller, 1950). 

A yet more specialized way to attract insect 

pollinators has been developed by a complex of 

rusts attacking Brassicaceae (Arabis spp.). Infected 

plants produce the same fragrances as Cirsium 

infected by P. punctiformis, plus many more 

(Raguso & Roy, 1998). Further, infected plant 

organs are morphologically modified to form 

flower-like structures called pseudoflowers. 

Intriguingly, these do not resemble the flowers 

of the host, but those of taxonomically unrelated 

plant species such as buttercups (Ranunculus spp.), 

which often grow in the same habitats (Roy, 1994). 

The combination of scent, shape, colour and 

nectar in this floral mimicry is necessary to 

attract a wide range of insects (Roy, 1994; Roy & 

Raguso, 1997). Several rust species can stimulate 

the production of such pseudoflowers on Arabis 

spp., including the macrocyclic heteroecious 

P. monoica which alternates with grasses, and 

correlated autoecious and microcyclic species 

(Roy et al., 1998). 

22.5.2 Uromyces 

Common species of Uromyces are U. ficariae, a 

microcyclic species forming brown telia on 

Ranunculus ficaria, and U. dactylidis with urediniospores 

and teliospores on grasses (Dactylis, 

Festuca and Poa) and aecia on Ranunculus spp. 

Uromyces dianthi produces uredinia and telia on 

Dianthus (carnation) and other ornamental flowers, 

with Euphorbia spp. as the alternate host. 

However, the most important species of Uromyces 

are those infecting legumes (Fabaceae), and 

because of the ease with which legumes such as 

Pisum, Phaseolus and Medicago can be cultivated in 

the laboratory, their rusts have been used for 

numerous studies of fundamental physiological 

aspects such as differentiation of infection 

structures and haustorial functioning, which

OTHER MEMBERS OF THE PUCCINIACEAE 

631 

have been mentioned at the beginning of this 

chapter. 

Uromyces appendiculatus is a macrocyclic autoecious 

rust on French bean (Phaseolus vulgaris) and 

many other leguminous plants. Several varieties 

have been distinguished. The fungus survives the 

winter as teliospores on plant debris or, in milder 

conditions, as urediniospores (McMillan et al., 

2003). As one would expect of a situation in which 

a rust fungus undergoing sexual reproduction is 

being controlled by the breeding of resistant 

cultivars, numerous (more than 200) physiological 

races of U. appendiculatus are known. Control is 

by means of resistant cultivars or, if these fail, 

with protectant fungicides (maneb and chlorothalonil). 

Strobilurin-type compounds are also 

now used against U. appendiculatus. Since beans 

are a higher-value crop than cereals, fungicide 

applications are generally more profitable. 

Uromyces viciae-fabae has a similar life cycle to 

that of U. appendiculatus, but it infects broad bean 

(Vicia faba) and numerous other plants. It is a 

cosmopolitan species but seems to cause lesser 

damage than U. appendiculatus. 

Uromyces pisi is heteroecious, producing spermogonia 

and aecia on Euphorbia cyparissias and 

uredinia and telia on various leguminous hosts, 

especially pea (Pisum sativum). Infections on the 

alternate host are of biological interest because 

the fungus infects systemically and causes its 

alternate host to produce pseudoflowers, at the 

expense of its real flowers (Pfunder & Roy, 2000). 

The name U. pisi is now known to cover a 

complex of several biologically distinct species 

which are united by their alternate host but 

infect different members of the Fabaceae as 

principal hosts (Pfunder et al., 2001). 

22.6 Other members of the 

Pucciniaceae 

22.6.1 Phragmidium 

All Phragmidium spp. are autoecious and confined 

to the Rosaceae. The two best-known species, 

both extremely common in Europe, are P. violaceum 

on leaves of the Rubus fruticosus species 

aggregate (bramble or blackberry; Plate 12c) and 

P. mucronatum on roses. Both are macrocyclic. The 

uredinial and telial stages are readily recognized 

from above as chlorotic or purple lesions, and 

the spores are formed on the underside of the 

host leaves. They are yellowish-orange (urediniospores) 

or violet to black (teliospores). The 

teliospores contain mostly 4 (P. violaceum) or 

6 8 (P. mucronatum) cells with very dark and 

rough walls, and are borne on a long stalk 

(pedicel) which becomes easily detached from the 

lesions. When teliospores are mounted in water, 

the base of the pedicel breaks and exudes a large 

amount of mucilage (Figs. 22.13c,d). In nature, 

this may facilitate the attachment of the teliospore 

to adjacent surfaces during overwintering 

(Ingold et al., 1981). The teliospores of P. mucronatum 

were among the first fungus spores illustrated 

by Robert Hooke in 1667 soon after the 

invention of the microscope (see Large, 1940). 

Phragmidium violaceum shows promise as a 

biocontrol agent against the spread of brambles 

which were introduced into Australia and are 

spreading there in their typically uncontrollable 

manner (Mahr & Bruzzese, 1998). Phragmidium 

mucronatum is not tolerated by rose breeders or 

hobby gardeners; it is controlled by fungicide 

applications. Removal of fallen leaves in autumn 

can also help to control the disease. 

22.6.2 Gymnosporangium 

There are about 60 species of Gymnosporangium 

which produce their spermogonia and aecia 

on members of the Rosaceae, and telia on 

Cupressaceae. Uredinia are not normally 

formed. One of the most commonly encountered 

species is G. fuscum (¼ G. sabinae), the pear trellis 

rust, which alternates between Juniperus spp. of 

the sabina group (principal host) and pear trees. 

The dikaryotic mycelium can survive for many 

years in the principal host, and repeated production 

of telia is associated with a spindle-shaped 

swelling or canker of the infected trunk or twig. 

Spore-bearing telia are produced in the spring 

as horn-like outgrowths which greatly expand 

during rainfall due to swelling of the long teliospore 

stalks (Plate 12d; Fig. 22.13f). Teliospores at 

the surface of a swollen telial horn germinate 

to release basidiospores at the time of leaf


bud of the alternate host. Between late spring 

and autumn, infected pear leaves show bright 

orange-coloured lesions up to 1 cm in diameter 

(Plate 12e). These give rise to spermogonia at the 

upper leaf surface, and later to aecia at the lower 

surface. The aecia are greatly swollen and elongated. 

Eventually, they rupture at their sides, 

leaving a cap joined to the aecium by trellis-like 

threads (Plate 12f). The characteristic tube-like 

aecia of Gymnosporangium are referred to as 

roestelioid, after the generic name Roestelia 

previously given to such aecial stages. Aeciospores 

infect susceptible Juniperus spp. in 

the autumn (Borno & van der Kamp, 1975). 

Gymnosporangium fuscum can cause serious 

damage to pear trees because heavy infections 

reduce the photosynthetic capacity of the trees, 

and yields and ultimately the trees themselves 

decline after severe successive infections. This 

species is very much on the increase in Europe 

and elsewhere, especially because of the planting 

of ornamental Juniperus spp. (e.g. Chinese juniper) 

and pear trees side-by-side in gardens. Whereas 

the pathogen needs to infect the alternate 

host afresh each year, it can survive almost 

indefinitely in its principal host once this has 

become infected. Several communities and 

countries have therefore launched eradication 

schemes to remove infected Juniperus trees. 

Since the basidiospores do not normally travel 

distances longer than about a mile, this approach 

can reduce the infection pressure to acceptable 

limits. Chemical control of G. fuscum on pear 

trees is possible but obviously not desirable 

(Ormrod et al., 1984). 

Several related species of Gymnosporangium are 

also commonly encountered, e.g. G. clavariiforme, 

which alternates between Juniperus communis 

(a plant not infected by G. fuscum) and Crataegus 

spp., or G. cornutum on J. communis and Sorbus 

aucuparia (mountain ash, rowan). Gymnosporangium 

juniperi-virginianae is the cause of North 

American cedar-apple rust, alternating between 

the ‘Eastern red cedar’ (Juniperus virginiana) and 

apple (Malus spp.). On the principal host, telia 

often develop from gall-like deformations called 

‘cedar-apples’. This species causes considerable 

economic damage in North America where it is 

native. It does not seem to be present in Europe as 

yet (Smith et al., 1988). It can be controlled by 

fungicide applications similar to those effective 

against apple scab caused by Venturia inaequalis 

(see p. 478). 

22.6.3 Hemileia vastatrix 

The phylogenetic position of H. vastatrix, the 

cause of coffee leaf rust, has not yet been 

resolved. It appears to be an ancient rust lineage 

possibly pre-dating the separation between 

Pucciniaceae and Melampsoraceae sensu Dietel 

(Wingfield et al., 2004). We assume that it belongs 

to the Pucciniaceae sensu Dietel because its 

teliospores are stalked. Coffee is one of the 

most valuable commodities on the world 

market, and H. vastatrix causes the most important 

disease of it. So far, only urediniospore, 

teliospore and basidiospore stages have been 

reported, and an alternate host has not been 

found. Therefore, it is likely that the disease is 

spread exclusively by urediniospores. Hemileia 

was so named because its urediniospores are 

unusual in being half smooth, with the other 

half of their surface spiny like the urediniospores 

of other rusts. Urediniospores of H. vastatrix 

infect coffee leaves in the typical rust fashion, 

i.e. they require free water for germination and 

form appressoria over stomata. Resistance is 

expressed as a hypersensitive response after the 

formation of the first haustorium (Silva et al., 

2002). Unusual features include details of appressorium 

formation (Coutinho et al., 1993), the 

fact that infection occurs exclusively through 

stomata located on the lower (abaxial) leaf 

surface, and the formation of urediniospores 

and teliospores through stomata (Ward, 1882), 

i.e. typical rust pustules rupturing the epidermis 

are not formed. Another remarkable feature is 

that removal of the coffee berries, which are not 

themselves infected by H. vastatrix, drastically 

reduces the severity of the disease (Monaco, 

1977). 

The story of coffee rust is fascinating and its 

first part has been told eloquently by Large 

(1940). The disease was discovered on cultivated 

coffee in Ceylon (now Sri Lanka) in about 1869. 

The origin of H. vastatrix seems obscure. Ceylon 

was then the major coffee-growing region for the

OTHER MEMBERS OF THE PUCCINIACEAE 

633 

British Empire in which coffee drinking was 

fashionable. Initial outbreaks of the rust were 

not taken seriously because severe infections, 

which led to the defoliation of trees, showed 

their effect only in subsequent seasons in the 

shape of a gradual debilitation of the coffee 

plants (see Brown et al., 1995). After the failure 

of several successive crops, H. Marshall Ward 

was sent to Ceylon in 1879 to investigate the 

problem, and he succeeded in elucidating the life 

cycle of H. vastatrix and the details of the 

infection process (Ward, 1882). Unfortunately, 

by that time it was too late to save the coffee 

production of Ceylon and other South East Asian 

countries to which the rust had spread in the 

meantime. As a consequence of coffee rust, tea 

became the main crop of Ceylon, and tea 

drinking was promoted throughout the Empire 

(Schuman, 1991). 

The spread of coffee rust to all major coffeegrowing 

regions of the world (except Hawaii) is 

charted in Fig. 22.14. It is probably the combined 

result of human travel and natural long-distance 

transport. The much-dreaded jump from West 

Africa, where the disease arrived in the 1960s, to 

Brazil probably occurred during a period between 

January and April in the late 1960s as a one-off 

transport of urediniospores by wind (Bowden 

et al., 1971). A similar chance event of wind-borne 

intercontinental rust spore traffic may have 

happened in June 1978 when the sugarcane rust 

(Puccinia melanocephala) arrived in the Dominican 

Republic, probably from Cameroon (Purdy et al., 

1985; Brown & Hovmøller, 2002). Within coffee 

plantations, urediniospores of H. vastatrix may be 

spread both by wind and by rain splash. 

Coffee rust can be controlled by fungicide 

applications, with copper-containing compounds 

being the most useful even today (Bock, 1962; 

Kushalappa & Eskes, 1989). Since the timing of 

fungicide application is crucial, disease forecast 

models to optimize fungicide applications are 

being developed. Resistance breeding is also 

promising. The main cultivated coffee plant, 

Coffea arabica, was clonally propagated by the 

Dutch in the late seventeenth century and is 

therefore genetically quite uniform across many 

coffee-growing areas, but the introduction of 

Fig 22.14 The journey of coffee rust (Hemileia vastatrix) 

aroundtheworld.Timepointsoffirstrecordsareindicated. 

Redrawn from Schuman (1991), with supplementary data from 

Monaco (1977) and Schieber and Zentmyer (1984).


resistance genes from wild coffee species can give 

rise to cultivars with stable partial resistance. 

Altogether 9 major resistance genes and about 30 

relatively stable races of H. vastatrix are known 

(Monaco, 1977; Kushalappa & Eskes, 1989). 

22.7 Melampsoraceae 

22.7.1 Cronartium 

About 20 species of Cronartium are known. They 

are macrocyclic and heteroecious, alternating 

between various dicotyledonous plants as principal 

hosts and Pinus spp. as alternate hosts. The 

one-celled teliospores of Cronartium are produced 

in long columns projecting out of the telia. The 

teliospores are attached to each other but not to 

their host tissue, and they are unstalked. In 

general, the mycelium on the alternate host is 

perennial whereas the principal host needs to be 

re-infected afresh each growing season. Reduced 

forms with aecia on Pinus spp. are named 

Peridermium (or Endocronartium). Their ability to 

re-infect the Pinus host by means of aeciospores 

produced from aecia indicates that these are 

aecidioid uredinia (Ono, 2002). Cronartium and 

Peridermium spp. form a well-resolved monophyletic 

group of rust species also clustering 

together with their telial hosts (Vogler & Bruns, 

1998). Economic damage is generally caused 

mainly by the infection of Pinus spp. The 

symptoms are similar between the various 

species considered below. 

Cronartium ribicola causes white pine blister 

rust, which alternates between Ribes spp. 

(currants, gooseberry etc.) and those Pinus spp. 

which produce their needles in groups of five 

(e.g. P. strobus). Infection of the alternate host 

proceeds by basidiospores germinating on the 

needles of Pinus spp. in autumn. During the 

following spring, infection spreads to the needle 

base and ultimately to the branches or main stem 

where lesions become visible as cankers. These 

produce spermogonia and aecia (Smith et al., 

1988). Large cankers can girdle the entire trunk 

of trees, causing host death and widespread 

economic and ecological damage to Pinus forests 

especially in North America and Europe. In 

summer, aeciospores infect Ribes spp., where 

uredinial and telial lesions arise on the leaves. 

Severe infections can cause premature leaf 

abscission, but this stage of the disease is not 

economically as serious as that on Pinus. Itisat 

present impossible to control C. ribicola. Since 

its basidiospores cannot travel long distances, a 

massive attempt at eradicating the principal host 

was launched in North America. However, this 

campaign failed because Ribes spp. are too 

abundant and re-grow easily from roots or 

seeds remaining in the soil (Maloy, 1997). 

Fungicide treatment of infected trees was 

attempted by aerial sprays with cycloheximide 

(actidione), but this was ineffective (Dimond, 

1966; Maloy, 1997). More recently, attention 

has turned towards the breeding of resistant 

cultivars. Although C. ribicola is probably of 

Asian origin and was introduced into Europe 

in the eighteenth century and to North America 

around 1900, major gene resistance does exist 

among individual plants of Pinus spp. previously 

unexposed to the rust (Kinloch & Dupper, 2002). 

Resistance is often based on a gene-for-gene 

interaction whereby incompatibility commonly 

occurs as a hypersensitive response at the stage 

of needle infection (Jurgens et al., 2003). Resistance 

breeding holds promise because the populations 

of C. ribicola in Europe and North America 

are genetically quite uniform. The alternative to 

resistance breeding is to give up P. strobus as a 

forestry tree, but the ecological damage to forests 

which regenerate by natural rejuvenation 

remains immense (Kinloch, 2003). 

Cronartium quercuum is the cause of fusiform 

rust especially on Pinus taeda and P. elliottii. These 

species were planted in the South-Eastern USA 

where C. quercuum originated on native, relatively 

resistant Pinus spp. The principal hosts are 

Quercus spp. The life cycle is similar to that of 

C. ribicola, as is the economic damage, with the 

exception that this species is still confined to the 

USA. The disease is now kept under control by 

the planting of rust-resistant cultivars (Powers & 

Kuhlman, 1997; Schmidt, 2003). 

Cronartium flaccidum causes resin top disease 

on Scots pine (Pinus sylvestris), P. nigra, P. pinaster 

and other species in Europe (Smith et al., 1988). 

The principal hosts are various herbaceous

MELAMPSORACEAE 

635 

Fig 22.15 Section through a telial lesion of 

Melampsora euphorbiae on Euphorbia peplus.The 

teliospores are formed in a crust-like layer beneath 

the epidermis. 

plants. A similar disease is caused by the purely 

aecial (anamorphic) Peridermium pini. Both species 

are genetically identical, and Hantula et al. (2002) 

have recommended that they be considered as 

one species. 

22.7.2 Melampsora and Melampsoridium 

In Melampsora spp. the unicellular teliospores 

are sessile and often form a subepidermal crust 

(Fig. 22.15). Germination is by an external 

metabasidium of the usual type. The aecia lack 

peridia so that they are diffuse instead of cupshaped. 

Such diffuse aecia are called caeomata 

(singular caeoma). Melampsora lini var. lini is an 

autoecious rust common on Linum catharticum, 

and M. lini var. liniperda infects cultivated flax. 

It was this fungus which Flor (1955, 1971) used 

for his pioneering work on the gene-for-gene 

hypothesis. Several Melampsora spp. (M. populnea, 

M. larici-populina, M. medusae, M. allii-populina) 

produce brightly coloured and extremely abundant 

uredinia and, later in the season, telia on 

Populus (poplar) trees (Plate 12g). Their alternate 

hosts are Larix, Abies, Picea, Pinus and Allium spp. 

(Smith et al., 1988). Some of these rusts seem to 

differ very little other than in their aecial host, 

and much more work is required before an 

acceptable species concept is in place. Further, 

hybridization between different rusts can occur 

(Spiers & Hopcroft, 1994). There is an even more 

bewildering complex of Melampsora rusts on 

willows (Salix spp.), alternating with Allium, 

Larix, Ribes or orchid species (Smith et al., 1988; 

Pei et al., 1993). The most important species is 

M. epitea, which alternates with Larix and exists 

as numerous races. Since willow and poplar trees 

can be important crops in certain forest situations, 

efforts at resistance breeding are being 

made (Ramstedt, 1999). 

Melampsoridium betulinum causes a rust on 

birch as its uredinial and telial host, on which it 

is extremely common everywhere. Larix is the 

alternate host. In contrast to Melampsora spp., 

aecia of Melampsoridium are surrounded by a 

peridium, and phylogenetic studies have also 

shown that the genera Melampsora and 

Melampsoridium are not particularly closely 

related (Maier et al., 2003).

23 

Ustilaginomycetes: smut fungi and their allies 

23.1 Ustilaginomycetes 

The Ustilaginomycetes are one of the four main 

classes of Basidiomycota and contain about 1500 

species (Kirk et al., 2001). In its present form as 

circumscribed by Begerow et al. (1997) and Bauer 

et al. (1997, 2001), this group is monophyletic. 

Hypha-producing Ustilaginomycetes are united 

by their lifestyle as ecologically obligate plant 

pathogens, often with an additional free-living 

(saprotrophic) yeast phase. They can be distinguished 

from the rust fungi in that haustoria are 

either altogether absent or, where present, take 

the shape of simple intracellular hyphae or 

hyphal extensions which invaginate the host 

plasmalemma but are not differentiated into a 

narrow neck and a wider haustorial body. 

Further, intracellular hyphae of Ustilaginomycetes 

usually secrete a thick sheath which is 

readily visible by transmission electron microscopy 

(see Figs. 23.6 and 23.17). The septa either 

lack perforations or contain simple pores or 

dolipores which are similar to those in the 

Urediniomycetes in lacking parenthesomes. 

True clamp connections are not usually found. 

The basidia of smut fungi produce numerous 

basidiospores whereas those of rust fungi usually 

produce only four. 

The class Ustilaginomycetes has been divided 

into three subclasses by Begerow et al. (1997, 

2000). We shall consider representatives of two 

of these. The Ustilaginomycetidae (Section 23.2) 

are the most important plant-pathogenic 

Ustilaginomycetes, causing smut-like symptoms. 

Typical members of the Exobasidiomycetidae 

(Section 23.4) cause other biotrophic diseases 

and are distinguished from the former by 

producing basidia directly from parasitic 

mycelium, not from teliospores. An exception 

is Tilletia, which is so similar to smuts in the 

Ustilaginomycetidae that we discuss it alongside 

them (p. 650). The third group, Entorrhizomycetidae, 

contains fungi which produce galls on the 

roots of Cyperaceae and Juncaceae (Vánky, 1994). 

Numerous Ustilaginomycetes live exclusively 

or predominantly as yeasts, and an example of 

this lifestyle is the order Malasseziales described 

on p. 670. 

Fungi causing smut-like disease symptoms 

(Fig. 23.7, Plate 12h) have arisen at least 

twice within the Basidiomycota, namely in the 

Ustilaginomycetes and the Urediniomycetes. 

Urediniomycetous smuts are found in the Microbotryales, 

and since these share many biological 

features with the ‘true’ smuts in the Ustilaginomycetes 

and have traditionally been studied by 

smut specialists, we shall consider the Microbotryales 

in this chapter (Section 23.3). Therefore, 

in our usage the term ‘smut fungus’ has a 

biological rather than a taxonomic meaning. 

23.2 The‘true’ smut fungi 

(Ustilaginomycetes) 

The word ‘smut’ describes the causal fungus or 

the symptoms of a particular group of plant 

diseases in which loose masses (sori) of dark

THE ‘TRUE’ SMUT FUNGI (USTILAGINOMYCETES) 

637 

spores are produced in infected plant organs. 

Leaves, stems, flowers and seeds of grasses and 

other herbaceous plants are particularly frequently 

attacked. The term ‘bunt’ is sometimes 

used for smut fungi infecting the ovaries of their 

hosts, the seed becoming filled with teliospores 

in place of the embryo. Host tissues from which 

the spores are released often appear as if burnt 

or scorched, and this is why de Bary (1853) 

used the term ‘Brandpilze’ to describe the smut 

fungi. Various names have been given to these 

spores, e.g. teliospore, chlamydospore, brand 

spore, melanospore, ustospore or ustilospore. 

We prefer to call them teliospores because their 

function in the life cycle of smut fungi is 

equivalent to that of teliospores in the rust life 

cycle, i.e. they are the site of nuclear fusion and, 

on germination, give rise to the promycelium in 

which meiosis occurs. 

Several good monographs have been written 

about smut fungi, especially by Vánky (1987, 

1994). The surface ornamentation of teliospores 

(Figs. 23.2, 23.9) and their method of germination 

(Figs. 23.3, 23.4, 23.5, 23.10, 23.12) as well as the 

type of symptoms and host range are important 

characters in identification. 

23.2.1 The life cycle of smut fungi 

The life cycle of smut fungi can be divided into 

two phases, a yeast-like monokaryotic (homokaryotic) 

form which grows saprotrophically but 

is unable to infect plants, and a predominantly 

dikaryotic (heterokaryotic) mycelial phase which 

is infectious on host plants but cannot grow 

saprotrophically (Fig. 23.1). The infectious dikaryotic 

mycelium is often systemic, showing interor 

intra-cellular growth. Meristematic host 

tissues are particularly densely colonized. 

Usually there are no specialized haustoria, but 

hyphae may enter or even grow through host 

cells, invaginating the host plasmalemma. 

Intracellular hyphae are surrounded by a partial 

or complete sheath (Fig. 23.6) which is formed 

partly by the secretory activity of the pathogen 

and partly by the contributions from the infected 

host cell (Bauer et al., 1997). During sorus 

development, the dikaryotic hyphae proliferate 

and mass together in intercellular spaces, often 

destroying the softer internal host tissues but 

remaining enclosed by the host epidermis. There 

are no phialides or other specialized sporeproducing 

structures, but most hyphal segments 

can become converted to spores. The sporogenous 

hyphae are composed of binucleate cells. 

After nuclear fusion, the walls thicken and 

gelatinize, and the cells fragment. They then 

enlarge and become globose, and finally a thick 

wall is laid down (Snetselaar & Mims, 1994; 

Banuett & Herskowitz, 1996). The gelatinous 

matrix disappears at maturity. The ripe, uninucleate, 

diploid teliospores have thick, usually 

dark walls which may be smooth or ornamented 

by spines or reticulations (Vánky, 1987, 1994; 

Piepenbring et al., 1998a,b). In some genera, e.g. 

Urocystis, a central fertile cell is surrounded by a 

group of sterile cells. 

The teliospores are commonly dispersed by 

wind or become attached to the surface of seeds. 

Teliospores of many smut fungi germinate in a 

similar way to those of rust fungi by forming a 

septate promycelium. The teliospore is therefore 

the probasidium, with the promycelium being 

the metabasidium. If this is septate, it is a 

phragmobasidium. Teliospore germination can 

proceed in several different ways which are 

shown in subsequent sections. Typically, numerous 

haploid basidiospores (often called sporidia) 

are produced by direct budding from segments 

of the promycelium, and these are unable to 

re-infect the host. Instead, they germinate by 

further budding to form elongated yeast cells 

which are capable of prolonged saprotrophic 

growth. Compatible yeast cells meeting on the 

surface of the host plant conjugate, and this 

initiates the dikaryotic hyphal stage which is 

able to infect the host plant. 

23.2.2 Mating systems 

Many smut fungi are heterothallic with a unifactorial 

(bipolar) mating system (i.e. one mating 

type locus with two alleles), but Ustilago maydis 

and a few other species are tetrapolar, with two 

mating type loci located on different chromosomes. 

The a locus has two idiomorphs and 

controls fusion of sporidia which is driven by 

the exchange of mating pheromones between

638 USTILAGINOMYCETES: SMUT FUNGI AND THEIR ALLIES 

Fig 23.1 The life cycle of Ustilago maydis, diagrammatic and not to scale.Teliospores are formed in galls developing from dikaryotic 

hyphae. Karyogamy (K) occurs in the teliospore, followed by meiosis (M) and germination to form a three-septate promycelium. 

Each segment buds off numerous haploid sporidia. Sporidia bud in a yeast-like manner and are capable of saprotrophic growth but 

unable to infect maize plants.When yeast cells or sporidia of compatible mating type meet, conjugation tubes are formed, and their 

fusion (plasmogamy, P) gives rise to a dikaryotic hypha which is infectious on maize.Open and closed circles represent haploid nuclei 

of opposite mating type; the diploid nucleus is drawn larger and half-filled. 

compatible cells. The multiallelic b locus controls 

growth of the dikaryon, as well as its ability to 

infect the host and to complete sexual development 

(see p. 643). In the bipolar species U. hordei, 

the genetic control of fusion and dikaryon growth 

is very similar to that in U. maydis, with the 

important differences that there are only 

two instead of multiple b alleles and that the 

a and b loci are tightly linked on the same 

chromosome (Lee et al., 1999). Genetic recombination 

during meiosis is suppressed in the region 

containing the a and b loci. This region is 

substantially larger than the mating type genes 

themselves, making up about one-sixth of the 

chromosome on which it resides. Hence, this 

chromosome is regarded as a primitive form of 

the sex chromosome as found, for example, 

in mammalian organisms (Fraser & Heitman, 

2004). Mammalian sex chromosomes are recognizably 

different when they are condensed at 

mitosis, the X chromosome being very much 

larger than the Y chromosome. Intriguingly, 

measurable size differences have also been 

found between the two sex chromosomes of the 

urediniomycetous smut, Microbotryum violaceum 

(Hood, 2002). 

The smut fungi are dimorphic, producing 

both yeast cells and true hyphae. This feature has 

aroused the interest of cell biologists, and 

especially Ustilago maydis is being used extensively 

as a tool to examine fundamental aspects 

of eukaryotic biology (see Fig. 23.8).


639 

entire infected host organs or galls may be 

dispersed, and teliospores or mycelium of smut 

fungi may be borne on or in seeds. 

The most common dispersal route in the 

smut fungi is by wind-blown teliospores, and 

the transatlantic wind-borne passage of African 

sugarcane smut, Sporisorium scitamineum, has 

been proposed as the most likely route of entry 

into the Caribbean. Teliospores of many smuts 

may adhere to the seeds of their host plants 

and germinate with them. Certain species causing 

loose smuts of cereals (see p. 639) systemically 

infect the living embryo of the cereal grain. 

Grains contaminated by external spore dusts or 

systemic infections can be spread by human 

transport. Insect dispersal is important in the 

anther smut, Microbotryum violaceum, which is 

related to the rust fungi (see p. 652). 

Fig 23.2 Teliospore surfaces of Ustilago spp. (a) Smooth 

surface in U. hordei. (b) Spiny surface in U. nuda.From 

Va¤nky (1994); original prints kindly provided by K.Va¤nky. 

23.2.3 Teliospore release and dispersal 

Piepenbring et al. (1998c) have written an 

excellent review of the teliospore as a dispersal 

unit in a wide range of smut fungi, and we can 

only summarize a few salient features here. 

Teliospores of most species are produced in a 

sorus enclosed by a thin layer of host tissue. They 

are generally released dry. Spore release is often 

by the simple rupture of the host epidermis 

surrounding the sorus, possibly as a result of 

pressure exerted by the expanding teliospores. 

The host epidermis may aid in the release of 

teliospores, e.g. if it is hit by water drops. The 

mechanism in this case is similar to that found 

in puffballs (see p. 578). Gusts of wind which 

shake infected host organs may also be effective 

in releasing smut spores over time. Alternatively, 

23.2.4 Ustilago species on 

monocotyledonous hosts 

Several Ustilago spp. cause diseases on grasses 

and cereals. Sori of the agriculturally most 

important species, U. hordei, U. nuda, U. tritici 

and U. avenae, are produced in place of the 

developing seeds. Other Ustilago spp. affect the 

leaves of their hosts, e.g. U. filiformis (formerly 

U. longissima), which causes leaf stripe smut 

on Glyceria spp. Ustilago maydis infects both 

vegetative and reproductive organs of its host 

(Plate 12h), causing gall-like deformations. This 

species is considered in detail on pp. 643 647. 

Many Ustilago spp. have also been described from 

dicotyledonous hosts, but it now seems that all 

of them belong to Microbotryum (Vánky, 1998, 

1999; Almaraz et al., 2002; see p. 652). 

Phylogenetic studies have shown U. hordei, 

U. nuda, U. tritici and U. avenae to be closely 

related to each other, to the point where it 

becomes difficult to distinguish individual 

species by DNA sequences and microscopy. They 

are regarded as the core species of Ustilago (Stoll 

et al., 2003). Since these species can hybridize 

with each other, it has been proposed that they 

should be merged into one taxon, U. segetum 

(see Bakkeren et al., 2000). However, because 

the existing names are so well-established and 

because well-known plant diseases are caused by


Fig 23.3 Teliospore germination 

in Ustilago avenae. (a) Germinating 

teliospore showing the four-celled 

promycelium, each cell of which 

is producing sporidia. Budding of 

detached sporidia is also shown. 

(b) Germinating teliospore showing 

fusion of the two terminal cells 

to initiate a dikaryon. (c) Fusion 

of conjugation tubes from two 

basidiospores to initiate a dikaryon. 

these cereal smuts, we prefer to keep their 

original names for the time being. The corn 

smut pathogen, U. maydis, is not closely related 

to the core Ustilago spp. and instead occupies an 

intermediate position between Ustilago and 

Sporisorium (Stoll et al., 2003). In total, there are 

about 230 Ustilago spp. and 190 Sporisorium spp. 

(Kirk et al., 2001), although such numbers 

obviously vary with the species concept adopted. 

The surface of teliospores is an important aid 

in identification. Ustilago hordei has a smooth 

teliospore surface whereas most other cereal 

smuts have spiny surfaces (Figs. 23.2a,b). Huang 

and Nielsen (1984) have shown that this difference 

between smooth and spiny surfaces is due 

to only two genes. Many of those Ustilago spp. 

now grouped with Microbotryum have teliospore 

surfaces with conspicuous reticulations or 

striations. There are also variations in the 

processes of teliospore germination in Ustilago 

(Ingold, 1983c; Vánky, 1994). The classical pattern 

is shown by U. avenae (Fig. 23.3), U. hordei and 

U. maydis in which the promycelium is threeseptate. 

All four cells give rise to sporidia, and 

compatible sporidia fuse following pheromone 

stimulation (see p. 643). When attached to a host 

plant surface, teliospores of U. avenae germinate 

in a different way; instead of producing sporidia, 

adjacent compatible cells of the promycelium 

fuse directly (Fig. 23.3b; Vánky, 1994). In U. nuda 

(Fig. 23.4), direct fusion of promycelium cells 

occurs both on agar and in nature. However, 

following synchronous division of the two nuclei 

in the fusion cell, septa are laid down such that 

a mosaic of both mono- and dikaryotic cells 

results. Compatible monokaryotic cells may fuse


641 

Fig 23.4 Teliospore germination in 

Ustilago nuda. (a) Three teliospores 

20 h after germination, showing 

various stages of development of 

the promycelium.The arrows 

indicate points where cell fusion 

has occurred. (b) A later stage 

showing the extension of 

mycelium from the fusion cells. 

(c) Two-day-old germinating 

teliospore showing repeated cell 

fusions (arrows). 

Fig 23.5 Teliospore germination in Ustilago 

filiformis. (a) Teliospore germination by successive 

development of sporidia. Note the absence of an 

extended promycelium.The first-formed sporidia 

are short. (b) Sporidium showing budding. 

(c) Sporidia conjugating. A dikaryotic mycelium 

arises following conjugation.


Fig 23.6 TEM of Ustilago hordei infecting 

a compatible barley cultivar.The host cell 

consists of a large vacuole (V) surrounded 

by a thin layer of cortical cytoplasm. 

The intracellular fungal hypha (F) has 

penetrated the plant cell wall (PW) and 

invaginated the host plasmalemma (single 

arrow); note the thick electron-dense 

sheath (Sh) between the hyphal wall and 

the host plasmalemma.The double arrow 

points to vesicles in the intercellular space 

(IS). Photomicrograph taken by G. Hu; 

reprinted from Hu et al.(2003),with 

permission from Elsevier. 

Fig 23.7 Loose smuts. (a) Infection of Ustilago avenae on oats. 

All seeds on the affected inflorescence have been replaced by 

teliospore sori. (b) Ustilago tritici causing loose smut on wheat. 

A healthy wheat ear is shown on the left. 

with each other again at a later stage (Nielsen, 

1988). In U. tritici there are also no sporidia, 

but here each uninucleate cell of the septate 

promycelium gives rise to a germ tube, and the 

dikaryophase is established by fusion of these 

germ tubes (Malik, 1974). Ustilago filiformis has 

teliospores which, on germination, do not 

produce an obvious promycelium, but merely a 

short tube from which sporidia are budded off 

successively (Fig. 23.5). All of the above fusion 

events ultimately result in a dikaryotic hypha 

which infects the host plant. 

In contrast to U. maydis, many small-grain 

cereal smuts entertain a gene-for-gene relationship 

with their hosts. In incompatible interactions, 

the infection hypha is encased in an 

unusually thick sheath as soon as it penetrates 

the first epidermal cell. This is closely followed 

by the death of the infected cell through a 

hypersensitive response (Hu et al., 2003). The 

breeding of resistant cultivars can be an 

effective means to control these pathogens 

(Smith et al., 1988). As we have already seen in 

the rust fungi (p. 625), the evolution of numerous 

races of smut fungi causes difficulties in 

cultivating cereals carrying major resistance 

genes. The spread of these races can be monitored 

in time and space by screening field 

isolates against a differential of cereal cultivars 

(Menzies et al., 2003). Distinct smut races show a 

high tendency to hybridize under natural conditions, 

so that new races can arise rapidly 

(Thomas, 1984).


643 

Ustilago hordei 

This is the type species of Ustilago, causing 

covered smut of barley and oats. Crop losses 

are usually less than 1% in well-managed 

agrosystems (Thomas & Menzies, 1997). The 

infection cycle has been described in detail by 

Hu et al. (2002). The term ‘covered smut’ implies 

that the teliospores produced in the cereal grains 

replace the internal tissues but remain covered 

by the outer layer (pericarp) of the grains and 

are released only during threshing. Teliospores 

attached to the outer surface of seeds will 

germinate at the time of host germination. 

The fusion of compatible monokaryotic yeast 

cells results in a dikaryotic hypha which infects 

the young seedling. The epidermal cells are 

penetrated directly from slightly swollen 

hyphal tips, which may be regarded as rudimentary 

appressoria. There then follows an extended 

phase of systemic growth without outward 

symptoms of infection. Colonization of the host 

is chiefly intracellular but also intercellular. 

Differentiated haustoria are not produced. 

Instead, hyphae grow through host cells, invaginating 

the plasmalemma in the process. A thick 

sheath is deposited between the plasma membranes 

of the host and the pathogen (Fig. 23.6). 

By the time the mycelium reaches the apical 

meristem (about 40 55 days post infection), 

the host has usually formed the inflorescence 

initials, and massive proliferation of the mycelium 

occurs from that stage onwards. The 

developing spike tissue becomes filled with 

hyphae which then branch profusely and form 

teliospores. This infection sequence of a prolonged 

symptomless colonization followed by 

symptom development in the reproductive structures 

of the host is typical of the small-grain 

cereal smuts but differs from the infection of 

maize by U. maydis (see below). 

Ustilago avenae, U. nuda and U. tritici 

These species cause loose smut of their cereal 

hosts, i.e. the kernels are replaced by sori 

producing teliospores, with entire glumes 

usually destroyed. Ustilago avenae infects oats 

(Fig. 23.7a) and false oat-grass, Arrhenatherum 

elatius. There are numerous races which are 

specific to different oat cultivars. The disease 

cycle is complex. Teliospores have been shown to 

survive for 13 years and thus the fungus can 

infect seedlings from teliospores dusted onto the 

outer surface of seeds. Additionally, it is capable 

of limited systemic infection of the seed pericarp 

which is initiated during flowering (Neergaard, 

1977), and such infections are genuinely seedborne. 

Either way, the fungus systemically 

colonizes the growing host plant and proliferates 

during flowering to produce a crop of teliospores. 

Systemically infected hosts flower slightly 

earlier than healthy plants, and they release 

their teliospores at the time when healthy plants 

flower. Teliospores released at that point can 

germinate on healthy flowers (Mills, 1967), 

leading to systemic infections which may be 

carried over to the next growing season within 

viable seeds. 

Ustilago nuda and U. tritici cause loose smut on 

barley and wheat, respectively (Fig. 23.7b). Their 

disease cycles are very similar to each other. 

Systemic infection of the host plant gives rise 

to smutted heads and, as in the case of U. avenae, 

flowering of smutted plants occurs slightly 

earlier than that of healthy plants, so that the 

disease can spread to uninfected flowers by 

means of teliospores. The normal entry point of 

dikaryotic mycelium was formerly thought to be 

the stigma of healthy flowers, but Batts (1955) 

showed that it is, in fact, the young tissue at 

the base of the ovary. The mycelium survives 

systemically in infected embryos. In spring, 

systemic infections spread when these embryos 

germinate. In contrast to U. avenae, teliospores of 

U. nuda and U. tritici are short-lived, rarely surviving 

for more than a few days under normal 

conditions. Hence, infection from teliospore dust 

on the surface of seeds does not seem to be an 

important infection route. 

23.2.5 Ustilago maydis 

This species is the cause of corn smut and is by 

far the most thoroughly researched member of 

the Ustilaginomycetes (reviewed by Kahmann 

et al., 2000). One of the early research highlights 

using U. maydis was on mitotic recombination, 

leading to the development of the ‘Holliday 

model’ to explain the exchange of DNA strands


at ‘Holliday junctions’ between paired DNA 

double helices (see p. 317; Holliday, 1962, 1964). 

Areas of ongoing research on U. maydis are 

described in subsequent sections. Work on 

U. maydis has greatly benefited from the ease 

with which the haploid phase of this fungus can 

be grown in culture and transformed by molecular 

biology tools. The complete genome of this 

fungus has now been sequenced, and this should 

stimulate further research. 

The teliospores of U. maydis are long-lived and 

can survive in the environment (e.g. the soil) for 

several years. Dikaryotic hyphae resulting from 

the fusion of haploid sporidia can infect any 

above-ground tissue of its host (wild and cultivated 

Zea mays) by entry through stomata or 

direct, appressorium-mediated penetration of the 

epidermis (Snetselaar & Mims, 1992; Banuett & 

Herskowitz, 1996). Infected host organs become 

strongly hypertrophied to form galls. This is 

in contrast to the small-grain cereal smuts 

described above, in which symptom development 

is confined to the developing seeds of the host, 

and infection usually occurs at the seedling stage 

followed by a prolonged symptomless phase. In 

U. maydis, the entire process from dikaryon 

formation on the plant surface to the release of 

mature teliospores may take as little as 2 weeks 

(Banuett & Herskowitz, 1996). In the field, infections 

by U. maydis are most commonly observed 

on the cobs presumably because the stigmata 

with their thin epidermal layer are most readily 

penetrated by the fungus (Snetselaar & Mims, 

1993). As a result of infection, the developing 

seeds on the corn cob become replaced by 

gall-like outgrowths (‘tumours’) which measure 

about 1 5 cm in diameter (Plate 12h). Although 

not generally welcomed by farmers, such infected 

cobs are prized as a delicacy in the Mexican 

cuisine (Pataky & Chandler, 2003). 

Monokaryotic yeast cells of U. maydis synthesize 

auxins, especially indole-3-acetic acid, in 

pure culture (see Basse et al., 1996), and infected 

hypertrophied host tissue also shows elevated 

concentrations of this plant growth hormone. It 

therefore seems likely that the production of 

growth hormones by U. maydis in planta contributes 

to the development of the striking disease 

symptoms, although this has not yet been 

formally proven. The mycelium of U. maydis 

ramifies in these hypertrophied tissues, followed 

by hyphal fragmentation and production of teliospores. 

Although the dikaryotic phase is obligately 

biotrophic in nature, U. maydis can be 

stimulated to complete its life cycle in artificial 

conditions if it is grown on living cell cultures of 

Zea mays separated from the dikaryotic mycelium 

by a membrane permitting the diffusion of 

metabolites (Ruiz-Herrera et al., 1999). Deviations 

from the life cycle as shown in Fig. 23.1 have 

been described by Kahmann et al. (2000). 

Mating and dikaryon establishment 

Ustilago maydis is heterothallic and has two 

mating type loci. A given dikaryon is fully 

pathogenic only if it contains different idiomorphs 

or alleles at both loci. Since it will 

produce haploid progeny of four genetically 

distinct types, the mating system is said to 

be tetrapolar. Locus a has two idiomorphs, 

a1 and a2, each of which encodes a mating 

pheromone and the receptor for the pheromone 

encoded by the opposite idiomorph. Two haploid 

cells will mate if they contain opposite idiomorphs 

at locus a, irrespective of their b alleles. 

Conjugation can be induced experimentally even 

between cells containing the same idiomorph if 

the matching pheromones are added. Mating is 

therefore purely driven by the pheromones 

which are peptides containing 13 (peptide a1) 

or 9 (peptide a2) amino acids derivatized with 

a lipid (farnesyl) side-chain (Spellig et al., 1994). 

A cell whose receptor has bound the pheromone 

of the opposite mating type will arrest its 

cell cycle in the G2 position and undergo a 

morphogenetic change to produce a thin flexible 

conjugation tube which grows chemotropically 

towards the pheromone source (Snetselaar et al., 

1996). 

The ability to infect maize plants and to 

complete the life cycle is tightly linked to the 

ability of the fusion cell to form dikaryotic 

hyphae. This is controlled by the b locus after 

conjugation of compatible cells. In contrast to 

the a locus which has two idiomorphs with low 

sequence homology, the b locus has about 25 

alleles which are genetically relatively similar to 

each other. Each allele encodes two proteins


645 

Fig 23.8 The roles of the a and b 

loci in the conjugation between 

monokaryotic yeast cells and 

the establishment of dikaryotic 

filamentous growth in Ustilago 

maydis.Signallingeventsare 

represented by dotted lines; 

diffusion or transport of signalling 

molecules is indicated by dashed 

lines. Based on Bo«lker (2001). 

called bE and bW (Fig. 23.8), and the dikaryotic 

phenotype depends on the formation of a 

heterodimer of proteins transcribed from different 

alleles. For instance, bE1 and bW2 can 

dimerize but bE1 and bW1 cannot. The heterodimer 

is a transcription factor which triggers 

signalling cascades involved in maintaining 

dikaryon stability, hyphal growth and virulence 

on maize. At the same time, further mating 

reactions are suppressed. 

Signalling events involved in conjugation and 

the subsequent dimorphic switch from yeast-like 

monokaryotic to hyphal dikaryotic growth 

are being extensively examined and have been 

reviewed, for example, by Banuett (1995), Bölker 

(2001), Martínez-Espinoza et al. (2002) and 

Feldbrügge et al. (2004). Although it is impossible 

to discuss the details here, we can summarize 

that a cAMP and protein kinase A signalling 

chain is involved in maintaining growth by 

budding, whereas a MAP kinase cascade is crucial 

for the switch to hyphal growth and pathogenicity. 

These two branches seem to converge on 

a transcription factor called Prf1 which is subject 

to phosphorylation at different sites by protein 

kinase A and a MAP kinase (see Fig. 23.8). 

Of course, the cAMP/protein kinase A and MAP 

kinase signalling chains fulfil many other


functions at subsequent developmental stages 

such as gall formation and teliospore production 

(Gold et al., 1997). For instance, the fuz7 gene 

product which encodes a MAP kinase kinase 

involved in the signalling chain shown in 

Fig. 23.8 is also involved in the process of 

hyphal fragmentation leading to teliospore production 

(Banuett & Herskowitz, 1996). Further, 

there is extensive cross-talk between the cAMP/ 

protein kinase A and MAP kinase chains at 

different time-points in development. 

The cytoskeleton 

Much valuable work has been performed on 

U. maydis to assign various cellular transport 

phenomena to particular elements of the cytoskeleton 

and their associated motor proteins. 

Thus, microtubules have been implicated in 

the transport of nuclei, mitochondria, vacuoles 

and the endoplasmic reticulum, as well as 

secretory vesicles in exocytosis and endosomes 

in endocytosis (Steinberg, 2000; Basse & 

Steinberg, 2004; Steinberg & Fuchs, 2004). 

Bidirectional movement can be achieved by 

kinesin motors which move towards the polymerizing 

end (plus end) of microtubules, and 

dynein which moves towards the minus end. 

Actin cables and their myosin motors are also 

involved in morphogenetic events and transport 

processes. Since the genome of U. maydis has been 

completely sequenced, the number of genes 

encoding myosin (3), dynein (1) and kinesin (10) 

is known (Basse & Steinberg, 2004) and further 

rapid progress on the role of the cytoskeleton 

in morphogenesis and cellular transport can be 

expected with U. maydis as an experimental 

organism. 

Mycoviruses and killer toxins in U. maydis 

Although mycoviruses are not uncommon in 

fungi, few of them have been investigated 

in detail. Two examples we have encountered in 

earlier chapters of this book are the virus-like 

particles in S. cerevisiae (p. 273) and related yeasts 

which contain double-stranded RNA (dsRNA) 

encoding killer toxins, and the hypovirulencecausing 

dsRNA viruses of Cryphonectria parasitica 

(p. 375) and Ophiostoma novo-ulmi (p. 366). 

Mycoviruses infecting Ustilago maydis are similar 

to those of S. cerevisiae in that they encode killer 

toxins. The first evidence of them was found 

when certain U. maydis strains killed sexually 

compatible strains upon anastomosis in mating 

assays. The cytoplasmic inheritance of the killing 

trait, the proteinaceous nature of the toxin and 

the presence of virus particles in killer strains 

were quickly established (Hankin & Puhalla, 1971; 

Wood & Bozarth, 1973). There are three types 

of virus (P1, P4 and P6) each encoding its own 

killer protein (KP) toxin. Day (1981) showed that 

virus-infected U. maydis strains are common in 

field populations. 

A great deal is now known about viruses of 

U. maydis (see Magliani et al., 1997; Martínez- 

Espinoza et al., 2002). Their genomes are fragmented 

into three size classes of dsRNA, whereby 

each size class can have several members. 

In total, there are six dsRNA fragments in P1, 

seven in P4 and five in P6, with one capsid able 

to accommodate either one H or one to several 

M chains (Bozarth et al., 1981). In all three 

viruses, a heavy (H) segment encodes the capsid 

protein and the replication machinery, and 

H segments are also essential for the maintenance 

of the medium-sized (M) and light (L) 

segments. The toxins are encoded by the 

M fragments, and their synthesis as prepropolypeptide 

chains followed by proteolytic 

cleavage and secretion of the mature toxins 

is similar to that of the S. cerevisiae killer 

toxins (p. 273). The function of the L segments 

is unknown at present. 

The modes of action of the three toxins seem 

to be diverse. The best-characterized is KP4 which 

is active as a monomer blocking certain types 

of Ca 2þ uptake channel. This activity can be 

observed in susceptible U. maydis strains as well 

as in mammalian cells, where it acts in a similar 

way to the black mamba snake venom, calciseptine 

(Gage et al., 2001, 2002). The KP1 and KP6 

toxins are released as two separate polypeptides 

after proteolytic cleavage, but in contrast to the 

yeast killer toxins these do not re-associate with 

each other by covalent (disulphide) bonds. Whilst 

the mode of action of KP1 is unknown, KP6 may 

form membrane pores which disrupt the ionic 

balance of the target cells (N. Li et al., 1999). The 

toxin-producing cell must obviously be resistant


647 

to its own toxin. In contrast to the S. cerevisiae 

system where the unprocessed toxin precursors 

bestow resistance, in toxin-producing U. maydis 

strains resistance is encoded by nuclear genes. 

Resistance is specific, i.e. a KP1-producing strain 

is sensitive to KP4 and KP6. All three toxins are 

also effective against other members of the 

Ustilaginales (Koltin & Day, 1975). 

Attempts have been made to transform 

wheat plants with the KP4 toxin gene of the 

U. maydis virus P4 in order to engineer cultivars 

with resistance against Tilletia caries (Clausen 

et al., 2000), but no recent reports seem to have 

been published on this subject. Even if cultivars 

with good resistance in the field can be 

produced, it is unlikely that a transgenic crop 

plant expressing a calciseptine-like toxin will 

gain acceptance with regulatory authorities or 

the general public. 

23.2.6 Tilletia 

There are about 125 species of Tilletia, all of which 

parasitize grasses (Poaceae). In economic terms, 

the most important pathogens are T. caries 

(¼ T. tritici) and T. indica on wheat, T. controversa 

on wheat and other cereals, and T. horrida on rice. 

Many other Tilletia spp. infect wild grasses (Vánky, 

1994). Teliospores of Tilletia spp. typically bear 

reticulate surface ornamentations (Fig. 23.9). 

They are long-lived in the soil and on the exterior 

of seeds. Infections are systemic and result in 

covered smut symptoms in the seeds. 

past, but are much less frequent now because the 

incidence of common bunt has declined. 

Crushed sori have a fishy smell caused by the 

presence of trimethylamine. For this reason, the 

disease is also known as ‘stinking smut’, and 

flour made from contaminated grain is unfit for 

human consumption. Since teliospores are not 

readily released in the field, Piepenbring et al. 

(1998c) have suggested that T. caries may be an 

example of a fungus that has adapted to humans 

as a dispersal vector. 

This fungus was a major pathogen in the past 

and occupies a special place in the history of 

plant pathology (Large, 1940; Ainsworth, 1981). 

In 1752, Mathieu Tillet, by careful experimentation, 

demonstrated that the common bunt 

disease was associated with dusting the seeds 

with bunt spores prior to sowing. He also 

reported that incidence of the disease was 

somewhat reduced by steeping the seeds in 

sea water and lime prior to sowing. In 1807, 

Bénédict Prévost observed the process of teliospore 

germination with his microscope, and he 

proposed that the bunt disease was caused by 

a living organism. Further, he discovered that 

teliospore germination was inhibited by copper 

salts, and that the treatment of wheat seeds with 

dilute copper sulphate solution was effective 

against infections of T. caries. The combination of 

copper and lime became known as the famous 

Bordeaux mixture only much later, in about 

Tilletia caries 

This species is cosmopolitan and causes ‘common 

bunt’, the best-known covered smut disease of 

wheat. The entire interior of the infected grain 

becomes converted to a greenish-brown teliospore 

sorus surrounded by the pericarp. Such sori 

are called ‘bunt balls’. The teliospores are not 

released until threshing, when they are dusted 

onto the surface of healthy grains. If heavily 

contaminated crops are processed, the teliospore 

concentrations in the air can be sufficiently high 

to cause dust explosions in mills or storage 

facilities. Respiratory allergies among millers 

caused by T. caries were also common in the 

Fig 23.9 SEM of teliospores of Tilletia caries.FromVa¤nky 

(1994); original prints kindly provided by K.Va¤nky.


Fig 23.10 Tilletia caries. 

(a) Germinating teliospore showing 

a non-septate promycelium and 

a crown of primary sporidia. 

(b) Two detached primary sporidia 

showing conjugation. A secondary 

sporidium has developed from 

one of the primary sporidia. 

(c) Primary sporidia attached 

to the promycelium showing 

conjugation. 

1882, when Alexis Millardet discovered its ability 

to control downy mildew of vines (see p. 119). 

The process of germination of T. caries teliospores 

is shown in Fig. 23.10. The diploid nucleus 

in the mature teliospore divides meiotically, 

and one or more mitotic divisions follow so that 

8 or 16 nuclei are formed. The promycelium 

is often but not invariably aseptate, and from 

its tip narrow curved uninucleate primary 

sporidia arise, corresponding in number to the 

number of nuclei in the young promycelium 

(Fig. 23.10a). The primary sporidia mate in pairs 

by means of short conjugation tubes, often whilst 

still attached to the tip of the promycelium 

(Fig. 23.10c). Detached primary sporidia may also 

conjugate. During conjugation, a nucleus from 

one primary sporidium passes into the other 

sporidium which therefore becomes binucleate. 

Each H-shaped pair of primary sporidia develops 

a single lateral sterigma on which a curved 

binucleate spore develops (Fig. 23.10b). This 

spore is projected actively from the sterigma 

using the surface-tension catapult mechanism, 

and it is sometimes referred to as the secondary 

sporidium. Because of its characteristic method 

of discharge, Buller and Vanterpool (1933) have 

interpreted this spore as a basidiospore. The 

secondary sporidium brings about infection of 

the host. 

Teliospores of T. caries (Fig. 23.9) are viable 

for up to 15 years and germinate along with the 

seeds if contaminated grain is sown. Secondary 

sporidia produce germ tubes which infect the 

coleoptiles of the seedlings. Infection is systemic, 

the mycelium growing through the tissues of the 

shoot, and by suitable techniques it is possible 

to isolate the dikaryotic mycelium from infected 

host tissues (Trione, 1972). Although infected 

plants may grow less vigorously than uninfected 

ones, they show no outward sign of 

infection until the ears are almost ripe. 

Tilletia controversa 

This species is closely related to T. caries and 

is most damaging on wheat, in addition to 

infecting other cereals and grasses. The crucial 

difference is that teliospores of T. controversa 

germinate at much lower temperatures than 

those of T. caries. In consequence, T. controversa 

causes bunt mainly on winter wheat, infecting


649 

overwintering plants under snow cover from soilborne 

teliospores (Purdy et al., 1963). In contrast 

to other Tilletia spp., spores dusted onto the seed 

surface are unimportant as inoculum because 

germination of winter wheat seeds precedes 

teliospore germination by a few months. The 

disease caused by T. controversa is called ‘dwarf 

bunt’ because infected plants show stunted 

growth. Like T. caries, T. controversa has a genefor-gene 

relationship with its host, and breeding 

for resistance is an efficient control method 

(Fuentes-Dávila et al., 2002). The life cycle of 

T. controversa is similar to that of T. caries, except 

that T. controversa has a bipolar multiallelic 

mating system whereas that of T. caries is bipolar 

with only two mating type alleles. 

Tilletia controversa is cosmopolitan but is not in 

itself a serious pathogen. However, it has 

acquired notoriety by being used as the reason 

for establishing import restrictions on wheat 

imports from the United States by China during 

the 1970s to 1990s (Mathre, 1996). 

Tilletia indica 

The disease caused by T. indica is called Karnal 

bunt, named after the city in India where it was 

first described (Mitra, 1931). It is also called 

partial bunt because the teliospore sori often fill 

only part of the infected wheat grain, leaving the 

embryo unaffected. In contrast to T. caries and 

T. controversa, T. indica does not appear to grow 

systemically. Instead, teliospores germinate by 

producing numerous (up to 180) haploid primary 

needle-shaped sporidia from the tip of the 

aseptate promycelium. The primary sporidia 

germinate by monokaryotic haploid hyphae, 

and these in turn produce a further crop of 

haploid monokaryotic secondary sporidia. Two 

types may be produced, namely a repetition of 

the needle-shaped form or a sausage-shaped 

sporidium liberated actively by the surfacetension 

catapult mechanism. In contrast to 

T. caries and T. controversa, H-shaped fusion cells 

are not formed and both types of secondary 

sporidium are monokaryotic and haploid. 

Secondary sporidia can germinate to produce a 

mycelium giving rise to further sporidia of either 

type (Dhaliwal, 1989). The actively liberated form 

enables the fungus to work its way up on the 

outside of the leaves of growing wheat plants 

until it reaches the flag leaf. There, fusion 

of compatible monokaryotic haploid hyphal 

segments may occur, with the resulting heterokaryotic 

mycelium causing infections of individual 

florets of the immature wheat ear (Goates, 

1988; Nagarajan et al., 1997). 

Occurrence and severity of Karnal bunt have 

increased in high-yielding crop systems, but the 

disease is not in itself serious, causing crop losses 

less than 1% per annum even in severe epidemics 

(Nagarajan et al., 1997). In addition, several 

resistant cultivars are available. Although bunt 

balls contain trimethylamine, flour made from 

crops with up to 4% infected grains is still fit for 

human consumption (Fuentes-Dávila et al, 2002). 

As in the case of T. controversa, the major threat 

posed by T. indica is a legal one. Countries as yet 

free from the disease may ban wheat imports 

from those affected by T. indica. For example, the 

United States imposed quarantine regulations 

to prevent the spread of Karnal bunt to North 

America, only to find bans imposed on US 

exports by other countries when T. indica was 

eventually discovered in Arizona in 1996 (Palm, 

1999). Rush et al. (2005) have given a fascinating 

account of the complex interactions between 

agriculture, politics, international trade and 

research in dealing with Karnal bunt in the 

United States, concluding that the threat posed 

by this disease was initially overstated. 

23.2.7 Urocystis 

The distinguishing feature of the genus Urocystis 

is that the teliospore consists of one or more 

melanized fertile cells surrounded by several 

sterile cells (Figs. 23.11, 23.12). This type of 

compound teliospore is called a spore ball. 

There are about 140 species (Vánky, 1994). An 

important species is U. tritici which causes leaf 

stripe-smut or flag smut on wheat in warm 

climates. This was formerly called U. agropyri, a 

name now applied in a more restricted sense to 

forms on wild grasses such as Agropyron and 

Elymus spp. (Fig. 23.11). The fertile cell of a spore 

ball of Urocystis germinates by producing an 

aseptate promycelium which gives rise to about 

four primary sporidia (Fig. 23.12). These sporidia


Fig 23.11 Teliospores of Urocystis agropyri. 

A dark-walled fertile cell is surrounded 

by several flattened hyaline sterile cells. 

Fig 23.12 Urocystis anemones. (a) Spore 

balls showing germination after 24 h 

incubation. A promycelium develops from 

a fertile cell, bearing a crown of three or 

four sporidia. (b) Development after 48 h. 

The sporidia have fused (arrow) and a 

septate infection hypha develops from the 

fusion cell. 

conjugate in pairs whilst still attached to the 

promycelium. The two haploid nuclei then 

migrate into an infection hypha which develops 

from the conjugation tube (Thirumalachar & 

Dickson, 1949). 

Urocystis tritici infects its wheat host by 

appressorium-mediated penetration of the 

infection hypha through the host epidermis 

(Nelson & Durán, 1984). Infection occurs at 

the early seedling stage and is systemic. The outbreak 

of symptoms is delayed, with the typical 

stripe-like sori breaking through the epidermis 

of several leaves after flowering of the host plant. 

Heavily infected plants may abort their tillers.


651 

Teliospores of U. tritici survive in the soil and 

attached to seeds (Fuentes-Dávila et al., 2002). 

Urocystis agropyri is common on wild grasses, and 

another common species is U. anemones which 

causes a leaf smut on Anemone and Ranunculus 

leaves. 

23.2.8 Control of smut diseases 

Control of loose and covered smuts presents very 

different problems. Whilst the surface of the 

grain is merely contaminated with the spores of 

covered smuts, in the case of loose smuts the ripe 

grain is already infected by a mycelium within the 

embryo. The control of covered smuts by means 

of fungicidal seed dressings is therefore simple, 

and it is standard practice for seed grains to be 

treated by seed merchants in this way. The first 

effective seed treatment was the steeping of seed 

grains in a dilute copper sulphate solution prior 

to sowing (Large, 1940). In the middle of the 

twentieth century, seed dressings containing 

organic mercury compounds were widely used, 

but these are now banned due to their high 

general toxicity. Instead, cocktails of fungicides 

are employed. In most countries with a welldeveloped 

agriculture, bunt of wheat is now a 

rare disease. For example, the incidence of bunt 

balls in seed samples sent to the Official Seed 

Testing Station at Cambridge fell from 12 33% 

in 1921 1925 to 0.2 0.3% in 1955 1957 

(Marshall, 1960). 

Control of the loose cereal smuts was impossible 

until the Danish plant pathologist Jens 

Ludwig Jensen invented the hot water treatment 

method in the 1880s (Large, 1940; Ainsworth, 

1981). This was based on the observation that 

Ustilago spp. are less heat-tolerant than cereals, 

and infected seeds could be effectively disinfected 

by soaking them first in cold water for 

5 h followed by a dip in hot water; 10 min at 

54°C for wheat and 15 min at 52°C for barley 

(Fischer & Holton, 1957; Ainsworth, 1981). 

Today, effective fungicidal seed dressings are 

available and these usually combine systemic 

fungicides such as carboxin (Fig. 23.13) or its 

derivatives with protectant fungicides such 

as captan, maneb or pentachloronitrobenzene 

(Kulka & von Schmeling, 1995). Such seed 

dressings control loose and covered smuts, in 

addition to numerous other fungal diseases. 

Since infection of next season’s grain with 

loose smuts occurs at flowering, one obvious 

method of control is to inspect crops grown for 

seed at flowering time and to assess the 

incidence of smutted heads. In these so-called 

seed certification schemes, only crops which 

contain fewer than a defined limit, e.g. one 

smutted ear in 10 000 ears, are approved for use 

as seed stocks (Doling, 1966). It is also possible to 

detect the presence of loose smut mycelium 

within the embryos by microscopic examination 

(Morton, 1961) or PCR-based methods (Pearce, 

1998). The latter can also detect the spores of any 

other fungus of interest on the seed coat, 

including covered smuts such as T. caries, 

T. controversa and T. indica. PCR-based methods 

are being developed rapidly, partly because 

of the need for rapid testing of exported or 

imported agricultural produce for contamination, 

and partly for the purpose of thwarting 

bioterrorist attacks (Schaad et al., 2003). 

If all else fails, many systemic fungicides, 

e.g. sterol demethylation inhibitors (see p. 410), 

are effective against the systemic smuts when 

sprayed onto the growing crop. In practice, these 

fungicides are often applied to control infections 

caused by non-smut cereal pathogens, with the 

suppression of Ustilago spp. as an additional 

bonus which often goes unnoticed by the 

farmer (Jones, 1999). 

Although many crop plants and their wild 

relatives possess resistance genes against smut 

fungi, smut-resistant cultivars are less important 

in an agricultural context than those with 

resistance against other biotrophic pathogens, 

e.g. rusts (see pp. 625 and 627) or powdery 

Fig 23.13 Molecular structure of carboxin, a systemic 

fungicide commonly applied as a seed dressing.Carboxin acts 

by inhibiting the enzyme succinate dehydrogenase (complex II) 

in fungal mitochondrial respiration (see Uesugi,1998).


mildews (p. 408). Avirulence genes involved in 

gene-for-gene interactions have been desribed 

for several cereal smuts (Sidhu & Person, 1972; 

Eckstein et al., 2002; Hu et al., 2003). The 

hypersensitive response in incompatible interactions 

is often microscopically small (Hu et al., 

2003). Field resistance against smut fungi may 

also occur as a combination of several genes 

(Nelson et al., 1998). An interesting case of singlegene 

resistance has been reported by Wilson 

and Hanna (1998) as trichome-less mutants of 

pearl millet (Pennisetum glaucum) showing a 50% 

reduction in disease severity caused by the 

smut Moesziomyces penicillariae. Curiously little is 

known about resistance mechanisms in Ustilago 

maydis despite its status as a well-examined 

‘model organism’ and the availability of its 

genome sequence. 

23.3 Microbotryales 

(Urediniomycetes) 

The order Microbotryales contains smut fungi 

with features almost indistinguishable from 

those described in the preceding section. This 

includes their general life cycle of teliospores 

germinating by means of a promycelium which 

produces haploid yeast-like sporidia, and the 

infection of host plants following establishment 

of a dikaryotic infection hypha. Intriguingly, 

however, phylogenetic studies have clearly 

shown the Microbotryales to belong to the 

Urediniomycetes (Blanz & Gottschalk, 1984; 

Begerow et al., 1997; Swann et al., 1999). There 

are certain microscopic details which distinguish 

them from Ustilaginomycetes, notably that 

growth by Microbotryum and allied species 

in planta is exclusively intercellular (Bauer et al., 

1997) and that the teliospores have a violetpurplish 

rather than brown pigmentation. 

The most important genus in the Microbotryales 

is Microbotryum which currently 

contains about 75 species (Vánky, 1998, 1999). 

All of them parasitize dicotyledonous hosts, and 

they can be resolved by DNA sequence analysis 

into two groups (Almaraz et al., 2002). The original 

genus Microbotryum parasitizes the anthers of 

plants belonging to the Caryophyllaceae, whereas 

species of the second group cause smuts on 

various organs of other host plants. Until 

recently, members of the second group were 

considered to belong to Ustilago. The eventful 

taxonomic history of these ‘dicot Ustilago’ spp. has 

been recounted by Vánky (1998, 1999); based on 

the findings of Almaraz et al. (2002) they will 

probably have to be given a new generic name, 

adding at least one further twist to the story. 

Good descriptions of many ‘dicot Ustilago’ spp. 

have been given by Vánky (1994, 1998). We shall 

devote our attention to Microbotryum sensu stricto, 

cause of anther smut on Caryophyllaceae. 

23.3.1 Microbotryum violaceum 

Anther smut of Caryophyllaceae has long 

fascinated biologists with a wide range of 

research interests. Although infection is systemic 

throughout the host plant, the disease symptoms 

are confined to the anthers in which pollen is 

replaced by purple teliospores. Several members 

of the Caryophyllaceae are infected, and there is 

evidence that Microbotryum violaceum (formerly 

called Ustilago violacea), the causal fungus, is 

undergoing speciation in diverse host plants 

(Antonovics et al., 2002), so that species delimitation 

is difficult at present (see Vánky, 1994). In 

dioecious hosts such as red or white campion 

(Silene dioica and S. alba), the flowers of infected 

female plants are stimulated to produce anthers, 

i.e. their morphology changes from female to 

male. A thorough review of the general biology 

of M. violaceum has been written by Day and 

Garber (1988). 

Life cycle and genetic recombination 

The diploid teliospores of M. violaceum are 

transported from diseased to healthy flowers 

by pollinating insects. They germinate by forming 

a promycelium (Fig. 23.14) which often 

separates into an exterior three-celled section 

and a one-celled fragment remaining in the 

teliospore. Each promycelium segment produces 

sporidia. The three-celled segment becomes 

readily detached from the teliospore and may 

continue to develop sporidia after separation.

MICROBOTRYALES (UREDINIOMYCETES) 

653 

Fig 23.14 Microbotryum violaceum. 

(a) Germinating teliospore showing three cells 

of the promycelium. (b) Detached three-celled 

promycelium segment producing sporidia. 

(c) Detached sporidia reproducing as yeast 

cells. 

In nutrient-rich conditions and at temperatures 

above 25°C, the haploid sporidia reproduce by 

yeast-like budding, whereas mating occurs at 

lower temperatures in nutrient-poor media 

such as tapwater agar. Microbotryum violaceum is 

heterothallic and bipolar, and it was the first 

smut fungus for which such an incompatibility 

system was demonstrated (Kniep, 1919). During 

mating, an a2 sporidium or yeast cell produces a 

conjugation tube which grows towards the a1 

cell. Provided that a-tocopherol (vitamin E) is 

present, fusion is followed by the production of a 

dikaryotic hypha which infects the flower of the 

host plant (Castle & Day, 1984). 

In the absence of a-tocopherol or on nutrientrich 

media, de-dikaryotization occurs and 

haploid or aneuploid yeast cells are formed by 

the loss of chromosomes. Several other complications 

exist in the life cycle of M. violaceum, 

illustrating the wealth of non-meiotic mechanisms 

of recombination encountered in fungi 

(Day & Garber, 1988; Day, 1998). For instance, 

nuclear fusion not associated with meiosis is 

readily inducible in M. violaceum, and this 

generates somatic diploids. Mitotic crossing-over 

occurs at a high frequency in somatic diploids. 

As already mentioned, M. violaceum has 

dimorphic mating type chromosomes (Hood, 

2002), and whilst the mating type locus is a 

hot spot for mitotic recombination, meiotic 

recombination does not occur in this region of 

the genome. 

Somatic diploids can be mated if they are 

homozygous for mating type, so that triploid or 

tetraploid strains can be generated. In nutrientrich 

media, these strains grow as yeast cells but 

are unstable due to the gradual loss of chromosomes. 

The size of the yeast cells is correlated 

with their ploidy level. There is also evidence for 

the activity of transposons in enhancing genetic 

recombination in M. violaceum (Garber & Ruddat, 

2002). The genetic flexibility of M. violaceum may 

explain the existence of numerous strains in 

nature. 

Fimbriae and conjugation 

The process of sporidial conjugation has been 

extensively studied in M. violaceum. Within 2 h of 

placing sporidia of opposite mating type on a 

suitable medium, a series of events occurs which 

culminates in the formation of conjugation tubes 

and plasmogamy. Poon and Day (1974) observed 

an early adhesion between the two sporidia 

before any wall-to-wall contact was established, 

and they discovered that this initial contact 

was mediated by fimbriae (Fig. 23.15) whose 

existence in fungi had not been appreciated 

previously. Subsequent investigations revealed 

that fungi from most major groups (Zygomycota, 

Ascomycota, Basidiomycota) possess such


Fig 23.15 Fimbriae of M. violaceum. Shadowing-TEM 

view. Reprinted from Gardiner and Day (1988) by 

copyright permission of the National Research 

Council of Canada; original print kindly provided by 

A.W. Day. 

fimbriae, and that these have a similar biochemical 

composition. Fimbriae can be of variable 

length (up to 20 mm) but have a uniform diameter 

of 7 nm. Most of the biochemical work on fungal 

fimbriae was done with M. violaceum, and this 

subject has been well reviewed by Celerin and Day 

(1998). 

Most fungal fimbriae consist of three structural 

components. The main component is 

proteinaceous, with strong homology to collagen 

which had been thought previously to exist only 

in animals (Celerin et al., 1996). The second 

component consists of polysaccharide glycosylation 

chains on the collagen protein. Whereas 

deglycosylated fungal collagen can still polymerize 

to form fimbriae, these become unstable in 

extreme conditions. Further, the glycosylation 

chains are involved in the specificity of mating 

recognition in M. violaceum, with the fimbrial 

protein component of a1 sporidia binding to 

the mannose residues on the proteins of the 

a2 fimbriae, i.e. acting as a lectin (Castle et al., 

1996). The third component of fungal fimbriae is 

a short (30 nucleotides) single-stranded fimbrial 

RNA (fRNA), the function of which is as yet 

unknown (Celerin et al., 1994). The fimbriae of 

M. violaceum do not traverse the cell wall, but 

are anchored to it by means of a protein which 

may be functionally analogous to mammalian 

fibrinogen. 

Whereas M. violaceum produces only one 

type of fimbria, other fungi have several 

morphologically distinguishable types (Gardiner 

& Day, 1988). In Candida albicans (p. 277), fimbriae 

play an important part in adhesion to human 

tissue and initiation of infection, and the 

fimbriae involved in this process are not made 

up of collagen (Yu et al., 1994). 

Host pathogen interactions 

Initial infection of the host plants by M. violaceum 

occurs if a pollinating insect carries teliospores 

from a diseased to a healthy flower (Jennersten, 

1988). Anther smut is thus a sexually transmitted 

disease. The entire flower is colonized by intercellular 

dikaryotic mycelium. Infection results 

in reproductive sterility of the host; in male 

flowers, the anthers become converted to teliospore 

sori whereas in female flowers, the female 

traits are suppressed and anthers are formed 

which carry teliospores. This development has 

been described in detail for infections of Silene 

latifolia (Uchida et al., 2003). Diploid female 

plants carry two X chromosomes in addition to 

22 autosomes, whereas male plants contain 

22 autosomes plus one X and one Y chromosome. 

The Y chromosome encodes genes that suppress 

the development of female traits and promote 

stamen development, thereby making the flower 

male. Microbotryum violaceum must therefore produce 

a signal called male-sterility restoration 

factor that substitutes for the Y chromosome in 

female flowers (Uchida et al., 2003). Its identity is 

as yet unknown, but it must be a signal molecule

EXOBASIDIALES (USTILAGINOMYCETES) 

655 

or transcription factor acting on genes encoded 

on the autosomes or the X chromosome, since 

the expression patterns of some male-specific 

genes in healthy male and infected female 

flowers are similar (Scutt et al., 1997). 

In perennial host species, M. violaceum can 

colonize the entire host in the course of 

1 2 years, overwintering systemically in the 

root system (Alexander & Antonovics, 1988). 

Infected plants acquire lifelong sterility, i.e. 

they will continue to produce flowers but these 

will all be male, developing anthers in which 

pollen grains are replaced by teliospores. 

The ecology of M. violaceum 

The ecological effects of M. violaceum infections 

have been considered by several workers. 

Systemically infected host plants flower earlier 

than healthy plants, and this may force pollinators 

such as bumblebees to visit infected flowers 

early in the season. Consequently, teliospore 

dispersal peaks earlier than pollen dispersal 

(Jennersten, 1988). In direct comparison, diseased 

flowers are less attractive to bumblebees 

(Shykoff & Bucheli, 1995), possibly because they 

contain less nectar and are asymmetric and 

smaller than healthy flowers (Shykoff & Kaltz, 

1998). A pollinator preference for healthy flowers 

may be advantageous to the pathogen because it 

enhances the opportunity for spreading the 

infection following an accidental visit to a 

diseased plant (Shykoff & Bucheli, 1995). 

Although systemically infected host plants 

produce an increased number of flowers which 

also remain open for longer, the drawback is 

that the root biomass is decreased, thereby 

potentially affecting the chance of the pathogen 

to overwinter systemically. Since healthy 

female flowers remain open for much longer 

than healthy male flowers, they are at greater 

risk of infection (Kaltz & Shykoff, 2001). As in 

many venereal diseases, a more attractive display 

draws a greater number of visitors, and one 

possible adaptation to M. violaceum is predicted to 

be a reduction in flower size. Another might be 

the change from a perennial to an annual habit, 

as this would prevent overwintering of the 

pathogen (Kaltz & Shykoff, 2001). In situations 

where perennial hosts are forced into an annual 

habit, e.g. near field borders or railway lines 

subject to regular clearing, infections by 

M. violaceum are rare or absent (Alexander & 

Antonovics, 1988). The interaction between 

M. violaceum and its hosts may therefore have 

different outcomes, ranging from local extinction 

of the host to that of the pathogen. 

23.4 Exobasidiales 

(Ustilaginomycetes) 

The order Exobasidiales (subclass Exobasidiomycetidae) 

is a well-defined group (Begerow et al., 

1997, 2002) of ecologically obligate, biotrophic 

plant pathogens containing less than 100 species. 

Most species cause systemic or limited infections 

of shoots or leaves, and these are often accompanied 

by hypertrophy of the infected tissue. 

The most important genus is Exobasidium. Fungi 

grouped in the Exobasidiales firmly belong to 

the Ustilaginomycetes and possess a haploid 

saprotrophic yeast-like phase and a dikaryotic 

biotrophic phase. However, they differ from the 

‘true smuts’ (Ustilaginomycetidae) in several 

aspects: 

1. They do not produce teliospores, but 

basidia are formed directly on the surface of 

the infected host. 

2. The basidium appears similar to that of 

the Homobasidiomycetes, i.e. it looks like a 

holobasidium, not divided into a pro- and metabasidium 

as in smut fungi (but see below). 

3. Basidiospores are violently discharged 

using the surface-tension catapult mechanism, 

and they often become septate after discharge. 

4. The mycelium is usually intercellular, 

with haustoria often present. These differ from 

the intracellular hyphae of smut fungi in not 

being completely surrounded by a sheath. 

Instead, a complex interaction apparatus is 

formed at the haustorial apex (Fig. 23.17). 

23.4.1 Exobasidium 

About 50 Exobasidium spp. are known. All of 

them cause either local infections of individual 

leaves or more widespread, sometimes systemic 

infections of whole shoots or shoot tips


Fig 23.16 Exobasidium japonicum. (a) Basidium on the lower surface of an evergreen azalea. (b) Freshly discharged aseptate 

basidiospores. (c) Basidiospore after a few hours’ incubation on potato dextrose agar.The spore has formed a transverse septum 

and has germinated. (d) Basidiospore after12 h.The germ tubes have branched and are budding off elongated yeast cells. 

Fig 23.17 Lobed haustorium of Exobasidium sp.Three 

interaction sites with the host cytoplasm are numbered. Site1 

is shown in median section, and the interaction ring is visible 

(arrowheads).Sites2and3areintangentialsection,showing 

electron-dense deposits (d).Tubulovesicular cytoplasmic 

structures involved in secretion of the electron-dense matter 

are also visible (arrows).The penetration site of the host wall 

is at the bottom of the picture (double arrowheads). 

Reprinted from Begerow et al.(2002),Mycological Progress, 

with permission of IHW-Verlag; original print kindly provided 

by D. Begerow. 

(Plates 12i,j). Infection commonly gives rise to 

hypertrophied tissue. Keys and descriptions have 

been given by Nannfeldt (1981) and Ing (1998). 

Frequently infected host plants include members 

of the Ericaceae, e.g. Vaccinium (bilberry, blueberry) 

in heaths, moors and forests, and ornamental 

azaleas and Rhododendron spp. in gardens. 

Cosmopolitan examples are E. japonicum on 

evergreen azaleas (Plate 12i; Fig. 23.16) and 

E. vaccinii on Vaccinium spp. (Plate 12j). A second 

group of host plants is the Theaceae family, with 

the tea plant (Camellia sinensis) a prominent 

casualty of E. vexans which adversely affects the 

quantity and quality of the tea harvest (Gulati 

et al., 1999). 

Infections by Exobasidium spp. are easily 

confused with symptoms caused by Taphrina 

(Plate 4a,c), and these two genera, although 

phylogenetically unrelated, have much in 

common. Plant tissues infected by Exobasidium 

are often swollen and show a pale or reddish 

discoloration. There is an obvious hormonal 

imbalance in the infected host tissue, although 

no detailed examinations have been carried out. 

Infected shoots are often affected in their reproductive 

development (Wolfe & Rissler, 1999). 

A whitish superficial layer of basidia is eventually 

produced on the surface of infected host 

tissue, and these carry about 2 8 sterigmata

EXOBASIDIALES (USTILAGINOMYCETES) 

657 

(Fig. 23.16a). Basidiospores are initially aseptate 

(Fig. 23.16b), but in many species they become 

septate after their discharge, and both cells can 

germinate by emitting germ tubes (Fig. 23.16c). 

Elongated haploid yeast cells are produced from 

these germ tubes or directly from the basidiospore 

cell (Fig. 23.16d). Several Exobasidium spp. 

grow as yeast cells in culture. Infection of host 

plants may occur from basidiospores or yeast 

cells and gives rise to a dikaryotic intercellular 

mycelium (Mims & Nickerson, 1986). Exobasidium 

spp. may overwinter systemically in their host, 

or as spores on the outside, e.g. in bud scales 

or bark. 

Haustoria are formed by the intercellular 

hyphae, and these show unique characteristics 

in being lobed and producing an electron-dense 

apical ring at the localized point of contact 

with the host plasmalemma. This then becomes 

elaborated into an apical cap which is associated 

with the host wall (Bauer et al., 1997) or 

directly with the host plasmalemma (Mims, 

1982). The ring and cap material is secreted 

by the haustorium from an elaborate tubular 

membrane system (Fig. 23.17). This cap may be 

homologous to the thick sheath which surrounds 

the intracellular hyphae of smut fungi (see 

Fig. 23.6). 

Although the basidia of Exobasidium look 

like typical club-shaped holobasidia, their 

development differs from that in the homobasidiomycetes 

(Mims et al., 1987). Nuclear fusion 

occurs in a subterminal cell (strictly speaking 

the probasidium), and then the nucleus migrates 

into the basidium proper where meiosis is 

completed. The basidium of Exobasidium is thus 

a metabasidium in disguise, and the pattern of 

basidial development is equivalent to that in the 

rust and smut fungi. A further unusual feature 

is that the hilar appendices of basidiospores on 

the basidium point outwards (Fig. 23.16a), not 

inwards as in Homobasidiomycetes.

24 

Basidiomycete yeasts 


Fungi living predominantly or exclusively as 

yeasts are encountered in three classes of 

Basidiomycota, namely the Heterobasidiomycetes 

(Chapter 21), Urediniomycetes (Chapter 22) 

and Ustilaginomycetes (Chapter 23). We shall 

discuss basidiomycete yeasts together in the 

present chapter because these organisms, 

although taxonomically diverse, are unified by 

many biological features. 

24.1.1 Ecology 

Little is known about the ecology of basidiomycete 

yeasts. They occur in marine and freshwater 

habitats, the soil and the plant rhizosphere, and 

especially on above-ground plant surfaces such 

as tree bark, leaves, flowers and fruits. A certain 

degree of specificity of yeast species relative to 

plant species or organs of a given plant host has 

been observed (Phaff, 1990). Basidiomycete yeasts 

may be found in all climatic zones from the 

arctic to the tropics. They generally exist as 

saprotrophic phylloplane organisms. When 

nutrients become available, there may be a 

steep increase in the population density of 

these yeasts. Many yeasts isolated from soil 

have their origin in vegetation which becomes 

incorporated into humus after leaf fall. 

Basidiomycete yeasts are not noted as plant 

pathogens, but some species can infect animals. 

Cryptococcus neoformans is one of the most serious 

fungal pathogens of humans (pp. 661 665). 

Members of another group (Malassezia spp.) live 

commensally on the skin of humans and other 

mammals, causing superficial dermatomycoses 

under suitable conditions (p. 671). 

Basidiomycete yeasts therefore share many 

ecological features with their ascomycete counterparts, 

and they are easily isolated following 

similar procedures, i.e. by plating out soil 

suspensions, leaf washings or filters bearing 

water samples onto standard agar media 

augmented with antibacterial antibiotics 

(p. 262). One good way to isolate ballistoconidium-forming 

yeasts is to attach a piece of 

vegetation to the underside of a Petri dish lid, 

permitting ballistosporic yeasts to shower their 

spores onto the agar medium. Within 2 3 days, 

yeasts such as Sporobolomyces spp. will grow and 

can be isolated in pure culture. Yeasts are 

preserved in an active state on agar slopes 

at 4°C. Lyophilized preparations can also be 

made from vegetative cells of many species, 

and these remain viable for several years. 

Many basidiomycete yeasts, the so-called 

‘red yeasts’, are coloured yellow, orange, pink 

or red due to the presence of carotenoids (see 

Fig. 24.8). Red yeasts are found in all three classes 

containing basidiomycete yeasts, but they are 

rare among ascomycetes (see p. 253 for the 

Lalaria state of Taphrina). Carotenoid production 

can be of commercial value, as in Phaffia 

rhodozyma which produces astaxanthin, an 

important food and feed pigment (p. 665). 

Other commercial applications of basidiomycete 

yeasts are as potential producers of lipid, e.g. as 

cocoa butter substitute (Ratledge, 1997), and as 

biocontrol agents against storage rots of fruits

INTRODUCTION 

659 

Fig 24.1 Basidiomycete yeasts 

as seen by light microscopy. 

(a) Budding in Dioszegia sp. 

(Heterobasidiomycetes).The yeast 

cells are isodiametric with a slightly 

pointed bud region. (b) Budding 

cells of Rhodotorulaglutinis 

(Urediniomycetes).This species 

produces a prominent polysaccharide 

capsule which has been revealed 

by mounting yeast cells in Indian 

ink. (c) Collarette at the site of 

repeated bud formation in 

Sakaguchia dacryoidea 

(Urediniomycetes). (d) Annellidic 

structure formed by a member of 

the Dioszegia hungarica group 

(Heterobasidiomycetes). 

(e) Ballistoconidium formation 

in Sporobolomycesroseus 

(Urediniomycetes). (f) Septate 

stalked basidium arising from a 

teliospore of Sporidiobolus ruineniae 

(Urediniomycetes). (a e) to same 

scale.Original print of f kindly 

provided by J. W. Fell. 

caused by filamentous fungi (Janisiewicz & 

Korsten, 2002). 

Detailed descriptions of basidiomycete yeasts 

along with their ascomycete counterparts may 

be found in Kurtzman and Fell (1998) and 

Barnett et al. (2000). A useful general introduction 

to the topic is that by Fell et al. (2001). 

24.1.2 Morphology and life cycles 

Asexual reproduction is mainly by budding. In 

contrast to ascomycete yeasts, the budding sites 

are confined to either or both poles of the 

vegetative cells which are usually ellipsoid or 

elongated (Figs. 24.1b,d) but may be isodiametric 

(Fig. 24.1a). Yeast cells may be coated by a 

prominent polysaccharide capsule (Fig. 24.1b), 

giving the culture a slimy appearance. Repeated 

budding at the same site may lead to the 

formation of collarettes (Fig. 24.1c) or even 

annellide-like structures (Fig. 24.1d). The formation 

of daughter cells is enteroblastic, i.e. only 

the inner wall of the mother cell extends to form 

the wall of the daughter cell. The whole budding 

yeast cell can thus be viewed as a phialide. This is 

in contrast to most ascomycete yeasts which bud 

in a holoblastic manner (i.e. the daughter wall is 

continuous with the entire wall of the mother 

cell). Given a little practice, it is often possible 

with the light microscope to recognize a basidiomycete 

yeast as such. Transmission electron 

microscopy has revealed differences between 

the two-layered cell walls of ascomycetes and 

the multi-layered lamellate walls of basidiomycete 

yeasts (Kreger-van Rij & Veenhuis, 1971). 

These differences have been correlated with the 

reaction of basidiomycete but not ascomycete 

yeasts with the diazonium blue B stain (Simmons 

& Ahern, 1987). 

Apart from budding, several genera of basidiomycete 

yeasts such as Sporobolomyces and its 

teleomorph Sporidiobolus (Urediniomycetes) or 

Bullera and its teleomorph Bulleromyces

660 BASIDIOMYCETE YEASTS 

(Heterobasidiomycetes) also produce conidia 

which are actively liberated in the manner of 

basidiospores, i.e. by means of the surfacetension 

catapult mechanism involving Buller’s 

drop (Fig. 24.1e). Since these are asexual propagules, 

they are called ballistoconidia. Their 

existence provided one of the first clues that 

the yeasts producing them belong to the Basidiomycota 

(Kluyver & van Niel, 1927). 

Sexual reproduction is relatively rare in 

basidiomycete yeasts except, of course, for those 

species which have dominant mycelial diploid or 

dikaryotic stages such as the smut fungi 

discussed in Chapter 23, or jelly fungi and allies 

(Chapter 21). Following mating between compatible 

yeast cells, a limited dikaryotic mycelium 

often bearing clamp connections may arise, and 

this produces basidia either directly or, more 

commonly, via thick-walled resting cells called 

teliospores. There, karyogamy occurs, i.e. the 

teliospores function as probasidia. Teliospores 

germinate in a manner described in detail for 

rust and smut fungi, namely by the production 

of a promycelium (¼ metabasidium) which 

may or may not undergo transverse septation. 

The basidiospores thus produced germinate by 

budding as yeast cells (Fig. 24.1f). 

Where present, septa can be examined by 

transmission electron microscopy for their ultrastructure, 

and this is an important feature in 

classification. In general, the septa of yeasts 

belonging to Urediniomycetes and Ustilaginomycetes 

contain simple pores whereas those of 

heterobasidiomycete yeasts have dolipores, often 

with a parenthesome (Fell et al., 2001). 

24.1.3 Phylogeny of basidiomycete yeasts 

In addition to examining morphological features 

as outlined above, several biochemical tests can 

be performed to characterize yeasts. Such tests, 

e.g. carbon source utilization, the identity of 

coenzyme Q or the spectrum of killer toxins 

produced, have been employed extensively in 

the past to identify yeasts and are still relevant 

today (Yarrow, 1998; Fell et al., 2001). However, the 

results are rarely clear-cut, and taxonomic confusion 

has resulted due to the extensive overlap 

of features between members of different taxa. 

Hence, the names of many basidiomycete yeasts 

are of descriptive rather than taxonomic value 

and may be found in several phylogenetically 

distinct clades (Table 24.1). For instance, the 

main feature to distinguish Sporobolomyces from 

Rhodotorula is the presence or absence (respectively) 

of ballistoconidia, and it is now known 

that these character states, and hence the two 

generic names, are of little taxonomic relevance. 

Major work is currently being carried out in 

order to establish phylogenetically coherent 

groups of yeasts, using especially ribosomal 

DNA but also increasingly other gene sequences. 

Valuable recent contributions to phylogeny at 

higher taxonomic levels are those by Fell et al. 

(2000, 2001) and Scorzetti et al. (2002) in which 

the heterobasidiomycete, urediniomycete and 

ustilaginomycete clades of yeasts have been 

circumscribed (Table 24.1). The integration of 

some of these clades into the taxonomy of 

filamentous basidiomycetes has yet to be accomplished. 

Additionally, numerous publications 

have dealt with the analysis of taxa at the level 

of genus or species. Hence, although it is 

generally estimated that only 1 5% of all 

basidiomycete yeasts have been discovered as 

yet, a large database of DNA sequences is already 

available. A convenient side effect of this work 

is that the identification of new isolates or at 

least their assignment to a given family or genus 

is a relatively straightforward matter if their 

rDNA sequences can be obtained. Biochemical 

tests and microscopy can then be used to verify 

and extend the identification. 

24.2 Heterobasidiomycete yeasts 

This is a large and morphologically diverse 

group of yeasts. We shall focus on two species 

which have been particularly well examined, the 

serious human pathogen Filobasidiella neoformans 

and the astaxanthin producer Phaffia rhodozyma. 

Trichosporon spp., which are occasional opportunistic 

human pathogens, are not further 

discussed. They show a diversity of growth 

forms, including hyphae, pseudohyphae, yeast 

cells, blastoconidia and arthroconidia.

HETEROBASIDIOMYCETE YEASTS 

661 

Table 24.1. Some important anamorph (A) and 

teleomorph (T) genera of basidiomycete yeasts and 

their approximate taxonomic position according 

to Fell et al. (2000, 2001) and Scorzetti et al. (2002). 

Heterobasidiomycetes (Section 24.2) 

1. Tremellales 

Fellomyces A 

Bulleromyces T ¼ Bullera A 

Cryptococcus A 

Dioszegia A 

Filobasidiella neoformans T ¼Cryptococcus 

neoformans A(p.661) 

Tremellayeast states (p. 605) 

2. Trichosporonales (exclusively anamorphic fungi) 

Cryptococcus A 

Trichosporon A 

3. Filobasidiales 

Filobasidium T ¼Cryptococcus A 

4. Cystofilobasidiales 

Cystofilobasidium T ¼Cryptococcus A 

Itersonilia perplexans A(seep.493) 

Xanthophyllomyces dendrorhous Tand 

Phaffia rhodozyma A(p.665) 

Urediniomycetes (Section 24.3) 

1. Microbotryum clade 

Microbotryum yeast states (see p. 652) 

Rhodotorula A 

2. Sporidiobolus clade 

Rhodosporidium T ¼ Rhodotorula A 

Sporidiobolus T ¼ Sporobolomyces A (p.666) 

3. Erythrobasidium clade 

Erythrobasidium T 

Sakaguchia T 


Sporobolomyces A 

4. Agaricostilbum clade 

Agaricostilbum T 

Bensingtonia A 

Sporobolomyces A 

Ustilaginomycetes (Section 24.4) 

1. Ustilaginomycetidae 

Pseudozyma A 

Ustilago yeast states (see p. 636) 

2. Exobasidiomycetidae 

Exobasidiumyeast states (see p.655) 


Tilletia yeast states (see p.636) 

Tilletiopsis A (yeast states of smutfungi) 

3. Malasseziales 

Malassezia A(p.670) 

24.2.1 Filobasidiella (Cryptococcus) 

neoformans 

The anamorph genus Cryptococcus comprises some 

30 40 species which are scattered throughout 

all 4 yeast-containing orders of the Heterobasidiomycetes, 

and with a range of different teleomorphs 

(Table 24.1). Clearly, therefore, the genus 

is polyphyletic. Cryptococcus spp. are ubiquitous, 

being found in all climatic zones on plant 

material and in the soil. One species, C. neoformans 

(teleomorph Filobasidiella neoformans), is a human 

pathogen and among the most serious causes 

of mycosis in man. Both individuals with a 

healthy immune system and, more frequently, 

immunocompromised patients such as AIDS 

sufferers or organ transplant patients, can be 

attacked. There is a vast amount of literature 

on C. neoformans, including an authoritative 

monographic treatment (Casadevall & Perfect, 

1998) and several good reviews (e.g. Kwon-Chung 

& Bennett, 1992; Mitchell & Perfect, 1995; 

Buchanan & Murphy, 1998). 

Varieties of C. neoformans and their habitats 

One important feature of C. neoformans is the 

coat of mucilage which surrounds actively 

growing yeast cells. There are four mucilage 

serotypes, A D, and these have been correlated 

with two varieties of C. neoformans, i.e. var. gattii 

(serotypes B and C) and var. neoformans (A and D). 

Franzot et al. (1999) have put forward evidence 

that the latter should be separated into var. 

neoformans (D) and var. grubii (A). Some serotypes 

cannot be assigned clearly to any one variety 

(e.g. serotype AD). Although the three varieties 

probably diverged some 18 37 million years 

ago, they still show occasional hybridization in 

nature and the ability to mate in the laboratory. 

Many of the hybrids isolated from nature are of 

recent origin, and there is evidence that human 

activity has brought together strains which were 

previously living in geographic isolation. Thus, 

the species C. neoformans may be undergoing 

de-diversification at present (Xu et al., 2000). 

The anamorph teleomorph connection is such 

that C. neoformans var. neoformans and var. grubii 

correspond to F. neoformans var. neoformans, 

whereas the teleomorph of C. neoformans var. 

gattii is F. neoformans var. bacillispora which differs


in that its basidiospores are rod-shaped rather 

than spherical or ellipsoid. 

As with most if not all fungi pathogenic to 

man, the ability of C. neoformans to cause disease 

is serendipitous, and the human body represents 

a dead-end in the life cycle of the pathogen. 

Disease outbreaks are preceded by contact of 

humans with the fungus in its natural habitat, 

but the precise identity of this has been difficult 

to track down. Ellis and Pfeiffer (1990a) noted the 

geographic co-occurrence of human cases caused 

by C. neoformans var. gattii and the distribution of 

Eucalyptus camaldulensis trees in Australia, and 

were able to show that the fungus is associated 

with the flowers, bark and litter of Eucalyptus. 

In other countries, different plants may also 

act as hosts. Further, clinical and environmental 

isolates of C. neoformans var. gattii in Australia 

have been shown to be genetically identical 

(Sorrell et al., 1996). Thirdly, the confinement of 

C. neoformans var. gattii to rural areas may explain 

why its abundance has barely increased in the 

wake of the AIDS epidemic, in marked contrast 

to var. neoformans and especially var. grubii which 

accounts for 99% of infections in AIDS patients 

(Mitchell & Perfect, 1995). Both these latter 

varieties are common in urban habitats, being 

associated with the nests and droppings of birds, 

especially pigeons (Emmons, 1955) but also caged 

birds. Although birds certainly spread the 

fungus, they are more likely to be vectors than 

primary hosts in nature because they are not 

themselves affected by cryptococcosis. As yet 

unidentified plants are probably the primary 

substratum, and Lazéra et al. (1996) have shown 

that C. neoformans var. neoformans (presumably 

including var. grubii) occurs in the hollows of 

living tree trunks. 

Whereas C. neoformans var. gattii, like 

Eucalyptus camaldulensis, is confined to tropical 

and subtropical areas, vars. neoformans and grubii 

are cosmopolitan. 

Life cycle 

The life cycle of F. neoformans is unusual in 

several respects (Kwon-Chung, 1998) as shown in 

Fig. 24.2. The fungus is heterothallic with a bipolar 

mating system (two mating types, a and a). 

The yeast cells are haploid and uninucleate, 

and they reproduce by budding. Conjugation 

between two cells of compatible mating types 

gives rise to a limited dikaryotic mycelium with 

septa bearing clamp connections. From this, 

elongated metabasidia arise and terminate in a 

swollen tip. Nuclear fusion occurs in the basidial 

stalk, and meiosis followed by repeated mitotic 

divisions in the swollen apex. This produces four 

patches which bud off a chain of basidiospores, 

each of which contains a single haploid nucleus. 

Meanwhile, mitosis continues in the basidial 

cytoplasm. Each patch can produce numerous 

basidiospores so that a column consisting of four 

chains is formed. The migration of nuclei into 

the basidiospores is random so that each chain 

may contain basidiospores of both mating types. 

This kind of basidium is unique to F. neoformans. 

‘Self-fertility’ is a frequently observed 

phenomenon in a mating type strains of 

F. neoformans and involves the production of a 

monokaryotic mycelium with incomplete clamp 

connections, giving rise to basidia and basidiospores 

presumably without meiosis (Wickes et al., 

1996). These should therefore be called conidia. 

Of all varieties of C. neoformans, strains containing 

mating type a are isolated much more 

frequently than a strains from natural situations 

as well as from patients (Kwon-Chung & Bennett, 

1978), and the ability of a but not a strains to 

form dry wind-dispersed conidia may explain 

their greater abundance in nature. Kwon-Chung 

et al. (1992), working on strains of C. neoformans 

var. neoformans which were genetically identical 

to each other except for their mating type, found 

that the a strain was also more virulent than the 

a strain. The conclusion was that the a idiomorph 

might encode virulence factors. 

Both a and a mating type idiomorphs of 

C. neoformans var. neoformans and var. grubii have 

now been sequenced (Lengeler et al., 2002) and 

were found to be unusually large (105 130 kb). 

Approximately 20 genes are encoded by the 

entire sequence, including pheromones, receptors, 

transcription factors and components of 

signalling cascades. Several genes are unique to 

either a or a, and even those common to both are 

arranged in different positions, making recombination 

within the mating type region impossible. 

Lengeler et al. (2002) have likened the


663 

Fig 24.2 Life cycle of Filobasidiella neoformans. Note that only the a but not the a mating type is able to reproduce by haploid 

conidia. Based partly on Kwon-Chung and Bennett (1992) and Kwon-Chung (1998).Open and closed circles represent haploid 

nuclei of opposite mating type; diploid nuclei are larger and half-filled. Key events in the life cycle are plasmogamy (P), karyogamy 

(K) and meiosis (M). 

mating type idiomorph of C. neoformans to the sex 

chromosomes of other organisms. This situation 

is most unusual for Basidiomycota which typically 

have two unlinked mating type loci (e.g. 

A and B in Coprinus cinereus or Schizophyllum 

commune; see p. 508) encoding a receptor/pheromone 

system and a transcription factor. 

Another, though structurally different, example 

of a sex chromosome may be found in Ustilago 

hordei (see p. 637). 

Infection and therapy 

The available evidence suggests that infection 

with C. neoformans is initiated by inhalation, and 

that the disease is not spread between humans. 

This is probably because the infectious particles 

must be very small (


5-fluorocytosine over several weeks is effective if 

the disease has been diagnosed sufficiently early 

(Mitchell & Perfect, 1995). For AIDS sufferers, ‘the 

therapeutic goal is to ablate the symptoms and 

signs of cryptococcosis until the patient dies of 

other causes’ (Kwon-Chung & Bennett, 1992). 

Antifungal drugs, especially fluconazole, may 

have to be administered for the rest of the 

patient’s life because of the high risk of relapses. 

Cryptococcosis, like certain other fungal 

diseases, is an AIDS-defining illness, i.e. patients 

diagnosed as HIV-positive and suffering from 

cryptococcosis are considered to have developed 

AIDS. 

Virulence factors 

Much work is being done to identify the properties 

which enable C. neoformans to cause disease 

(reviewed by Buchanan & Murphy, 1998; 

Casadevall & Perfect, 1998; Perfect, 2004). The 

most important and obvious virulence factor is 

the capsule which surrounds actively growing 

yeast cells of C. neoformans and protects them 

from adverse environmental effects. It also seems 

to inhibit the phagocytosis of yeast cells by 

macrophages. The capsule can be visualized by 

light microscopy of yeast cells mounted in India 

ink and can be rather more substantial than that 

shown for Rhodotorula in Fig. 24.1b. The major 

capsule polysaccharide of C. neoformans is a linear 

a-(1,3)-mannan chain, of which roughly every 

third mannose moiety is substituted with a 

single b-(1,2)-glucuronic acid unit. The presence 

of xylose determines the antigenic properties of 

the capsule; one (serotype D), two (A), three (B) or 

four (C) xylose residues may be present for every 

three mannose moieties (Cherniak & Sundstrom, 

1994). The capsule polysaccharides are produced 

in such profusion that they can be detected in 

the blood serum and other body fluids of 

infected patients, and this is an important 

diagnostic tool (Kwon-Chung & Bennett, 1992). 

Mutants unable to produce a capsule in the host 

are apathogenic. 

Both C. neoformans var. gattii and vars. grubii/ 

neoformans have been shown to undergo switches 

in colony phenotype from smooth to mucoid, 

wrinked or pseudohyphal. Switching between 

smooth and mucoid appears to be readily 

reversible in the mammalian host in var. gattii, 

but less so in the latter two. The mucoid type is 

characterized by an increase in the thickness of 

the polysaccharide capsule. In C. neoformans var. 

neoformans and var. grubii a thick capsule coincides 

with an enhanced resistance to antimycotics, 

and mucoid strains may be selected by 

prolonged chemotherapy (Guerrero et al., 2006). 

In mice infected with C. neoformans var. gattii, Jain 

et al. (2006) have shown that mucoid forms are 

associated preferentially with pulmonary infections, 

presumably because of an enhanced 

resistance to intracellular digestion by phagocytes. 

Smooth cells with their thinner coat were 

preferentially isolated from infected brain tissue. 

In contrast to morphotype switching in Candida 

albicans (p. 277), no sexual function has been 

suggested for switching in C. neoformans. 

A second important virulence factor is melanin. 

The ability of C. neoformans to synthesize 

melanin distinguishes this species from other 

members of the genus, and the melanized cell 

wall has been suggested to protect the cell against 

oxidative stress such as that encountered during 

the oxidative burst after ingestion by macrophages 

(Wang et al., 1995). The pathway of 

melanin biosynthesis in C. neoformans is different 

from the dihydroxynaphthalene (DHN) route 

found in most fungi (see Fig. 12.46). The precursor 

molecule is 3,4-dihydroxyphenylalanine (DOPA) 

which cannot be synthesized by C. neoformans 

but, if present, can be oxidized to quinones by a 

laccase-type enzyme, and these quinones spontaneously 

polymerize to melanin (Salas et al., 1996). 

Catecholamines such as DOPA are present at high 

levels in the brain, and this may explain the 

preferential accumulation of C. neoformans in 

brain tissue (Polachek et al., 1990). 

A third important factor is, of course, the 

ability of C. neoformans to grow at 37 39°C, 

which is unique among Cryptococcus spp. Several 

gene products are required for growth at 37°C, 

and prominent among them is calcineurin, 

a Ca 2þ -regulated serine/threonine phosphatase 

involved in eukaryotic cellular signalling 

(Odom et al., 1997). Calcineurin is the target of 

a complex formed between a cyclophilin protein 

involved in protein folding, and cyclosporin A 

(see Fig. 12.24a), an immunosuppressive drug


665 

widely used to prevent the graft rejection 

reaction after organ transplantations. In vitro, 

growth of C. neoformans is inhibited by cyclosporin 

A at 37°C but not at lower temperatures. 

The use of cyclosporin A for human antifungal 

therapy is impossible because its immunosuppressive 

activity outweighs the antifungal effect. 

However, Cruz et al. (2000) have reported cyclosporin 

derivatives which are antifungal but do 

not have immunosuppressive properties, i.e. they 

appear to interfere with fungal calcineurin 

signalling but not with the equivalent human 

signalling chain involved in the immune 

response. It remains to be seen whether these 

substances are sufficiently specific for use as new 

antifungal drugs. 

24.2.2 Phaffia and Xanthophyllomyces 

Phaffia rhodozyma and its putative teleomorph 

Xanthophyllomyces dendrorhous have aroused 

considerable interest because they are among 

very few fungi producing the commercially 

valuable carotenoid pigment astaxanthin (see 

Fig. 24.8), and probably the only ones to do so in 

pure culture. Astaxanthin is of importance in the 

fish farming industry because salmonid fish 

(salmon and trout) require a minimum level of 

astaxanthin in their food for healthy growth. 

One reason for this may be that these fish 

contain high levels of polyunsaturated fatty 

acids which are susceptible to peroxidation by 

reactive oxygen species such as the hydroxyl 

radical (HO) or superoxide radical (O 2 ). 

Astaxanthin and the related pigment canthaxanthin 

are also responsible for the orange 

pigmentation of salmon steak. In nature, astaxanthin 

travels the food chain phytoplankton ! 

zooplankton ! larger crustaceans ! salmon. 

Simple methods to extract and analyse astaxanthin 

from Phaffia and salmon have been 

described by Weber and Davoli (2003). In view 

of the correlation between oxidative processes 

and cancer or degenerative diseases related to 

ageing, astaxanthin is also gaining popularity 

as a ‘nutraceutical’, i.e. an additive to the 

human diet. 

Astaxanthin is now produced commercially 

by total chemical synthesis, by extracting it from 

the exoskeletons of shellfish, or by microbial 

fermentation using Phaffia or the alga 

Haematococcus pluvialis. Whereas wild-type strains 

of Phaffia synthesize a limited amount of astaxanthin 

(typically less than 300 mgg 1 dry 

weight), the astaxanthin levels in strains used 

for industrial production are at least 10-fold 

higher. In-depth reviews of biotechnological 

aspects of astaxanthin production have been 

written by Johnson and An (1991) and Johnson 

and Schroeder (1995a,b). 

It is unclear why, among the numerous red 

yeasts, Phaffia and Xanthophyllomyces are the only 

ones as yet known to synthesize astaxanthin. 

Part of the answer may lie in their unusual 

habitat, all strains known to date having been 

isolated from the slime fluxes of broad-leaved 

trees, especially birch (Betula spp.) in Alaska, 

Japan, Scandinavia and Russia (Phaff, 1990). 

Schroeder and Johnson (1995) have presented 

evidence that birch sap contains a photosensitizer, 

i.e. a substance that becomes energized by 

UV light. When this passes on its excitation 

energy, it can transform ground-state oxygen 

(triplet oxygen, 

3 O 2 ) to the reactive singlet 

oxygen ( 1 O 2 ) state. This can be returned to its 

ground state under dissipation of the excess 

energy as heat by astaxanthin and other carotenoids. 

Astaxanthin appears to be necessary for 

the survival of Phaffia under the oxidizing 

conditions prevalent in birch sap. In fact, 

cultivation and mutant studies have shown 

that astaxanthin is able to protect its producing 

organism against a wide range of oxidative 

stresses caused by H 2 O 2 , singlet oxygen and the 

hydroxyl and superoxide radicals, and that 

astaxanthin biosynthesis is increased under 

such conditions (Schroeder & Johnson, 1993). 

In contrast, b-carotene is the main pigment at 

low oxygen partial pressure, i.e. Phaffia cultures 

grown under reduced aeration appear yellow 

instead of orange (see Fig. 24.8). 

The original isolate of Phaffia is a purely 

asexual strain, but other isolates show sexual 

reproduction under suitable conditions characterized 

by nitrogen starvation and the presence 

of polyols (Kucsera et al., 1998). This perfect state 

was named Xanthophyllomyces dendrorhous, and 

there is still disagreement as to whether Phaffia


and Xanthophyllomyces represent the same or 

closely related species (Fell & Blatt, 1999; 

Kucsera et al., 2000). Xanthophyllomyces appears 

to be homothallic, vegetative cells being diploid. 

Mating can occur between a mother cell and its 

bud, giving rise to a tetraploid zygote (Kucsera 

et al., 1998). A long thin aseptate metabasidium is 

formed, and the fusion nucleus migrates to 

the tip of it, undergoing meiosis in the course 

of the journey. About 2 7 diploid basidiospores 

are produced and released passively (Fig. 24.4c). 

Vegetative reproduction is by budding (Fig. 

24.4a), but the nuclear events are unusual in 

that the mother nucleus migrates into the bud 

and divides there, followed by the return of one 

of the daughter nuclei to the mother cell 

(Slaninova et al., 1999). Thick-walled chlamydospores 

(Fig. 24.4b) are occasionally formed, and 

these germinate by mitotic budding, i.e. they are 

not equivalent to the teliospores of other 

basidiomycete yeasts. The life cycle of 

Xanthophyllomyces rhodozyma is summarized in 

Fig. 24.3. In general, there is a considerable 

variation between different isolates; for instance, 

the number of chromosomes ranges from 7 to 17 

(Kucsera et al., 2000). 

24.3 Urediniomycete yeasts 

Yeasts belonging to the Urediniomycetes appear 

to fall into four phylogenetic groups (see 

Table 24.1), some of which still need to be 

integrated into higher taxa (families and 

orders). Many species contain carotenoids, i.e. 

they are red yeasts. Some of them, especially 

species belonging to the Sporodiobolus clade 

(provisional order Sporidiales), are extremely 

common in the environment. For this reason, 

we shall consider them here. There are two 

important genera in the Sporidiales, Sporidiobolus 

(anamorph Sporobolomyces) and Rhodosporidium 

(anamorph Rhodotorula). 

24.3.1 Sporidiales 

In addition to budding, Sporobolomyces spp. also 

form asexual spores which are ejected from a 

sterigma into the air by the surface-tension 

catapult mechanism and are therefore called 

ballistoconidia. If an agar culture is incubated 

upside down, a mirror image of the colony will 

be deposited as spores on the Petri dish lid. For 

this reason, Sporobolomyces is known as a mirror 

yeast. One of the most frequently encountered 

species, S. roseus, is now known to represent a 

Fig 24.3 Life cycle of 

Xanthophyllomyces dendrorhous. 

Vegetative cells are diploid and 

reproduce by budding.The fungus 

is homothallic, and fusion between 

mother and daughter cell establishes 

a tetraploid zygote which forms an 

elongate aseptate basidium in which 

meiosis occurs.The diploid 

basidiospores germinate by budding. 

Xanthophyllomyces can survive 

unfavourable conditions by means 

of thick-walled chlamydospores. 

Half-filled circles represent diploid 

nuclei; tetraploid nuclei are larger and 

divided into four segments. Key events 

in the life cycle are plasmogamy (P), 


UREDINIOMYCETE YEASTS 

667 

Fig 24.4 Microscopic features of Phaffia rhodozyma (a) and 

Xanthophyllomyces (b,c), a closely related teleomorph. 

(a) Vegetatively dividing yeast cells. (b) Thick-walled 

chlamydospore in the process of germination bybudding about 

3 h after transfer to a fresh medium. (c) Aseptate elongate 

basidia of Xanthophyllomyces sp. producing basidiospores at 

their tips. All images to same scale. 

complex of several species which are difficult to 

distinguish by any means other than DNA 

sequencing (Bai et al., 2002). Rhodotorula spp. 

also reproduce vegetatively by budding but are 

unable to produce ballistoconidia. Apart from 

this difference, the two genera are very close to 

each other, overlapping in phylogenetic trees 

and also possessing similar life cycles. 

Life cycle 

The budding phase of Sporobolomyces roseus is 

uninucleate, and nuclear division occurs at the 

time of bud formation (Buller, 1933). If ballistoconidia 

are to be formed, a conical sterigma 

develops vertically and bears an asymmetric 

spore which strongly resembles a basidiospore 

(Figs. 24.1e and 24.5). A daughter nucleus passes 

into this spore. Following the fusion of Buller’s 

drop with the adaxial blob, the spore is flicked 

away for a distance of about 0.1 mm. Colonies of 

S. roseus begin to form ballistoconidia after 

2 3 days on most agar media, and they are 

recognized by the presence of numerous satellite 

colonies outside of the margin of the parent 

colony. A single sterigma may produce a second 

or even a third spore, and occasionally two or 

three sterigmata arise from one cell. 

Although S. roseus can form pseudohyphae 

and true hyphae, no sexual reproduction has 

been observed. However, a related species, 

Sporidiobolus (Sporobolomyces, Aessosporon) salmonicolor 

(formerly also called S. odorus), does undergo 

the full sexual cycle (Fig. 24.7). This species is 

heterothallic with a bipolar (unifactorial) mating 

system (Fell & Statzell-Tallman, 1981). Following 

conjugation between compatible haploid uninucleate 

cells, a dikaryotic mycelium with clamp 

connections develops and eventually produces 

globose binucleate teliospores (Fig. 24.6; Bandoni 

et al., 1971). Karyogamy follows. Meiosis occurs 

during teliospore germination, which gives 

rise to an aseptate metabasidium. This buds 

off haploid monokaryotic basidiospores at its 

tip. Life cycles of this kind have also been 

described in some other members of the 

Sporidiales, with minor variations such as 

the presence of transverse septa in the metabasidia, 

or the absence of ballistoconidia (see 

Fig. 24.1f). 

There is, however, a complication in the life 

cycle of S. salmonicolor because, according to 

van der Walt (1970), yeast cells may be haploid 

or diploid. The diploid cells are larger than the 

haploid ones. Both types are capable of reproducing 

by budding and by producing ballistoconidia, 

but only the diploid cells can additionally 

develop directly into thick-walled teliospores. 

These germinate by means of a short aseptate 

promycelium producing yeast-like basidiospores 

at its tip (Fig. 24.7). 

According to Fell and Statzell-Tallman (1998), 

a similar life cycle is found in Rhodosporidium 

toruloides (anamorph Rhodotorula glutinis). In this 

species, diploid yeast cells are thought to arise if 

there is a failure of meiosis during teliospore 

germination. In contrast to the observations by


Fig 24.5 Sporobolomycesroseus.(a c) 

Various stages in the budding of cells. 

(d) Cell bearing a sterigma and a 

ballistoconidium. (e) Cell with two 

sterigmata. (f) Cell with three sterigmata. 

van der Walt (1970) on Sporidiobolus, the diploid 

yeast cells of R. toruloides do not develop into 

teliospores directly, but first produce a mycelium 

which in turn forms teliospores. Conjugation 

between haploid cells of compatible mating 

type is mediated by peptide hormones. One of 

them, rhodotorucine A, has been identified as 

an undecapeptide with a farnesyl side chain 

(Kamiya et al., 1979). 

Some species of Rhodosporidium and Sporidiobolus 

are entirely homothallic, and here all yeast 

cells seem to be diploid (Fell & Statzell-Tallman, 

1998; Statzell-Tallman & Fell, 1998). Meiosis 

in a diploid yeast cell establishes a clamped 

dikaryotic mycelium which produces teliospores. 

Germinating teliospores give rise to metabasidia 

which produce diploid basidiospores. 

Ecology 

Sporobolomyces, Rhodotorula and other yeasts 

belonging to the Urediniomycetes are found in 

diverse habitats such as the soil (Sláviková & 

Vadkertiová, 2003) and the sea, including deep 

sea locations (Nagahama et al., 2001). However, 

their most prominent habitat is healthy and 

moribund vegetation (Nakase, 2000) from which 

they can be isolated throughout the year. 

Together with the black yeast Aureobasidium 

(Ascomycota; see p. 484), they form a major 

component of the phylloplane yeast population. 

Breeze and Dix (1981) have estimated that 

yeasts (including ascomycetes) produce up to 

50 times more biomass than hyphal fungi 

on Acer leaves throughout the growing season. 

Sporobolomyces roseus is the most abundant phylloplane 

yeast, comprising for example 76% of the 

yeast population on grapes (de la Torre et al., 

1999). Scanning electron microscopy studies have 

shown that cells of S. roseus may form sheets 

of mucilage by which they adhere to the leaf 

surface. There is no evidence that the growth of 

the yeasts causes corrosion of the cuticle (Bashi & 

Fokkema, 1976). There is interest in the suggestion 

that Sporobolomyces or Rhodotorula on leaf 

surfaces may compete with foliar pathogens, 

and that biological control of the pathogens 

might be possible (Fokkema & van der Meulen, 

1976). Such an approach is especially promising 

in the control of post-harvest diseases 

because the incubation conditions can be more 

precisely controlled (Janisiewicz & Bors, 1995; 

Janisiewicz & Korsten, 2002). Many Sporobolomyces

UREDINIOMYCETE YEASTS 

669 

Fig 24.6 Sporidiobolus salmonicolor. 

(a) Budding cell. (b) Cell with 

sterigmata. (c) Conjugation of 

haploid cells and initiation of a 

dikaryotic hypha. (d) Young 

dikaryotic hyphae, the original 

conjugants obscured.The arrow 

indicates the first clamp 

connection. (e) Late stage of 

chlamydospore development; 

the paired nuclei are visible. 

After Bandoni et al.(1971). 

and Rhodotorula spp. appear to be associated with 

lesions caused by plant pathogens such as rust 

fungi, or by parasites such as nematodes. 

Ballistoconidia of Sporobolomyces are frequent 

in the air, especially during warm summer 

nights, and concentrations of these spores 

may reach values of up to 10 6 m 3 (Gregory & 

Sreeramulu, 1958). Such high concentrations are 

a cause for concern because Sporobolomyces has 

been shown to be a respiratory allergen (Evans, 

1965). 

Phylloplane yeast populations occupy an 

exposed habitat and are therefore susceptible 

to environmental changes. Sporobolomyces roseus 

has been proposed as an indicator of air quality, 

low colony counts correlating with heavy air 

pollution (Dowding & Richardson, 1990). The 

results can be superimposed on those obtainable


Fig 24.7 Possible life cycle of Sporidiobolussalmonicolor.Both diploid stages (large split nuclei) and haploid stages (small black or white 

nuclei) exist and can reproduce by budding and ballistoconidium formation. Plasmogamy of two yeast cells of compatible mating 

types or conversion of a diploid yeast cell leads to the formation of a teliospore which undergoes meiosis upon germination. 

Failure of meiosis in the metabasidium or conjugation between two haploid yeast cells could give rise to diploid yeast cells. 

Key events in the life cycle are plasmogamy (P), karyogamy (K) and meiosis (M). 

with the biomonitoring of lichens (see p. 454), 

and both groups of organisms are susceptible 

to SO 2 . 

Phylloplane yeasts including S. roseus are also 

sensitive to UV radiation, and enhanced irradiation 

leads to a decline in their abundance on 

leaves (Newsham et al., 1997). However, some 

protection may be afforded by the carotenoids 

produced by red yeasts, since carotenoid-deficient 

mutants are more sensitive to UV light 

than the red wild-type strains. Pure-culture 

studies with Sporobolomyces and Rhodotorula spp. 

often show enhanced production of carotenoids 

under oxidative stress such as high aeration or 

the addition of radical generators. Further, the 

carotenoid spectrum may also change; if it does, 

the shift is commonly from g- and/or b-carotene 

under reduced oxygen pressure to torulene 

and oxidized carotenoids (e.g. torularhodin) 

at oxidative stress (Fig. 24.8; Sakaki et al., 2002; 

Davoli et al., 2004). This may represent an 

adaptive strategy because many of the oxygencontaining 

carotenoids (i.e. xanthophylls) have 

superior anti-oxidant properties as compared 

to b-carotene (Martin et al., 1999). Other metabolites 

(e.g. vitamin E) or enzymes (superoxide 

dismutase, catalase) with anti-oxidant activities 

may also be produced by red yeasts so that 

the correlation between carotenoid production 

and anti-oxidant protection is not always 

absolute. 

24.4 Ustilaginomycete yeasts 

Most yeasts belonging to the Ustilaginomycetes 

are the monokaryotic stages of smut fungi 

(Section. 23.2) or of Exobasidium (Section 23.4) 

and live saprotrophically on plant surfaces.

USTILAGINOMYCETE YEASTS 

671 

Fig 24.8 Examples of the effect of aeration on carotenoid production in red yeasts belonging to the Basidiomycota. In most red 

yeasts, carotenoid biosynthesis progresses via lycopene at least to the first end-group cyclization to give g-carotene. Several yeasts 

adjust their carotenoid spectrum in response to the level of oxidative stress in their environment. In Sporobolomyces and Rhodotorula 

spp. (Urediniomycetes), g-carotene and/or the bicyclic b-carotene accumulate under microaerophilic conditions (dotted arrow), 

whereas torulene and oxygen-containing carotenoids (xanthophylls) such as torularhodin are produced under oxidative stress 

(solid arrows). In contrast, in Phaffia rhodozyma (Heterobasidiomycetes) the b-carotene produced at low partial oxygen pressure 

is directly oxidized to bicyclic xanthophylls (notably astaxanthin) under oxidative stress. 

Here we shall briefly consider a third group 

of Ustilaginomycetes, the Malasseziales, which 

colonize the skin of warm-blooded animals, 

i.e. mammals and birds. Good accounts of 

this order have been written by Ashbee and 

Evans (2002), Crespo Erchiga and Delgado 

Florencio (2002), Inamadar and Palit (2003) and 

Batra et al. (2005). 

24.4.1 Malasseziales 

This group has been named after the French 

pathologist Louis C. Malassez who was one of the 

pioneers in this field. Following an eventful 

taxonomic history, there is now only one 

genus, Malassezia (formerly Pityrosporum) with 

seven species (Guillot & Guého, 1995; Guého 

et al., 1996). All of them are haploid without 

known sexual stages. 

The yeast cells show several unusual characteristics 

by which they can be recognized. 

Budding is enteroblastic, with the daughter cell 

arising in a unipolar fashion from an exceptionally 

broad ring-like bud scar of the mother cell 

(Guého & Meyer, 1989). The ultrastructure of 

Malassezia is most unusual. The cell wall is thick, 

with its inner surface sculptured into spiral 

ridges (Fig. 24.9) which cast the plasma 

membrane into corresponding grooves (David 

et al., 2003). There is considerable morphological 

plasticity in some Malassezia spp., notably 

M. furfur, in that the shape of yeast cells may 

change from globose to elongated after repeated 

subculturing. Hyphae may also be formed under 

certain conditions. 

All but one species (M. pachydermatis) are 

obligately lipophilic and are isolated from skin 

samples if standard agar media are overlaid with 

a thin film of olive oil. It is possible to isolate 

most Malassezia spp. from the skin of humans 

and other animals, with M. pachydermatis


Fig 24.9 Malassezia pachydermatis. 

Freeze fracture image of a budding cell 

showing the inner surface of the wall. 

The spiral ridges are not seen in the collar 

region. From David et al. (2003), by copyright 

permission of Scripta Media,Brno.Original 

image kindly provided by M. David, M.Gabriel 

and M. Kopecka¤. 

showing a predilection for dogs and cats where it 

can cause skin infections (Guillot & Bond, 1999). 

Most healthy humans carry Malassezia spp., but 

the species composition and density of colonization 

are altered in patients affected by dermatitis 

(Sugita et al., 2001; Crespo Erchiga & Delgado 

Florencio, 2002). The pattern of colonization is 

dependent upon several factors, e.g. the degree of 

sweating and the amount of lipid produced. 

Malassezia spp. are often most abundant on 

people in early adulthood because at that age 

the lipid-producing sebaceous glands at the base 

of the hair shaft are most active. A clear role 

in pathogenesis has been demonstrated only 

for M. globosa which causes a superficial mycosis 

known as pityriasis versicolor in adults below 

middle-age (Gupta et al., 2002). The disease is 

more common in the tropics than in cooler 

climates. Infected skin areas differ in pigmentation 

from the normal skin. Infections are 

associated mainly with the hyphal growth form 

of M. globosa whereas commensal growth is yeastlike 

(Crespo Erchiga & Delgado Florencio, 2002). 

Occasionally, Malassezia spp. also cause contaminations 

of catheters. 

The association of Malassezia spp. with 

dandruff has been suggested but is not yet 

proven (Piérard-Franchimond et al., 2000). Evidence 

in favour of the argument is that dandruff, 

like pityriasis versicolor and other superficial 

skin infections caused by Malassezia spp., disappears 

upon treatment with shampoos or lotions 

containing selenium sulphide or other topical 

antifungal agents (Kwon-Chung & Bennett, 

1992). Further, some Malassezia infections are 

more common in immunocompromised patients 

than in healthy subjects, and there is evidence 

of both humoral and cell-mediated immune 

responses against Malassezia in immunocompetent 

humans (Ashbee & Evans, 2002).

25 

Anamorphic fungi (nematophagous and 

aquatic forms) 

Throughout this book we have attempted to 

consider fungi showing predominantly or purely 

asexual reproduction together with their known 

or suspected teleomorphs. However, certain 

groups of taxonomically diverse fungi colonizing 

the same specialized habitats or substrates 

are best understood in their ecological context, 

especially if they show strikingly similar adaptations 

and morphology despite their different 

evolutionary histories. Two cases illustrating 

such convergent evolution among anamorphic 

fungi are the nematophagous habit and the 

aquatic habitat, which we shall consider in turn 

in this chapter. 

25.1 Nematophagous fungi 

Nematodes are a very varied group of invertebrates. 

They are particularly common as freeliving 

saprotrophic species in the soil, around 

plant roots, on dung and in all kinds of decomposing 

plant matter, as well as in freshwater and 

marine habitats. Most saprotrophic nematodes 

feed on bacteria, although fungal hyphae may 

also be consumed. Other species parasitize 

animals, releasing their eggs or motile stages 

into the environment when their hosts defaecate. 

Plant-parasitic species chiefly attack roots as freeliving 

or sedentary organisms. Sedentary species 

form adult stages inside plant root tissues where 

they cause the economically important root knot 

diseases (Meloidogyne spp.) or root cyst diseases 

(Heterodera spp. and Globodera spp.). Plant-parasitic 

nematodes are readily recognized because their 

mouth parts are modified as stylets with which 

they penetrate plant tissues. Gravid females of 

cyst nematodes enlarge, and their bodies become 

converted into a hardened cyst containing the 

eggs. 

Fungi have evolved a range of mechanisms 

to attack nematodes, which can be grouped 

into three broad categories described below. 

A summary of genera and their taxonomic 

relationships is presented in Table 25.1. 

Nematophagous fungi are common in most 

types of soil which are rich in organic matter, 

and they have been found in arctic, temperate 

and tropical climates (see Dix & Webster, 1995). 

There is no strong evidence of host selectivity. 

Predatory nematophagous fungi produce 

a sizeable mycelium in the soil, with trapping 

devices formed at intervals along the length 

of the hyphae. The varied and occasionally 

spectacular trapping mechanisms have captured 

the imagination of generations of mycology 

students. The most common traps are sticky 

knobs, adhesive networks, non-constricting 

rings or constricting rings (see pp. 675 680). 

Penetration of captured nematodes is followed 

by the growth of trophic hyphae throughout the 

nematode body, and digestion of its contents. 

Because most predatory nematophagous fungi

674 ANAMORPHIC FUNGI 

Table 25.1. Examples of the diversity of nematophagous fungi. 

Genus Taxonomic affinity Mode of parasitism 

Predatory fungi 

Acaulopage, Stylopage Zygomycota Adhesive hyphae 

Gamsylella, Dactylellina, 

Arthrobotrys (incl. Dactylella, 

Dactylaria, Monacrosporium, 

Duddingtonia) 

Drechslerella (incl. Arthrobotrys, 

Dactylella, Monacrosporium) 

Nematoctonus (Hohenbuehelia), 

Pleurotus 

Endoparasitic fungi 

Haptoglossa 

Orbiliaceae 

(Ascomycota) 

Orbiliaceae 

(Ascomycota) 

Pleurotaceae (euagarics 

clade,Basidiomycota) 

Plasmodiophoromycota 

or Oomycota 

Adhesive knobs, columns, 

nets, non-constricting rings 

Constricting rings 

Adhesive or poisonous knobs 

Gun cells (see Fig. 3.9) 

Myzocytium, Nematophthora Oomycota Encysting zoospores 

Catenaria Chytridiomycota Encysting zoospores 

Harposporium, Drechmeria, 

Verticillium, Hirsutella 

Clavicipitaceae 

(Pyrenomycetes, 

Ascomycota) 

Ingestion or attachment 

of conidia 

Egg and cyst parasites 

Rhopalomyces Zygomycota Hyphal colonization of eggs 

Pochonia chlamydosporia 

Paecilomyces lilacinus 

Clavicipitaceae 

(Pyrenomycetes, 

Ascomycota) 

Ascomycota (incertae 

sedis) 

Hyphal colonization of cysts 

Hyphal colonization of eggs 

have a high saprotrophic potential, including 

the ability to degrade cellulose, nematodes are 

probably utilized mainly as a nitrogen supplement 

(Barron, 1992). 

In the endoparasitic nematophagous fungi 

(see p. 680) there is no extensive mycelial 

development outside the nematode host, and 

these species must therefore be regarded as 

obligate parasites in ecological terms. They 

exist in the soil as spores which may either 

become attached to the body of the host, 

or become ingested. The spores then germinate 

and penetrate the animal, developing a 

mycelium within the body of the nematode. 

Only reproductive hyphae (conidiophores) penetrate 

to the outside of the dead colonized 

nematode. 

Parasites of eggs and cysts (p. 684) are found 

in several different taxonomic groups. Typically 

these fungi can be isolated from the soil or 

rhizosphere as well as from nematode eggs or 

cysts, and are therefore viewed as opportunistic 

saprotrophs. The most thoroughly studied 

representatives are Paecilomyces lilacinus and 

Pochonia chlamydosporia (formerly Verticillium 

chlamydosporium).

NEMATOPHAGOUS FUNGI 

675 

We owe much of our knowledge of nematophagous 

fungi to the numerous publications 

by Charles Drechsler. These are cited in many of 

the general accounts given by Duddington 

(1955, 1957), Barron (1977, 1981), Dowe (1987), 

Gray (1987), Nordbring-Hertz (1988) and Dix 

and Webster (1995). A superb film has been 

produced by Nordbring-Hertz et al. (1995). Cooke 

and Godfrey (1964) have provided a key to 

identification. 

25.1.1 Predatory fungi belonging to 

Ascomycota 

Predatory nematophagous fungi are easy to 

study by means of the sprinkle-plate technique. 

A small pinch of soil is added to a Petri dish 

containing tapwater agar or dilute cornmeal 

agar, and the dish is incubated for a few weeks at 

room temperature. Saprotrophic nematodes 

present in the soil will crawl out over the agar 

surface, feeding on bacteria. If predatory fungi 

are present in the soil, they develop structures 

for trapping nematodes, and the trapped dead or 

dying animals are easy to see with a dissecting 

microscope. Conidia will be produced around 

colonized nematodes, and if these are transferred 

to standard media such as cornmeal agar, 

mycelial colonies will grow. Whilst a few 

zygomycetes belonging to the order Zoopagales 

trap nematodes by secreting an adhesive from 

undifferentiated hyphae or short hyphal 

branches upon contact with nematodes 

(Drechsler, 1962; Saikawa & Morikawa, 1985), 

and two basidiomycete genera also trap nematodes 

(see Fig. 25.7), the most striking predatory 

species are conidial forms of Ascomycota. 

Detailed species descriptions may be found in 

the works by van Oorschot (1985) and Rubner 

(1996). 

The taxonomy of predatory ascomycetes has 

traditionally been based on the morphology of 

conidia, especially the number of septa, and the 

degree of clustering of conidia on the conidiophore. 

However, DNA-based phylogenetic 

approaches have confirmed long-held suspicions 

that these criteria are artificial, and that more 

natural taxa can be obtained by grouping 

predatory ascomycetes according to the type of 

trap they form. These results have been summarized 

and discussed by Scholler et al. (1999). All 

known trap-forming ascomycetes described so 

far belong to the family Orbiliaceae (Hagedorn & 

Scholler, 1999), with some species shown to 

produce an apothecium referrable to Orbilia 

itself (Pfister, 1997). This family is still of 

uncertain affinity (incertae sedis) within the 

Ascomycota but may belong to the Pezizales. 

The following trapping structures have been 

described. 

Adhesive knobs and lateral branches. 

Single-celled globose knobs, covered by a sticky 

secretion and spaced at intervals along a hypha, 

form the morphologically simplest trapping 

organs. These knobs are borne directly on the 

hypha or on short lateral branches in such a way 

that a nematode may become attached to several 

knobs (Fig. 25.1). A different type of sticky knob 

is produced on thin stalks (see Fig. 25.5b). 

Sometimes a nematode attached to an adhesive 

knob may pull it off the subtending hypha by its 

violent movement, but respite is only temporary 

because penetration of the host may still occur 

from such detached knobs. Barron (1977) has 

suggested that detachable knobs may provide an 

effective means of dispersal. In some species, 

lateral knob-bearing branches may develop 

in sufficient proximity to each other for anastomosis 

to take place, and this results in the 

formation of a primitive two-dimensional sticky 

network. Scholler et al. (1999) have proposed 

two genera to accommodate fungi with 

knob-like traps, namely Dactylellina (formerly 

Monacrosporium, Arthrobotrys and Dactylella spp.) 

for species with stalked knobs, and Gamsylella 

(formerly Dactylella spp.) for forms with unstalked 

knobs and/or primitive nets. 

Adhesive nets. One of the most common 

types of trap is a three-dimensional adhesive 

network formed by anastomosis of the recurved 

hyphal tips of a lateral branch system. The 

network is lifted above the general level of the 

mycelium. The entire surface of the network is 

covered by an adhesive, as shown by scanning 

electron microscopy (Fig. 25.2; Nordbring-Hertz, 

1972), and a nematode which thrusts its body 

into the network is quickly immobilized. 

Scholler et al. (1999) have grouped fungi


Fig 25.2 Scanning electron micrograph of the adhesive net of 

Arthrobotrys oligospora, showing the glue covering the hyphal 

surface. Reproduced from Nordbring-Hertz (1972) by 

copyright permission of Physiologia Plantarum.Original 

photograph kindly provided by B. Nordbring-Hertz. 

Fig 25.1 Gamsylella sp.Hyphae showing short lateral branches 

modified as sticky knob traps, with nematodes attached at 

several points.This species would be called Monacrosporium sp. 

in traditional nomenclature because of the single conidium 

produced at the end of the conidiophore. 

producing traps of this kind in the genus 

Arthrobotrys. Adhesive nets are illustrated for 

A eudermata (syn. Monacrosporium eudermatum, 

Duddingtonia flagrans) in Fig. 25.3 and for 

A. robusta (Fig. 25.4). Arthrobotrys oligospora 

(Fig. 25.2) is by far the most thoroughly investigated 

member of the genus. 

Non-constricting rings. A number of predatory 

fungi ensnare their prey by three-celled 

rings which are formed by recurvature of the tip 

of a lateral branch, followed by its anastomosis 

with itself. Non-constricting rings have a sticky 

inner surface. A nematode thrusting its body 

into such a loop may become tightly wedged 

inside it, and may find it impossible to 

retract. The point of junction of the loop to 

the subtending hypha is often weak, and the 

struggling nematode may detach the loop. 

Occasionally, a single nematode bearing several 

loops may be seen. The detached loops are still 

capable of penetrating and killing the nematode. 

The action of this trap is passive, i.e. there is 

no inflation of the ring. Fungi producing 

non-constricting rings also form stalked 

adhesive knobs and are included in 

Dactylellina (Scholler et al., 1999). An example is 

D. haptotyla (syn. Dactylaria candida), shown in 

Fig. 25.5. 

Constricting rings. The most dramatic type of 

trap is the constricting ring trap, which develops


677 

Fig 25.3 Arthrobotrys eudermata 

(syn. Monacrosporium eudermatum, 

Duddingtonia flagrans). 

(a) Conidiophore with its single 

attached conidium. Several 

detached conidia are also shown, 

one germinating. (b) Trapped 

nematode showing infection 

bulb and assimilative hyphae. 

(c) Adhesive trapping networks. 

in the same way as the non-constricting ring but 

differs from it in that the three ring cells are able 

to inflate rapidly following stimulation by 

mechanical contact with the inner ring surface. 

Inflation occludes the lumen of the ring, severely 

constricting any nematode trapped in it. The 

surface of constricting rings does not carry any 

adhesive. Fungi producing constricting rings 

have been assigned to the genus Drechslerella by 

Scholler et al. (1999) and were formerly distributed 

in Arthrobotrys and Dactylella. This type of 

trap is illustrated in Fig. 25.6. 

The mechanism of ring closure is of interest. 

The insertion of a fine glass rod into a ring 

by means of a micromanipulator, followed by 

gentle friction of one of the cells, can trigger off 

the closure of the trap. Other stimuli, such as 

heat or a stream of dry air, are also effective. The 

enlargement of the cells is accompanied by 

vacuolation of their contents, and by elastic 

stretching of the inside wall of the ring, 

whilst the outer wall does not change shape 

(Estey & Tzean, 1976). Ring closure is complete 

within 0.1 s. Enlargement of the three cells


Fig 25.4 (a c) Arthrobotrys robusta. 

(a) Conidiophores and conidia. 

(b) Mycelium with anastomosing 

traps. (c) Nematode caught in trap. 

(d) Arthrobotrys oligospora.Two 

conidiophores showing the sequence 

of conidial development. 

making up the ring is not simultaneous, but one 

cell inflates a fraction of a second before the 

others. By immersing rings in 0.3 0.5 M sucrose 

and inducing trap closure by heat, Muller (1958) 

succeeded in slowing down the rate of ring 

closure by a factor of 100, so that the process 

took about 10 s. Estimations of the volume 

change of the cells during constriction showed 

a threefold increase. 

Several physiological changes must take place 

during closure. Chen et al. (2001) have provided 

evidence of a signalling chain in which a physical 

stimulus at the inner ring surface activates a 

trimeric G protein, and transduction of this 

signal via inositol trisphosphate, Ca 2þ and 

calmodulin (see Fig. 12.48) leads to the release 

of osmotically active molecules within the ring 

cells, coupled with the opening of water channels 

at the plasma membrane surface. Muller 

(1958) estimated that there must be an uptake of 

18 000 mm 3 of water in 0.1 s, and water uptake 

may therefore take place over much of the


679 

Fig 25.5 Dactylellina haptotyla (syn. Dactylaria candida). (a) Conidiophore arising from the substrate, producing a terminal cluster of 

septate spindle-shaped conidia. (b) Stalked unicellular knob traps. (c) Non-constricting ring traps. (b,c) to same scale. 

surface of the ring cells. Since the inner part of 

the ring wall rapidly changes shape, it is likely 

that there is a slippage of microfibrils making 

up the wall. Dowsett et al. (1977) showed that 

the inner (luminal) wall of the ring cells in 

Drechslerella (Dactylella) brochopaga is thicker than 

the outer wall. The luminal wall is initially fourlayered, 

but the two external wall layers rupture 

during expansion. 

The threefold increase in cell volume and the 

commensurate increase in surface area, together 

with the process of vacuolation, clearly necessitate 

a rapid rearrangement of membrane material 

within the cell. Heintz and Pramer (1972) 

discovered a labyrinth of membrane-bound 

material close to the plasma membrane on the 

inside of unexpanded ring cells in Drechslerella 

(Arthrobotrys) dactyloides. In expanded rings, a 

more usual type of plasma membrane organization 

was found, suggesting that the membranebound 

inclusions had contributed to the 

formation of the enlarged plasma membrane 

(see also Dowsett et al., 1977). 

25.1.2 Predatory fungi belonging to 

Basidiomycota 

Nematode-destroying basidiomycetes seem to 

be confined to two closely related genera, 

Hohenbuehelia and Pleurotus, both belonging to 

the Pleurotaceae in the euagarics clade (p. 541; 

Thorn et al., 2000). Both genera contain woodrotting 

species forming clamped hyphae. 

Hohenbuehelia produces a Nematoctonus anamorph 

which is of relevance in nematode capture 

(Fig. 25.7). 

The unusual killing mechanism of Pleurotus 

spp. has been described by Barron and 

Thorn (1987). Hyphae produce minute unicellular 

lollipop-shaped spathulate cells which secrete 

droplets of a toxin-containing liquid. Various 

toxins have been identified (p. 682). Nematodes 

touching such a drop show dramatic symptoms 

of a shrinkage of the head region and deformation 

of the oesophagus. Onset of symptoms is 

within one to several minutes and is quickly 

followed by lethargy, so that the affected 

nematode becomes immobilized close by. 

Hyphae of Pleurotus show rapid tropic growth 

towards orifices of the paralysed nematode, and 

colonization ensues within one to several hours 

(Fig. 25.7a). 

Hohenbuehelia possesses two modes of parasitism. 

Hourglass-shaped unicellular mycelial 

branches produce a large drop of non-toxic glue 

by which nematodes are trapped in the usual 

predatory way (Fig. 25.7b). In addition, both


Fig 25.6 Drechslerella sp. 

(a) Conidiophore with a single 

terminal conidium typical of the 

former genus Monacrosporium. 

(b) Three-celled constricting ring 

traps. (c) Two traps, one inflated. 

(d) Nematode caught in constricting 

ring trap. (e) Germinating conidium. 

Hohenbuehelia basidiospores and Nematoctonustype 

conidia produce sticky drops (Barron & 

Dierkes, 1977). Drops are formed at the tapering 

ends of the conidia which are sometimes bent 

at an angle, attaching them to the cuticle of 

a nematode brushing them (Figs. 25.7c,d). 

Hohenbuehelia therefore shows a transition of 

predatory and endoparasitic features (Poloczek 

& Webster, 1994). There are also transitions 

between Hohenbuehelia and Pleurotus because 

Thorn et al. (2000) have described a 

Hohenbuehelia sp. producing both sticky knobs 

and toxin-secreting lollipop-shaped branches. 

Unidentified toxins have also been shown to be 

present in the sticky drops on Nematoctonus-type 

conidia (Giuma et al., 1973). 

25.1.3 Endoparasitic nematophagous fungi 

Several genera of anamorphic fungi include 

forms which are endoparasitic. Although some 

of these fungi can be grown in pure culture in 

the laboratory, in nature probably most of them


681 

Fig 25.7 Nematode-trapping Basidiomycota. (a) Growth of Pleurotus hyphae towards buccal cavities of two nematodes killed 

at za distance by secreted toxins. (b d) Nematoctonus state of Hohenbuehelia. (b) Hourglass-shaped cell producing an adhesive. 

(c) Production of an awl-shaped conidium from a hypha bearing clamp connections. (d) Conidia attached to the cuticle of a dead 

nematode by a sticky knob at the tip of a bent neck. Infection has given rise to trophic hyphae. (b,c) to same scale. 

are obligate parasites without a free-living 

saprotrophic phase. In some species, the conidia 

attach themselves to the cuticle of the host and, 

on germination, penetrate into the body cavity, 

eventually filling it with hyphae. Drechmeria 

coniospora (Figs. 25.8a c) has conical conidia 

which, at maturity, bear a globose, adhesive 

knob at the narrow end. Such conidia readily 

adhere to the cuticle of a nematode which 

brushes past them, and they become preferentially 

attached to the buccal end of nematodes 

(Jansson et al., 1985). In some other forms, infection 

follows ingestion of a conidium. When the 

crescent-shaped conidia of Harposporium anguillulae 

are ingested, the pointed end of the spore 

becomes lodged in the wall of the oesophagus 

and, upon germination, penetrates the body 

cavity from within (Aschner & Kohn, 1958). The 

conidiophores emerging from the dead host bear 

sessile, subglobose phialides (Figs. 25.8d,e). The 

mycelium within the host may form chlamydospores 

which presumably survive in the soil when 

the body of the nematode decays. 

Little is known about the taxonomic position 

of endoparasitic fungi. Several genera contain 

members parasitizing soil invertebrates other 

than nematodes. For instance, the teleomorph of 

Harposporium, Podocrella (syn. Atricordyceps), is 

related to the insect-parasitic genus Cordyceps in 

the Clavicipitaceae (see p. 360). There are also 

numerous examples of lower fungi adopting 

an endoparasitic mode of life, such as Catenaria 

anguillulae (Chytridiomycota) and Myzocytium 

spp. (Oomycota) which infect nematodes by 

means of zoospores, or Haptoglossa which 

produces the spectacular gun cells shown in 

Fig. 3.9. 

Although endoparasitic fungi can sometimes 

be observed on soil-sprinkle plates, a more 

efficient technique for their detection is the 

Baermann funnel. A conical funnel is fitted with 

rubber tubing at its base, and the opening is 

sealed with a clamp. The funnel is lined with 

tissue paper or filter paper; the soil sample is 

filled into the funnel and submerged in water. 

Nematodes will migrate through the filter paper


Fig 25.8 Endoparasitic 

nematophagous fungi. (a c) 

Drechmeria coniospora. (a) Dead 

nematode containing hyphae, and 

bearing emergent conidiophores. 

(b) Conidiophores. (c) Mature 

conidia showing terminal adhesive 

bulbs. (d,e) Harposporium anguillulae. 

(d) Dead nematode showing the 

extent of internal mycelium, and 

external conidiophores. 

(e) Enlargement to show details 

of conidiophores which bear 

subglobose phialides and 

sickle-shaped phialoconidia. 

and congregate at the bottom of the tube, 

from which they can be collected onto tapwater 

agar plates and observed by microscopy. 

After a few hours’ incubation, non-motile nematodes 

may be found, some of them infected with 

endoparasitic fungi. These may develop reproductive 

structures. Bailey and Gray (1989) 

have discussed various isolation techniques for 

nematophagous fungi. 

25.1.4 Nematode fungus interactions 

Stimulation of trap formation 

Many nematophagous fungi do not produce 

trapping organs in pure culture, but the addition 

of nematodes or nematode extracts will 

induce their development within 24 48 h. The 

inducing molecules include small oligopeptides 

containing non-polar and aromatic amino 

acids, such as the phenylalanyl-valine dipeptide 

(Friman et al., 1985). These are present in 

exudates from nematodes (Nordbring-Hertz, 

1977). Other substances, such as horse serum or 

yeast extract, are also effective in inducing trap 

formation, and in natural substrates such as soil 

or dung conidia may germinate directly by 

formation of a trap (Persmark & Nordbring- 

Hertz, 1997). 

In general terms, the readiness to form 

traps has been found to differ between various 

genera and is inversely correlated with their 

saprotrophic capacity (Cooke, 1964; Barron, 

1992). Nordbring-Hertz and Jansson (1984) have 

categorized nematophagous fungi into three 

groups. Thus, the net-forming genus Arthrobotrys


683 

(group 1), credited with the highest competitiveness 

in soil, forms its traps only upon induction 

by the presence of nematodes, whereas producers 

of knobs and rings (Dactylellina, Gamsylella 

and Drechslerella; group 2) form traps more 

readily but have a more limited capacity to 

survive saprotrophically in soil. The obligate 

end of the spectrum from saprotrophy to 

parasitism among nematophagous fungi is 

occupied by some of the endoparasitic fungi 

(group 3). The conidia of these species form sticky 

drops constitutively and have no saprotrophic 

ability. 

Mycelium with traps whether formed 

constitutively or induced by the presence of 

nematodes has been shown to attract nematodes 

significantly more strongly than mycelium 

without traps (Field & Webster, 1977; Jansson & 

Nordbring-Hertz, 1980). The strength of attraction 

can be correlated with the saprotrophic 

capacity of the fungus in question, i.e. group 3 

fungi exert the highest attraction to nematodes, 

with group 2 fungi being intermediate and 

group 1 fungi attracting nematodes to a lesser 

extent even if trap formation has been induced 

(Jansson & Nordbring-Hertz, 1979). The identity 

of the nematode-attracting substances is as 

yet unknown. 

Adhesion 

The strength of adhesion of a trap or conidium 

to the nematode prey is remarkable, and much 

work has been carried out to characterize the 

glue involved. This has been summarized by 

Nordbring-Hertz (1988) and Tunlid et al. (1992), 

who presented evidence of the involvement of 

lectins, i.e. proteins that bind to specific carbohydrate 

residues (receptors). Different predatory 

and endoparasitic nematophagous fungi differ 

in the kind of lectin they produce, and this 

may partially account for the specificity of binding 

observed in some cases, e.g. in Drechmeria 

coniospora whose conidia attach mainly to the 

buccal end of its prey. It seems that the lectins are 

located within the glue on the trap or conidium, 

and that the carbohydrate-based receptors recognized 

by the lectins are part of the glycosylation 

chains of proteins on the nematode surface. 

Toxins 

The capture of a nematode by a predatory fungus 

is soon followed by its death, sometimes after 

a quick but violent struggle. In the case of 

constricting ring traps, the stricture of the body 

may well be a contributory cause of death, 

but there is evidence that toxins are also 

produced by certain fungi. Stadler et al. (1993) 

isolated the common fatty acid linoleic acid as 

a nematicidal principle of Arthrobotrys oligospora 

and other species. Linoleic acid was produced 

at higher amounts by trap-forming cultures 

than by uninduced ones, and it was highly toxic 

against nematodes in vitro, even reproducing 

the typical symptoms of hyperactivity followed 

by paralysis. In the case of Pleurotus spp., two 

toxins have been isolated, namely trans-2-decenedioic 

acid (Kwok et al., 1992) and linoleic acid 

(see Anke et al., 1995). The production of antibacterial 

antibiotics by numerous nematophagous 

fungi has been interpreted as a substrate 

defence strategy against bacterial competitors 

during the colonization of a killed nematode 

(Anke et al., 1995). 

The infection process 

Infection of nematodes often begins before 

the animal is dead. Enzymatic and turgor 

pressure-driven mechanisms have been implicated 

(Veenhuis et al., 1985; Dijksterhuis et al., 

1990). Since the nematode cuticle consists 

mainly of collagen-type proteins and because 

serine proteases of the subtilisin type are known 

from a wide diversity of nematophagous fungi, 

these are generally assumed to play an important 

role in infection of the host and its 

subsequent degradation (Åhman et al., 2002; 

Morton et al., 2004), and their transcription is 

enhanced by the presence of nematode cuticle 

(Åhman et al., 1996). A subtilisin from A. oligospora 

has even been found to possess nematotoxic 

properties, hinting at several roles which these 

proteases may play during infection (Åhman 

et al., 2002). 

Details of the infection process differ between 

predatory and endoparasitic nematodes. In 

predatory species, penetration of the cuticle is 

by means of an appressorium or a hypha emitted 

by that part of the trap which is in contact


with the cuticle. Immediately within the nematode 

body, the penetration hypha swells to 

form a globose vesicle, the infection bulb 

(see Fig. 25.3b), from which assimilative hyphae 

radiate throughout the animal, now dead. The 

cytoplasm of traps of most predatory fungi 

contains an unusual abundance of dense bodies 

(microbodies) identified as peroxisomes. Their 

function is currently unknown but may be 

related to storage (Veenhuis et al., 1989). Similar 

organelles, though of different cytological 

origin, are seen in the assimilative hyphae 

within the nematode. It is likely that they 

are involved in amino acid assimilation and/or 

the degradation of lipids during the digestion 

of the nematode contents (Dijksterhuis et al., 

1993). 

The sequence of infection-related development 

in the endoparasitic conidial species 

Drechmeria coniospora and Verticillium balanoides 

has been described by Dijksterhuis et al. (1990, 

1991) and Sjollema et al. (1993). A hypha growing 

out through the adhesive pad at the conidial 

apex forms an appressorium on the nematode 

cuticle; this mediates penetration. There is no 

infection bulb, and the nematode may remain 

alive while the trophic hyphae proliferate 

within its body. As in predatory species, numerous 

microbodies and lipid droplets are seen 

within the trophic hyphae. The extent of mycelium 

produced by endoparasitic nematophagous 

species in nematodes is often limited, with 

most of the captured biomass being converted 

to conidia. 

25.1.5 Opportunistic parasites of eggs 

and cysts 

Numerous saprotrophic soil fungi have been 

shown to be associated with the eggs and cysts 

of nematodes, especially sedentary species parasitizing 

plant roots (Stiles & Glawe, 1989). Even 

though some host specialization may occur, all 

fungi colonizing nematode eggs and cysts are 

currently considered opportunistic parasites 

(Siddiqui & Mahmood, 1996). They reproduce as 

conidia and/or chlamydospores, like most soil 

fungi. Infection is by means of hyphal tips, and 

no specialized infection structures are formed 

apart from appressoria in some species. 

Nematode eggs contain chitin in addition to 

collagen, and chitinases as well as serine 

proteases have been demonstrated in fungal 

egg parasites (Morton et al., 2004). The most 

important species as potential biological control 

agents are Pochonia chlamydosporia which 

produces conidia and multicellular melanized 

chlamydospores, and Paecilomyces lilacinus 

(Siddiqui & Mahmood, 1996; Kerry & Jaffee, 

1997). 

25.1.6 Biological control of nematodes by 

parasitic fungi 

Some nematodes are serious parasites of plants 

and animals, and attempts have been made to 

use all three ecological groups of nematophagous 

fungi described above predatory, endoparasitic 

and egg- or cyst-colonizing forms for biological 

control. Although the promise held by nematophagous 

fungi is high and some success has been 

reported, no commercial breakthrough has as 

yet been achieved. 

Predatory nematophagous fungi tend to 

show only limited competitiveness in nonnative 

soils (Siddiqui & Mahmood, 1996). 

Although this may preclude their use in the 

biological control of plant-parasitic nematodes, 

the situation is different with animal parasites. 

Many trap-forming fungi occur on dung along 

with the larval stages of nematodes parasitizing 

herbivorous animals. Biological control should 

therefore be feasible, but a major obstacle is 

the requirement for the spores of such potential 

biocontrol agents to survive the stringent 

passage through the herbivore gut. This 

ability has been demonstrated for Arthrobotrys 

eudermata (syn. Duddingtonia flagrans), which is 

unusual among predatory fungi in forming 

thick-walled chlamydospores in addition to 

conidia. There is considerable current interest 

in biological control based on feed supplemented 

with chlamydospores of A. eudermata 

(reviewed by Larsen, 2000). 

There are obvious problems in using endoparasitic 

nematophagous fungi for biological 

control due to practical difficulties in producing 

sufficient inoculum of many species, and

AQUATIC HYPHOMYCETES (INGOLDIAN FUNGI) 

685 

the fundamental problem of their low saprotrophic 

capacity. The latter feature may be 

responsible for observations of a tight coupling 

between the population dynamics of root cyst 

nematodes and those of their fungal endoparasite, 

Hirsutella rhossiliensis (Jaffee, 1992). 

This species can be grown in pure culture, and 

although conidia generated in this way are 

not infectious, hyphal inoculum might be 

useful for biological control in the future 

(Kerry & Jaffee, 1997). 

Opportunistic egg and cyst parasites, notably 

Pochonia chlamydosporia and Paecilomyces lilacinus, 

possess a high ability to colonize plant roots in 

agricultural soils, and are therefore potentially 

useful in the biological control of plant-parasitic 

nematodes. Both have suppressed root knot 

and cyst nematodes in experiments under controlled 

conditions (Siddiqui & Mahmood, 1996), 

although a major problem is that egg masses or 

cysts embedded in root tissue cannot be attacked 

by either fungus (Kerry, 2000). Pochonia chlamydosporia 

has been associated with the suppressive 

properties of agricultural soils against the cereal 

cyst nematode (Kerry et al., 1982). 

25.2 Aquatic hyphomycetes 

(Ingoldian fungi) 

If a sample of foam from a rapid stream flowing 

through deciduous woodland is examined 

microscopically, especially in autumn after leaf 

fall, it will be found to contain a rich variety 

of conidia of unusual shape (Fig. 25.9). Many 

are quite large, spanning 100 mm or more. These 

conidia belong to aquatic hyphomycetes which 

grow on decaying leaves and twigs. They are 

also referred to as Ingoldian fungi in honour 

of C. T. Ingold who pioneered their study. If 

decaying leaves are collected from the stream 

and incubated in a shallow layer of water at 

a temperature of 10 20°C, numerous conidiophores 

of these fungi will develop in a few 

hours. Ingoldian fungi have a worldwide 

Fig 25.9 Conidia of aquatic 

hyphomycetes from river foam. 

(a) Volucrispora sp. (b) Alatospora acuminata. 

(c) Clavatosporalongibrachiata.(d)Tricladium 

splendens.(e)Lemonniera aquatica. 

(f) Lemonniera terrestris.(g)Articulospora 

tetracladia.(h)Clavatospora stellata. 

(i) Anguillospora crassa.(j)Anguillospora sp. 

(k) Heliscus lugdunensis. (l) Unidentified. 

(m) Margaritispora aquatica. 

(n) Tumularia aquatica.


distribution. An excellent guide to the group 

has been written by Ingold (1975) himself, and 

Webster and Descals (1981) have provided keys 

to the then-known species. Over 300 species 

have been described so far. Two common spore 

shapes can be recognized the tetraradiate or 

branched conidium, and the sigmoid or steephelix 

type. Both types of spore may develop 

in a variety of different ways, and it is clear 

that these spore shapes represent a number of 

separate lines of convergent evolution. Evidence 

for the view that tetraradiate and sigmoid 

propagules have evolved independently several 

times is provided by (1) developmental studies, 

(2) anamorph teleomorph connections, and 

(3) observations of the occurrence of 

tetraradiate propagules in unrelated aquatic 

organisms. 

Table 25.2 lists some of the connections 

between aquatic hyphomycetes and different 

groups of ascomycetes and basidiomycetes. It is 

obvious that some anamorph genera, e.g. 

Tricladium or Anguillospora, are unnatural (polyphyletic), 

i.e. they are not made up of related 

species. The teleomorphs for which connections 

have been established develop more readily on 

submerged or partially submerged wood than on 

leaves, although a few leaf-borne teleomorphic 

states have been described. The pleomorphic 

nature of Ingoldian fungi, as in other fungal 

groups, presents problems of nomenclature. 

Strictly, the name adopted should be that of 

Table 25.2. Examples of the taxonomic diversity of Ingoldian fungi (based on Webster, 1992 and Descals 

et al., 1998). 

Anamorph genus Teleomorph genus Taxonomic affinity 

Branched conidial Ascomycota 

Actinosporella Miladina Pezizales 

Anavirga Vibrissea Helotiales 

Articulospora Hymenoscyphus Helotiales 

Casaresia Mollisia Helotiales 

Clavariopsis Massarina Dothideales (Loculoascomycetes) 

Dwayaangam Orbilia Orbiliaceae 

Geniculospora Hymenoscyphus Helotiales 

Tricladium 

Hymenoscyphus, 

Helotiales 

Hydrocina,Cudoniella 

Varicosporium Hymenoscyphus Helotiales 

Branched conidial Basidiomycota 

Taeniomyces Fibulomyces Polyporoid clade (Homobasidiomycetes) 

Ingoldiella Sistotrema Polyporoid clade (Homobasidiomycetes) 

Crucella Camptobasidium Atractiellales (Urediniomycetes) 

Sigmoid conidial Ascomycota 

Anguillospora 

Mollisia, Pezoloma, 

Helotiales 

Hymenoscyphus, Loramyces 

Anguillospora Orbilia Orbiliaceae 

Anguillospora Massarina Dothideales (Loculoascomycetes) 

Flagellospora Nectria Hypocreales (Pyrenomycetes) 

Conidial Ascomycota of other shapes 

Heliscus,Cylindrocarpon Nectria Hypocreales (Pyrenomycetes) 

Dimorphospora Hymenoscyphus Helotiales 

Tumularia Massarina Dothideales (Loculoascomycetes)


687 

the teleomorph, but in practice, because the 

teleomorphs are less frequently encountered 

than the anamorphs, it is the name of the 

latter which is generally used. 

25.2.1 Tetraradiate and other branched 

conidia 

A few examples of the development of branched 

conidia illustrate great variation which can be 

followed by making observations of spore development 

over a period of a few hours on leaf 

fragments bearing conidiophores or from pieces 

of agar culture incubated in water. In some cases 

development is aided by placing culture pieces 

in special flow cells which permit microscopic 

observations to be made under continuous water 

flow over time. 

Phialidic tetraradiate conidia 

A good example is Lemonniera aquatica 

(Fig. 25.10a), probably the most common of the 

six species in this genus. Conidiophores develop 

from mycelium embedded in the leaf tissues or 

from chlamydospores or sclerotia, and terminate 

in 1 3 phialides. From the tip of the phialide 

a tetrahedral conidium primordium develops, 

and the four corners of the tetrahedron extend 

simultaneously to form cylindrical arms which 

may become septate. The mature conidium is 

thus attached centrally to the phialide at the 

point of divergence of the arms. When the firstformed 

conidium is detached to be carried away 

by water currents, a second conidium develops, 

and others follow. 

Phialides of Alatospora (Fig. 25.10b) develop 

singly at the tips of short, inconspicuous conidiophores. 

Midway along the length of an 

elongated spore initial, two divergent lateral 

arms arise and extend simultaneously. 

Heliscus lugdunensis (Fig. 25.10c) is a common 

early colonizer of the bark of twigs which have 

fallen into streams. Its conidiophores develop on 

sporodochium-like pustules and branch repeatedly, 

terminating in phialides. Conidia which 

develop underwater are clove-shaped with short, 

conical projections at the upper end, whereas 

more cylindrical conidia are produced under 

aerial conditions, e.g. on a twig incubated in 

a moist chamber or on agar culture. The 

Fig 25.10 Three phialidic aquatic hyphomycetes. 

(a) Lemonniera aquatica.(b)Alatospora acuminata.(c)Heliscus 

lugdunensis. 

teleomorph is Nectria lugdunensis which forms 

bright red perithecia on half-submerged twigs. 

Blastic tetraradiate conidia 

There are numerous examples of blastic conidial 

development in aquatic hyphomycetes. 

Articulospora tetracladia (Fig. 25.11a) forms short 

conidiophores extending from mycelium within 

a leaf. At the tip of the conidiophore the first 

arm develops as a cylindrical bud. At the apex 

of this first arm, three further cylindrical buds 

develop in turn. A narrow constriction or 

joint marks the point of attachment of these 

later-formed arms to the first (hence the name 

Articulospora, a jointed spore). The mycelium and


Fig 25.11 Two blastic aquatic hyphomycetes. (a) Articulospora 

tetracladia.The arms of the conidia develop successively. 

(b) Clavariopsis aquatica.The top-shaped body of the conidium 

develops first, followed by simultaneous development of the 

three thinner arms. 

Fig 25.12 Tricladium splendens. (a) Stages in blastic 

development of conidia. A club-shaped main axis develops 

lateral arms successively from different points along its length. 

(b) Mature detached conidia. 

conidia of Articulospora are hyaline. The teleomorph 

is an inoperculate discomycete, 

Hymenoscyphus tetracladius. 

Clavariopsis aquatica (Fig. 25.11b) has dark 

mycelium and conidia. The conidia have a 

broad, obconical body with a rounded tip 

bearing three cylindrical arms which develop 

simultaneously. The mature conidium usually 

has a single septum in the central body. In 

culture, a spermogonial state has been found, 

a dark-coloured pycnidium containing minute, 

colourless spermatia. The teleomorph belongs to 

the genus Massarina (Loculoascomycetes). 

Tricladium splendens (Fig. 25.12) also has darkcoloured 

mycelium and conidia. The apex of the 

conidiophore develops a club-shaped swelling 

which becomes septate and forms the main axis 

of the conidium. A bud develops at one point on 

the main axis, to be followed by a second, at 

a different point. The arms taper and are 

constricted where they join the main axis. Its 

teleomorph is Hymenoscyphus splendens. 

Tetrachaetum elegans (Fig. 25.13) has a hyaline 

mycelium and conidia which are relatively large, 

spanning up to 200 mm. The conidium develops 

by the curvature of the main axis which is 

narrowly cylindrical. Two laterals arise at a 

common point about halfway along the main 

axis, and develop simultaneously. Varicosporium 

elodeae (Fig. 25.14) and Dendrospora erecta 

(Fig. 25.15) bear blastoconidia which are more 

highly branched, with further branches developing 

from the primary laterals. 

Branched conidia with clamp connections and 

dolipore septa 

A number of branched conidia found in water or 

foam have clamp connections at their septa, 

showing that they are basidiomycetes. They


689 

Fig 25.13 Tetrachaetum elegans.The main axis of the conidium 

bends and, at the point of curvature, two lateral arms arise 

simultaneously. 

obtained in cultures derived from a conidium. 

The teleomorph is a species of Fibulomyces 

probably belonging to the polyporoid clade. 

Ingoldiella hamata (Fig. 25.17), a tropical 

aquatic fungus, has large, dikaryotic conidia 

with numerous clamp connections. The basidial 

state is Sistotrema hamatum (polyporoid clade) 

with eight-spored basidia. Single basidiospores 

germinate to form monokaryotic mycelia on 

which monokaryotic conidia develop. These 

closely resemble dikaryotic conidia but lack 

clamp connections. 

There are other aquatic hyphomycetes with 

basidiomycetous affinities indicated by the 

possession of dolipore septa within the mycelium 

and the conidium. Examples include 

Dendrosporomyces prolifer and D. splendens which 

have conidia with a strong morphological resemblance 

to Dendrospora, and Tricladiomyces malaysianum 

with spores resembling those of a 

Tricladium but with dolipore septa (Nawawi, 

1985). 

25.2.2 Sigmoid conidia 

A similar range of different types of conidial 

ontogeny can be demonstrated for sigmoid 

conidia. 

Phialoconidia 

Flagellospora curvula (Fig. 25.18a) has narrow, 

sigmoid phialoconidia developing from phialides 

on a sparsely branched conidiophore. A more 

richly branched, penicillate arrangement of 

phialides is found in F. penicillioides (Fig. 25.18b), 

which has a Nectria teleomorph. 

Fig 25.14 Varicosporium elodeae. Branched 

blastoconidia formedby repeatedbranching of the lateral arms 

which develop mostly from one side of the main axis. 

include Taeniomyces (Fig. 25.16) which has a 

conidium somewhat resembling a Tricladium, 

but with a single clamp connection at the 

septum lying between the two arms. The conidium 

is dikaryotic, and the basidial state has been 

Blastoconidia 

Anguillospora has blastic, sigmoid conidia, but 

evidence from the known teleomorphs indicates 

that this form-genus is very heterogeneous, 

including species from unrelated groups of 

Ascomycota (see Table 25.2). There are also 

differences in the mechanism of conidial 

separation. Anguillospora longissima (Fig. 25.19) 

has dark mycelium and conidia. The conidia 

develop as club-shaped swellings from the 

apices of conidiophores. The conidium becomes 

septate and helically curved. Conidial separation 

is rhexolytic, brought about by the collapse


Fig 25.15 Dendrospora erecta. 

Much-branched blastoconidia formed 

by repeated branching of lateral arms 

which develop on all sides of the main 

axis of the conidium. 

Fig 25.16 Taeniomyces gracilis. 

(a) Mature detached conidia. Note 

the clamp connection between the 

lateral arms. (b) Basidial state 

(Fibulomyces sp.). 

of a special separating cell at the base of the 

conidium. The contents of the separating cell 

disintegrate, and the cell wall breaks down at 

a line of weakness near the middle. When the 

conidium separates, it carries at its base a little 

collar which represents half of the empty separating 

cell. Similarly, the apex of the conidiophore 

bears a collar after detachment of the 

first conidium. The conidiophore may develop a 

second conidium by percurrent extension 

through the remnants of the first separating cell 

and, after several conidia have been formed, a 

succession of collars may be found at the tip of 

the conidiophore. The teleomorph of A. longissima 

is a pseudothecium-forming species of 

Massarina found on twigs in streams. 

A second species, A. furtiva, has conidia which 

closely resemble those of A. longissima, but cultures 

derived from such conidia have developed 

apothecia of an inoperculate discomycete, 

Pezoloma sp. In A. furtiva there is no separating 

cell and conidium separation is schizolytic, 

i.e. by dissolution of a septum at its base 

(Descals et al., 1998). In A. crassa, which has fatter


691 

Fig 25.17 Ingoldiella hamata. (a) Developing dikaryotic conidia. 

Note that the septa bear clamp connections. (b) Mature 

dikaryotic conidia. (c) Monokaryotic conidium lacking clamp 

connections. 

conidia, separation is also brought about by 

septum dissolution, and this species also has an 

inoperculate discomycete as its teleomorph, 

Mollisia uda. 

Lunulospora curvula (Fig. 25.18c) has crescentshaped 

blastoconidia which develop from 

specialized conidiogenous cells at the apex of 

dark conidiophores. This fungus is more 

common in warmer countries than in temperate 

regions, and in Britain its season of maximum 

abundance is in late summer and autumn. 

25.2.3 Other types of spore 

Not all aquatic hyphomycetes have branched 

or sigmoid conidia. Margaritispora aquatica 

forms hyaline, globose phialoconidia bearing 

a few conical protrusions (Fig. 25.20a), whilst


Fig 25.18 Three aquatic 

hyphomycetes with sigmoid conidia. 

(a) Flagellospora curvuula 

conidiophores with phialides and 

sigmoid phialoconidia. (b) Flagellospora 

penicillioides conidiophores with 

phialides and phialoconidia. 

(c) Lunulosporacurvula,showingblastic 

development of crescent-shaped 

conidia. 

Fig 25.19 Anguillospora longissima,anaquatic 

hyphomycete with blastic sigmoid conidia. 

(a) Detachment of conidium showing the 

remnants of the separating cell, and percurrent 

proliferation. (b) Developing conidia.The arrow 

marks a separating cell. (c) Mature detached 

conidia.


693 

Tumularia aquatica (Fig. 25.20b) has pear-shaped 

or broadly fusiform blastoconidia which separate 

by septal dissolution. The teleomorph of this 

fungus is Massarina aquatica which forms pseudothecia 

on submerged wood in streams. 

25.2.4 The significance of spore shape 

in aquatic fungi 

We have seen that tetraradiate conidia may 

develop in a variety of ways and are produced 

both by Ascomycota and Basidiomycota. 

Tetraradiate propagules have also been found 

as secondary conidia of Entomophthoraceae 

attacking aquatic insects (see Fig. 7.42; Descals 

et al., 1981), and as basidiospores in the marine 

fungi Digitatospora marina (Homobasidiomycetes) 

and Nia vibrissa (gasteromycetes) (Doguet, 1962, 

1967). The brown alga Sphacelaria also forms 

tetraradiate propagules. There is thus ample 

evidence for the view that this type of structure 

has evolved repeatedly in aquatic environments. 

The functional significance of convergent evolution 

of tetraradiate and sigmoid spore shapes has 

been discussed by Webster (1987). Experimental 

studies have shown that tetraradiate propagules 

are more effectively trapped by impaction onto 

underwater objects than spores of more conventional 

shape. This is because a tetraradiate 

propagule making contact with a surface will 

achieve a three-point landing, a very stable form 

of attachment. Attachment is aided by secretion 

of mucilage at the tips of the arms which quickly 

develop ‘appressoria’ and germ tubes, but the 

fourth arm not in contact with a surface fails 

to differentiate in this way (Read et al., 1991, 

1992a,b; Jones, 1994). Once appressoria have 

been formed, the propagules are very resistant 

to detachment. 

Trapping efficiency may not be the only 

advantage of a tetraradiate propagule because 

these spores may also be found among leaves in 

terrestrial habitats (Bandoni, 1972; Park, 1974). 

Fig 25.20 (a) Margaritispora aquatica, 

conidiophores, phialides and 

phialoconidia. (b) Tumularia aquatica, 

conidiophores and blastoconidia.


Bandoni (1974) has advanced the idea that 

tetraradiate spores may be adapted to movement 

in surface films of water. 

Although sigmoid spores are less efficiently 

trapped than tetraradiate spores, they, too, can 

develop in different ways and in unrelated 

groups of fungi which have adopted an aquatic 

habit, suggesting that their shape has selective 

value. Observations on sigmoid spores moving 

with the current flow in flat capillary tubes show 

that as they approach a surface they tumble end 

over end and come to rest with one spore tip in 

contact with the surface. Immediately after 

arrest, the spore swings parallel to the current, 

thus minimizing the shear forces acting to 

detach the spore (Webster & Davey, 1984). As in 

tetraradiate spores, the tips of the arms of 

sigmoid spores secrete mucilage, possibly in 

response to a thigmotropic stimulus associated 

with their tumbling movements. Mucilage is also 

present on the outside of the sigmoid spore of 

Mycocentrospora filiformis prior to it making 

contact with a surface (Au et al., 1996). Current 

flow forces the spore into contact with the 

surface at a second point along its length. 

Germination occurs by the development of 

a germ tube from that end of the spore which 

is in contact with the surface. Thus, in contrast 

to the three-point contact associated with tetraradiate 

spore shape, sigmoid spores make two 

points of contact with surfaces to which they 

adhere. 

25.2.5 Spores in stream foam 

Foam is an effective trap for both tetraradiate 

and sigmoid spores (see Fig. 25.9). Spores 

suspended in water or caught in stream foam 

rarely germinate and many studies on the 

distribution and seasonal abundance of aquatic 

hyphomycetes using preserved foam samples 

have been made. In experiments in which air 

bubbles were passed through concentrated 

suspensions of conidia, the concentration of 

suspended spores fell very rapidly. Tetraradiate 

conidia were removed more readily than conidia 

of sigmoid or other shape (Iqbal & Webster, 

1973a). Comparisons of spores collected in foam 

or by Millipore filtration from the same stream 

indicates that the spore content of foam overrepresents 

the tetraradiate type of conidium 

in relation to other spore types known to be 

present. It cannot be assumed that all propagules 

found in stream foam originate from within 

the stream. Some come from fungi growing on 

the living leaves of riparian trees and the spores 

are brought into the stream in raindrops or 

from rainwater draining down the tree trunks. 

Such fungi have been distinguished as terrestrial 

aquatic hyphomycetes (Ando & Tubaki, 

1984a,b). 

25.2.6 Adaptations of Ingoldian fungi to 

the aquatic habitat 

Ingoldian fungi represent an ecological group of 

fungi sharing a common habitat, typically leaves 

and twigs in rapidly flowing streams. It is 

believed that they have been derived from 

terrestrial ancestors and are able to colonize 

their habitat by virtue of a number of adaptations. 

These include effective spore attachment 

mechanisms associated with tetraradiate and 

sigmoid spore shape, rapid germination, and 

rapid growth and sporulation enhanced by 

turbulence and rapid water flow (Webster & 

Towfik, 1972; Sanders & Webster, 1980). 

Physiological adaptations include the possession 

of a range of enzymes enabling them to degrade 

their substrata (see below), and an ability to 

grow at low temperatures, sometimes approaching 

0°C, so that they can continue growth 

and sporulation on submerged deciduous tree 

leaves after the autumn pulse of leaf fall 

(Koske & Duncan, 1974). Despite their typical 

environment, many aquatic hyphomycetes can 

survive for several weeks on dried leaves 

previously colonized in streams and brought 

out by flooding or by falling water levels (Sanders 

& Webster, 1978). It is possible that overland 

dispersal is achieved if colonized dried leaves 

are blown about by wind and re-deposited in 

streams. 

25.2.7 Ecophysiological studies 

There have been extensive studies on the ecology 

and physiology of Ingoldian hyphomycetes 

stimulated by the discovery that they play an


695 

essential role in rendering leaves which they 

colonize in streams more palatable and nutritious 

to aquatic invertebrates feeding on them 

(Bärlocher, 1992; Dix & Webster, 1995; see below). 

Ecological studies have been facilitated by the 

fact that these fungi can, in general, be recognized 

to a high degree of certainty from their 

spores, which is not the case for most other 

groups of fungi. 

Distribution 

Ingoldian hyphomycetes have a worldwide distribution 

from the equator to the Arctic. They are 

found most frequently in babbling brooks overhung 

by deciduous trees and are less abundant 

in wider rivers or where streams flow through 

afforested regions in which trees have been clearfelled 

on both sides (Metwalli & Shearer, 1989). 

They are relatively infrequent in streams in 

mountainous or moorland areas devoid of 

riparian trees, but can grow there on plants 

such as rushes (Juncus spp.). As rivers flow 

towards the sea and the brackish condition is 

encountered in the estuaries, Ingoldian hyphomycetes 

decline in frequency. A few species grow 

in lakes, but the lotic (flowing) habitat is 

preferred to the lentic (smooth). 

Substrates 

The main substrates for aquatic hyphomycetes 

are leaves of deciduous trees. In general these 

fungi show little host specificity but certain tree 

leaves support a richer fungal population with 

more abundant sporulation than others (Gulis, 

2001). A particularly rich mycota is associated 

with the leaves of alder (Alnus glutinosa), a 

common riparian tree, and this is possibly correlated 

with their relatively high nitrogen content 

due to the fact that Alnus can fix gaseous N 2 . 

In contrast, the leaves of beech (Fagus sylvatica) 

are a poor substrate. Needles of conifers are 

resistant to colonization by aquatic hyphomycetes, 

related partly to their thick cuticles and 

also to the presence of compounds inhibitory to 

mycelial growth (Bärlocher & Oertli, 1978a,b). 

Wood which has fallen into streams is an 

important substratum because it is more enduring 

than leaves, which decompose more rapidly 

and are consumed by animals or scoured by 

water currents, so that they may not survive in 

great quantity to provide inoculum for the next 

season’s autumnal input. Additionally, colonized 

wood is a substratum for the development of 

teleomorphs (Shearer, 1992). Living riparian tree 

roots also support a population of aquatic 

hyphomycetes (Fisher et al., 1991; Sridhar & 

Bärlocher, 1992a,b), with roots of alder and 

willow (Salix) particularly important because 

they extend into streams. Aquatic hyphomycetes 

have even been reported from beech roots 

growing in woodland soil (Waid, 1954). In 

lowland streams and rivers a few species may 

colonize living and decaying leaves of in-stream 

macrophytes (Kirby et al., 1990). Treeholes, 

cavities formed within tree trunks where the 

stumps of fallen branches have decayed, intermittently 

fill with rain water. Samples of the 

water and the leaf and other debris which 

accumulates in treeholes reveal the frequent 

presence of Ingoldian fungi such as Alatospora 

acuminata (Gönczöl & Révay, 2003). 

Spore concentrations in streams 

Concentrations of aquatic hyphomycete spores 

in streams can be readily estimated by the 

filtration of water samples through a Millipore 

filter (preferably with 8 mm pore size, to facilitate 

rapid filtration) followed by treatment which 

stains the spores and renders the filter transparent. 

Concentrations reach a peak soon after the 

main period of autumnal deciduous leaf fall 

in temperate countries. Spore counts as high as 

2 3 l0 4 l 1 have been made in October and 

November in Britain and elsewhere (Iqbal & 

Webster, 1973b). As the leaves are decomposed, 

consumed or swept downstream, the concentration 

of spores in suspension may fall to undetectable 

levels. This points to the significance of 

colonization of more enduring woody substrata 

and also growth in the roots of riparian trees 

which extend into the water. 

Feeding of invertebrates on aquatic 

hyphomycetes 

It is now becoming clear that aquatic hyphomycetes 

play an important role in the cycling of 

nutrients in streams (e.g. Kaushik & Hynes, 1968, 

1971; Bärlocher & Kendrick, 1973a,b; Suberkropp


& Klug, 1976, 1980). Streams bordered by trees 

receive the bulk of their fixed carbon input not 

from attached macrophytes or algae, but from 

leaves, twigs and other debris shed by trees and 

other plants. Such material is relatively poor in 

nitrogen or is otherwise unpalatable to the 

invertebrate animal population. The colonization 

of leaf litter by aquatic fungi and bacteria is 

an important part of the ‘processing’ which 

makes it a more attractive substrate to animals 

(Berrie, 1975). There are two main reasons for 

this, namely pre-digestion and enrichment in 

organic nitrogen. 

First, the activities of the fungi soften the leaf 

tissues. Aquatic hyphomycetes possess a range of 

pectolytic, cellulolytic, proteolytic and ligninolytic 

enzymes capable of degrading leaf tissues 

(Suberkropp & Klug, 1980; Chamier, 1985; Zemek 

et al., 1985; Gessner et al., 1997). Colonized 

softened leaves are more easily grazed and 

shredded than uncolonized leaves by aquatic 

invertebrates such as Gammarus and Asellus and 

by the larvae of aquatic insects feeding directly 

on leaf tissue or on particulate organic matter 

released into streams as leaves decay. In general, 

aquatic animals do not possess enzymes capable 

of degrading the cell walls of leaf tissue, but the 

enzymes present within ingested leaf fragments 

may continue to be active within the animals’ 

guts. When presented with a choice of uncolonized 

or colonized leaf tissue, either as separate 

discs or as patches on the same leaf, caddis fly 

larvae feed preferentially on colonized tissue 

(Arsuffi & Suberkropp, 1985). 

Second, the protein content of leaf material is 

enhanced by microbial colonization. Aquatic 

fungi can concentrate inorganic nitrogen 

present in solution in the water at low concentrations 

but in large total amounts and, making 

use of the organic matter in the leaves, manufacture 

microbial protein. Fungi can make up 

over 90% of the microbial biomass which develops 

on decomposing leaves in streams. Aquatic 

animals may feed directly on the fungal mycelium 

and on fungal spores. Detritivorous animals 

such as Gammarus pulex and Asellus aquaticus 

fed on a fungus diet make a much greater 

weight increase than those fed solely on a diet 

of uncolonized leaves. They are also more 

fecund, i.e. produce more eggs per brood 

(Graca et al., 1993). In order to sustain their 

restricted growth rate on leaf diets, the animals 

consume about 10 times more leaf material 

(by dry weight) than individuals fed on fungus 

diets. Thus aquatic hyphomycetes play a very 

important role as intermediaries in the diet 

of aquatic invertebrates and their major food 

source, the leaves of riparian trees. Since aquatic 

invertebrates in turn provide the food source 

of other animals, including fish, the activities 

of aquatic hyphomycetes are vital to the food 

chain in maintaining stream productivity. 

25.3 Aero-aquatic fungi 

If leaves and twigs from the mud surface of 

stagnant pools or slow-running ditches are 

rinsed and incubated at room temperature in 

a humid environment (e.g. a Petri dish or plastic 

box lined with wet blotting paper), fungi with 

very characteristic large conidia usually develop 

within a few days. The common feature of the 

conidia of these fungi is that they trap air as they 

develop, which assists in floating off the conidia 

if the substratum is submerged in water. Conidia 

of this type have been termed bubble-trap 

propagules (Michaelides & Kendrick, 1982). 

Such fungi grow vegetatively on leaves and 

twigs, often in water with quite low amounts 

of dissolved oxygen. Under submerged conditions 

these fungi do not sporulate, but do so 

only after incubation under aerial conditions 

in which a moist interface between air and water 

is provided, as might happen at a pond margin 

as the water dries up and previously submerged 

twigs or leaves become exposed to air. They have 

therefore been termed aero-aquatic fungi. 

Aero-aquatic fungi are an ecological group 

of organisms without phylogenetic coherence, 

as shown in Table 25.3. Although the taxonomy 

of the group is fairly well known (see e.g. Linder, 

1929; Moore, 1955; Webster & Descals, 1981; 

Goos, 1987; Voglmayr, 2000), it is likely that 

many more species remain to be discovered. 

Careful studies should also reveal new ascomycetous 

teleomorphs because several species

AERO-AQUATIC FUNGI 

697 

Table 25.3. Examples of the taxonomic diversity of aero-aquatic fungi. 

Anamorph genus Teleomorph genus Taxonomic affinity 

Oomycota 

Medusoides (oogonium) Pythiogetonaceae (Pythiales) 

Ascomycota 

Clathrosphaerina Hyaloscypha Helotiales 

Helicoon Orbilia Orbiliaceae 

Helicodendron Mollisia, Hymenoscyphus Helotiales 

Helicodendron Lambertella, Herpotrichiella Chaetothyriales (see p.484) 

Helicodendron Tyrannosorus Dothideales (Loculoascomycetes) 

Pseudaegerita Hyaloscypha Helotiales 

Basidiomycota 

Aegerita Bulbillomyces Polyporoid clade 

Aegeritina Subulicystidium Polyporoid clade 

(Unknown) Limnoperdon (basidiocarp) Gasteromycetes 

Akenomyces (Sclerotium) (Unknown) Incertae sedis 

of aero-aquatic fungi form microconidial synanamorphs 

in culture, the spores of which fail 

to germinate. These are probably spermatia. 

25.3.1 Development of propagules 

There are various ways in which conidia of aeroaquatic 

hyphomycetes may develop. In Helicoon 

(Fig. 25.21a) they develop as cylindrical or barrelshaped 

spirals. The conidia vary in colour 

from hyaline to black. The direction of coiling 

of the spirals (looking upwards from the apex of 

the conidiophore) is clockwise in H. richonis 

whereas in some other helicosporous fungi the 

direction of coiling is counter-clockwise. The 

direction appears to be constant for a given 

species. In Helicoon the conidia themselves do 

not branch, but in Helicodendron (Hd.) which is 

clearly a polyphyletic anamorph genus, the 

conidia may bear further conidia as lateral 

branches (Figs. 25.21b,c; 25.22a). Beverwijkella 

pulmonaria, probably an anamorphic ascomycete 

(Fig. 25.23a), forms uni- or bi-lobed, balloon-like 

structures. At the surface, aggregates of dark, 

thick-walled, tightly packed cells develop, with 

air trapped inside the cavity which they enclose 

(Michaelides & Kendrick, 1982). Spirosphaera, 

another anamorphic ascomycete, achieves the 

same end by the formation of globose 

propagules made up of richly branched, 

incurved hyphae (Fig. 25.23b). Yet another way 

of entrapping air within the propagule is 

shown by Clathrosphaerina zalewskii which forms 

hollow, spherical propagules with a lattice wall, 

resembling practice golf balls. These clathrate 

structures are formed by the repeated dichotomy 

of the arms of the developing conidium, which 

then curve inwards and join firmly where 

the tips of the arms touch (Figs. 25.22b, 25.24). 

This fungus has a minute inoperculate discomycete 

teleomorph, a species of Hyaloscypha 

whose apothecia develop in air on twigs or 

pieces of wood which have previously been 

submerged. 

Several bubble-trap propagules are also 

known among Basidiomycota. An example 

is Aegerita candida (teleomorph Bulbillomyces 

farinosus), which forms its conidia (bulbils) 

and basidia on the surface of wet, previously 

submerged wood. The propagule is made up 

of tightly clustered aggregates of inflated, 

dikaryotic clamped cells between which air is 

entrapped (see Figs. 18.8 and 25.22c). The 

propagules of Aegeritina tortuosa (teleomorph 

Subulicystidium longisporum) which also grows on 

wet wood resemble those of A. candida but are 

not clamped.


Fig 25.21 Some aero-aquatic helicosporous fungi. (a) Helicoon 

richonis.(b)Helicodendron triglitziense.(c)Helicodendron 

conglomeratum.The central spore is drawn in optical section to 

show the trapped air bubble. 

25.3.2 Ecophysiological studies 

Although aero-aquatic fungi are taxonomically 

diverse, they share several common physiological 

features which help in understanding their 

ecology (for references see Webster & Descals, 

1981; Dix & Webster, 1995; Voglmayr, 2000). 

Simple techniques have aided studies of their 

ecology. Quantitative studies on colonization 

and survival have been made using small discs 

of leaves of beech, Fagus sylvatica. Sterile or 

artificially inoculated discs can be submerged 

among the accumulated leaf detritus in a pond 

and recovered at intervals in order to monitor 

the development of conidia for quantifying 

colonization. 

The bubble-trap propagules of aero-aquatic 

fungi are hydrophobic and float ungerminated 

at the water surface of stagnant ponds. Autumn-


699 

Fig 25.22 Propagules of aero-aquatic fungi which have 

developed at the surface of moist leaves incubated in air. 

(a) Helicodendron giganteum. Note that secondary conidia 

can develop as branches from the first-formed conidia. 

(b) Clathrosphaerinazalewskii.(c)Aegerita candida. All images 

to same scale.Reprinted from Dix and Webster (1995); original 

micrographs kindly provided by P. J. Fisher. 

shed leaves which fall onto the water are rapidly 

colonized (Premdas & Kendrick, 1991). The leaves 

eventually sink to the bottom of the pond and 

growth of the fungi continues so long as 

dissolved oxygen is available in the water. 

Underwater colonization may also take place 

by leaf-to-leaf contact, shown by the fact that 

sterilized beech leaf discs submerged among 

detritus develop conidia of aero-aquatic fungi 

when later incubated under suitable conditions 

out of water. If there is a substantial accumulation 

of fallen leaves, the metabolic activity of 

decomposer organisms will lead to anaerobic 

conditions and the evolution of hydrogen 

sulphide (H 2 S) which is toxic at low concentrations 

to eukaryotic organisms. Anaerobic conditions 

are evidenced by the sulphurous smell of 

disturbed mud and by the black colour of the silt 

caused by the accumulation of metallic 

sulphides, especially iron sulphide. Although 

aero-aquatic hyphomycetes grow best at atmospheric 

oxygen levels, their growth in anoxic 

conditions is still superior to that of other fungi 

(Fisher & Webster, 1979). Under strictly anaerobic 

conditions, five species of Helicodendron 

showed almost 100% survival for 6 months, and 

substantial survival even after 12 months (Field & 

Webster, 1983). Survival in most cases appears to 

be by thick-walled hyphae because chlamydospores 

and sclerotia are rarely found. Similar 

comparative studies of the survival of aeroaquatic 

fungi and aquatic hyphomycetes under 

anaerobic conditions in the presence of low 

concentrations of H 2 S showed better survival of 

aero-aquatic fungi than aquatic hyphomycetes 

(Field & Webster, 1985). 

Following a prolonged period of submersion 

under the anaerobic or near-anaerobic conditions 

of the bottom silt of a pond, it takes several 

days for sporulation of aero-aquatic fungi to 

commence in air. Incubation in well-aerated 

water before exposure to air improves the 

recovery, suggesting that a period of aerobic 

growth is a stimulus to sporulation. For most 

species studied, exposure to light also enhances 

sporulation (Fisher & Webster, 1978). 

Aero-aquatic fungi (Helicodendron spp.) grown 

on a homogenized beech leaf mash can survive 

on the soil surface for several months if airdried 

(Fisher, 1978), suggesting a capacity for 

vegetative existence out of water, a conclusion 

confirmed by reports of some species from soil 

(Abdullah & Webster, 1980). Dispersal of colonized 

wind-blown leaves from one body of water 

to another is clearly a possibility. Other possible


Fig 25.23 Air-trapping 

multicellular propagules of 

two aero-aquatic fungi. 

(a) Beverwijkella pulmonaria. 

(b) Spirosphaera sp. 

Fig 25.24 

Clathrosphaerina zalewskii.Conidial development.


701 

means of dispersal are the carriage of wind-borne 

ascospores and basidiospores of the teleomorphs, 

passive dispersal of conidia by waterfowl, and 

conidium dispersal at the water surface during 

flooding. 

Aero-aquatic fungi show some host specificity. 

Leaves and twigs of broad-leaved trees are 

colonized by a wide range of species, but leaves 

of coniferous needles such as Pinus have a more 

restricted mycota including Hd. fractum and 

Hd. hyalinum. Monocotyledonous hosts such as 

grasses, rushes and sedges support few species, 

but exceptions are Hd. praetermissum, Spirosphaera 

carici-graminis and S. minuta. Fruiting of Aegerita 

and Aegeritina is supported on woody substrates 

rather than leaves, whereas Pseudaegerita spp. 

fruit both on rotten wood and on leaves. There 

are also differences in frequency in relation to 

water chemistry (Voglmayr, 2000). For example 

B. pulmonaria, Hd. conglomeratum, Hd. tubulosum 

and Helicoon fuscosporum are found in eutrophic 

waters, Spirosphaera minuta is characteristic 

of oligotrophic conditions, and Candelabrum 

desmidiaceum is mostly found in dystrophic 

conditions. Other species have a wider tolerance. 

Helicodendron triglitziense and S. floriformis are 

two very common species found in dystrophic 

to eutrophic waters. 

Like so many fungi described in this book, 

aero-aquatic species have adopted, by convergent 

evolution, a suite of flexible characters which 

has enabled them to explore a habitat of 

extremes, in this case the amphibious environment 

involving changes between anaerobic and 

aerobic conditions, and between aquatic and 

terrestrial lifestyles.

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Index 

Page numbers with images are underlined, those with explanations of concepts are printed in bold. 

ABC transporters 280, 383, 439 

Absidia 183 

Absidia corymbifera 184 

Absidia glauca 172, 176, 185 

Absidia spinosa 173, 176, 184 

Acaulospora 221 

acervulus 231, 387 

Achlya 86–91; aplanetic forms 93; 

asexual reproduction 87, 88; 

hyphae 80; relative sexuality 91; 

sex hormones 88–89, 90, 91; sexual 

reproduction 88–91 

Achlya ambisexualis 88, 89, 91 

Achlya bisexualis 88 

Achlya colorata 69, 87–88 

Achlya heterosexualis 88 

Achlya klebsiana 87 

Acrasiomycetes (acrasid cellular 

slime moulds) 40–41 

Acrasis rosea 41 

Acremonium 316, 339, 341 

Acremonium chrysogenum 303, 349 

Acremonium salmosynnematum 349 

actin cap 9 

actin filaments 9, 10, 51, 65–66, 158, 

258, 271, 646; in ascospore 

formation 323; in graviperception 

549; in penetration peg 381 

actin-myosin 46, 51, 72; see also 

cytoskeleton 

actin ring 259, 271, 301 

adaxial blob (drop) 493–494, 496 

adhesins 277 

adhesion pad 615 

adhesives 66, 205, 364, 378, 381, 395, 

438; in nematophagous fungi 683 

adhesorium 59 

adnate gills 523 

adnexed gills 523 

adult plant resistance; see host 

resistance 

aeciospore 613, Pl. 12 

aecium 612, 613, 622, Pl. 12; caeoma 

635; roestelioid aecium 632 

Aegerita 701 

Aegerita candida (teleom. Bulbillomyces 

farinosus) 506, 697, 699 

Aegeritina 701 

Aegeritina tortuosa (teleom. 

Subulicystidium longisporum) 697 

aequi-hymenial gills 522 

aero-aquatic fungi 506, 696–701; 

anamorph-teleomorph connections 

697; ecophysiology 698–701 

aethalium 50, Pl. 1 

aflatoxins 304, 305, Pl. 4 

Agaricus 532–536 

Agaricus arvensis 532 

Agaricus bisporus 15, 533; breeding 

536; cultivation 525, 532–534; 

life cycle 535; mating system 506, 

535; morphogenesis 534–535; var. 

burnettii 536; var. eurotetrasporus 536 

Agaricus bitorquis 532 

Agaricus brunnescens; see Agaricus 

bisporus 

Agaricus campestris 496, 521, 532; 

mating system 506 

Agaricus macrosporus 532 

Agaricus silvaticus 515, 532 

Agaricus tabularis 532 

Agaricus xanthodermus 532 

age of fungi; see evolution 

ageing 271 

agglutination 254, 265 

aggregation; see Dictyostelium 

discoideum 

Agrobacterium transformation 536 

agroclavine 354 

AIDS 279, 306–307, 661–662, 664 

air pollution monitoring, lichens 454; 

Rhytisma 442; Sporobolomyces roseus 

669 

Ajellomyces 290 

Ajellomyces capsulatus 289; 

see Histoplasma capsulatum 

Ajellomyces dermatitidis; 

see Blastomyces dermatitidis 

Alatospora acuminata 685, 687 

Albugo 122–125 

Albugo bliti 124 

Albugo candida 122, 123, 124–125, Pl. 2; 

haustorium 122; oospore 124 

Albugo tragopogonis 122, 125 

alcohol and fungi; see coprine 

alcoholic fermentation 254, 262 

alder, leaf blister 251 

Aleuria 417–419 

Aleuria aurantia 243, 419, Pl. 6; 

mycorrhiza 419 

aleuriaxanthin 419 

algal parasites 127 

alkaloids 354, 364, 539, 541; 

biosynthesis 354; commercial 

production 354; see Claviceps 

purpurea, Neotyphodium 

allergens; see asthma 

allyl amines 279, 280 

Allomyces 155–160; Brachy-Allomyces 160; 

Cystogenes 159; Eu-Allomyces 156; life 

cycle 158; polyploidy 159; 

sex hormones (parisin and sirenin) 

156 

Allomyces anomalus 155, 160 

Allomyces arbuscula 155, 157 

Allomyces macrogynus 155, 158 

Allomyces moniliformis 155, 159 

Allomyces neo-moniliformis 159 

Alternaria 469–471; plant diseases 472; 

sexual ancestors 469 

Alternaria alternata 470 

Alternaria brassicae 469, 471 

Alternaria brassicicola 469 

Alternaria solani 469 

Alternaria tenuissima 469 

alternate host 610 

alternation of generations 155, 

160, 229 

alveoli 427 

Amanita 540–541; poisoning 540 

Amanita caesarea 540, Pl. 9 

Amanita fulva 540 

Amanita muscaria 526, 540–541, Pl. 9 

Amanita pantherina 540 

Amanita phalloides 540–541; poisoning 

540 

Amanita rubescens 521, 540; trama 524 

Amanita vaginata 492, 540 

Amanita verna 540 

Amanita virosa 540 

a-amanitin 539, 540 

Amanitopsis 540 

Amauroascus 290 

Amauroderma rugosum 518

818 INDEX 

amerospore 23 

2-aminopyrimidine-type fungicides 

410 

amixis 176 

ammonia, as signal molecule 42 

amoebae 40, 41, 42, 49, 55; ‘social 

amoebae’ 44, 46 

amoeboid plasmodium 55, 60 

Ampelomyces quisqualis 412 

amphigynous fertilization 109 

amphithallism 506, 535, 538 

amphotericin B 260, 279, 291, 

306–307, 663 

amylase 282 

amyloid staining 28, 241; of ascus tip 

334; of ascus wall 414, 419; of 

basidiospore 566 

Amylostereum 571 

Anaeromyces 151 

anamorph 32, 38 

anamorph-teleomorph relationships 

32, 38, 299; see aero-aquatic fungi, 

aquatic hyphomycetes, Cordyceps, 

Epichloe, nematophagous fungi 

Anaptychia ciliaris 448 

anastomosis 3, 227, 377, 625 

anastomosis groups 594 

andromorph 32 

anaerobic fungi 79, 150 

angiocarpic hymenophore 520, 521, 

522–525 

Anguillospora crassa (teleom. Mollisia 

uda) 685, 690 

Anguillospora furtiva (teleom. Pezoloma) 

690 

Anguillospora longissima (teleom. 

Massarina) 689, 692 

anisokont zoospore 24, 55, 64 

annellide 233, 234, 368 

annulus 520, 533 

anther smut 652 

antheridiol 88, 89, 90–91 

antheridium in Oomycota 29, 77, 85, 

89, 101; monoclinous and diclinous 

85, 101; in Ascomycota 296, 307, 416 

anthracnose 388, 389 

antifreeze proteins 537 

antioxidants 482, 670 

Aphanomyces 94–95 

Aphanomyces astaci 79, 94 

Aphanomyces euteiches 79, 94 

Aphanomyces patersonii 94 

aphanoplasmodium 48 

apical apparatus; see ascus 

apical paraphysis; see paraphysis 

Apiocrea chrysosperma; see Sepedonium 

chrysospermum 

aplanetism 92 

Aplanopsis 93 

aplanospore 2, 15, 24, 64, 165–214, 

216–223, 224, 225 

apomixis 85, 160 

apophysis 46; of basidiospore 490 

apoptosis in fungi 534 

apothecium 245, 246, Pl. 6, Pl. 7; 

cleistohymenial 422; 

gymnohymenial 422; 

hemiangiocarpic 439 

apple, brown rot 306, 432, 433, 537; 

canker 343; cedar-apple rust 632; 

powdery mildew 390, 405; scab 478, 

479; spur canker 432 

appressorium, in Blumeria 396; 

in Botrytis 438; in Colletotrichum 388; 

in Magnaporthe 378–381; in 

Metarhizium 364; in Piptocephalis 202; 

in Pythium, Phytophthora 100; in 

Tapesia 440; in Uromyces 615, 616 

Aqualinderella fermentans 79 

aquatic fungi 577; see aero-aquatic 

fungi, aquatic hyphomycetes 

aquatic hyphomycetes 685, 686–696; 

adaptations to aquatic habitat 694; 

anamorph-teleomorph connections 

686; branched clamped conidia 

688–689; ecophysiology 694–696; 

foam 685, 694; invertebrate feeding 

695–696; sigmoid spores 686, 

689–691, 694; spore concentrations 

695; tetraradiate conidia 686, 

687–688, 693 

Arabidopsis thaliana 62, 118, 122 

arboriform hypha 518 

arbuscule (of VAM) 218, 220, 221 

archaeology 479, 610 

Archiascomycetes 250–260, Pl. 4 

Arcyria denudata 51, Pl. 1 

Armillaria 549–550; orchid mycorrhiza 

598; rhizomorphs 16, 17, 550 

Armillaria bulbosa 511, 550 

Armillaria cepistipes 550 

Armillaria lutea 550 

Armillaria luteobubalina 550 

Armillaria mellea 547, 549; 

dikaryotization (Buller 

phenomenon) 510; orchid 

mycorrhiza 550; unusual life cycle 

507 

Armillaria ostoyae 550 

Armillaria tabescens 550 

Arrhenosphaera 286 

Arthrobotrys 676; induction of 

nematode traps 682 

Arthrobotrys eudermata 677, 684; 

chlamydospores 684 

Arthrobotrys oligospora 676, 678 

Arthrobotrys robusta 678 

arthroconidium 281, 421, 422, 502, 

599, 600 

Arthroderma 293 

Articulospora tetracladia (teleom. 

Hymenoscyphus tetracladius) 685, 687, 

688 

Ascobolus 419–423; ascus development 

238; mating behaviour 420–421 

Ascobolus carbonarius 420 

Ascobolus crenulatus 420; and hyphal 

interference 540 

Ascobolus furfuraceus 420, 422, Pl. 6; 

apothecium development 422; 

hormonal control 421; mating 421 

Ascobolus immersus 420, 421; ascospore 

wall 237; gene recombination 423; 

mating 421; turgor pressure in 

ascus 242 

Ascobolus scatigenus, mating 420 

Ascobolus stictoideus 422 

ascocarps (ascomata) 21, 245, 246; 

see epigeous, hypogeous 

Ascochyta (teleom. Didymella) 464 

Ascochyta fabae 464 

Ascochyta pisi 464, 465 

Ascochyta rabiei 464 

Ascocoryne 444 

ascogenous hypha 236, 296, 307, 309, 

318, 418 

ascogonium 296, 307, 309, 318, 416 

ascohymenial development 315, 459 

ascolocular development 455, 459 

ascomycetes, classification 247–249; 

phylogeny 248; significance 246–247 

ascorbic acid; see vitamin C 

Ascosphaera 286–287 

Ascosphaera apis 288, 289 

Ascosphaerales 286–289 

ascospore 25–26; alignment in ascus 

323–324; appendages 238, 322; 

cleavage 237, 267, 422; discharge 

242–245, 318; eclosion 336, 338; 

multi-spored projectiles 318, 420; 

puffing 243, 415, 427, 442; tendrils 

245; wall layers 321, 333

INDEX 

819 

ascospore-delimiting membrane 

(ascus vesicle) 237, 238, 422 

ascospore wall 237–239 

ascosporogenous yeast 265 

ascostroma 246, 459 

ascus apical apparatus 241, 242, 335, 

349, 358, 375; annulus 241; 

bilabiate 241; operculate versus 

inoperculate 241 

ascus development 236, 237 

ascus vesicle; see ascospore-delimiting 

membrane 

ascus wall 239, 240, 241; bitunicate 

239, 429, 459; ectotunica 240, 459, 

460; endotunica 240, 459, 460; 

fissitunicate 239, 455, 459; 

prototunicate 241; rostrate 239, 

455; unitunicate 239 

Aseroe rubra 592, Pl. 11 

Ashbya; see Eremothecium 

aspergillomarasmine A 478 

aspergillosis 306 

Aspergillus 297–301; anamorphteleomorph 

relationships 308; 

cell-cycle 301; conidiophores 298, 

299; conidiogenesis 299–301; 

sclerotia 308; teleomorphs 299, 

308–310; uniseriate versus biseriate 

298 

Aspergillus carbonarius 305 

Aspergillus clavatus 306 

Aspergillus flavus 302, 306, 308; 

aflatoxins 305 

Aspergillus fumigatus 306, 308 

Aspergillus nidulans (teleom. Emericella 

nidulans), conidiogenesis 299, 301; 

conidiophore 301, 302; parasexual 

cycle 230; penicillin production 303 

Aspergillus niger 308; citric acid 

production 303; conidiogenesis 

299 

Aspergillus ochraceus 305 

Aspergillus oryzae 276, 302, 305, 308 

Aspergillus parasiticus 302, 308, Pl. 4 

Aspergillus sojae 302 

Aspergillus versicolor 304 

astaxanthin 665, 671 

Asterionella formosa, and Rhizophydium 

141 

Asteromella 481 

asthma 306, 471, 483, 560, 647, 669; 

‘mushroom worker’s lung’ 542 

Astraeus 586; boletoid clade 579 

Atricordyceps 349, 681 

Aureobasidium pullulans 231, 261, 

484–485, 486, 668 

Auricularia auricula-judae 208, 493, 504, 

601, 602, Pl. 11; basidiospore 

germination 601; basidium 489, 602; 

dolipore septum 499; life cycle 603 

Auricularia mesenterica 602 

Auricularia polytricha, cultivation 602 

Auriculariales 601–604; basidial 

septation 601; lunate microconidia 

601, 602 

Auriscalpium 572 

Auriscalpium vulgare 567, 572; dolipore 

septum 499 

autodigestion 537 

autoecious 613 

autophagocytosis 11, 13, 381 

autophagosome 273 

Auxarthron 290 

auxiliary zoospore 76, 83 

auxins (of host plants) Albugo 122; 

Plasmodiophora 60; Taphrina 253; 

Ustilago maydis 644 

avirulence gene products 484, 619 

avoidance response (fugitropism) 168 

axoneme 68 

azoles 279, 291 

azygospore 179, 181 

bacterial endosymbionts of fungi: 

Geosiphon pyriforme 221; Laccaria 553; 

Morchella 428; Rhizopus microsporus 

183 

Baermann funnel 681 

ballistospores 28; Ascomycota 

242–245; Basidiobolus 205; 

Basidiomycota 493, 495–496, 660; 

Entomophthora 216; Epicoccum 467; 

Erynia 213; Furia 219; 

Peronosclerospora 125 

banana, Panama wilt 347; postharvest 

anthracnose 388 

barberry and Puccinia graminis 

620–622; barberry eradication 622 

barley, covered smut 643; dwarf rust 

628; leaf-blotch 462; leaf-spot 478; 

loose smut 643; net-blotch 478; 

powdery mildew 398; stripe rust 

627; see mlo allele 

barrage phenomenon 325, 365, 428 

Basidiobolus microsporus 207 

Basidiobolus ranarum 203–208; 

germination patterns 204, 205–206; 

life cycle 208; pathogenicity 207; 

phylogeny 37, 166, 203; sexual 

reproduction 207, 209 

basidiocarps (basidiomata) 22, 

517–523; development 519–522, 

534–535, 545 

basidiomycete yeasts 658, 659, 

660–672; ecology 658–659; 

isolation 658; phylogeny 660, 661; 

versus ascomycete yeasts 659; 

see Heterobasidiomycetes, 

Urediniomycetes, 

Ustilaginomycetes 

Basidiomycota 487–513; asexual 

reproduction 501–506; 

classification 512; dikaryotization 

498; life cycle 492; mating systems 

506–510; mycelial cords 500; 

phylogeny 512; plasmogamy 498; 

relationship with Ascomycota 511; 

rhizomorphs 500; sclerotia 501; 

see basidium, basidiospore 

basidiospore 26, 27, 28; development 

490–492, 493; discharge 493–495; 

germination 496; numbers 495, 

497; see adaxial blob, Buller’s drop, 

hilar appendix, hilar appendix 

body, surface tension catapult 

basidium; development 488–490; 

morphology 487–488; nuclear 

events 490, 492; holobasidium 

versus phragmobasidium 488; 

probasidium versus metabasidium 

490; chiastobasidium versus 

stichobasidium 490; 

see epibasidium, furcate basidium, 

heterobasidium, phragmobasidium, 

tremelloid basidium 

bassianolide 363 

Batkoa 203 

Beaumont period 114 

Beauveria bassiana 361–362, 363; in 

biological control 363 

beauvericin 363 

bellows mechanism 580–581, 588, 639 

benomyl 410; resistance 410 

benzaldehyde 630 

benzimidazole fungicides 410 

benzothiadiazole 410, 412 

Bettsia 286 

Beverwijkella pulmonaria 697, 700, 

701 

bifactorial mating 507 

binding hypha 518 

biological clock 331

820 INDEX 

biological control 263; of fungi 340, 

342, 347, 377, 412–413, 433–434, 

485, 551, 569, 596, 668; of insects 

211, 363–364; of nematodes 684; of 

weeds 631 

bioremediation 531 

biotechnology; see bread-making, 

brewing, biological control, 

biotransformation, citric acid 

fermentation, enzyme production, 

food production, griseofulvin, 

penicillin, riboflavin production, 

saké, wine production 

biotransformation 167, 197 

biotrophy in mycoparasites 191, 201; 

in plant pathogens; see Blumeria 

graminis, Cladosporium fulvum, 

Exobasidiales, Peronosporales, 

Uredinales, ustilaginomycetous 

smuts 

bipolar; see heterothallism 

Bipolaris 471–472 

Bipolaris sorokiniana (teleom. 

Cochliobolus sativus) 472, 474 

birch, rust 635; sap and 

Xanthophyllomyces 665; witches’ 

broom 251, Pl. 4 

bird’s nest fungi; see Crucibulum cyathus 

Biscogniauxia mediterranea 333 

Biscogniauxia nummularia 333 

biseriate; see Aspergillus 

Bisporella citrina 444, Pl. 7 

bitunicate; see ascus wall 

biverticillate; see Penicillium 

conidiophores 

Bjerkandera adusta 519, 562 

black yeasts 486 

Blakeslea trispora 174, 194, 195 

Blakeslea unispora 195 

blastic conidiogenesis 231; 

see holoblastic, enteroblastic 

Blastocladiales 153–162; bipolar 

germination 155; life cycles 

155–160; zoospore 153–155 

Blastocladiella 160–162; Cystocladiella 

160; Eucladiella 160 

Blastocladiella emersonii 153, 154, 

161, 162 

Blastocladiella variabilis 160 

blastoconidium 435, 484, 503, 504 

Blastomyces dermatitidis 289, 290–292 

Blumeria graminis 390, 393, 394, 

395–399, 400, 401; appressorium 

396; attachment 395; chasmothecia 

400, 401; conidia 395, 399; formae 

speciales 395; gene-for-gene 

interactions 398; haustorium 393, 

394, 397–398, 399; infection process 

395, 396, 397; life cycle 399–401; 

primary germ tube 396; races 395, 

408; secondary germ tube 396; 

signalling 396 

‘boat-hook’ spines 82, 84 

boletoid clade 555–560, Pl. 9; 

gasteromycetes 579, 585–588; 

phylogeny 516–517, 555, 585 

Boletus 557–558; related to 

gasteromycetes 578 

Boletus appendiculatus 557 

Boletus badius 515, 557, Pl. 9 

Boletus chrysenteron 556, 557 

Boletus edulis 556, 557; cultivation 526, 

557; trama 524 

Boletus erythropus 557, Pl. 9 

Boletus luridus 557 

Boletus parasiticus 557 

Boletus rubinellus 489; basidiospore 

development 491–492, 493 

Boletus satanas 557 

boom-and-bust cycle 619 

Bordeaux mixture 112, 119, 253, 

410, 647 

bothrosome; see sagenogen 

Botryotinia fuckeliana 430, 434–435; 

see Botrytis cinerea 

Botryotinia porri 436 

Botryotrichum (teleom. Chaetomium) 332 

Botrytis cinerea (teleom. Botryotinia 

fuckeliana) 4, 7, 32, 121, 403, 

434–435; attachment 438; fungicide 

resistance 439; life cycle 437; 

macroconidia 434, 436; 

microconidia 435; pathogenicity 

mechanisms 436–439, 475; sclerotia 

19; septum 228 

Bovista 581 

bow-tie reaction 570, 571 

bramble rust 631 

brassicas, Albugo white blisters 122, 

125; blackleg 463; club-root 55–56, 

57; powdery mildew 402; see also 

oilseed rape 

bread-making 274 

breeding for resistance (in plants) 63, 

119, 138, 347, 368, 408–410, 440, 

625–627, 633–634, 642 

Bremia lactucae 120, 121, 122 

Brettanomyces 275 

brewing 274–275 

broad bean, anthracnose 387, Pl. 5; 

leaf- and pod-spot 464; net-blotch 

466; rust 631 

brown-rot (of wood) 529, 529–530, 

556, 559–560, 563–564 

bubble-trap propagules 696, 698 

bud scar 271, 283 

bulbil 490, 505 

Bulbillomyces farinosus (anam. Aegerita 

candida) 505, 506, 697 

bulbous hyphae 378, 381; see infection 

hyphae 

Bulgaria inquinans 445, Pl. 7 

Buller phenomenon 510, 570 

Buller’s drop 493–494, 495 

Bullera 659 

Bulleromyces (anam. Bullera) 659 

bunt 637; common bunt 647; dwarf 

bunt 649; Karnal bunt 649 

Byssochlamys 307–308 

Byssochlamys nivea 306, 307 

Ca 2þ channels, stretch-activated 9–10, 

66, 615 

Cadophora 439 

Caecomyces 151 

caeoma 635 

Caespitotheca forestalis 393 

calcineurin signalling 664 

calciseptine 646 

callose 397 

calmodulin 384, 385 

Calocera cornea 598, 601 

Calocera viscosa 600, 601, Pl. 11; 

basidiospore germination 600, 601; 

basidium 489 

Calostoma 585 

Calvatia 581 

Calvatia excipuliformis 582, Pl. 11 

Calvatia gigantea 581, 582 

cAMP (cyclic AMP) 41, 105, 384, 645; as 

hormone 42 

Candelabrum desmidiaceum 701 

Candida 276–280 

Candida albicans 226, 276–280, 291, 654; 

candidiasis 278–280; cryptic sexual 

phase 277; dimorphism 277; drug 

resistance 279–280;mating 277–278; 

switching 278; treatment 279–280 

Candida dubliniensis 276, 280 

Candida glabrata 276, 278, 280 

Candida inconspicua 276 

Candida krusei 276, 280

INDEX 

821 

Candida parapsilosis 227, 280 

Candida tropicalis 280 

Candida utilis; see Pichia jadinii 

candidiasis 278–280; treatment 

279–280 

canker (of plants) 333, 342, 343, 

376, 634; self-healing 376 

cantharelloid clade 574–575; 

phylogeny 516–517 

Cantharellus 574 

Cantharellus cibarius 574, Pl. 10; 

cultivation 526; post-meiotic 

mitosis 490 

Cantharellus cinnabarinus 574 

Cantharellus tubaeformis 574 

canthaxanthin 574 

capilliconidia 205, 206 

capillitium 51, 581 

Capronia 486 

captan 479, 651 

carbendazim 410 

carboxin 651 

b-carotene 170, 175, 195, 434, 665, 

Pl. 12 

carotenoids 143, 150, 156, 185, 253, 

414, 456, 574, 598, 605, 613 

caspofungin 279, 291 

Catenaria allomycis 153 

Catenaria anguillulae 153, 681 

cattle; see grazing animals 

Caulochytrium 127 

caulocystidium 525 

cdc2 51, 256 

cell cycle 51, 256–257, 270–272 

cellulase 339–340, 396, 530 

cellulose 528; in fungal cell walls 6, 

42, 67, 75, 127; as substrate 148, 

150, 529–530 

cell wall 5, 6; in Mucorales 167; in 

Saccharomyces cerevisiae 270 

cell wall, biosynthesis 6–8 

cell wall-degrading enzymes 375, 396, 

438, 596 

centrum 242, 318 

cephalodium (in lichens) 451 

cephalosporins 303–304, 350 

Cephalotrichum stemonitis 230, 368, 370 

Ceratiomyxa fruticulosa 46, 47, Pl. 1 

Ceratobasidiales 594–598; 

basidiocarps 595; basidium 595; 

see Rhizoctonia 

Ceratobasidium 594; see Rhizoctonia 

Ceratocystis 369–373; versus Ophiostoma 

364, 373 

Ceratocystis coerulescens 373 

Ceratocystis fagacearum 369, 373 

Ceratocystis fimbriata 369 

Ceratorhiza (teleom. Ceratobasidium) 594 

cerato-ulmin 366, 368 

Cercospora 481–482 

Cercospora beticola 481, 484 

Cercospora coffeicola 481 

Cercospora zea-maydis 481 

cercosporin 482, 485 

cereal rusts 627–629; origin 628 

cereals, downy mildews 126; ergot 

352; eyespot 439, 441; leaf blotch 

439; mosaic viruses 62; powdery 

mildew 393–399, 400, 401; sharp 

eyespot 596; take-all 385–386; see 

also individual cereals 

Chaenothecopsis 246 

Chaetocladium brefeldii 191, 192 

Chaetocladium jonesii 191 

Chaetomium 331–332; perithecial 

development 332 

Chaetomium brasiliense 332 

Chaetomium cochliodes 331 

Chaetomium elatum 331–332 

Chaetomium globosum 332 

Chaetomium piluliferum 332 

Chaetomium thermophile 331 

Chaetothyriales 486 

chalk brood disease; see honey bees 

chasmothecium 246, 392, 401, 

409; in oversummering 401; 

viability 405 

cheese production 303 

cheilocystidium 525 

chemotaxis 42, 100, 106 

chemotaxonomy 454 

chemotropism 201, 330, 586 

Chernobyl accident 454 

cherry, witches’ broom 251; silver-leaf 

571 

chestnut, blight 376 

chiastobasidium 490 

chickpea, blight 464 

chitin (in cell walls) 5, 6, 55, 67, 127, 

153, 165, 255, 538; bud scar 261; 

spiral growth 171 

chitosan (in cell walls) 6, 165 

chitosomes 6, 7, 168 

chlamydospore 29, 30, 81, 105, 218, 

345, 347, 484, 486, 504, 505, 545, 

667; see teliospore 

3-chloroanisylalcohol 530, 531, 532 

Chlorociboria 444 

Chlorociboria aeruginascens Pl. 7 

chloromethane 532 

chlorothalonil 631 

Choanephora cucurbitarum 173, 179, 

193, 194, 202 

Chondrostereum purpureum 571, Pl. 10 

Chromista 67; see Straminipila 

Chrysonilia 327, 329 

Chrysosporium 290, 293, 294 

Chytridiales 134–145 

Chytridiomycota 71, 127–164, Pl. 3; 

classification 134; flagellar 

apparatus 129, 130; germination 

(monopolar versus bipolar) 131; 

inoperculate and operculate species 

129; life cycles 131; microbody-lipid 

complex 130, 131; sexual 

reproduction 132–133; thallus 128; 

zoospore 129–131 

Chytriomyces hyalinus 132 

cinerean 438 

circadian rhythm 331, 590 

cirrhus 315, 332, 465 

citric acid fermentation 303 

citrinin 305 

citrus fruit rot Pl. 4; see Penicillium 

italicum, P. digitatum 

Cladina 458 

Cladina rangiferina 458, Pl. 8 

Cladina stellaris 458 

Cladochytrium 142–144 

Cladochytrium replicatum 142, 143, 144 

Cladonia 448, 457–458 

Cladonia convoluta 452 

Cladonia cristatella 450 

Cladonia floerkiana 457, Pl. 8 

Cladonia pyxidata 450, 457 

Cladophialophora 486 

Cladosporium 481–484; Mycosphaerella 

teleomorphs 482; spores 22–23 

Cladosporium cladosporioides 483 

Cladosporium echinulatum 482 

Cladosporium fulvum 483–484, 619; 

biotrophy 483 

Cladosporium herbarum 482–483, 485 

Cladosporium humile 482 

Cladosporium macrocarpum 485 

clamp connection 499, 500–501, 569; 

versus crozier 512 

Clastoderma 51 

Clathrosphaerina zalewskii (teleom. 

Hyaloscypha) 697, 699–700 

Clathrus archeri 591–592 

Clathrus ruber 591–592, Pl. 11

822 INDEX 

Clavaria 575–576; ericoid mycorrhiza 

576 

Clavaria argillacea 576 

Clavaria vermicularis 576 

Clavariadelphus pistillaris 515, 576 

Clavariopsis aquatica (teleom. 

Massarina) 688 

Clavatospora longibrachiata 685 

Clavatospora stellata 685 

Claviceps 349 

Claviceps africana 349, 355 

Claviceps fusiformis 349, 355 

Claviceps microcephala 350 

Claviceps paspali 349, 355 

Claviceps phalaridis 355 

Claviceps purpurea 349–351, 352, 

353–355; alkaloids 353, 354, 355; 

ascospore discharge 241; control 

355; ergotism 352–353; life cycle 

349–350, 351, 352; sclerotia 19, 20, 

350, 352 

Claviceps purpurea var. spartinae 355, 

Pl. 5 

Claviceps sorghi 349 

Clavicipitales 316, 348–364; alkaloids 

349 

Clavicorona pyxidata 489 

Clavulina 575–576 

Clavulina cristata 574, 575 

Clavulina rugosa 575 

cleavage of cytoplasm 98, 106, 

158, 172 

cleistohymenial; see apothecium 

cleistothecium 245, 246, 285, 309, 

313, 314 

cleptobiosis 451, 456 

Clitocybe 552 

Clitocybe clavipes 521 

Clitocybe geotropa 552 

Clitocybe nebularis 552, 553 

Clitocybe odora 552 

club root 55–56, 57; see Plasmodiophora 

brassicae 

CO 2 fixation 162 

Coccidioides immitis 290–293 

Coccidioides posadasii 293 

Coccomyxa 452, 456 

Cochliobolus 460, 471–477; Bipolaris 

anamorphs 475; mating type 

idiomorphs 477; pathology 475–477 

Cochliobolus carbonum 477; HC-toxin 

476 

Cochliobolus cymbopogonis, ascus 

discharge 243, 244 

Cochliobolus heterostrophus (anam. 

Bipolaris maydis) 477; T-toxin 476 

Cochliobolus sativus (anam. Bipolaris 

sorokiniana) 475–476; 

prehelminthosporol 476 

Cochliobolus victoriae 476–477, 619; 

origin 477; victorin C 476 

cocoa, pod rot 103; frosty pod rot 551; 

witches’ broom 547, 550 

Coelomomyces 127, 153 

coelomycetes 231 

coenocytic hypha 2, 75, 167 

coffee, berry disease 388; eyespot 481; 

leaf rust 632–634 

collagen 654 

Colletotrichum 231, 387, 389; infection 

strategies 389 

Colletotrichum capsici 388 

Colletotrichum coccodes 388–389 

Colletotrichum coffeanum 388 

Colletotrichum destructivum 388 

Colletotrichum gloeosporioides 387, 389 

Colletotrichum gossypii 388 

Colletotrichum graminicola 387, 388 

Colletotrichum lindemuthianum 388, 

Pl. 5 

Colletotrichum musae 388–389 

Collybia 546, 552 

Collybia butyracea post-meiotic mitosis 

490 

Collybia tuberosa 501 

columella; in puffballs 584; in 

Zygomycota 166, 167, 182, 184–185, 

192, 208 

Comatricha 51 

co-metabolism 531 

compound appressorium 595 

Conidiobolus 203, 208–211; eversion 

mechanism in conidium discharge 

208 

Conidiobolus coronatus 209, 210, 211; 

insecticidal toxin 211; loriconidia 

211; villose conidia 210 

conidiogenesis 31, 231–235, 299, 

300, 301; blastic versus thallic 232; 

hormonal control 301; see holoblastic, 

enteroblastic, thallic 

conidiogenone 301 

conidioma 230 

conidiophore 230, 298, 310 

conidium (conidiospore) 30–32; 

unitunicate versus bitunicate 

(Entomophthorales) 203, 215; 

see arthroconidium, 

blastoconidium, oidium, 

phialoconidium, spermatium 

conifers, butt rot 567; root rot 573, 

Pl. 2 

Coniophora 558 

Coniophora puteana 570 

Coniothyrium minitans 433 

conjugate nuclear division 499 

connective 300, 327 

convergent evolution 673, 686, 

693, 701 

copper, as fungicide 479, 633, 647, 

651; see Bordeaux mixture 

coprine 538, 539 

Coprinellus 537 

Coprinopsis 537 

Coprinus 536–540; life cycle 492; 

mating behaviour 538; sclerotium 

537; stipe elongation 538 

Coprinus atramentarius 522, 537–538; 

and alcohol 538 

Coprinus cinereus 22, 489, 498, 501, 521, 

533, 538; basidiospore development 

491, 492, 493, 494; dikaryotization 

(Buller phenomenon) 510; 

gravitropism 549; mating type 

alleles 508, 509; oidia 502, 503 

Coprinus comatus 533, 537; mating 

system 506; phylogeny 536; related 

to gasteromycetes 578 

Coprinus congregatus 499 

Coprinus curtus 537 

Coprinus domesticus 537 

Coprinus ephemerus f. bisporus, mating 

system 506 

Coprinus heptemerus, hyphal 

interference 540 

Coprinus micaceus 537 

Coprinus plicatilis 537 

Coprinus psychromorbidus 537 

Coprinus sterquilinus, mating system 

506; phylogeny 536; sclerotia 

537–538 

Coprobia granulata 229 

coprophilous fungi 238; Ascobolus 419; 

Basidiobolus 203–208; Coprinus 537; 

Mucor 181; Pilaira 189–190; Pilobolus 

185–189 

Cordyceps 360–362; perithecial stroma 

362; sclerotium 360 

Cordyceps bassiana (anam. Beauveria 

bassiana) 362 

Cordyceps brittlebankisoides (anam. 

Metarhizium anisopliae) 363

INDEX 

823 

Cordyceps capitata 362 

Cordyceps militaris 20, 361, Pl. 5 

Cordyceps ophioglossoides 314, 362, Pl. 4; 

host-jumping 362 

Cordyceps sinensis 361, 362 

Cordyceps subsessilis (anam. 

Tolypocladium inflatum) 349, 364 

coremium 230, 310, 311 

Coriolus; see Trametes 

corn; see maize 

correlated rust species 614 

cortina 520, 553, 555 

Cortinarius 555; related to 


Cortinarius orellanus 555 

Cortinarius purpureus 553 

Costantinella cristata 428 

cotton, anthracnose 388 

Craterellus cornucopioides 574 

crayfish plague (Aphanomyces astaci) 

94 

Cribraria 51 

Crinipellis 546 

Crinipellis perniciosa 547, 550 

Crinipellis roreri 551 

Cronartium 634–635; teliospore 634 

Cronartium flaccidum 634 

Cronartium quercuum 634 

Cronartium ribicola 634; canker 634 

crook root; see watercress 

crozier 236, 418; versus clamp 

connection 512 

Crucibulum 582, 585 

Crucibulum vulgare, mating-type 

factors 509 

cruciform mitosis; see Plasmodiophora 

brassicae 

crustose lichens 447, Pl. 8 

Cryphonectria parasitica 375–377; 

basidium 662; biological control 

377; hypovirulence 376–377; 

Hypovirus 376–377; mating types 

662; pheromones 377; vegetative 

incompatibility 377; virus 

transmission 377 

Cryptococcus 661 

Cryptococcus neoformans 608, 

661–665; infection biology 663–664; 

life cycle 662, 663; mucilage 

capsule 661, 664; natural habitat 

662; switching of phenotypes 664; 

var. gattii 661; var. grubii 661; var. 

neoformans 661; virulence factors 

664–665 

Ctenomyces serratus 293, 294 

cucumber necrosis virus (CNV) 148 

cultivation of mushrooms 525, 

602, 607; mycorrhizal fungi 527, 

558, 566; see Agaricus bisporus, 

Auricularia polytricha, Lentinula 

edodes, Tremella fuciformis 

Cunninghamella 196 

Cunninghamella bertholettiae 196 

Cunninghamella echinulata 196 

Cunninghamella elegans 196 

Curvularia 471–472 

Curvularia cymbopogonis 472, 475 

Curvularia lunata (teleom. Cochliobolus 

lunatus) 475 

cutinase 396, 438, 615 

Cyathus 582–585; splash cup 582 

Cyathus olla 582 

Cyathus stercoreus 582, 584 

Cyathus striatus 582; mating type 

factors 509 

cyazofamid 113 

cycloheximide 373, 634 

cyclosporin A 350, 364, 664 

Cylindrocarpon 342, 345, 348 

Cylindrocarpon destructans (teleom. 

Nectria radicicola) 348 

Cylindrocarpon heteronema (teleom. 

Nectria galligena) 348 

Cylindrosporium concentricum 

(teleom. Pyrenopeziza brassicae) 439 

cystesium 525 

cystidiole 525 

cystidium 522, 524, 525 

cytochalasins 364 

cytokinins (of host plants), in 

Plasmodiophora 60; in Taphrina 253 

cytoskeleton 8, 9–10, 81, 258, 646; in 

spore cleavage 87, 158; see actin, 

microtubules 

Cyttaria 445 

Cyttaria darwinii Pl. 7 

Dacrymycetales 598–601; epibasidia 

599–600; life cycle 598 

Dacrymyces stillatus 493, 598–599, 600; 

basidiospore germination 599, 600 

Dacrymyces unisporus 598 

Dactylelina 675–676; induction of 


Dactylelina haptotyla 679 

Daldinia 334 

Daldinia concentrica 236, 333–335, Pl. 5 

Daldinia fissa 334 

Daldinia loculata 334 

damping-off 96, 97, 102, 595, Pl. 2 

dandruff and Malassezia 672 

Dasyscyphus 25 

Dasyscyphus virgineus Pl. 7 

trans-2-decenoic acid, nematicidal 

properties 683 

decurrent gills 523 

de-dikaryotization 502, 630, 653 

de-diversification 661 

defence mechanisms; see host defence 

demethylation inhibitors (DMI) 651; 

see imidazoles, triazole 

demicyclic 613 

Dendrospora erecta 688, 690 

Dendrosporomyces prolifer 689 

Dendrosporomyces splendens 689 

dense-body vesicles 87, 107; see 

fingerprint vacuoles 

depletion zone 222 

Dermateaceae 439–440 

dermatitis and Malassezia 672 

dermatophytes 293 

desert truffle 427 

destruxins 364 

dextrinoid staining (with iodine) 241 

2,4-diacetylphloroglucinol 386 

diacylglycerol (DAG) 384 

diallyl disulphide 434, 435 

Diaporthales 316, 373–377 

Diaporthe (anam. Phomopsis) 373–375, 

605; ecology 375 

Diaporthe ambigua 375 

Diaporthe helianthi 375 

Diaporthe phaseolorum 373–375; 

pycnidium 374; sexual 

reproduction 374 

Diaporthe toxica 375 

diazonium blue B stain 659 

Dichotomocladium 191 

diclinous antheridium 85 

Dictydium 51 

Dictyophora; see Phallus 

dictyospore 23, 469, 470 

Dictyosteliomycetes (dicytostelid 

cellular slime moulds) 41–45 

Dictyostelium discoideum 42–45; 

aggregation 42, 44–45; cheater 

strains 44; life cycle 43 

Dictyuchus sterile 91, 93–94 

Didymella (anam. Ascochyta) 464 

didymospore 23 

diffluent sporangium 173 

diffuse extension growth 538

824 INDEX 

Digitatospora marina 693 

dikaryotization 498, 613; legitimate 

and illegitimate 510; see Buller 

phenomenon 

dimethyl disulphide 436, 591 

dimethyl sulphide 424 

dimitic basidiocarp construction 519 

dimorphism, sexual 436; yeast-hypha 

3, 181, 226; in Candida albicans 227, 

277; in Onygenaceae 291; in 

phialidic conidiogenesis 301, 302; 

in smut fungi 638 

Dioszegia 659 

diplanetism 81, 85 

diploid Eumycota 277, 666–667 

Dipodascus 282 

Dirina massiliensis f. sorediata 447, 

454 

Discosphaerina fulvida (anam. 

Aureobasidium pullulans) 484 

Discula destructiva 373 

disease forecasting, Hemileia vastatrix 

633; Phytophthora infestans 113; 

Uncinula necator 403; Venturia 

inaequalis 479 

dispersal; see insects; mites 

dissepiments 519 

distoseptate 472, 473–474, 476, 478 

dithiocarbamates 112, 119, 253, 410 

dogwood, anthracnose 373 

dolipore septum 497, 498, 499, 594, 

597, 606; breakdown for nuclear 

passage 497, 600 

Doratomyces; see Cephalotrichum 

dormant kinetosome; 

see kinetosome 

Dothideales 480–486; lichens 455 

double discharge of asci 405 

downy mildews Pl. 2; 

see Peronosporales 

Drechmeria coniospora 349, 681, 682; 

adhesion to nematodes 683; 

infection process 684 

Drechslera (teleom. Pyrenophora) 471, 

477–478 

Drechslera tritici-repentis 476 

Drechslerella 677, 680; induction of 

nematode traps 683; ring 

constriction 678 

Drechslerella brochopaga 679 

Drechslerella dactyloides 679 

drugs (against human pathogens) 279, 

280; see allyl amines, 

amphotericin B, azoles, 

caspofunginterbinafine, 

5’-fluorocytosinegriseofulvin, 

griseofulvin, terbinafine, triazole 

dry rot 558–560; control 560 

Duddingtonia flagrans; see Arthrobotrys 

eudermata 

Dumontinia; see Sclerotinia tuberosa 

Dutch elm disease 366–368, Pl. 5; 

control 368 

earth stars 588 

Echinobotryum 368, 370 

echinocandins 260, 280 

Echinosteliales (Myxomycota) 51 

Echinostelium 51 

eclosion; see ascospore 

ectomycorrhiza (sheathing 

mycorrhiza) 21, 314, 424, 526, 527, 

552, 573, 585–586 

ectotunica; see ascus wall 

efrapeptins 364 

eelgrass (Zostera) wasting 72 

Elaphomyces 313–314, Pl. 4 

Elaphomyces granulatus 313 

Elaphomyces muricatus 313 

elater 51, 52 

electric field (around hypha) 13, 14 

elm, Dutch elm disease 366–368 

Emericella (anam. Aspergillus) nidulans 

229, 310; Woronin bodies 228; 

see Aspergillus nidulans 

encystment (of zoospores) 68, 76–77, 

83, 84, 87, 100, 106, 131 

endocytosis 11, 13, 272 

Endogone 221 

Endogone flammicorona 221 

Endogone lactiflua Pl. 3 

endophytic fungi 333–334, 429, 484; 

of grasses see Neotyphodium; related 

to pathogens 347, 359, 375, 389, 

441, 462; xylotropic endophyte 336 

endoplasmic reticulum (ER) 11 

endospore, endosporium (of spore 

walls) 26, 417 

endospores 205, 206 

endotunica; see ascus wall 

enteroblastic conidiogenesis 31, 232, 

299, 300, 659 

entomopathogenic fungi; see insect 

pathogens 

Entomophaga 203 

Entomophthora 203 

Entomophthora muscae 215–217, Pl. 3; 

infection 216, 218; penetration 216 

Entomophthora sepulchralis 217, 218 

Entomophthorales 202–217 

enzyme production 303, 339–340, 

562 

epibasidium 593, 595 

Epichloe 355–357; ascospore 

germination 356, 358; infection of 

grasses 356; spermatization by 

insects 356 

Epichloe baconii 355, 357 

Epichloe clarkii 356 

Epichloe festucae 356, 359 

Epichloe typhina 355, 358, Pl. 5 

Epicoccum 30 

Epicoccum nigrum 466; active conidial 

discharge 466 

Epidermophyton 293 

epigeous fruit-bodies 414 

epiphragm 583, 584 

epispore, episporium (of spore walls) 

26, 417 

Eremascus 286–287 

Eremascus albus 287 

Eremascus fertilis 287 

Eremothecium 262, 284 

Eremothecium ashbyi 284 

Eremothecium coryli 284, 304 

Eremothecium gossypii 284 

ergometrine 353, 354 

ergosterol 279; biosynthesis 279, 412 

ergot 350, 352 

ergotamine 353, 354 

ergotism 352–353 

ergovaline 360 

ericoid mycorrhiza 444, 576 

Erynia 203, 211–215; resting bodies 

211 

Erynia conica 213–215; conidial types 

213, 214 

Erynia neoaphidis 211, 212, 213; 

asexual reproduction 213; infection 

of aphids 212–213; penetration 212; 

protoplasts 212 

Erysiphales 390–413; appendages 391, 

392–393; chasmothecium 392; 

conidia 390; conidial surface and 

taxonomy 394, 395; control 

408–413; phylogeny and evolution 

392–393 

Erysiphe 401, 402, 403–404 

Erysiphe betae 402 

Erysiphe cruciferarum 401 

Erysiphe heraclei 402 

Erysiphe pisi 398, 402

INDEX 

825 

Erysiphe polygoni 402 

Erysiphe trifolii 402; resistance 

breeding 408 

ethanol; see alcoholic fermentation 

ethirimol 410 

ethnomycology 541 

ethylene 389 

euagarics clade 516–517, 532–555, 

Pl. 9; gasteromycetes 579, 581–585 

Eumycota 38 

Eupenicillium 311–313 

Eupenicillium crustosum 313 

Eurotiales 297–314; anamorphteleomorph 

connections 299 

Eurotium repens 230, 308, 309 

euseptate 473 

evolution of fungi 35, 133, 165, 221, 

246, 511; co-evolution with host 

plants 116, 393 

exhabitant (of lichens) 446 

Exidia glandulosa 603–604; basidium 

489, 604 

Exobasidium 655–657, Pl. 12; basidium 

656, 657; haustorium 656, 657 

Exobasidium japonicum 656 

Exobasidium vaccinii 656, Pl. 12 

Exobasidium vexans 656 

Exobasidiales 655–657; biotrophy 655, 

656; exocytosis; see secretion 

Exophiala 486 

extrahaustorial matrix 103, 398, 617 

extrahaustorial membrane 617 

eyespot (of zoospore) 72 

fairy rings 13, 532, 546, 547, 552 

famoxadone 113 

fatty acids, in biological control 412 

fenpropimorph 411 

Fenton reaction 530 

fibrosin bodies 404, 405 

Fibulomyces 689, 690 

Filobasidiella neoformans 661; see 

Cryptococcus neoformans 

fimbriae 176, 202, 275, 277, 653, 654; 

fimbrial RNA 654 

fingerprint vacuoles, see dense-body 

vesicles 76, 107 

fish farming 665 

fish pathogens, Saprolegnia 81 

fission yeast 254 

fissitunicate; see ascus wall 

flagellar apparatus 129–130, 153 

Flagellospora 342 

Flagellospora curvula 689, 692 

Flagellospora penicillioides (teleom. 

Nectria) 689, 692 

flagellum 23, 69; retraction 155; 

straminipilous (tinsel) flagellum 24, 

67–70; whiplash flagellum 68, 69, 

153 

Flammulina 546 

Flammulina velutipes 169, 548–549, 

Pl. 9; cultivation 525, 548; 

gravitropism 548, 549; oidium 502, 

503, 548; trama 524 

flexuous hypha 622 

flocculation 275 

floral mimicry 614 

fluconazole 279, 664 

5’-fluorocytosine 279, 280, 663 

fly agaric 541; see Amanita muscaria 

foliose lichens 447, Pl. 8 

Fomes fomentarius 560 

Fomitopsis pinicola 529 

food production 167, 181, 302–303; 

see cultivation of mushrooms 

food spoilage 298; canned food 307 

foot cell, in Aspergillus 308, 309; in 

Blumeria 394 

form-genus 23 

formae speciales 120, 345, 346, 395, 621 

fosetyl-Al 113, 119 

fossil fungi 35, 133, 203, 221, 246, 363, 

512, 526, 579; lichens 454 

free gills 523 

French bean rust 631 

fruity smells 371, 373 

fruticose lichens 447, Pl. 8 

fucosterol 90 

Fuligo septica 51, Pl. 1 

fumonisin 348 

fungi, key features 1–2 

fungicide resistance 279–280, 410, 

439; see ABC transporters 

fungicides, against Phytophthora 112, 

113; against powdery mildews 410, 

411–412; see also allyl amines; 

2-aminopyrimidine, azoles, 

benzimidazole, Bordeaux mixture, 

captan, carboxin, copper, 

dithiocarbamate, imidazoles, 

maneb, myclobutanil, morpholine, 

phenylamide, phosphonate, 

quinoxyfen, strobilurin, 

sulphur dust and lime, triazole 

fungistasis 534 

funiculus 581, 584 

furcate basidium 598, 599–600 

Furia 203 

Furia americana 217, 219, Pl. 3 

Fusarium 30, 342–343, 344, 345–348; 

biological control 347; endophytes 

347; macroconidium 343, 344, 347; 

microconidium 343, 344; 

mycotoxins 348; plant diseases 346; 

wilts 345, 346 

Fusarium culmorum 347 

Fusarium heterosporum Pl. 5 

Fusarium moniliforme (teleom. 

Gibberella fujikuroi) 339 

Fusarium oxysporum 345–347 

Fusarium venenatum 339 

fusion biotroph 191 

fusion septum 176 

Gabarnaudia (teleom. Sphaeronaemella) 

372 

Gaeumannomyces graminis 385, 386, 595 

Galactomyces 281–282 

Galactomyces candidus 4, 13, 30, 281 

Galactomyces geotrichum; see G. candidus 

gamma-particles 154 

gametangio-gametangiogamy 132, 

133, 229 

gametangio-gametogamy 132, 229 

gametangium 177; hypogynous versus 

epigynous 156, 157, 159, 163 

gametogamy: isogamy, anisogamy, 

oogamy 132 

Gamsylella 675, 676; induction of 


Ganoderma 564 

Ganoderma adspersum 565 

Ganoderma applanatum 560, 561, 

564, 565 

Ganoderma lucidum 561, 564 

gasterocarp 577 

gasteromycetation 578 

gasteromycetes 575, 577–592, Pl. 11; 

boletoid clade 586–589; dispersal 

580; euagarics clade 580, 581–585; 

evolution 578–579; gomphoidphalloid 

clade 589–592; life cycle 

577; phylogeny 579, 580; 

propagules 580 

Gastroboletus 578 

Gastrosuillus 578 

Gastrosuillus laricinus 578 

Geastrum, gomphoid-phalloid clade 

579 

Geastrum triplex 588, 589 

gemma 30, 590

826 INDEX 

gene conversion 319, 423 

gene-for-gene hypothesis 114, 118, 383, 

398, 408, 477, 484, 619, 642, 649 

generative hypha 518 

genet 558, 586 

Geniculosporium 333, 337, 424 

Genistellospora homothallica 225 

Geoglossum 443 

Geolegnia 93 

Geosiphon pyriforme 221 

Geotrichum candidum (teleom. 

Galactomyces candidus) 235 

germination, auto-inhibitors 378, 

387, 614 

germination patterns, variability 

208, 210, 214, 496; in 

Heterobasidiomycetes 600, 602, 608 

germ pore (of spores) 26, 27, 239, 

614, 615 

germ slit (of spores) 239, 332–333, 479 

germ sporangium 178 

Gibberella-Fusarium complex 345 

Gibberella fujikuroi 339 

Gibberella zeae, turgor pressure in 

ascus 242 

gibberellins 339 

Gigaspora decipiens 218 

Gilbertella persicaria 172, 177, 179 

gills; see lamellae 

girdling 342, 376, 634 

gleba 424, 425, 577, 581, 588, 591 

Gliocladium 340, 341 

gliotoxin 339 

gloeocystidium 566, 572 

gloeoplerous hypha 518, 568 

Gloeotulasnella cystidiophora 595 

Glomales 29, 37, 217–222 

Glomerella 387–388 

Glomerella cingulata (anam. 

Colletotrichum gloeosporioides) 387 

Glomerellaceae 316, 386, 389 

Glomeromycota 221 

Glomus mosseae 218, 220, 221 

glucans, in cell walls 5, 6,75 

glucan matrix 15, 438 

glycerol, in turgor generation 381 

glycogen (storage reserve) 28, 76, 

381, 392 

Golgi apparatus 11, 66–67, 71, 75, 

165, 272 

Golovinomyces 403 

Golovinomyces cichoracearum 403; 

resistance breeding 408 

Golovinomyces cucurbitacearum 404 

Golovinomyces orontii 403 

Gomphidius 558 

gomphoid-phalloid clade 575–576; 

phylogeny 516–517; gasteromycetes 

579, 588–592 

Gonapodya 127, 162 

Gonapodya prolifera 162 

gooseberry, powdery mildew 390, 404 

grape-vine, bunch rot (grey mould) 

436; dead-arm 375; downy mildew 

119; powdery mildew 390 

Graphium 366, 368, 372 

Graphium penicillioides 372 

Graphium ulmi 366, 367 

grasses, choke disease 355; crown rust 

628; endophytes 357–360; powdery 

mildew 393–401 

gravitropism 169, 522, 548, 549 

grazing animals, fescue toxicosis 358; 

lupinosis 375; mycoses 295; 

ryegrass staggers 359 

‘green bridge’ 401, 408, 627 

green fluorescent protein (GFP) 263 

greenhouse gases 532 

grevillins 557, 558 

grey mould 434, 436 

griseofulvin 293, 304 

gut-stage cells of Basidiobolus 206 

Gymnoascus reessii 295, 296 

gymnocarpic hymenophore 520, 521 

gymnohymenial; see apothecium 

Gymnopus 546 

Gymnosporangium 631–632 

Gymnosporangium clavariiforme 632 

Gymnosporangium cornutum 632 

Gymnosporangium fuscum 613, 629, 

631–632, Pl. 12 

Gymnosporangium juniperi-virginianae 

632 

gymnothecium 245, 246, 285, 289, 

293, 294, 297 

Gyrodon 579 

Gyromitra esculenta 415 

gyromitrin 415 

H þ ATPases 12, 14, 221, 398, 617, 

618 

hallucinogenic mushrooms 541, 546; 

see ergotism 

halo; see host defence mechanisms 

hamathecium 241 

hapteron 584 

Haptoglossa 54, 63, 64–66, 681; gun cell 

64, 65, 66; taxonomy 54 

haptor 205 

Harpella melusinae 223, 224, 225; 

asexual reproduction 223–225; 

sexual reproduction 225 

Harpellales 223; phylogeny 166, 225 

Harpochytrium 162 

Harposporium anguillulae 349, 681, 682 

Hartig net 21, 526, 527, 586 

hart’s truffle 314 

haustorial branches 605, 606 

haustorial mother cell 615 

haustorium 103, 105, 118, 381, 399, 

615–616, 617–618; intraparietal 

452; see Albugo candida, Blumeria 

graminis, lichens, Peronospora, 

Phytophthora infestans, Piptocephalis, 

Uredinales 

hazel, powdery mildew 406 

HC-toxin 476, 477 

heavy metal accumulation; mercury 

536 

Helicodendron 697; ecophysiology 

699–701 

Helicodendron conglomeratum 698, 701 

Helicodendron fractum 701 

Helicodendron fuscosporum 701 

Helicodendron giganteum 699 

Helicodendron hyalinum 701 

Helicodendron praetermissum 701 

Helicodendron triglitziense 698, 701 

Helicodendron tubulosum 701 

Helicoon 697 

Helicoon richonis 697, 698 

helicospore 23 

Heliscus 342 

Heliscus lugdunensis (teleom. Nectria 

lugdunensis) 685, 687 

Helminthosporium 30–31, 471 

Helminthosporium velutinum 472, 473 

Helotiales (inoperculate 

discomycetes) 429–445, Pl. 7; 

classification 429, 430; lichens 

455 

Helvella 423; ectomycorrhiza 423 

Helvella crispa 423, Pl. 6 

Helvella lacunosa 423 

hemiangiocarpic 545; see apothecium, 

basidiocarp development 

Hemiascomycetes 261–284; versus 

Archiascomycetes 261–262; 

importance 262; isolation 262; 

occurrence 262 

hemibiotrophy 388, 475, 550 

hemicellulase 530

INDEX 

827 

hemicellulose 528 

Hemileia vastatrix 632–634; longdistance 

spread 633 

Hemitrichia serpula 51 

het genes 325–326, 330 

Heterobasidiomycetes 593–608, Pl. 11; 

parenthesome 499, 593; taxonomy 

593, 594 

heterobasidiomycete yeasts 659, 

660–666 

Heterobasidion abietinum 568 

Heterobasidion annosum 519, 567; 

blastoconidium (Spiniger) 504, 568; 

control 569 

Heterobasidion parviporum 568 

heterobasidium 593; 

see phragmobasidium 

heteroecious 613 

heterogenic incompatibility; 

see vegetative incompatibility 

heterokaryosis 351, 359; restricted 

versus unrestricted 330 

heterokont zoospore 24, 71 

heterothallism 174, 330, 506–507; 

bipolar 506; modified tetrapolar 

605; physiological 435; tetrapolar 

507 

1,16-hexadecanediol 384 

hilar appendix (of basidiospore) 27, 

490, 491, 492 

hilar appendix body 491–492 

hilum (of basidiospore) 27, 490 

Hirsutella 360 

Hirsutella rhossiliensis, as nematode 

endoparasite 685 

Hirsutella sinensis (teleom. Cordyceps 

sinensis) 362 

Histoplasma capsulatum 289, 290–292, 

307 

Hohenbuehelia 542; nematode-trapping 

679, 681 

holdfast 223, 224 

Holliday model 319, 643 

holobasidium 488 

holoblastic conidiogenesis 31, 232 

holocoenocytic 569 

holomorph 32 

holothallic conidiogenesis 235 

homing reaction (in basidiomycete 

fertilization) 502, 503 

homing sequence (in zoospores) 100 

Homobasidiomycetes 514–564, 

565–576, Pl. 9, Pl. 10, Pl. 11; eightclade 

system 514, 517; 

hymenophore arrangement 514, 

515; phylogeny 516 

homogenic incompatibility 325 

homothallism 319–320, 330, 506; 

primary 506; secondary 

(¼ pseudohomothallism) 179, 

506–507, 535; unclassified 506 

honey bees, chalk brood disease 288 

honeydew 349 

hook cell; see crozier 

hops, powdery mildew 404 

horizontal gene transfer 305 

horizontal resistance; see host 

resistance 

horizontal transmission of inoculum 

357 

Hormonema dematioides 227 

hormones; see antheridiol, cAMP, 

conidiogenone, oogoniol, parisin, 

sirenin, trisporic acid; see also plant 

growth hormones, sex hormones 

host defence mechanisms 397; halo 

397; papilla 397, 408; 

see hypersensitive response, 

oxidative burst, PR proteins 

host differentials 625, 628, 642 

host-jumping 362 

host-pathogen recognition; 

see gene-for-gene hypothesis 

host resistance; adult plant resistance 

410, 620; field (horizontal, partial, 

minor gene) resistance 115, 408, 

619; major gene (vertical) resistance 

114, 408, 619, 626 

hot water treatment (of seeds) 651 

Hülle cells 308, 310 

human pathogens 196, 211, 471; 

see Aspergillus flavus, Aspergillus 

fumigatus, Blastomyces dermatitidis, 

Candida albicans, Coccidioides immitis, 

Cryptococcus neoformans, 

Histoplasma capsulatum, 

Paracoccidioides brasiliensis, 

Penicillium marneffei, Pneumocystis, 

Trichosporon 

Humicola insolens; see Scytalidium 

thermophilum 

hybrid ascus 319 

hybrid vigour 477 

Hydnangium 578 

Hydnotrya 423 

Hydnum repandum 515, 575 

Hydnum rufescens 574, 575 

hydrogenosome 151 

hydrophobins 8, 327, 364, 366, 452, 

519, 535, 545 

Hygrocybe 546 

Hygrocybe coccinea 546, Pl. 9 

Hygrocybe conica 546 

Hygrocybe psittacina 546 

Hygrophoropsis aurantiaca 501 

Hygrophorus 546 

hymenium 525 

Hymenoascomycetes 315 

hymenochaetoid clade 573–574; 

phylogeny 516–517 

Hymenomycetes 513 

hymenophoral trama 523, 524 

hymenophore 515 

Hymenoscyphus ericae 444 

Hymenoscyphus splendens 688 

Hymenoscyphus tetracladius 688 

Hymenostilbe 360 

hyperplasia 56 

hypersensitive response 62, 115, 400, 

408, 618; in nectrotrophs 438–439, 

476 

hypertrophy 56, 58, 60–61, 136, 137, 

547, 550, 644 

hypha 2, 4; in Ascomycota 227; in 

Basidiomycota 501; in Oomycota 

75–76; Spitzenkörper 3, 4–5, 7, 10; 

vessel hypha 17 

hyphal analysis 517, 518, 519, 562; 

see momomitic, dimitic, sarcomitic, 

sarcotrimitic, trimitic 

hyphal body 203, 216, 364 

hyphal branching 13 

hyphal coiling 340, 342 

hyphal interference 540, 569 

hyphal tip 3, 4–5, 8; and Ca 2þ gradient 

9–10 

Hyphochytriomycota 24, 70, 71 

Hyphochytrium catenoides 70 

Hyphochytrium peniliae 71 

Hypholoma fasciculare 554 

Hypholoma sublateritium 553, 554 

hyphomycetes 231 

hyphopodium 386 

hyphosphere 534 

Hypocrea 339–341 

Hypocrea gelatinosa 340, 341 

Hypocrea jecorina (anam. Trichoderma 

reesei) 340 

Hypocrea poronioidea 341 

Hypocrea pulvinata 339, 340, Pl. 5 

Hypocrea rufa (anam. Trichoderma viride) 

340

828 INDEX 

Hypocrea virens (anam. Trichoderma 

virens) 340 

Hypocreales 316, 337–348; anamorphs 

316, 338, 339; lichens 455; 

taxonomy 339 

hypogeous fruit bodies 313, 414, 

423 

hypothallus, of Myxomycetes 49, 52 

hypovirulence 368, 376–377 

Hypoxylon 335–336, 607 

Hypoxylon fragiforme 333, 335–336, 

337; eclosion of ascospores 338 

Hypoxylon mammatum 333 

Hypoxylon multiforme 337 

Hypoxylon rubiginosum 335 

Hypovirus 376–377; CHV-1 genome 

376; transmission 377 

hysterothecium 459 

ibotenic acid 539, 541 

idiomorphs 267; see mating-type 

imidazole-type fungicides 479 

imperfect state; see anamorph 

inaequi-hymenial gills 522 

incertae sedis 289 

incompatibility, homogenic versus 

heterogenic 325 

indole 630 

infection bulb 684 

infection hypha; bulbous or 

primary 378, 381, 388; secondary 

388 

infection mechanisms; see Blumeria 

graminis, Haptoglossa, Magnaporthe 

grisea, nematophagous fungi, 

Plasmodiophora brassicae, Uredinales 

infection plaque 440, 441 

Ingoldiella hamata (teleom. 

Sistotrema hamatum) 243, 689, 691 

inhabitant (of lichens) 446 

ink-caps 537; see Coprinus 

Inonotus 573 

inoperculate discomycetes 429; 

see Helotiales, Lecanorales 

insect associations; see Amylostereum, 

Epichloe, Ganoderma, Laboulbeniales, 

Trichomycetes 

insect dispersal and fertilization 290, 

293, 538, 571, 580, 654; in Claviceps 

349; in Epichloe 356; in Ophiostoma 

365; Phallus 590–591; in Uredinales 

621, 630 

insect diseases; muscardine disease 

362–363 

insect pathogens; see Ascosphaera apis, 

Beauveria bassiana, Conidiobolus 

coronatus, Cordyceps, Entomophthora 

muscae, Erynia neoaphidis, Harpella 

melusinae, Metarhizium anisopliae; of 

mosquito and black fly larva 

see Coelomomyces, Erynia conica, 

Lagenidium giganteum 

integrin 9, 615 

inter-costal veins 27, 327 

interference competition; see hyphal 

interference 

internal proliferation 83, 99, 144 

invasive growth 8 

investing hyphae 416 

involutin 555, 557 

g-irradiation resistance 417 

isidium 448 

isozyme analysis 34 

isthmus 300 

Itersonilia perplexans 493; ballistospore 

discharge 494–495 

ITS (internal transcribed spacer) 35 

itraconazole 306–307 

jelly fungi 593, Pl. 11 

keratinolytic fungi 102, 293 

Kickxellales 166, 225 

killer toxins 273–274, 646–647 

killer yeasts 273 

kinetosome 68, 130, 162; dormant 

kinetosome 71, 129, 162 

kresoxim methyl 410, 412 

Kretzschmaria deusta 333 

Laboulbeniales 226 

Labyrinthula 72, 73 

Labyrinthulomycota 71–72, 73, 74 

Laccaria 552; ectomycorrhiza 552; 

related to gasteromycetes 578 

Laccaria amethystina 552 

Laccaria bicolor 552 

Laccaria laccata 552 

laccase 439, 530 

Lactarius 566 

Lactarius deliciosus 566, Pl. 10 

Lactarius deterrimus 566 

Lactarius lignyotellus 491 

Lactarius pyrogalus 566 

Lactarius quietus 566 

Lactarius rufus 519, 566 

Lactarius torminosus 566 

Lactarius turpis 566 

lactifer (lacticiferous hypha) 519, 566, 

568, 569 

Laetiporus 564 

Laetiporus sulphureus 504, 505, 519, 

562, 564, Pl. 10 

Lagenidium giganteum 79 

Lalaria 252, 658 

lamellae 522–523; attachment to stipe 

523; see aequi-hymenial, inaequihymenial 

Langermannia; see Calvatia 

latent infections 375, 388, 628 

latex 551 

Lecanora 455 

Lecanora conizaeoides 450, 454–455 

Lecanora (Sphaerothallia) esculenta 455 

Lecanora muralis 455, Pl. 8 

Lecanorales 446–458; rostrate ascus 

dehiscence 455; see lichens 

lecanoric acid 453 

Leccinum 558 

Leccinum scabrum 558 

Leccinum versipelle 558 

lectins 175, 683 

legislation (in plant diseases) 138, 649 

legumes, Ascochyta diseases 464; leafspot; 

see also individual legumes 466 

Lemonniera aquatica 685, 687 

Lemonniera terrestris 685 

Lentinula 546 

Lentinula edodes; cultivation 525 

Lentinus tigrinus 521; secotioid form 578 

Leotia lubrica 444, Pl. 7 

Leotiales; see Helotiales 

Lepista 552 

Lepista nuda 552 

Lepista saeva 552 

leprose lichens 447 

Leptographium 366 

Leptosphaeria 460–464, 472; anamorphs 

461; versus Phaeosphaeria 462–464 

Leptosphaeria acuta (anam. Phoma acuta) 

231, 461, 462, 463; endophytic stage 

462 

Leptosphaeria biglobosa 463 

Leptosphaeria coniothyrium 461 

Leptosphaeria maculans (anam. Phoma 

lingam) 461, 463–464 

lethal reactions, in Physarum 

polycephalum 48, 52 

Letharia vulpina 452 

lettuce, big-vein virus (LBVV) 148; 

downy mildew 120 

Leveillula 407

INDEX 

829 

Leveillula taurica 407 

Lewia (anam. Alternaria) 460, 469 

Lewia infectoria 469, 470 

Liceales (Myxomycota) 51 

lichen acids 453 

lichen desert 454 

lichenicolous fungi 451 

lichenicolous lichens 451 

lichenometry 447 

lichens 446–458, Pl. 8; air pollution 

454; chimaera 457; haustorium 450, 

452; nutrition 451–452; phylogeny 

226, 454; pigments 452, 453, 454; 

pure-culture studies 446; 

reproduction 448; secondary 

metabolism 453; stratification 447, 

448; taxonomy 448, 449, 454–455; 

thallus establishment 448–449, 450, 

451; thallus morphology (crustose, 

foliose, fruticose) 447–448 

lignin 528; degradation 530–532 

lignin peroxidase 530, 531 

Limnoperdon 577 

linoleic acid, nematicidal properties 

683 

lipid (storage reserves) 28–29, 71, 78, 

86, 350, 381, Pl. 12; in oospore 

arrangement (Oomycota) 86 

lipid sac 154 

locule 315, 459 

Loculoascomycetes 315, 459–486 

loline 359, 360 

lolitrem 359, 360 

long-distance dispersal 400, 586, 610, 

624, 633, 639 

Lophodermiella 441 

Lophodermium 441 

LSD 554 

Lunulospora curvula 691, 692 

lupinosis 375 

Lycogala epidendron 51, Pl. 1 

Lycoperdon 581 

Lycoperdon perlatum 582 

Lycoperdon pyriforme 581, 583 

Lyophyllum 552 

lysergic acid 354 

lysigenous perithecial development 

315, 459 

lysine biosynthesis, DAP and AAA 

pathways 67, 71, 75, 165 

macroconidia; see Botrytis cinerea, 

Fusarium, Neurospora, Sclerotinia 

macrocyclic (rusts) 613 

macrocysts 42 

Macrolepiota 536; related to 

gasteromycetes 579, 581 

Macrolepiota procera 533, 536; and 

mercury accumulation 536 

Macrolepiota rhacodes 536 

macronematous 230 

macrophages 291 

macrophore (in Phycomyces) 168 

Magnaporthaceae 316, 377–386 

Magnaporthe grisea 378, 379–382, 383, 

384–385, 388, 396; appressorium 

formation 378–381; appressorium 

maturation 381; conidium 

germination 378; gene-for-gene 

relationship 383; penetration 381; 

signalling 384, 385 

Magnusiomyces 282 

maize, anthracnose 388; cms-T 

mutation 477; grey leaf spot 481; 

Northern leaf spot 477; root and 

stalk rot 95; rust 630; smut 643; 

Southern leaf blight 477 

major gene resistance; see host 

resistance 

Malassezia 671–672; dandruff 672; 

ultrastructure 671, 672 

Malassezia furfur 671 

Malassezia globosa 672 

Malassezia pachydermatis 671, 672 

Malasseziales 671–672 

Malbranchea 289, 290, 292, 295 

maneb 113, 631, 651 

manganese peroxidase 530 

manna lichen 455 

mantle (of ectomycorrhiza) 21, 526, 527 

MAP kinase 384, 385, 645 

Marasmius 18, 546–548 

Marasmius androsaceus 548 

Marasmius oreades 511, 546, 547 

Marasmius ramealis 548 

Marasmius rotula 548 

Margaritispora aquatica 685, 691, 693 

Massarina 688, 690 

Massarina aquatica 693 

Massospora 203 

mastigoneme; see tripartite tubular 

hair 

mating behaviour, Ascomycota 229, 

266–270, 278, 322–324, 330–331; 

Basidiomycota 506–510; 

Chytridiomycota 131–133; 

Oomycota 101–102; Zygomycota 

173–181 

mating-type, Ascomycota: idiomorphs 

277, 320, 330, 436, 464, 469, 477; 

loci 268; multiple alleles 387; 

switch 268, 269, 270, 277 

mating-type, Basidiomycota: A and B 

loci 508, 509–510, 662; heterodimer 

formation 509, 645; multiple alleles 

507; structure 508–510 

medicinal fungi 361, 562, 565, 608 

Megacollybia platyphylla 500, 502, 511 

meiosporangium, meiospore 156, 176 

Melampsora 635, Pl. 12 

Melampsora epitea 635 

Melampsora euphorbiae, telium 635 

Melampsora lini var. lini 635; 

gene-for-gene concept 619 

Melampsoridium betulinum 635 

melanin 16, 177, 298, 381, 664, Pl. 4; 

DHN melanin biosynthesis 381; 

DOPA melanin 664 

Melzer’s iodine 28, 241–242, 566 

membrane channels (stretchactivated); 

see Ca 2þ 

membrane cycling 12, 272 

memnospore 22, 29 

meningoencephalitis 663 

Meripilus giganteus 501 

meristem arthroconidium 390, 391 

meristospore 205, 206 

merosporangium 166, 195, 201 

mesospore 629 

metabasidium 490, 611, 637 

metalaxyl 113, 119, 126 

Metarhizium anisopliae 361, 363, 364; 

penetration 364 

methylhydrazine 415 

metula 298, 310, 311 

Microascales 316, 368–373 

Microascus 368–369; perithecium 

formation 369 

microbodies 71, 684 

microbody-lipid complex (MLC) 130, 

131 

Microbotryales 609, 636, 652–655; 

intercellular growth 652; life cycle 

652; phylogeny 652 

Microbotryum 639; dicot Ustilago 652 

Microbotryum violaceum 652–655; 

conjugation 653; ecology 655; 

fimbriae 653, 654; host-pathogen 

interactions 654–655; life cycle 652; 

sex chromosomes 638, 653; somatic 

diploids; systemic infection 655; 

teliospore germination 653

830 INDEX 

microconidium 291, 329, 343, 

346, 435 

microcyclic (rusts) 614 

microcyst 41–42 

microfilaments; see actin 

Micromucor 197 

micronematous 230 

microphore (in Phycomyces) 168 

Microsphaera 401–403 

Microsphaera (Erysiphe) alphitoides 390, 

402, 403 

Microsporum 235, 293, 294 

microtubules 9–10, 79, 106, 158, 258, 

270, 615, 646; arrangement in 

flagella 68; ascospore formation 

323; nuclear migration 499 

millet, ergot 349 

Minimedusa polyspora 505 

mint rust 613 

mirror yeast 666 

mites, dispersal of fungi 448 

mitochondria 4, 155, 264; cristae of 

inner membrane 67, 68, 71, 165 

mitogen 385 

mitosporangium, mitospore 159 

mitosporic fungi 32 

mlo allele (barley) 397, 408, 475 

Moesziomyces penicillariae 652 

molecular clock 35 

Mollisia 439 

Mollisia cinerea 439, Pl. 7 

Mollisia uda 691 

Monilia 432 

Monilinia fructicola 432 

Monilinia fructigena 31, 430, 432, 433; 

sclerotium 432 

Monilinia laxa 432 

Monilinia polystroma 432 

Moniliopsis (teleom. Thanatephorus) 594 

Monoblepharidales 162–164; zoospore 

162, 163 

Monoblepharella 162 

Monoblepharis 162–164; sexual 

reproduction 163 

Monoblepharis macrandra 163, 164 

Monoblepharis polymorpha 163 

Monoblepharis sphaerica 164 

monoclinous antheridium 85 

monomitic basidiocarp construction 

519 

Monosporascus cannonballus 237 

monoverticillate; see Penicillium 

conidiophores 

Montagnea 578 

Morchella 427–428; cultivation 428; 

ectomycorrhiza 427–428; 

endobacteria 428; saprotrophic 

populations 427; sclerotia 428 

Morchella angusticeps 427 

Morchella conica 427 

Morchella crassipes 427 

Morchella deliciosa 427 

Morchella elata 427 

Morchella esculenta 427, Pl. 6 

Morchella semilibera 427 

morpholine-type fungicides 410 

morphological heterothallism 200 

Mortierella 197–200; zygospores 198, 

200 

Mortierella alpina 197 

Mortierella capitata 200 

Mortierella chlamydospora 197 

Mortierella ericetorum 200 

Mortierella humilis 197 

Mortierella hyalina 198 

Mortierella indohi 199 

Mortierella isabellina 197 

Mortierella polycephala 197 

Mortierella ramanniana 197 

Mortierella rostafinskii 199 

Mortierella stylospora 197 

Mortierella umbellata 198, 200 

Mortierella (Umbelopsis) vinacea 25, 

197 

Mortierella wolfii 197 

Mortierella zonata 197, 199 

mucilage, in yeasts 659, 661; (in 

attachment) see adhesives 

Mucor 180–181 

Mucor azygospora 179, 181 

Mucor bainieri 179 

Mucor circinelloides 181 

Mucor fragilis 181 

Mucor genevensis 175, 179 

Mucor hiemalis 172–173, 176, 179, 181; 

azygospore 179 

Mucor indicus 181 

Mucor lusitanicus 181 

Mucor miehei 181 

Mucor mucedo 167, 172, 179 

Mucor piriformis 173, 179 

Mucor plasmaticus 173 

Mucor plumbeus 30, 173, 182, 189 

Mucor pusillus 178, 181 

Mucor racemosus 181, 182 

Mucor rouxii, yeast stage 167, 168, 

181 

Mucor spinosus 181 

Mucorales 165–200; homothallism 

173; mating behaviour 178–179; sex 

hormones 174; sexual reproduction 

173–178; sporangium development 

171–173 

mucormycosis 181, 183 

muscimol 539, 541 

mushroom poisoning 415, 540, 

555–556; Emperor Claudius 540 

Mutinus caninus 589, 591–592 

mycelial cords 15, 500, 502, 559; in 

mycorrhiza 526, 585 

Myceliophthora roreri; see Crinipellis 

roreri 

mycelium 2; dikaryotic 3, 492, 497, 

501; heterokaryotic 3, 227, 497; 

homokaryotic 2, 227, 496; 

monokaryotic 3, 492, 496; mycelial 

strands 15; rhizomorphs 16, 17–18 

Mycena 166, 551–552; latex 551; orchid 


Mycena galericulata 551 

Mycena galopus 551, 570 

Mycena pura Pl. 3 

Mycena sanguinolenta 551 

Mycena stylobates 551 

myclobutanil 479 

mycobiont (of lichens) 446 

Mycocentrospora filiformis 694 

mycoheterotrophy 526 

mycolaminarin 76, 83, 87, 107 

mycoparasitism 97, 127, 191, 546, 

556, 605 

mycophagous insects 565, 591 

mycorrhiza 218; see ectomycorrhiza, 

ericoid mycorrhiza, orchid 

mycorrhiza, VAM 

mycoses, Basidiobolus 207; Fusarium 

343; Mucorales 181, 183; Pythium 

insidiosum 102; Scopulariopsis 369; 

see human pathogens 

Mycosphaerella 464, 480–481, 484; 

anamorphs 481; diseases 480, 481; 

pseudothecium 481, 482 

Mycosphaerella dianthicola 

(anam. Cladosporium 

echinulatum) 482 

Mycosphaerella graminicola (anam. 

Septoria tritici) 481, 483; genetic 

diversity 481 

Mycosphaerella macrospora 

(anam. Cladosporium humile) 482 

Mycosphaerella tassiana (anam. 

Cladosporium herbarum) 482

INDEX 

831 

mycosporine-alanine 387 

mycotoxins 302, 304, 305–306, 347, 

348, 470 

Mycotypha microspora 202 

Mycovellosiella 483 

Mycovellosiella fulva; see Cladosporium 

fulvum 

mycoviruses 329, 375–376; 

transmission 377; see Hypovirus 

Myriosclerotinia curreyana 430; 

see Myrioconium, Sclerotinia curreyana 

myxamoeba 49 

Myxomycetes 47–53, Pl. 1 

Myxotrichum chartarum 296, 297; 

taxonomic position 297, 444 

Myzocytium 681 

nasse apicale 241 

necrotrophy 388, 432, 434, 438 

Nectria 341–343, 689 

Nectria cinnabarina 341–342, 344, 600, 

Pl. 5 

Nectria coccinea 341 

Nectria galligena (anam. Cylindrocarpon 

heteronema) 341, 343, 344, 348 

Nectria haematococca 344 

Nectria (anam. Heliscus) lugdunensis 687 

Nectria mammoidea 345 

Nectria radicicola (anam. Cylindrocarpon 

destructans) 348 

Nematoctonus (teleom. Hohenbuehelia) 

679, 681 

nematodes 673 

nematophagous fungi 63, 64, 349, 

542, 673–685; adhesion 683; 

adhesive knobs 675, 676, 679; 

adhesive nets 675, 676; biological 

control 684; constricting rings 

676–679; egg and cyst parasites 674, 

684; endoparasitic fungi 674, 

680–682; infection process 683; 

non-constricting rings 676; 

predatory fungi 673, 675–680; 

taxonomy 674; toxins 683; trap 

induction 682–683; trophic hyphae 

673, 684 

Neobulgaria 444 

Neocallimastigales 150–153 

Neocallimastix 151 

Neocallimastix frontalis 151 

Neocallimastix hurleyensis 151, 152 

Neocallimastix patriciarum 151 

Neoerysiphe galeopsidis 404 

Neonectria 348 

Neotyphodium (teleom. Epichloe) 355, 

358; alkaloids 358–359, 360; 

mutualistic symbiosis 359; origin 

359 

Neotyphodium coenophialum 342 

Neotyphodium lolii 358, 359 

Neotyphodium typhinum 358 

Neozygites 203 

Neurospora 326–331; as a genetic tool 

327; life cycle 327–330 

Neurospora africana 327 

Neurospora crassa 11, 229, 237, 320, 

327, 329; biological clock 331; life 

cycle 327, 328, 329–330; mating 

behaviour 330–331 

Neurospora dodgei 327 

Neurospora intermedia 326 

Neurospora sitophila 327 

Neurospora terricola 327 

Neurospora tetrasperma, ascospore 26, 

228, 237; pseudohomothallism 

323–324, 506 

neurosporoxanthin 329 

Nia vibrissa 577, 579, 693 

Nigrospora 30 

Nodulisporium 333, 334, 335 

Nodulisporium tulasnei 335 

Nostoc 221, 446, 456 

Nowakowskiella 144–145 

Nowakowskiella elegans 144, 145 

Nowakowskiella profusa 129, 144 

nuclei 4, 5, 79, 228, 497, 501, Pl. 12; 

conjugate division 499; nuclear 

migration 498 

numbers of species of fungi 1, 226 

numbers of spores 497 

nutrient uptake 12–13, 14 

nystatin 279 

oak, powdery mildew 402, 403; wilt 

369 

oats, covered smut 643; crown rust 

628; leaf necrosis 476; loose smut 

642, 643; Victoria cultivar 476, 619 

ocellus 186 

ochratoxin A 304, 305 

odours 371, 373, 424, 591, 630 

Oedocephalum 419, 420, 504 

Oedogoniomyces 162 

Oidiodendron 295, 444 

Oidiopsis 408 

oidium 421, 502, 503, 538 

Oidium 390 

Oidium tuckeri 403 

oilseed rape, leaf spot 439; blackleg 

461, 463 

oleaginous fungi 167 

Olpidium 145–148; fossil 133; 

transmission of viruses 147–148; 

zoospores 146 

Olpidium bornovanus 146–148 

Olpidium brassicae 127, 146–147, 148 

Omphalotus 546 

Omphalotus olearius 501 

one-gene-one-enzyme hypothesis 327 

onions, leaf blight 468; white rot 434 

Onygena 290, 293 

Onygena corvina 290, 293 

Onygena equina 290, 293 

Onygenales 289–297 

oogamous fertilization 28, 77, 162 

oogoniol 90 

oogonium 29, 77, 86, 89, 101 

Oomycota 24, 38, 64, 75–126, P. 2; 

hypha 75–76; sexual reproduction 

77, 78; taxonomy 80; zoospore 76, 

77 

ooplast 78, 86, 102, 110 

oosphere 29, 102, 109 

oospore 28, 29, 77, 102, 109–110, 

164; centric, subcentric, 

subeccentric, eccentric types 86 

oosporein 363 

operculate discomycetes 414; 

see Pezizales 

operculum 241, 414, 417, 418; 

see ascus apical apparatus 

Ophiostoma 364–366; perithecium 364, 

365, 366; versus Ceratocystis 364, 373 

Ophiostoma himal-ulmi 366–367 

Ophiostoma novo-ulmi 366; control of 

Dutch elm disease 368 

Ophiostoma piceae 365 

Ophiostoma ulmi 366, 367 

Ophiostomatales 316, 364 

opisthokont zoospore 24 

-opsis form (of Uredinales) 613 

Orbilia 675 

Orbiliaceae 675 

orchid mycorrhiza 550, 596, 597, 598 

orellanine 539, 555 

organohalogens, fungal origin 530 

Orpinomyces 151 

Oudemansiella canarii 489 

Oudemansiella mucida 548 

Oudemansiella radicata 547, 548; 

basidium 488 

Ovulariopsis 406

832 INDEX 

oxalate crystals 173, 529 

oxalic acid 433, 438, 447, 529 

oxidative burst 291, 397, 438, 475, 540 

oxidative stress 434, 664; and 

carotenoid production 434, 665, 

670, 671 

oyster mushroom; see Pleurotus 

Ozonium 537 

Pachysolen tamophilus 262 

Paecilomyces 299, 360 

Paecilomyces lilacinus, as nematode egg 

parasite 684; biological control 685 

Paecilomyces militaris (teleom. Cordyceps 

militaris) 361 

Palmella stage of Basidiobolus ranarum 

206 

Panaeolus 546 

Panaeolus semi-ovatus 546 

Panaeolus sphinctrinus 543, 546 

Pandora 203 

Panellus stypticus 489, 491 

papilla; see host defence mechanisms 

Paracoccidioides brasiliensis 289, 

290–292 

paracrystalline bodies 141 

paragynous fertilization 109 

paraphysis 241, 315, 414, 461; apical 

paraphysis 337, 343, 461; in 

Basidiomycota 522, 525 

parasexual cycle 115, 230, 345 

parasitic fungi; see individual host 

plants; algae, insects, 

mycoparasitism, mycoses, 

nematodes, rotifers 

Parasola 537 

Parauncinula septata 393 

parenthesome 497, 498–499, 573, 593, 

606 

parietin 453, 456 

parisin 156 

parthenogenesis 85, 179 

partial veil 520 

pathogenesis-related proteins; 

see PR proteins 

patulin 304, 306–307 

pavement cracking 538 

Paxillus 555 

Paxillus atrotomentosus 555 

Paxillus involutus 501, 555, 556; 

post-meiotic mitosis 490 

pea, blight 464; leaf and pod spot 464; 

powdery mildew 402 

peach, leaf curl 251; brown-rot 432 

pea truffle; see Endogone 

pear trellis rust 631, Pl. 12 

pectin 528 

pectinolytic enzymes 433–434, 

438, 529 

peloton 597 

Peltigera 456 

Peltigera canina 456, Pl. 8 

Peltigera polydactyla 456, 457 

penetration peg 381, 396 

penicillin 303, 304 

Penicillium 297–299, 310–313; 

conidiophore 298, 299; mono-, 

bi-, ter-, quaterverticillate 298, 310, 

311; sclerotium 313 

Penicillium aurantiogriseum 312 

Penicillium camemberti 303, 311 

Penicillium chrysogenum 303 

Penicillium citrinum 311 

Penicillium claviforme 230 

Penicillium cyclopium 301 

Penicillium digitatum 311–312, Pl. 4 

Penicillium expansum 306, 311, 312 

Penicillium griseofulvum 293, 304, 311 

Penicillium italicum 311–312 

Penicillium janczewskii 304 

Penicillium marneffei 307; dimorphism 

301 

Penicillium notatum 303 

Penicillium roqueforti 303, 311 

Penicillium spinulosum 311 

Penicillium verrucosum 305 

Penicillium verruculosum 311 

Peniophora 605 

Peniophora gigantea; see Phlebiopsis 

gigantea 

Peniophora quercina 515 

pentachloronitrobenzene 651 

peramine 359, 360 

percurrent conidiogenesis 469 

perfect state; see teleomorph 

periclinal thickening 232 

Peridermium 634; see Cronartium 

Peridermium pini 635 

peridiole 577, 583, 584, 586, 589, 590 

peridium 314, 424, 577, 587, 622 

perifungal membrane 597 

Périgord truffle 426 

periphysis 243, 315, 621 

periplasm (in oosphere formation) 86, 

109 

periplasmic space 270 

perispore, perisporium (of spore 

walls) 26, 237, 417, 420 

perithecial hairs 331, 332 

perithecial stroma 246, 335, 

336–337, 348, 352–353, 360, 362, 

373, Pl. 5 

perithecium 245, 246, 317; 

development 315; in Microascus 369; 

in Nectria 337; in Ophiostoma 

364–366; in Sordaria 318–319; in 

Xylaria 333 

Peronosclerospora 125 

Peronosclerospora sorghi 125–126 

Peronospora 116–119; control 119; 

haustorium 117–118; oospores 118; 

sporangiophore 117 

Peronospora destructor 116, 119 

Peronospora farinosa 116 

Peronospora manshurica 118 

Peronospora parasitica 116, 117, 

118–119, 122, Pl. 2 

Peronospora tabacina 116, 119 

Peronospora trifoliorum 119 

Peronospora viciae 119 

Peronosporales (downy mildews) 

115–125; biotrophy 116; life cycle 

116; origin 116; relationships with 

Pythiales 115 

peroxisome 684 

Pertusaria pertusa 25 

Pesotum 366 

Petriella 368 

Peziza 419 

Peziza succosa 419 

Peziza vesiculosa Pl. 6 

Pezizales (operculate discomycetes) 

414–428, Pl. 6; classification 415; 

phylogeny 415 

Pezoloma 690 

pH sensing 433 

Phaeolus 576 

Phaeosphaeria 460, 462–464; 

anamorphs 461 

Phaeosphaeria avenaria (anam. 

Stagonospora avenae) 462 

Phaeosphaeria (anam. Stagonospora) 

nodorum 231, 462–463, 481 

Phaffia rhodozyma 665–666; 

see Xanthophyllomyces dendrorhous 

phagocytosis 40, 45, 55 

phalloidin 539, 540 

Phallus duplicatus 591 

Phallus impudicus 15, 500, 591, 592, 

Pl. 11; mycelial cord 15, 591; odours 

591 

Phallus indusiatus 589, 591–592

INDEX 

833 

Phallus ravenelii 591 

Phanerochaete chrysosporium 565; 

white-rot 530–532 

Phanerochaete velutina 570 

phaneroplasmodium 48, 51, Pl. 1 

Phellinus 573 

Phellinus igniarius 573, Pl. 10 

Phellinus noxius 573 

Phellinus pomaceus 573; chloromethane 

emission 532, 574 

Phellinus robustus 574 

Phellinus weirii 573 

phenylacetaldehyde 591, 630 

phenylamides 112 

phenylethanol 591, 630 

pheromones; see sex hormones 

phialide 31, 232, 233–234, 300 

phialoconidium 300, 465; dry and 

slimy 233 

Phialophora 386, 439 

Phlebiopsis gigantea 569 

phoenicoid fungi 417 

Pholiota 554 

Pholiota nameko 555 

Pholiota squarrosa 554, Pl. 9 

Phoma 462, 464–465, 466; versus 

Phomopsis 465 

Phoma acuta 462–463 

Phoma betae 466 

Phoma epicoccina 466; see Epicoccum 

nigrum 

Phoma lingam 463; Plenodomus 464; 

see Leptosphaeria maculans 

Phoma medicaginis 464, 465 

phomopsins 375 

Phomopsis 373–375; a-conidium 373, 

374; b-conidium 373, 374, 464; 

ecology 375; versus Phoma 465; 

taxonomy 374 

Phomopsis helianthi 375 

Phomopsis phaseoli 373; see Diaporthe 

phaseolorum 

Phomopsis viticola 375 

phomozin 375 

phosphonate fungicides 113 

photobiont (of lichens) 446 

photoreceptors 169 

photosensitizers 482, 665 

phototropism, ascus tip 420, 427; 

sporangiophore 168, 169, 170, 185, 

188 

Phragmidium 631 

Phragmidium mucronatum 631; 

teliospore 629 

Phragmidium violaceum 631, Pl. 12; 

biocontrol of bramble 631 

phragmobasidium 488, 489, 593, 

637 

phragmospore 23 

Phycomyces blakesleeanus 168, 169, 184; 

heterothallism 174; life cycle 180; 

phototropism 168, 169–170; 

sporangiophore development 

168–170, 171; sporangium 

development 171–173; zygospore 

development 176, 186; zygospore 

germination 178 

Phycomyces nitens 179, 184 

Phycomycetes 33 

Phyllactinia 405 

Phyllactinia guttata 237, 390, 406, 407; 

chasmothecium 407, 409 

phylloplane yeasts 668 

phylogeny 33, 36–37, 69, 166, 248, 

512, 516 

Physarales (Myxomycota) 51 

Physarum polycephalum 48, 50, 51–53, 

Pl. 1; life cycle 49; smart network 52 

physiological heterothallism 435 

physiological races; see races 

Physoderma alfalfae 153 

Physoderma maydis 153 

phytoalexins 115, 383, 438, 464 

Phytophthora 95, 102–115; asexual 

reproduction 103–106; 

chlamydospore 105, 106; oospore 

109–110; sexual reproduction 

109–111; sporangium germination 

104; zoospore 106, 107–108; 

zoospore encystment 106; zoospore 

release 105 

Phytophthora alni 103 

Phytophthora cactorum 102, 106, 

109–110 

Phytophthora cinnamomi 102, 107, 

108 

Phytophthora drechsleri 103 

Phytophthora erythroseptica 29, 68, 103, 

109, 116, Pl. 2 

Phytophthora fragariae 103 

Phytophthora infestans 78, 95, 111–115; 

disease forecast 113; epidemiology 

111–112; fungicides 112–113; 

haustorium 103, 105; life cycle 

95–96, 101, 102; origin and spread 

111; physiological races 114; potato 

late blight 111–115, Pl. 2; tomato 

late blight 115 

Phytophthora nicotianae 103 

Phytophthora palmivora 103 

Phytophthora ramorum 103 

phytotoxins 375, 388, 470, 476, 478, 

482, 568; see cercosporin, HC-toxin, 

prehelminthosporol, T-toxin, 

victorin C 

Pichia 281 

Pichia guilliermondii 263 

Pichia jadinii 281 

Pichia pastoris 263, 281 

Pichia stipitis 262 

Piedmont truffle 426 

pigments; see carotenoids, lichens, 

melanin, pulvinic acids 

Pilaira 189–190 

Pilaira anomala 190 

pileocystidium 525 

pileus 517 

Pilobolus 185–189; sporangium 

discharge 189; vector for 

nematodes 188 

Pilobolus crystallinus 185, Pl. 3 

Pilobolus kleinii 185, 188 

Pilobolus umbonatus 185 

pine, needlecast 441; rusts 634 

pionnote 345 

Piptocephalis 201; appressorium 202; 

haustorium 202 

Piptocephalis freseniana 201 

Piptocephalis fimbriata 202 

Piptocephalis unispora 201 

Piptocephalis virginiana 201, 202 

Piptocephalis xenophila 201 

Piptoporus betulinus 339, 560, 561, 

562–563; mating system 506 

Piromyces 151 

Pisolithus 12, 527, 586; boletoid clade 

579; ectomycorrhiza 586 

Pisolithus marmoratus 586 

Pisolithus tinctorius (¼ P. arhizus) 586, 

Pl. 11 

Placopsis gelida 451 

plant growth hormones; see auxins, 

cytokinins, ethylene, gibberellins 

plant resistance; see host resistance, 

breeding for resistance 

plasmodiocarp (of Myxomycetes) 50 

Plasmodiophora brassicae 54–57, 58, 

59–61; club root symptoms 55–56, 

57; club root control 62–63; 

cruciform mitosis 55, 59; life cycle 

56; infection process 57, 58–59, 65; 

plant hormones 60–61, 253

834 INDEX 

Plasmodiophoromycota 24, 38, 54–66; 

amoebae 55; phagocytosis 55; 

taxonomy 54 

plasmodium 3, 40, 47, 55; 

see amoeboid, aphano-, phanero-, 

proto- 

Plasmopara nivea 119 

Plasmopara pusilla 120 

Plasmopara pygmaea 120 

Plasmopara viticola 78, 116, 119, 410 

plectenchyma 520 

Plectomycetes 285–314, Pl. 4; 

lichenized ancestors? 454; 

taxonomy 286 

Plenodomus 464 

pleomorphism 32 

Pleospora 460, 466–469, 472 

Pleospora bjoerlingii (¼ P. betae) 466 

Pleospora herbarum 31, 466, 468; 

ascospore perisporium 237, 468; 

pseudothecium development 

461 

Pleospora scirpicola 466; ascospore 

appendage 239, 460; bitunicate 

ascus 460 

Pleosporales 460–480; pseudothecium 

development 460–461 

pleurocystidium 525 

Pleurotus 541–542; cultivation 525, 

542; nematode-trapping 679, 681; 

nematotoxic substances 683 

Pleurotus cystidiosus 542 

Pleurotus ostreatus 533, 542 

Pleurotus tuberregium 542 

plum, pocket plum 251; silver leaf 

571; witches’ broom 251 

Pluteus 541 

Pluteus cervinus 541; trama 524 

Pneumocystis 250, 259–261 

Pneumocystis carinii 259 

Pneumocystis jirovecii 259 

pneumonia 259 

Pochonia chlamydosporia, as nematode 

egg parasite 684; biological control 

685 

Podaxis 578 

Podaxis pistillaris 578 

podetium 457 

Podocrella (anam. Harposporium) 349, 

681 

Podosordaria tulasnei 15, 18 

Podosphaera 404–405 

Podosphaera clandestina 404, 405 

Podosphaera leucotricha 390, 405 

Podosphaera xanthii, resistance 

breeding 408 

Podospora 320–326; versus Schizothecium 

320; mating systems 322–324 

Podospora anserina 320–326; ascospore 

development 321, 322; mating type 

idiomorphs 325; post-meiotic 

mitosis 323–324; senescence 326; 

vegetative incompatibility 325–326, 

377 

Podospora curvicolla 320 

Podospora curvula 320 

Podospora decipiens 320, 322 

Podospora pleiospora 320, 322 

pollen (as substrate) 73, 74, 140 

polyketides 304 

Polymyxa betae 54, 57, 59, 62 

Polymyxa graminis 54, 62 

polyplanetism 81, 85 

polyploidy 159 

polyporoid clade 560–566; phylogeny 

516–517, 560 

Polyporus brumalis 561 

Polyporus mylittae 18, 20, 501, 502 

Polyporus squamosus 561, 562, 564 

Polyporus tuberaster 501 

polyunsaturated fatty acids (PUFA) 74, 

167, 197 

poplar, leaf blister 251 

poroconidium 232, 468, 469, 470, 

472, 473 

post-harvest diseases 388, 432 

post-meiotic mitosis, in Ascomycota 

323–324; in Basidiomycota 490 

potato, black dot disease 388; black 

scurf 595; late blight 111, Pl. 2; 

mop-top virus 62–63; pink rot 103, 

Pl. 2; powdery scab 61, 63; wart 

disease 134, Pl. 3 

powdery mildews 390; control by 

breeding, fungicides, biological 

control 408–413; see Erysiphales 

PR proteins 119, 410 

predacious yeasts 282, 283 

prehelminthosporol 475, 476 

pre-thallus (lichens) 450 

primary mycelium 492, 496 

principal host 610 

principal zoospore 76 

prion-like proteins 326 

probasidium 490, 610, 637 

proconidium 327 

progametangium 174, 176 

promycelium 488, 489, 611, 612, 637 

prosorus 134 

proteases 683 

protein glycosylation 11, 654 

protenchyma 519 

proto-aecium 611, 622 

protocorm 596 

Protomyces 250–251, 261 

proton pumps; see H þ ATPases 

protoperithecium 318, 329 

protoplasmodium 48 

Protosteliomycetes (protostelid 

plasmodial slime moulds) 

45–47 

Protostelium 46, 47 

prototunicate; see ascus wall 

Protozoa 37, 40, 54, 67 

Psathyrella 537 

Pseudeurotium, sectoring 229 

Pseudoaegerita 701 

pseudoaethalium 50 

Pseudoallescheria 368 

Pseudocercospora 481 

Pseudocercospora herpotrichoides 439 

Pseudogymnoascus 444 

pseudohomothallism 322, 323, 330, 

506, 570; see secondary 

homothallism 

Pseudohydnum gelatinosum 604 

pseudohypha 2, 3, 227, 272 

Pseudoidium 401, 402 

Pseudomonas, in biological control 347, 

386, 596; induction of fruiting in 

Agaricus 534 

pseudoparaphysis 242, 460 

pseudoparenchyma 285, 520 

pseudoplasmodium 3, 42, 44 

pseudorhiza 547, 548 

pseudosclerotium 550 

pseudothecium 245, 246; Pleospora 

type 460–461 

Pseudotulostoma 314 

Pseudozyma 412 

psilocin 539, 554 

Psilocybe 554 

Psilocybe cubense 554 

Psilocybe merdaria, secotioid form 

578 

Psilocybe mexicana 554 

Psilocybe semilanceata 553, 554 

psilocybin 539, 546, 554 

psoromic acid 453 

Puccinia, pathway 624; versus Uromyces 

629 

Puccinia caricina 630, Pl. 12

INDEX 

835 

Puccinia coronata 476, 612, 619, 628; 

homothallism 628; host resistance 

genes 628; teliospore 629; 

Tranzschel’s Law 614 

Puccinia distincta Pl. 12 

Puccinia graminis 620, 621–627; on 

barberry 621–622; basidiospores 

621; basidium 489; crop losses 620; 

cultivation on simple media 618; 

host Sr resistance genes 626; 

life cycle 610, 611, 612–613, 621–622; 

formae speciales 621; f. sp. secalis 622; 

f. sp. tritici 622, 624–627; 

physiological races 621, 625, 626, 

627; somatic hybridization 625 

Puccinia hordei 628 

Puccinia lagenophorae 612, 613 

Puccinia melanocephala 633 

Puccinia menthae 613, 630 

Puccinia mesnieriana 614 

Puccinia monoica 630; floral mimicry 

630 

Puccinia obscura 612 

Puccinia poarum 630 

Puccinia punctiformis 630 

Puccinia recondita 627 

Puccinia sorghi 629 

Puccinia striiformis 408, 627–628 

Puccinia triticina 627; host Lr resistance 

genes 627 

PUFA; see polyunsaturated fatty acids 

puff balls 581, 582, Pl. 11 

puffing; see ascospore puffing 

pullulan 485 

pulvinic acids 453, 455, 555, 557, 585 

pycnidiospore 465 

pycnidium 231, 374, 462, 464, 

465–466 

Pycnoporus cinnabarinus 531 

pyramiding (of resistance alleles) 408, 

619, 627 

Pyrenomycetes 315, 316–366, 

367–389, Pl. 5; taxonomy 316 

Pyrenopeziza brassicae 436, 439, 440 

Pyrenophora (anam. Drechslera) 460, 

472, 477–478; phytotoxins 478 

Pyrenophora teres 478 

Pyrenophora tritici-repentis 476, 478 

Pyricularia grisea 378 

Pyricularia oryzae (teleom. Magnaporthe 

grisea) 378 

Pyronema 415–417; antheridium 416; 

ascogenous hypha 416; ascogonium 

416; crozier 416; ecology 417; 

investing hyphae 416; trichogyne 

416 

Pyronema domesticum 229, 415, 416, 

417, 418, Pl. 6; sclerotium 415 

Pyronema omphalodes 415, 417 

Pythiales 95–115; asexual 

reproduction 95; hormones 96; 

sexual reproduction 95, 100 

Pythiogeton zeae 95 

Pythiopsis cymosa 92, 93 

Pythium 95–96, 97, 98–102, Pl. 2; 

asexual reproduction 97–100; 

biological control 340; ecology 

102; sexual reproduction 

100–102 

Pythium acanthicum 97 

Pythium aphanidermatum 97–98 

Pythium debaryanum 97, 98, 100, 101 

Pythium gracile 97 

Pythium heterothallicum 101 

Pythium insidiosum 79, 102 

Pythium mamillatum 100, 101 

Pythium middletonii 99 

Pythium monospermum 69 

Pythium multisporum 95 

Pythium nunn 97 

Pythium oligandrum 97 

Pythium splendens 101 

Pythium sylvaticum 95, 101 

Pythium ultimum 97, 100, 101 

Pythium undulatum 30, 99, Pl. 2 

quaterverticillate; see Penicillium 

conidiophores 

quinoxyfen 410, 412 

Quorn 339 

races 114, 138, 395, 619, 621, 643 

radioactive pollution 454 

Ramaria 576 

Ramaria botrytis 576, Pl. 10 

Ramaria stricta 576 

Ramichloridium 486 

ramoconidium 483 

ramus 310, 311 

RAPD analysis 34 

raspberry, cane blight 461 

reactive oxygen species (ROS) 326, 

482, 665 

receptacle 591, 592 

receptive hypha 612 

recombinant proteins, production 

263, 281 

red yeasts; see basidiomycete yeasts 

regulated secretion (in zoospore 

encystment) 77, 106 

reindeer lichen 458 

relative sexuality 77, 91, 95 

replacement disease 350 

resistance; see breeding, fungicide 

resistance, host resistance 

respiratory allergens; see asthma 

resting sporangium 56, 144, 147, 149, 

157, 159, 161 

Reticularia lycoperdon 50, 51, Pl. 1 

reticuloperidium 285, 289, 296–297 

retraction septum 203, 602 

RFLP analysis 34 

rhexolytic secession 235, 285, 289, 505 

Rhizina undulata 414 

rhizinae 447, 456, 457, Pl. 8 

Rhizocarpon geographicum 447, 451, Pl. 8 

Rhizoctonia 594–598; anastomosis 

groups 594; biological control 340, 

596; hyphae 594, 597; sclerotia 18, 

19, 501 

Rhizoctonia cerealis (teleom. 

Ceratobasidium cornigerum) 596; 

orchid mycorrhiza 596, 597 

Rhizoctonia goodyerae-repentis 596 

Rhizoctonia repens 596 

Rhizoctonia solani (teleom. 

Thanatephorus cucumeris) 594–595; 

anastomosis groups 594; orchid 

mycorrhiza 596; sclerotium 595 

rhizoids 3, 128, 141, 149–150, 155 

rhizomorph 16, 17–18, 500, 502, 550 

rhizomycelium 128, 142, 143, 144, 145 

Rhizophlyctis 148 

Rhizophlyctis harderi 131 

Rhizophlyctis oceanis 150 

Rhizophlyctis rosea 129, 147–148, 

149–150, 153; cellulose degradation 

148 

Rhizophydium 133, 139, 140, 141–142; 

fossil 133 

Rhizophydium planktonicum 140–142; 

parasitizing Asterionella 141 

Rhizophydium pollinis-pini 139 

Rhizophydium sphaerocarpon 139 

Rhizopogon 558, 587, Pl. 11; boletoid 

clade 579 

Rhizopogon luteolus 588 

Rhizopogon roseolus 588 

Rhizopogon vinicolor 588 

Rhizopus 182–183 

Rhizopus arrhizus 182 

Rhizopus azygosporus 179

836 INDEX 

Rhizopus microsporus 182 

Rhizopus oryzae 182 

Rhizopus rhizopodiformis 182 

Rhizopus sexualis 29, 173, 177, 183; 

zygospore development 176, 178 

Rhizopus stolonifer 166, 172–173, 176, 

179, 182, 184, Pl. 3 

rhizoxin 183 

Rhodocollybia 546 

Rhodosporidium toruloides 667 

Rhodotorula 667; carotenoid 

production 671; ecology 668 

Rhodotorula glutinis (teleom. 

Rhodosporidium) 659, 667 

Rhynchosporium secalis 439 

Rhynie chert 35, 133, 246, 454 

Rhytisma acerinum 441, 442–443 

Rhytismataceae 440 

riboflavin production 284 

rice, foolish seedling disease 339; 

rice blast 378 

ring wall building 232 

ringworm 293 

Robigalia 610 

roestelioid aecium 632, Pl. 12 

Rogation Sunday 610 

root exudates 434, 435 

root rot, Phytophthora and Pythium 102, 

Pl. 2 

rose, powdery mildew 404; rust 631 

Rosellinia necatrix 333 

rostrate; see ascus wall 

rotifers 64 

rRNA (ribosomal RNA) analysis 35, 36 

rumen fungi; see Neocallimastigales 

rumposome 130 

Russula 566; ectomycorrhiza 566; 

orchid mycorrhiza 598 

Russula atropurpurea 567 

Russula cyanoxantha, trama 524 

Russula emetica 566 

Russula fellea 566 

Russula ochroleuca 566 

russuloid clade 566–572; phylogeny 

516–517 

rust fungi 610; cereal rusts 627–629; 

see Uredinales 

Rutstroemia echinophila Pl. 7 

rye, ergot 350; eyespot 439 

Saccharomyces 263 

Saccharomyces cerevisiae 10–11, 229, 

232, 256; alcoholic fermentation 

262, 274–275; ascospore cleavage 

267; bread-making 274; cell cycle 

270, 271, 272, 301; cell wall 270; 

cytology 264; killer toxins 273–274, 

646; life cycle 265–266; mating 

266–270; membrane cycling 272; 

morphogenesis 270–272; 

pheromones 267; pseudohyphae 

272; vacuole 273 

Saccharomyces pastorianus 263 

Saccharomycopsis 282–284 

Saccharomycopsis fibuligera 282, 283 

Saccobolus 420 

sagenogen 68, 73 

Saitoella 250 

Sakaguchia dacryoidea 659 

saké 276 

salicylic acid 412 

sanguinolentous hypha; see lactifer 

Saprochaete 282 

Saprolegnia 9, 24, 30, 79, 81–86, 

Pl. 2; asexual reproduction 82, 

83–85; cyst 84; hypha 80; life cycle 

78; ooplast arrangement 86; 

sexual reproduction 85, 86; 

zoospore 76 

Saprolegnia litoralis 85 

Saprolegnia parasitica 81, 85 

Saprolegnia polymorpha 81 

Saprolegniales 79–95; hypha 79; 

nutrition 81 

sap-stain (of wood) 364, 371, 373 

sarco-hypha 518 

sarcomitic basidiocarp construction 

519 

sarcotrimitic basidiocarp 

construction 519 

Sarcoscypha 419 

Sarcoscypha australis Pl. 6 

Sauternes wine 438 

Sawadaea 403 

Sawadaea bicornis 404, 405 

Schizochytrium 74 

schizogenous perithecial 

development 315, 318, 338 

schizolytic secession 235 

Schizophyllum 542 

Schizophyllum commune 7–8, 489, 499, 

542, 543–544, 545; dikaryotization 

(Buller phenomenon) 510; fruiting 

in the laboratory 544; 

hydrophobins 545; mating type 

factors 508, 543 

Schizosaccharomyces 250, 261 

Schizosaccharomyces japonicus 253 

Schizosaccharomyces octosporus 253, 

254, 255 

Schizosaccharomyces pombe 51, 253–259; 

cell cycle 256, 257, 301; cell walls 

255; life cycle 255; morphogenesis 

258, 259; pheromones 255 

Schizosaccharomycetales 253–259 

Schizothecium 320 

Schizothecium tetrasporum 321, 322 

Schizothecium vesticola 320 

Scleroderma 557, 585–586; boletoid 

clade 579, 585 

Scleroderma bovista 586 

Scleroderma citrinum 515, 586, 587 

Scleroderma verrucosum 586, 587 

Sclerosporaceae 125–126 

Sclerospora 125 

Sclerospora graminicola 126 

sclerotial stroma 430 

Sclerotinia, macroconidium 430; 


sclerotium (sclerotial stroma) 20, 

430 

Sclerotinia (Myriosclerotinia) curreyana 

430, 431, Pl. 7; Myrioconium-type 


sclerotium 431 

Sclerotinia fructigena; see Monilinia 

fructigena 

Sclerotinia fuckeliana; see Botryotinia 

fuckeliana 

Sclerotinia laxa; see Monilinia laxa 

Sclerotinia (Stromatinia) narcissi, mating 

behaviour 435 

Sclerotinia porri; see Botryotinia porri 

Sclerotinia sclerotiorum 431–434; 

biological control 433; infection 

biology 432; mating behaviour 436; 

oxalic acid 433; pH sensing 433; 

sclerotium 432, 434 

Sclerotinia trifoliorum, mating 

behaviour 436 

Sclerotinia (Dumontinia) tuberosa 431, 

432 

sclerotium 18, 19, 20–21; in 

Myxomycetes 49; see Aspergillus, 

Botrytis, Claviceps, Cordyceps, 

Morchella, Penicillium, Polyporus 

mylittae, Rhizoctonia, Sclerotinia, 

Sclerotium 

Sclerotium cepivorum 431, 434; sclerotia 

and root exudates 434, 435 

Sclerotium rolfsii, sclerotium 20, 501 

scolecospore 23

INDEX 

837 

scolytid beetles 366 

Scopulariopsis 368 

Scopulariopsis brevicaulis 234, 369 

Scytalidium thermophilum 534 

secondary metabolism 453 

secondary mycelium 492, 497 

secondary resource capture 554 

secondary sporidium 648, 649 

secotioid fruit-bodies 578 

secretion of proteins 10–11, 13 

sectoring (of mycelium) 228, 229 

seed-borne fungi 433, 463, 466, 470, 

478, 643 

seed certification 651 

seed dressing 651 

segregation, first-division versus 

second-division in meiosis 319 

senescence 326 

separating cell 235 

Sepedonium chrysospermum (teleom. 

Apiocrea chrysosperma) 556, 585, Pl. 9 

septins 271, 301 

Septoria 462, 481 

Septoria tritici 481, 483 

septum, Ascomycota 227, 228; 

distoseptate versus euseptate 472; 

formation 258, 259; in hypha 2; 

pores 261; see distoseptate, 

dolipore, parenthesome 

Serpula lacrymans 556, 558–560; 

control 560; mycelial cord 16, 559; 

reproduction 559; var. domesticus 

559–560 

sex chromosomes 638, 653, 663 

sex hormones (pheromones); 

see Achlya, Allomyces, Ascobolus 

furfuraceus, Blakeslea trispora, 

Saccharomyces cerevisiae, 

Schizosaccharomyces pombe, Tremella 

mesenterica, Ustilago maydis 

sexual agglutination; 

see agglutination 

sexual dimorphism 436 

shiitake mushroom; see Lentinula 

edodes 

shuttle-streaming 51 

side body complex 155 

signalling 10, 277, 384, 645; in 

appressorium formation 384–385, 

396; calcineurin 664; cross-talk 385, 

646; heterodimer formation 509, 

645; hydrophobicity 384; 

mycoviruses 376; ring constriction 

in Drechslerella 678 

Simulium, as hosts for Erynia conica 

213; and trichomycetes 223–224 

single-cell protein (SCP) 263 

sinuate gills 523 

sirenin 158 

Sistotrema hamatum (anam. Ingoldiella 

hamata) 504, 689 

skeletal hypha 518 

skeleto-ligative hypha 518 

slime moulds 38, 40, Pl. 1 

slime moulds (cellular); see Acrasiomycetes, 

Dictyosteliomycetes 

slime moulds (plasmodial); see 

Protosteliomycetes, Myxomycetes 

slime net 71, 72, 73, 74 

Smittium culisetae 222, 224 

smut fungi 636; covered smut 643; 

loose smut 642, 643; 

see Microbotryales, ustilaginomycetous 

smuts 

soft-rot (of wood) 331 

somatic diploids 

somatic hybridization 625 

somatogamy 132, 229 

soralium 448 

Sordaria 317, 318–320; ascospore 

discharge 244; mating systems 

318–319 

Sordaria brevicollis 320 

Sordaria fimicola 68, 229; ascospore 

perisporium 237; ascus apical 

apparatus 241 

Sordaria heterothallis 320 

Sordaria humana, ascospore wall 237, 

239 

Sordaria macrospora 320 

Sordariales 315, 316, 317–332 

soredium 448, 450 

sorghum, ergot 349; anthracnose 388 

sorocarps 41, 45 

sorus 60, 636, 639 

sour rot 282 

soy sauce 302 

Sparassis 564 

Sparassis crispa 561 

spectrin 9 

spermatium 231, 329, 376, 431, 435, 

442, 611, 622 

spermatozoid 162, 164 

spermodochidium 431 

spermogonium 442, 611, 612, 622, 

Pl. 12 

Sphacelia segetum (teleom. Claviceps 

purpurea) 349 

Sphaerobolus 588; gomphoid-phalloid 

clade 579 

Sphaerobolus stellatus 588, 589–590; 

peridiole 589–590; peridiole 

discharge 589 

sphaerocyst 519 

Sphaeronaemella fimicola 371, 372 

Sphaeronaemella helvellae 371 

Sphaerotheca 404–405; fibrosin bodies 

404 

Sphaerotheca (Podosphaera) fuliginea 404 

Sphaerotheca (Podosphaera) macularis 

404; resistance breeding 408 

Sphaerotheca (Podosphaera) mors-uvae 

390, 404; resistance breeding 408 

Sphaerotheca (Podosphaera) pannosa 404, 

405–406 

spherule, of Myxomycetes 49; in 

Coccidioides 291–292 

Spinellus fusiger 166, 551, Pl. 3 

Spiniger 504, 568; see Heterobasidion 

annosum 

spiral growth 171 

Spirosphaera 697, 700 

Spirosphaera carici-graminis 701 

Spirosphaera floriformis 701 

Spirosphaera minuta 701 

Spitzenkörper; see hypha 

Spizellomyces 145 

Spizellomycetales 145–150 

splash cup 580, 582, 584–585 

Spongospora nasturtii 54, 59, 61 

Spongospora subterranea 54–55, 59, 

61–62; vector for plant viruses 62 

sporabola 495 

sporangiolum 166, 191, 193, 194, 

196, 197 

sporangiophore, development 

168–170, 171; microphores and 

macrophores 168; in Mucorales 165 

sporangiospore 24, 165, 168 

sporangium 25; one-spored 32; 

see sporangiolum; of Mucorales 

171–173; of Myxomycetes 50; of 

Phytophthora 104, 106; of Pythium 

98–99; of Saprolegnia 82 

spore print 532 

spores, different kinds 22–23; see also 

conidium, numbers of amero-, 

aplano-, asco-, ballisto-, basidio-, 

chlamydo-, dictyo-, didymo-, helico-, 

memno-, oo-, phragmo-, scoleco-, 

sporangio-, statismo-, stauro-, xeno-, 

zoo-, zygo-

838 INDEX 

Sporidiales 609, 666–670; 

see urediniomycete yeasts 

Sporidiobolus 659; see Sporobolomyces 

Sporidiobolus ruineniae 659 

Sporidiobolus salmonicolor 667, 669; 

life cycle 670 

sporidium, in Haptoglossa 64, 65, 66; 

in smut fungi 637, 648 

Sporisorium 640 

Sporisorium scitamineum 639 

Sporobolomyces 658–659; ecology 668 

Sporobolomyces roseus (teleom. 

Sporidiobolus) 659, 666–667, 668; air 

pollution 669; carotenoid 

production 671; ecology 668 

Sporobolomyces salmonicolor (teleom. 

Sporidiobolus) 667, 670 

sporocarp 46, 47, Pl. 1 

sporocyst 288 

sporodochium 231, 342–343, 466, Pl. 5 

sporophores, of Myxomycetes 50 

sporopollenin 177 

Sporormiella 460–461, 479 

Sporormiella intermedia 479, 480 

Sporoschisma 234 

Sporothrix 366 

Sporothrix schenckii 364 

Sporotrichum 505, 564 

Sporotrichum pulverulentum 566 

sprinkle-plate technique 675 

squamule 448 

squamulose lichens 447 

Stagonospora 462, 464 

Stagonospora avenae; see Phaeosphaeria 

avenaria 

Stagonospora nodorum; see Phaeosphaeria 

nodorum 

St. Anthony’s fire; see ergotism 

statismospore 28, 577 

statolith 548 

staurospore 23 

steliogen 46 

Stemonitis axifera 51, Pl. 1 

Stemphylium (teleom. Pleospora) 467, 

468, 472 

Stemphylium vesicarium 468 

stereothecium 423 

Stereum 569–572, 605; mating 569 

Stereum gausapatum 569 

Stereum hirsutum 567, 569–570; bow-tie 

reaction 571; mating 569 

Stereum rugosum 568, 569 

Stereum sanguinolentum 569; mating 

570 

sterigma 489, 494 

sterigmatocystin 305 

sterols 89, 96, 424; biosynthesis 411 

stichobasidium 490 

stinkhorns 589, 590 

stipe 517 

storage rots; see post-harvest diseases 

Straminipila 37, 67, 75; phylogeny 69 

straminipilous flagellum; see flagella 

strobilurins 410, 546, 551 

strobilurin-type fungicides 113, 410, 

412, 479, 481, 627, 631; resistance 

412 

Strobilurus 546 

Strobilurus tenacellus 412 

stroma 231, 430; see sclerotial stroma, 

substratal stroma 

Stropharia 554 

Stropharia aeruginosa 554 

Stropharia aurantiaca 554 

Stropharia semiglobata 521, 553, 554 

Stüben bodies 155 

stylospore 197 

sub-gleba 581, 583 

substomatal vesicle 615, 616 

substratal stroma 430 

Subulicystidium longisporum 697 

sudden infant death syndrome 259 

sugar beet, blackleg 466; leaf spot 

481; powdery mildew 402; 

yellow-vein virus 62 

sugarcane, rust 633; smut 639 

Suillus 558; related to gasteromycetes 

578–579 

Suillus bovinus 558 

Suillus granulatus 558, Pl. 9 

Suillus grevillei 526, 556, 558; related to 


Suillus luteus 558 

sulphur dioxide 454 

sulphur dust and lime 403, 410 

suprahilar plage 493 

surface tension catapult 493, 494, 496, 

611, 648, 655, 660 

survival of propagules 23, 51, 73, 111, 

155, 613, 643, 648 

suspensor 176, 177; appendages 177 

swarmer 46, 49, 137, 156, 160 

sympodula 332, 337, 472, 475 

synanamorph 32, 341–342, 366, 466 

Syncephalastrum racemosum 195 

Syncephalis 201 

Synchytrium 134–139 

Synchytrium aecidioides 139 

Synchytrium lagenariae 138 

Synchytrium endobioticum 127, 134–138, 

Pl. 3; control 138; hypertrophy 136; 

life-cycle 135 

Synchytrium fulgens 138 

Synchytrium macrosporum 134 

Synchytrium mercurialis 139, 140 

Synchytrium taraxaci 139, Pl. 3 

Synchytrium trichosanthidis 138 

synnema 230 

systemic acquired resistance (SAR) 

119, 412 

Syzygites megalocarpus 172–173, 

175–176, 179, 184, 187 

T-2 toxin 348 

Taeniomyces gracilis (teleom. 

Fibulomyces) 689, 690 

take-all 385–386; take-all decline 386, 

596 

Talaromyces 312, 313 

Tapesia acuformis 439–440, 441 

Tapesia yallundae (anam. 

Pseudocercospora herpotrichoides) 

439–440, 441, 596 

Taphrina 250–253, 261 

Taphrina amentorum 251, Pl. 4 

Taphrina betulina 251, Pl. 4 

Taphrina epiphylla 253 

Taphrina deformans 251–252, 253, Pl. 4; 

plant hormones 253; control 253 

Taphrina insititiae 251 

Taphrina populina 251 

Taphrina pruni 251 

Taphrina tosquinetii 251 

Taphrina wiesneri 251 

Taphrinales 251–253 

taxonomy 32–35, 38 

teleomorph 32 

teliospore 488, 489; pedicel 629, 631; 

in rust fungi 610, 612, 623; in smut 

fungi 637, 639, 660; in yeasts 667, 

670 

telium 610, 612, 623, Pl. 12 

terbinafine 279, 293 

Terfezia (desert truffle) 427 

Termitomyces 552 

terverticillate; see Penicillium 

conidiophores 

Tetrachaetum elegans 688, 689 

tetrapolar; see heterothallism 

tetraradiate propagules 214, 687–688, 

693 

textura angularis 464

INDEX 

839 

thallic conidiogenesis 30, 235; 

see holothallic, thallic-arthric 

thallic-arthric conidiogenesis 235 

thallus 3, 64, 73; epibiotic and 

endobiotic 128; holocarpic and 

eucarpic 71, 128; lichens 447–448, 

Pl. 8; monocentric and polycentric 

71, 128; variability 134; 

trichomycetes 223 

Thamnidium elegans 191, 192 

Thanatephorus 594, 595; see Rhizoctonia 

Thaxterogaster 578 

Thelephora terrestris 572, Pl. 10; orchid 


thelephoroid clade 572; phylogeny 

516–517 

thermotolerance 306–307, 331 

Thielaviopsis 371 

Thielaviopsis basicola 232, 234, 372 

Thielaviopsis thielavioides 371 

thigmotropism 174–175, 615 

Thraustochytriales 73–74 

Thraustochytrium 73–74 

Thraustotheca clavata 91, 92 

thrush 279 

Tilletia 647; secondary sporidium 648, 

649; systemic infection 648 

Tilletia caries 647–648; teliospores 647; 

teliospore germination 648; 

trimethylamine 647 

Tilletia controversa 648 

Tilletia indica 649 

Tilletiopsis 412 

tobacco, blue mould 116, 119; 

necrosis virus (TNV) 148 

Tolypocladium inflatum 349, 363, 364; 

see cyclosporin 

tomato, anthracnose 388; Fusarium 

wilt 347; late blight 115; leaf mould 

483 

Totivirus 273 

trama 524 

Trametes hirsuta 529 

Trametes (Coriolus) versicolor 499, 

560–562, 563, Pl. 10; vegetative 

incompatibility 510, 511, 518 

transgenic plants 433 

transposable elements 345, 439, 653 

Tranzschel’s Law 614 

Trebouxia (lichen photobiont) 446, 

448, 450, 452, 455 

Tremella 605–608; basidiospore 

germination patterns 605, 608; 

haustorial branches 605, 606 

Tremella encephala 605, 607 

Tremella foliacea 607 

Tremella frondosa 607, 608 

Tremella fuciformis 607; 

exopolysaccharides 608 

Tremella globospora 605, 606 

Tremella mesenterica 605, Pl. 11; 

life cycle 607; mating 605; sex 

hormones 605 

Tremellales 604–608; parenthesome 

604, 606; yeast stage 604 

tremelloid basidium 604, 606, 608 

tremerogen 605 

Trentepohlia (lichen photobiont) 446, 

452, 455 

tretic conidial development 31, 

232, 472 

triadimefon 410, 411 

triazole-type fungicides 293, 306, 410, 

411, 627; resistance 411 

Trichia floriforme 51, 52 

Trichiales (Myxomycota) 51 

Trichoderma 340; biological control 

342, 434, 551, 569, 596 

‘Trichoderma effect’ (on sexual 

reproduction in Phytophthora) 96, 

124 

Trichoderma harzianum 340, 342, 569 

Trichoderma reesii (teleom. Hypocrea 

jecorina) 339; cellulases 340 

Trichoderma stromaticum 551 

Trichoderma virens (teleom. Hypocrea 

virens) 340, 342 

Trichoderma viride (teleom. Hypocrea 

rufa) 340, 341 

Trichoglossum 443 

Trichoglossum hirsutum 443, 444 

trichogyne 330, 416 

Tricholoma 552 

Tricholoma gambosum 552 

Tricholoma matsutake 552; cultivation 

527 

Tricholoma sulphureum 552 

Trichomycetes 166, 222–225 

Trichophyton 293, 294–295 

Trichophyton mentagrophytes 294 

Trichophyton rubrum 294 

Trichophyton schoenleinii 294 

Trichophyton verrucosum 294, 295 

trichospore 223, 224 

Trichosporon 660 

trichothecenes; see T-2 toxin 

Trichurus 371 

Tricladiomyces malaysianum 689 

Tricladium splendens (teleom. 

Hymenoscyphus splendens) 232, 

685, 688 

tridemorph 410, 411 

trimethylamine 647, 649 

trimitic basidiocarp construction 518, 

519 

Trimorphomyces papilionaceus 594 

tripartite tubular hair (TTH) 24, 

68–69, 70 

Triphragmium ulmariae 629 

trisporic acid 174, 175 

trophocyst 185, 187 

truffles 414; see Elaphomyces, Endogone, 

Rhizopogon, Tuber, Terfezia 

truffle flies 424 

TTH; see tripartite tubular hair 

T-toxin 476, 477 

Tuber 423–427; ascospore 425; boar 

hormone 5a-androst-16-en-3a-ol 

424; dimethyl sulphide 424; 

ectomycorrhiza 424, 426; life cycle 

424–426; saprotrophic phase 426; 

yields 427 

Tuber aestivum 426 

Tuber albidum 426 

Tuber magnatum (Piedmont truffle) 426 

Tuber melanosporum (Périgord truffle) 

424–425, 426, 427; brûlé 426; 

inoculation of trees 427 

Tuber puberulum 425 

Tuber rufum 425 

Tubercularia state of Nectria cinnabarina 

231, 342, 344 

Tulasnellales 594; basidium 595 

Tulasnella 574 

Tumularia aquatica (teleom. Massarina 

aquatica) 685, 691, 693 

turbinate cells 142, 143 

turf-grass blight 72 

turgor pressure 7–8, 80, 83, 208; in 

ascospore discharge 242; in 

appressorium 381 

Typhula 501 

ubiquitin 272 

Umbelopsis 197 

Uncinocarpus 292 

Uncinula 401, 403 

Uncinula (Erysiphe) necator 390, 403, 

410 

uniseriate; see Aspergillus 

unitunicate; see ascus wall 

universal veil 520

840 INDEX 

Uredinales 609–635, Pl. 12; biotrophy 

616–618; control 627; cultivation 

on simple media 618; life cycle 610, 

611, 612–614; haustorium 615–616, 

617–618; host resistance 618–620; 

infection process 614–616; 

monokaryotic versus dikaryotic 

penetration and haustoria 614, 616; 

phylogeny 610; spore types 

611–613; systemic infections 630 

urediniomycete yeasts 659, 666–670; 

life cycle 667–668, 670; 

phylogeny 661, 666 

Urediniomycetes 609, Pl. 12; 

see Uredinales 

urediniospore 610, 612, 615, 623; 

adhesion pad 615; attachment 615 

uredinium 610, 612, 623, Pl. 12 

Urocystis 649–651 

Urocystis agropyri 649, 650 

Urocystis anemones 651; teliospore 


Urocystis tritici 649 

Uromyces 628, 630–631; infection 

processes monokaryotic versus 

dikaryotic 616 

Uromyces appendiculatus 614–615, 631; 

adhesion pad 615; teliospore 629; 

thigmotropism 615, 616 

Uromyces dactylidis 630 

Uromyces dianthi 630 

Uromyces ficariae 630 

Uromyces pisi 631 

Uromyces viciae-fabae 615–616, 631; 

haustorium 617 

Usnea florida Pl. 8 

usnic acid 452, 453, 455, 458 

ustilaginomycete smuts 636–652; 

control 651–652; intracellular 

hyphae 637; life-cycle 637, 638; 

mating system 637; mating-type 

loci 637; sheath 637, 642; systemic 

growth 643; teliospore 637, 639 

ustilaginomycete yeasts 670–672; 

see Malassezia 

Ustilaginomycetes 636; subclasses 

636; see Exobasidiales, 

Malasseziales, ustilaginomycetous 

smuts 

Ustilago 639–647; phylogeny 639; 

teliospore germination 640–641; 

teliospore surface 639, 640 

Ustilago avenae 637; basidium 489; 

teliospore germination 636 

Ustilago filiformis 639; teliospore 

germination 641, 642 

Ustilago hordei 639, 643; sheath 642; 

systemic growth 643 

Ustilago maydis 643–647, Pl. 12; 

cytoskeleton 646; dikaryon 

establishment 644, 645, 646; life 

cycle 638; mating system 605, 

644; mating type factors 508; 

killer toxins 646–647; pheromones 

644 

Ustilago nuda 643; teliospore 


Ustilago segetum 639 

Ustilago tritici 642, 643 

vaccines against fungi 291 

vacuoles 4, 5, 11, 12–13, 66, 76, 

273, 585; in basidium 

development 488, 489–490; in 

zoospore cleaveage 87 

valley fever 293 

VAM (vesicular-arbuscular 

mycorrhiza) 218–221; physiology 

221–222 

Varicosporium elodeae 688, 689 

variegatic acid 557, 585 

Vascellum 581 

vegetative incompatibility 53, 227, 

365; in Basidiomycota 510, 511; in 

Daldinia concentrica 334; in Physarum 

polycephalum 48, 53; inPodospora 

anserina 325–326; in Trametes 

versicolor 511, 562 

Venturia 478, 481 

Venturia inaequalis 478, 479; control of 

ascospore inoculum 478–479; 

fungicides 479, 632 

veratryl alcohol 530, 531, 532 

vertical resistance; see host resistance 

vertical transmission of inoculum 

357 

Verticillium balanoides, nematode 

infection process 684 

Verticillium lecanii 412 

vesicle, conidiophore 298, 302; 

sporangium 95, 98; sub-stomatal 

616; VAM 218, 220 

viability of propagules; see survival 

victorin C 476 

vines; see grape-vines 

viridin 339 

viruses, fungi as vectors 62, 147–148; 

see mycoviruses 

vitamin C 434 

Volucrispora 685 

volva 520 

Volvariella 545; life cycle 545 

Volvariella bombycina 545; cystidia 525; 

fruiting in the laboratory 545; 

secotioid form 578 

Volvariella speciosa 543 

Volvariella surrecta 543, 546 

Volvariella volvacea 545–546; 

cultivation 525 

vomitoxin 348 

vulpinic acid 452, 453 

watercress, crook-root disease 61, 63 

water-moulds 79 

weathering of rocks 447 

weight-lifting by Coprinus basidiocarps 

538 

wheat, black stem rust 620; brown 

leaf rust 627; common bunt 647; 

dwarf bunt 649; eyespot 439; glume 

blotch 462; Karnal bunt 649; 

leaf blotch 462, 481, 483; leaf 

stripe-smut 649; loose smut 642, 

643; stripe rust 627; tan-spot 478 

whiplash flagellum; see flagella 

white-rot (of wood) 333, 529, 530–532, 

541, 560, 573, 601, Pl. 10 

wilts 345, 346, 366, 369 

wind dispersal 399 

wine production 275–276 

witches’ brooms 251 

wood 528; degradation 527–532 

Woronin bodies 227, 228, 261, 287 

Xanthophyllomyces dendrorhous 

665–666, 667; astaxanthin 

production 665; basidium 667; 

life cycle 666 

Xanthoria 455 

Xanthoria parietina 455, 456, Pl. 8; mite 

dispersal 448 

xenospore 22 

xerocomic acid 585 

Xerocomus 557 

xerophilic fungi 286, 298, 305 

Xylaria 335 

Xylaria carpophila 333, 335 

Xylaria hypoxylon 231, 334, 335, 336 

Xylaria longipes 335, Pl. 5; apical 

apparatus 241, 242 

Xylaria polymorpha 335 

Xylariales 316, 332–336

INDEX 

841 

yeasts 3; see Archiascomycetes, black 

yeasts, Hemiascomycetes, Mucor 

rouxii, Tremellales 

zearalenone 348 

Zoopagales 200–202, 675 

Zoophthora 203 

zoospore 23, 24, 57; auxiliary and 

principal 76, 81, 83; Chytridiomycota 

129–130, 131, 146, 153, 154, 

155, 163; cyst 84, 87, 94; Hyphochytrium 

70; Labyrinthulomycota 73; 

Oomycota 76, 77, 95; in Phytophthora 

107–108; in Pythium 100; as vectors 

for viruses; see viruses, fungi as 

vectors 

Zostera; see eelgrass (Zostera) wasting 

Zygomycota 165–215, 216–225, Pl. 3; 

phylogeny 166 

zygophore 174 

Zygorhizidium affluens 142 

Zygorhizidium planktonicum 132, 133, 

142 

Zygorhynchus 182 

Zygorhynchus heterogamus 172, 182 

Zygorhynchus moelleri 173, 175, 182, 

183 

Zygorhynchus psychrophilus 182 

zygosporangium 173 

zygospore 28, 29, 165, 174, 177, 183, 

186, 200, 209; formation 176–177; 

investment 177; germination 

178–179

Introduction to Fungi, Third Edition

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