nmm sP

THE 

BRITISH SMUT FUNGI 

^ 

(USTILAGINALES) 

By 

G. C. AINSWORTH, B.Sc, PH.D. 

,\ 

DEPARTMENT OF BOTAUTT, 

UNIVERSITY COLLEGE, EXETER 

and 

KATHLEEN SAMPSON, M.Sc. 

UNIVERSITY COLLEGE OF WALES, ABERYSTWYTH 

U^ sP 

/ 

THE COMMONWEALTH MYCOLOGICAL INSTITUTE 

KEW, SURREY 

1950 

nmm 

ttetUffj*

^ 

The Commonwealth Mycological Institute 

is a part of the 

Gommonweahh Agricultural Bureaux 

Organization 

PBINTBD IN aKBAJ BSITAIST

FOREWORD 

THIS volume was started whilst Dr. Ainsworth was on the staff of the 

Commonwealth Mycological Institute. In order to obtain a satisfactory 

basis for the identification of tropical smuts it has been found necessary, 

in this as in other groups, to become well acquainted with the species 

present in this country. The results of his studies are incorporated in this 

work, for the systematic part of which he is chiefly responsible. Miss 

Sampson, formerly Senior Lecturer in Agricultural Botany, University 

College of Wales, Aberystwyth, whose lifelong study of the Ustilaginales 

has given her a wide knowledge of these fungi, especially their biology, 

has collaborated with Dr. Ainsworth to produce this very valuable contribution 

to mycological Uterature. 

The authors have been conservative in their nomenclature, in my 

opinion quite rightly, and no new species and only three new combinations 

are proposed. Following the lead given by Dr. G. H. Cunningham in 1924 

and since followed by others, the authors regard the loose smut of wheat 

(Ostilago tritici) as specifically identical with the earher-named loose smut 

of barley {U. nvda) and on morphological grounds alone it is difficult to 

see how a change of name of the latter fungus, so important to plant 

pathology, can be avoided. Furthermore, they follow Fischer in uniting 

the covered smuts of oats [U. kplleri) and barley {U. hordei) as one species 

{U. hordei). The Institute has undertaken to use the names of fungi 

recommended in the List of Common British Plant Diseases, and the names 

for these and a few other species discussed now need reconsideration by 

the authorities responsible for the list. Until their decision is known the 

names in current use in the Review of Applied Mycology are being retained 

here. 

The compilation of this monograph focuses attention on the gaps in our 

knowledge of the germination of many of the species and it is hoped that 

its publication will stimulate interest in this group of fungi, which is of 

such great importance to agriculture. 

S. P. WILTSHIRE 

Director 

COMMONWEALTH MYCOLOGICAI, INSTITUTE, 

KEW, SUKBEY 

23 December 1948

PREFACE 

THE last general account of the British Smuts based on an examination of 

specimens and on observations on their biology is that by Plowright in his 

Monograph of the British Uredineae and Vstilagineae, 1889. Since the 

publication of that book many more species have been recorded for the 

country and the outlook on the biology of the Ustilaginales has changed. 

This work is an attempt to meet the need for a new systematic treatment 

of the Smuts of this country and to provide a general account of the 

Order. 

The recent census of the Ustilaginales recorded for Britain {Trans. Brit, 

mycol. Sac, xxiv, pp. 294^311, 1940) was the first step in bringing up to 

date the knowledge of the British Smuts. The present work may be 

regarded as the second step. All the British collections in the national 

herbaria have been examined, published records have been scrutinized,, 

and descriptions based on British material have been prepared. The 

addition of notes on spore germination, infection of the host, and racial 

specialization to the descriptions of morphology will, the authors hope, 

encourage much-needed work on the biology of these fungi. 

We are indebted to the Keeper of the Herbarium of the Royal Botanifc 

Gardens, Kew, for permission to examine material in the Kew Herbarium 

and to the Keeper of Botany at the British Museum (Natural History) for 

access to the collection of British Smuts in his care, while Mr. W. C. Moore 

very kindly placed the Smut collections in the Herbarium of the Ministry 

of Agriculture's Plant Pathology Laboratory, Harpenden, at our disposal. 

Acknowledgement is also due to Professor W. Stiles for the loan of specimens 

from the Plowright and Grove Herbaria at the University of Birmingham. 

Much useful material was received from Mr. E. A. Ellis whose 

collection of East Anglian Smuts provided a number of interesting records. 

We should also like to thank Dr. R. W. G. Dennis, Dr. Malcolm Wilson, 

Mr. W. G. Bramley, and Dr. P. O'Connor for specimens and to record our 

gratitude to the late Dr. Alexander Smith for material and information. 

Acknowledgement is. made to Dr. J. H. Western and the Cambridge 

University Press for Plate 1, Figs. 1, 3, and 5; to Mr. D. E. Green and the 

Royal Horticultural Society for Plate 2, Fig. 4; to the Plant Pathology 

Laboratory, Harpenden, for Plate 1, Fig. 2, and Plate 2, Fig. 3; and to 

Dr. H. L. White and the Experimental and Research Station, Cheshunt, 

for Plate II, Fig. 2. Grateful thanks are given to Frances H. Ainsworth 

for making the large number of tracings from which the text-figures 

illustrating spore germination were selected.

6 PBEFACE 

We also acknowledge the bibHographical assistance of Miss G. M. Roseveare 

of the Commonwealth Bureau of Pastures and Forage Crops, 

Aberystwyth, the kindness of Mr. C. E. JEubbard of the Kew Herbarium 

for his help with the identification and nomenclature of grasses, and the 

similar assistance with sedges from Mr. E. Nelmes'of the same institution.. 

Finally, we must record our thanks to Dr. S. P. Wiltshire for the interest, 

he has maintained in this project. 

19 November 1948 

G. C. AINSWORTH 

University College, Exeter 

KATHLEEN SAMPSON 

Malmsmead, Lacey Green, Aylesbury, Bucks.

PREFACE 

INTRODUCTION . 

Eoonomic importance . 

Smut diseases in Britain 

CONTENTS 

BIOLOGY. . . . . \ 

Entrance and invasion of the host 

Formation of the chlamydospotes 

Germination of the chlamydospores 

Development of sporidia on the host 

Growth in culture 

CYTOLOGY 

GENETICS 

Incompatibility 

Gametophyte in culture 

Spore and soral characters 

Germination of hybrid spores 

Pathogenicity . 

Mutation 

TECHNIQUE 

Collection and examination of herbarium material 

Harvesting, storage, and germination of chlamydospores 

Media for growth in culture 

Preparation of monosporidial cultures . 

Tests for the compatibility of monosporidial lines 

Infection of the host . 

Control 

Fixatives 

Stains . 

CLASSIFICATION 

THE BRITISH SMUT FUNGI 

Ustilaginales 

Key to genera 

Ustilaginaceae 

Tilletiaceae 

Graphiolaceae 

Doubtful and excluded species 

REFERENCES 

INDEX . 

9 

10 

10 

13 

13 

15 

17 

21 

24 

27 

29 

29 

30 

32 

34/ 

35 

35 ^ 

39 

39 

40 

41 

41 

42 

43 

46 

48 

49 

51 

53 

53 

54 • 

54 

81 

111 

112 

113 

133

INTRODUCTION 

THE smut fungi, which are represented in Britain by seventy-four species, are 

nearly all parasites of flowering plants. They inhabit stems, leaves, and floral 

organs and are most easily recognized in the fruiting condition, when they 

produce a sorus of spores, which are, in the mass, usually dark in colour and 

often powdery. The sorus may be naked or covered by a membrane of fungal 

origin; it may consist of spores only or be traversed by a columella of sterile 

mycelium or by threads of host tissue. The spores (chlamydospores) are onecelled 

and thick-walled. They are single or united in balls, which may contain 

both fertile and sterile cells. The wall of the spore is smooth or ornamented in 

various ways. Rarely the spores carry hyaline appendage, but they are always 

without stalks and arise from a closely septate mycelium which is generally used 

up completely in spore formation. 

The chlamydospore, though not the only unit of dispersal, is certainly the 

most important means of dissemination in many smuts. In some species germination 

may occur while the spores are still embedded in the host tissue; in others, 

spores, ripe for dispersal, are not necessarily ripe for germination and time must 

elapse before this process begins. Mature chlamydospores in certain species of 

economic importance are known to remain viable for a pericfd of several years. 

Those who have studied the early development of a soruti agree in finding, two 

nuclei in the very young chlamydospore. These fuse and it is generally accepted 

that the mature chlamydospore contains a single diploid nucleus. Meiosis occurs 

in the promycelium, the germ-tube produced when a ripe chlamydospore starts 

growth. Haploid nuclei pass into the sporidia or branches arising from the 

promycelium, and become paired when the appropriate gametic elements unite. 

Fusion of nuclei is, however, delayed until the last stages of sporogenesis. It 

seems probable, therefore, that the parasitic mycehum of many smut fungi is 

dicaryophytic and that the gametophytic phase in nature is often very short, 

sometimes limited to one cell. Entyloma and alUed genera are exceptional since 

they produce haploid sporidia freely on the living host. 

Smuts, as a rule, develop easily on culture media, and studies have been made 

of their saprophjîc growth and the segregation of gametophytic characters. 

Most of the species so far investigated are heterothaUic, carrying one or more 

pairs of allelomorphic genes, which govern the fusion of haplonts. While progress 

has been made in genetics, our knowledge of the cytology of smuts is scant. 

The Ustilaginales is a compact and clearly defined group embracing the 

Ustilaginaceae and the TiLletiaceae together with a family of somewhat uncertain 

afiBnities, the Graphiolaceae. The Graphiolaceae comprises three species 

parasitic on the leaves of'palms. It is represented in this country by the exotic 

OrapJiiola phoenicis in which the chlamydospores, united in chains within a 

compact fructification, bud in situ to form sporidia which are dispersed. The 

other two famiUes are differentiated by the morphology of the promyceHum 

arid its branches. In the Ustilaginaceae the germ-tube soon becomes septate and 

buds laterally; in the TUletiaceae it remains at least for a time non-septate and 

produces a terminal whorl of branches. Whether lateral or terminal, these 

branches are the gametic elements which ultimately fuse in pairs. In both

10 THE BRITISH SMUT FUNGI 

families copulation can occur between cells of the promycelium or between 

sporidia abstricted from it. In a smut like TJstilago avenae the sporidia bud 

repeatedly on a suitable medium and give rise to a gelatinous-looking colony 

with superficial configurations and colours which remain constant for a particular 

monosporidial line. In certain members of the Tilletiaceae aerial sporidia, 

which are discharged with a droplet of water as in. Hymenomycetes, develop on 

the host and in culture. 

The subdivision into genera, which follows similar lines in both the UstUaginaceae 

and the Tilletiaceae, is based on the nature of the sorus and the aggregation 

of the spores. The ornamentation and the size of the spores and the size 

and covering of the sorus are characters mainly used to separate species. A 

number of species include races which differ only in their host relationships, and 

some of these have been given specific rank. The authors hold the view that it 

is best to restrict the use of Latin binomials to biotypes which differ morphologically 

and to designate physiologic races in some other way. 

ECONOMIC IMPOETANCB 

The "Dstilaginales is a group of great economic importance. It includes fungi 

pathogenic for many crop plants of both temperate and tropical regions. Cereal 

crops in all countries are particularly liable to suffer heavy losses from smuts. 

Wheat, barley, oats, rye, maize, sorghum, rice, and millet are each susceptible 

to one or more species, and there is a very extensive literature on methods 

designed for controlling the smut diseases of these plants. Sugar-cane smut and 

onion smut are also major diseases, while among those of less importance are the 

smut diseases of certain fodder grasses and of various ornamental plants. 

No smut is pathogenic for man or animals, although there are reports from 

North America of air-borne spores of cereal smuts causing respiratory allergy 

in man (Wittich & Stakman, 1937; Harris, 1939 a, 1939 b). There are also reports 

from the Argentine of sheep and horses being poisoned by eating grass infected 

by Ustilago bullata (Marchionatto, 1930), and in Yugoslavia a disorder in children 

known as ' ustilaginism' has been attributed to poisoning by V. maydis (see 

Mayerhofer & Dragi§ic, 1938). The toxic effect of V. maydis was studied by 

Hunt & Thompson (1938), but the active principle could not be identified. 

SMUT DISEASES IN BEITAIN 

Cereals. Bunt of wheat (Tilletia caries) was known to the Romans (for an 

interesting historical survey, see Woolman & Humphrey, 1924) and has long 

been recognized in this country. An early reference to the disease is that by 

Jethro TuU in his Horse-hoeing Husbandry, 1733, which includes a chapter ' Of 

Smuttiness': an account of wheat bunt of particular interest for its recommendation 

of seed treatment as a control measure. Steeping the seed in brine is advocated, 

a 'cure' which is stated to have been discovered accidentally about 

seventy years before, when a shipload of wheat was sunk near Bristol one 

autumn, and at the following harvest all the wheat in England happened to be 

smutty except the produce of wheat salvaged from this wreck. 

During recent years bad attacks of bunt have been few, although in England 

and Wales alone the disease is still responsible for the loss or spoilage of thousands

INTRODUCTION H 

of bushels of wheat each year (Moore, 1945). Bunt was more common after the 

1914-18 War, probably due to the shortage of reliable seed, but since then iheve 

has been a steady decline. The proportion of bunted samples in the wheat 

examined by the Official Seed Testing Station at Cambridge was 33 per cent, in 

1921-2, ihe peak year during the past quarter of a century, from which it fell to 

5-1 per cent, in 1932-3, and to 1-2 per cent, in 1940-1 (Moore, 1943), a fall which 

must, at least in.part, be attributed to the more general use of seed dressed with 

more efficient fungicides. 

Rye is occasionally attacked by bunt and by the stripe smut of rye {Urocystis 

occulta); see Moore (1948). It is interesting to note that T.foetida, a smut very 

closely allied to T. caries and a frequent cause of wheat bunt both in North 

America and in central Europe, has never been found in this country. Flag smut 

of wheat {U. agropyri, often as U.tritici), also, is unrecorded for Britain although 

a damaging disease in Australia, the United States, and other parts of the world, 

including southern Europe. Wheat in these islands is, however, not uncommonly 

affected by loose smut caused by Ustilago nuda (or 17. tritici, as the physiologic 

race of this species which attacks wheat is usually called). In this smut floral 

infection takes place and the resultmg seed has mycelium within the tissues, so 

that treatment of the surface of the seed does not eradicate the infection. The 

disease is not of great importance in Great Britain, but whenever healthy seed 

is unobtainable, infected seed may be subjected to the hot-water treatment. 

Barley is subject to infection by a different physiologic race of the same fungus, 

but, again, loose smut of barley is usually not serious. During the period 

1922-31 it was recorded in 6-9 to 15-5 per cent, of the samples examined by the 

Official Seed Testing Station, but in only 1-3 to 7-1 per cent, during the succeeding 

decade (Moore, 1943). 

Barley is also subject to a covered smut {Ustilago hordei), the spores of which 

contaminate the seed, and so are vulnerable to seed treatment with a suitable 

fungicide. Oats are attacked by both covered and loose smuts, caused by a 

physiologic race of U. hordei (frequently distinguished as U. kolleri) and by 

U. avenae, respectively, but, in routine disease surveys, these two diseases are 

not usually distinguished. Loose smut is the commoner of the two, but covered 

smut is not uncommon on strigosa varieties in mid-Wales. Both diseases may 

be prevented by seed treatment. 

Grasses. Grasses are often found infected by smuts, and Sampson & Western 

(1941) surveyed their occurrence "on grasses of agricultural importance. Apart 

from occasional spoilage of hay crops, such as occurred in Northamptonshire, 

Lancashire, and Leicestershire in 1936 (Moore, 1943), the smuts are, economically, 

diseases of secondary importance on grasses in this country. 

Onion. Onion smut (Urocystis cepulae) was first recorded in England in 1918 

(Cotton, 1919), when irtvestigation showed that the disease had probably 

occurred in onions and leeks near Edinburgh in 1912. It occurs most frequently 

in the northern counties, but in 1942 it appeared in the Evesham area of 

Worcestershire. The disease is a serious one and is scheduled by the Ministry 

of Agriculture under the Destructive Insect and Pests Acts. Its presence on 

any land or plants must be notified to the Ministry or to one of the Ministry's 

inspectors. Up to the end of 1942 there had been eighty-seven records from 

eleven counties (see Moore (1948), p. 51, for distribution map).


Ornamental plants. The smuts which affect ornamental plants are usually of 

minor importance. Dahlia smut (Entyloma caleTidulae f. dahliae), which is 

widely distributed, is occasionally sufficiently severe to warrant treatment with 

Bordeaux mixture, and anther smut {Ustilago violacea) at times does damage to 

carnations under glass (White, 1936). Other smiit diseases, which on occasion 

attract attention, are those of cultivated violets (Vrocystis violae), gladioH 

(U. gladiolicola), and calendula {Entyloma calendulas).

FIG. 1. Vstilago avenae on Arrhenatherum 

elatius. 

I I 

FIG. 3. Vstilago striiformis 

on Holcus lanatus. 

FIG. 2. Vstilago nuda on wheat. 

\ . 

FIG. 4. Vstilago grandis on FiG. 5. Vstilago hypodytes on 

Phragmites communis. Elymus arenarius. 

\

BIOLOGY 

ENTRANCE AND INVASION OF THE HOST 

IT seems to be generally true that smut fungi can enter the host only at points 

where the tissue is relatively young. Varying with the species, infection occurs 

through the plumule on emergence from the seed (Tilletia caries, Ustilago avenae, 

and others), axillary buds {U. maydis), immature leaves {Entylomaficariae), or 

young ovaries (Ustilago nuda). As tissues age, they become more resistant to 

attack and finally attain immunity, even in susceptible varieties. In oats, for 

example, infection by smut rarely occurs after the shoot is more than one iach 

in length, and onion seedlings escape attack if penetration does not occur before 

the first leaf emerges from the cotyledon (Walker & Jones, 1921; Anderson, 

1921). Evans (1933) studied the development of Urocystis cepulae mycelium in 

the cotyledon, showing how its advance slowed down as the tissue approached 

maturity, until finally the invading hyphae failed to pass beyond the sub-cuticular 

layer of the outer epidermal wall. The cotyledons of onions at a critical 

age showed minute sub-cuticular vesicles, consisting of fungus mycelium which 

had pierced the cuticle and digested a portion of the cell wall but had not succeeded 

in. entering the cell and establishing an active infection centre. 

A similar response to invasion is made when highly resistant varieties of 

wheat, oats, and rye are attacked by certain races of smuts. Penetration of the 

outer wall occurs but growth does not extend beyond the epidermal cell (Woolman, 

1930; Western, 1936b; Ling, 1940b). In less resistant varieties the parasite 

progresses for a time, even reaching the stele of the host, but fails to enter the 

flower primordia and does not sporulate (Sampson, 1933). This so-called 'latent 

infection' may aifect adversely the growth and yield of wheat varieties like 

Heils Dickkopf which have been regarded as immune from bunt (Zade, 1931). 

In susceptible varieties of our common cereals, once the smut has passed the 

barrier of the epidermal wall, it usually grows from cell to cell without causing 

necrosis or any apparent disturbance to the host. Seedlings infected by bunt can 

sometimes be recognized by their distorted growth and mottled foUage (Churchward, 

1934; Johnston & Lefebre, 1939; Churchward, 1940), and it is not rare to 

find infected seedlings sensitive to winter conditions, but, normally, no external 

symptoms distinguish seedlings that carry the myceUum of smut fungi. 

The growth of the smut mycehum is, at first, both intra- and intercellular, but, 

after a time, more and more intercellular mycelium is found. SpeciaUzed 

haustoria (Fig. 20 a), common in some species, are not formed by the cereal 

smuts, but short hyphae can sometimes be seen penetrating the cells. Infected 

seedlings of susceptible varieties carry mycehum in the mesocotyl, coleoptUe, 

young leaves, and finally in the growing-point itself (Kolk, 1930, Sampson, 1933). 

Once this is reached, the fungri rarely fails to develop spores since changes in 

temperature, water supply, manuring, and Ught have very little restraining 

efi'ect (Sampson & Western, 1938; Reed, 1938). 

Cereal smuts, which fructify in the inflorescence, penetrate the leaves of adult 

plants only to a shght extent, but, where conditions especially favour the fungus, 

sori may develop in lines along the flag leaf. Even Tilletia caries and T. foetida 

wUl sometimes form ehlamydospores in wart-like galls on leaves (Plor, 1932).

^^ THE BBITISH SMUT FUNGI 

Young healthy mycelium is full of granular protoplasm with an affinity for 

stains, such as gentian violet, saffranin, and fast green, but in older tissue 

portions of the mycelium may be empty and coUapsed, sometimes having the 

form of a long filiform strand, sometimes thick with an enveloping sheath 

(Kolk, 1930; Woolman, 1930; Western, 1936 b; Evans, 1933). It is not always 

easy to find mycehum in older plants, but it does not disappear entirely, and 

sometimes sporulation occurs in late tillers induced to develop by removing 

those first formed and smut-free. 

Some smuts which attack perennial plants are systemic, hibernating in underground 

stems or bulbs and reappearing each year to form spores in the appropriate 

part of the host. Mycelium of Ustilago vaillantii, for example, can be 

found at the base of bulbs of the grape hyacinth, where the mycelium forms 

botryform haustoria, consisting of a cluster of short inflated branches. Each 

year mycelium passes into the young inflorescence and sporulates in the anthers, 

replacing the pale yellow pollen by dark chlamydospores but having otherwise 

little effect on the host (Massee, 1914). De Bary recorded a plant of Saponaria 

officinalis in the Freiburg Botanic Garden, which was for ten successive years 

affected with U. violacea, and Plowright refers to plants in his garden at King's 

Lynn of Golchicum autumnale, Agropyron repens, and Arrhenatherum elatius 

which carried their respective smuts for at least six years (Plowright, 1889). 

Among the perennial economic grasses infected by a smut mention may be 

made of timothy and smooth-stalked meadow grass, which are sometimes 

severely injured by stripe smut (Davis, 1926; Kreitlow & Myers, 1944). ^ 

In some smut diseases the area of infection is localized, the fungus sporulating 

not far from the seat of invasion. U. maydis, for example, which attacks 

axiUary buds or young floral organs, produces in a comparatively short time 

small or large swellings containing spores. Each gall or ball usually represents 

a separate infection. Species of Entyloma, which attack the leaves of many 

different plants, form angular Ibsions, the chlamydospores developing round 

each infection centre in a typical leaf spot, except where very heavy infection 

destroys the whole lamina. 

Before emergence of the ear it is not possible to distinguish with certainty 

in the field plants of wheat, oats, or barley systemicly infected by smuts, but 

careful records and measurements have shown that the growth of the host is 

affected in several ways. Oat plants carrying smut produce extra tUlers, while 

growth in height is often considerably reduced (Talieff & Grigorovitch, 1923; 

Sampson, 1929; Welsh, 1932). Even smut-resistant varieties may be adversely 

affected in growth and vigour (Hubbard & Stanton, 1934; Stevens, 1936). 

Bunt of wheat may either promote or retard tillering but it almost" invariably 

reduces height (Zade, 1931; Lang, 1917a; Mourashkinsky, 1925; Viennot- 

Bourgin, 1937), the magnitude of the effect depending on the variety and the 

physiologic race of the fungus (Holton, 1935; Aamodt e( aL, 1936; Schlehuber, 

1937). The effect of bunt on the form of the wheat ear also varies. A broadawned 

ear like that of American Club (Triticnim compactum), if bunted, is 

abnormally long and awnless; a lax ear, like that of Hen Gymro (T. vulgare), 

when attacked by bunt is shorter and the awns are also reduced in length 

(Sampson & Davies, 1927; DiUon Weston, 1929). Wheat plants infected by 

U. nuda are said to be markedly stunted and their dry weight at flowering time

FIG. 1. Melanotaenium FIG. 2. Ustilago violalamii 

on Lamiuni alhuni. cea on carnation. Longitudinal 

section of infected 

flower. 

..-'^- . ^ 

^./ 

FIG. 4. Entyloma calendulae f. dahliae 

dahlia leaflet. 

^ 

/ 

FIG. 3. Vrocystis cepulae on 

onion. 

FIG. 5. Entyloma ficariae on 

Ranunculus ficariae. Under-gnrface 

of leaf showing sporidia.

BIOLOGY 15 

less than the normal, in spite of an increased rate of assimilation (KoursanofF, 

1926). The dwarfing effect of a smut on a grass is well illustrated by the fact that 

plants of Agrostis tenuis infected by Tilletia decipiens are so stunted that they 

were described as a distinct species (see p. 86). 

U. hypodytes, which attacks several forage grasses, causes sterility, long leafy 

shoots developing in place of normal inflorescences. The morphology and 

anatomy of such diseased shoots in Elymus arenarius and the distribution of 

mycelium have been described by Viennot-Bourgin (1937) and by Bond (1940). 

A peculiar type of proliferation, whereby individual flowers are replaced by 

leaves, stems, and rudimentary panicles, is often seen in sorghum infected by 

head smut, Sphacelotheca reiliana (Potter, 1914). Finger-like galls develop from 

the axillary buds of Panicum antidotale attacked by Tilletia tumefaciens Sydow 

(Mundkur, 1944), and tuberous bodies up to an inch in length are formed 

from underground shoots of Lamium album infected by Melanotaenium lamii 

(Plate II, Fig. 1). 

FORMATION OF THE CHLAMYDOSPOEES ' 

The formation of a sorus is preceded by the massing of mycehum in that part 

of the plant where spores are destined to develop. The details of sporogenesis 

appear to differ with the species. Comparatively few have been examined in 

detail, none in recent years. A few types have been selected here for individual 

consideration. 

USTrLAGiNACBAE. Lutman (1910) described the development of spores in the 

oat race of Ustilago hordei as follows: ' The first indication of spore formation 

in the fungal hyphae is a much branched and contorted condition of some of the 

hyphal tips. These are at the same time inter-cellular and this knotting up of 

the hyphal tips frequently occurs at the angles of the host cells where they may 

be wedged apart considerably. These swollen ends of the hyphae are multinucleated, 

each one containing ten to fifteen nuclei. The cell walls now begin 

to gelatinize from the inside, a clear zone appearing between the protoplasm and 

the darker staining wall. The nests or pustules of hyphae continue to grow and 

swell and their waUs become so completely gelatinized at this stage that all that 

seems to be present is a tangle of hyphae of irregular shape and varying diameter, 

without walls, and lying in a clear matrix. At the same time, the walls 

of the host cells immediately adjacent lose the capacity to take up the stain, 

the gelatinization of the fungal walls having apparently extended to the walls 

of the host cells also.' The changes in the ceU wall, referred to by Lutman and 

by others as gelatinization, appear to accompany sporogenesis in several 

members of the Ustilaginaceae. The chemical changes involved have not been 

studied. A visible swelling is associated with a loss of staining capacity, with 

the result that the protoplasts appear in sections as deeply stained masses 

separated by a clear space, the gelatinized wall. The development of spines 

within the gelatinous matrix has been studied recently by Hutchins & Lutman 

(1938) (see p. 50). 

Lutman was unable to distinguish the nuclei with certainty in U. hordei, but 

he suggests that the small, somewhat angular segments of hyphae finally 

separated are binucleate. They become round, develop a thick waU, and form

16 


the chlamydospores, which are uninucleate when mature. The process was 

found to be similar in V. maydis. 

Several workers, who have studied the early stages of sporogenesis in species 

of Ustilago, refer to a tendency for spores to develop in chains (Schroeter, 1877; 

Fischer von Waldheim, 1869). Massee (1914), working with U. vaillantii, states 

that the vegetative mycelium is broken up by transverse walls into uninucleate 

cuboid segments, which become binucleate by the dehquescence and disappearance 

of alternate septa. Sartoris (1924) has described the formation of spores in 

JJ. heufleri. Mycelium in the host, Erythronium americanum, is always intercellular, 

spreading but a little way from the point of infection. The hj^hae 

cause the separation and disintegration of the host cells, finally forming a 

pustule, which segments to give mature chlamydospores in seven to ten days. 

The mycelium, 3 to 5 /u. in diameter, is said to be multinucleate with the nuclei 

nearly always associated in loose pairs. As segmentation proceeds, two nuclei 

are left in each cell, which rounds off and becomes free. The wall thickens and 

the surface becomes gelatinized which makes it difficult to follow the fate of the 

nuclei. In a few cases binucleate spores were seen, but the probability is that 

fusion usually takes place as the wall thickens and develops the two distinct 

layers, which are characteristic of the mature chlamydospore. 

The development of spores in U. vuijckii, a species inhabiting the capsules of 

Luzula spp., presents some interesting features. The cells are connected by 

clamp-connexions, apparently similar to those found in many Hymenomycetes, 

and the spores develop in chains, alternating with clamps which bear a strong 

resemblance to antheridia (Liro, 1924). 

THiLBTiACBAB. In Tilletia and in Entyloma the chlamydospores arise at the 

ends of short side-branches (Fischer von Waldheim, 1869). Lutman (1910) 

described the process in E. nympheae as follows: 'A short lateral branch, dense 

with cytoplasm and binucleate, is put out from one of the larger hyphae. As it 

grows in length and thickness, the two nuclei, which at first lie parallel with the 

long axis of the cell, come to be side by side. The stalk of the spore becomes 

vacuolate, and finally a large vacuole seems to cut off the hypha bearing it and 

the wall develops .behind. The wall of the spore thickens and becomes covered 

with minute spines. The axis becomes apiculate by the thickening of the end 

wall and a large vacuole develops and pushes the nucleus to one side.' 

Several writers have described the spiral coiling of hyphae which initiates 

spore formation in Vrocystis (Kiihn, 1858; De Bary, 1866; Wolif, 1873; Winter, 

1881). Anderson (1921) studied sporogenesis in U. cepuJae. The onset of spore 

formation is indicated by the massing of mycelium between the cells. Instead 

of growing in long, straight, slender strands, the myceUum is branched, twisted, 

and interwoven into dense tangles, which push the cells apart and increase the 

areas of intercellular space, within which spores are subsequently formed. The 

hyphae become highly vacuolated and the protoplasm stains deeply. The spore 

arises as a lateral or terminal branch which curves back on itself in the form of a 

crozier. Protuberances mark the origin of branches which ultimately form the 

sterile cortical cells. The central fertUe cell appears to be the enlarged terminal 

cell of the crozier, though it is not certain that this is always its origin. As the 

fertile cell enlarges, the surrounding hyphae become tightly pressed against it

BIOLOGy 17 

and united with it, finally breaking up into separate elements, which appear as 

scattered, conical cells with flat bases firmly attached to the surface of the 

central cell. There appearsto be no gelatinization of the walls as in the Ustilaginaceae. 

At maturity the fertile cells contain a single nucleus, 3 to 4 /x in diameter 

with a prominent, deeply staining nucleolus 0-6 ft in diameter. A single 

small nucleus (about 0-6 (i) is found in each accessory cell. The corresponding 

ceUs are without nuclei in U. violae (Dangeard, 1894 a), and Blizzard (1926) 

records the disappearance of nuclei in the sterile cells of U. cepulae. 

In U. occulta the cells of the vegetative hyphae are for the most part binucleate. 

During sporogenesis some of the cells enlarge and their nuclei soon fuse, so that 

they are almost uniformly uninucleate by the time they can be recognized as 

spores. At this stage the nucleus is relatively large and a nucleolus is visible. 

The cells of those hyphae, which envelop the spore initial and form, the 

sterile cells, remain for a time binucleate but ultimately their nuclei disappear 

(Stakman, Cassell, & Moore, 1934). 

In Doassansia deformans the baU of spores begins as a tangled mass of hyphae 

in one of the intercellular spaces of hypertrophied host tissue. At this stage the 

cytoplasm is very dense, and, in all ceUs where nuclei can be seen clearly, they 

are in pairs. At first all the cells are ahke, but those inside soon begin to lose 

their contents and become transparent. The outer cells divide and contribute 

to the sterile cells in the centre. Finally, in the nearly mature spore ball the 

external cells with dense cytoplasm contain two nuclei in various stages of 

fusion. A felted layer of hyphae surrounds the mature ball (Lutman, 1910). 

GEAPHIOLACEAB. GrapMola phoenicis, which grows on the fronds of the date 

palm, has been investigated by KilHan (1924). The vegetative myceUum and the 

young fructifications are formed of uninucleate cells. Those at the base of the 

central plectenchyma give rise to a growing tissue composed of elongated cells 

containing several dicaryons. Finally, these form a block of ceUs, each with two 

nuclei which ultimately fuse. These cells, which correspond to chlamydospores, 

are not themselves disseminated. They germinate in situ by budding off uninucleate 

sporidia which are dispersed through an opening at the top of the 

fructification. 

GERMINATION O? THS: CHLAMYDOSPOEES 

The rest period. The chlamydospores of smuts, Uke seeds, vary widely in 

longevity. Spores of different species differ in their ability to germinate at the 

time of dissemination; some are capable of immediate growth, others must pass 

through an after-ripening period. Many workers have experienced difficulties 

in obtaining germination and have recorded the variable results given by different 

collections of the same species. This is not surprising when it is understood 

that germination depends, not only on the conditions under which a test is 

made, but also upon the age of the spores, the degree of maturity at the time 

of harvest, and the method of storage. Moreover, closely related species and 

physiologic races vary in the time of year when their spores germinate in nature. 

In the genera Entyloma and Doassansia, where the chlamydospores are held 

somewhat firmly by the host tissue, germination often occurs in situ as a continuous 

process of development which results in the dissemination of sporidia


and the infection of new leaves in the current season. That spores of the same 

species can also overwinter is shown by the infection of healthy shoots which 

occurs if old leaves carrying chlamydospores are Spread over the soil in spring. 

Setchell (1892) found that in D. alismatis most spores, from a mature sorus 

would germinate while still in the leaf, but dry leaves kept for nearly a year in 

the laboratory still contained some spores capable) of growth. In D. sagittariae 

and in D. occulta germination only occurs in spring, while in D. obscura it takes 

place in nature during October. 

Germination in situ is not the normal process for srhuts with dusty sori, 

which permit dissemination of spores, but in many species immediate germination 

is possible and spores are viable over a long period of time. In some species, 

notably the loose smut of wheat and barley which infects at flowering time, 

germination reaches a maximum during the summer, falls rapidly in the autumn, 

and is often negligible in collections only a year old. Stakman (1913), however, 

found no loss in viability after ten months' storage. Viability could perhaps be 

maintained even in this species over a longer period by controlled methods of 

harvesting and storage. Collections of spores of the loose smut of oats, which 

were allowed to mature in parchment bags, gave good germination results and 

remained viable for several years, while others harvested in the field soon after 

the emergence of the diseased panicle quickly lost their viability. In a certain 

collection of the covered smut of oats a maximum figure for germination was 

not obtained until some weeks after harvest, but once reached no falling off 

occurred for at least 2| years (Sampson, 1928). Davis (1924), working with 

Ustilago striiformis on Agroatis palustris, Phkum pratense, Poa pratensis, and 

Dactylis glomerata found that the spores required an after-ripening period of 

240 days when stored in the laboratory, or 265 days in. the field, before giving 

satisfactory germination. A similar result was obtained by Kreitlow (1943 a) 

working with the same smut on Poa, but one collection on Agrostis gave a germination 

of 50 to 75 per cent, without any period of storage. Fischer (1940) also 

obtained good germination of fresh spores in a closely related smut collected on 

Agropyron pauciflorum and Elymus glaucus. Kreitlow (1943 b) reduced the 

need for an after-ripening period by growing the host at 32° C. and by storing 

smutted leaves in a moist chamber at 35° C, but results by these methods may 

be erratic (Leach, Lowther, & Ryan, 1946). Exposure to chloroform fumes for 

one minute or to a 10 per cent, citric acid solution for five minutes shortened 

the after-ripening period by about one month (Davis, 1924). 

Forms of Urocystis anemones also differ in time of germination, since Kniep 

(1921) found that those collected from the creeping buttercup would grow at 

once and infect the young leaves, while spores taken from the wood anemone, 

a plant that quickly dies down, germinated only in spring, when the new growth 

was breaking through the soil. 

In view of such facts it is not surprising that collections from herbaria have 

given variable results. Fischer (1936 b) tested for germination material from 

the Plant Pathology Herbarium in the State College of Washington. Among 

387 specimens examined, 80 had viable spores. The most noteworthy examples 

of longevity were Tilletia foetida (25 years), T. caries (18 years), Ustilago hordei 

(23 years), U. bullata (10 years), U. avenae (13 years), Sphacelotheca sorghi 

(13 years), and Entyloma calendulae f. dahliae (10 years). Sobel (1933) recorded

BIOLOGY 19 

eermination in a collection of U. hordei from oats 13| years old and Noble (1934) 

germinated Urocystis tnitici after storage at low humidity for 10 years. Fischer 

suggests that, on the whole, members of the Tilletiaceae survive longer than the 

tJstUaginaceae, but the record for viabihty is that quoted by C. S. Wang (1936) 

for Ustilago crameri from Setaria italica which gave 1 per cent, germination 64 

years after harvest. Fischer's data from exsiccati confirm the importance of 

maturity as a factor in the potential life of a collection of spores. 

Environmental conditions, {a) Temperature. From experiments on the germination 

of chlamydospores of the more important economic species, it appears 

that growth will take place over a wide range of temperatures. In the species of 

Ustilago that attack the temperate cereals, the cardinal temperature points for 

germination fluctuate round the following values: minimum, 5° C.; optimum, 

22° C.; maximum, 30° C. (Herzberg, 1895; Bartholomew & Jones, 1923; Jones, 

1923 a; Novopokrovsky & Skaskin, 1925; Rump, 1926; Yen, 1937). Somewhat 

similar figures are given for U. striiformis (Davis, 1924). The corresponding 

points for certain smuts on maize and mUlet are about five or even ten degrees 

higher (Jones, 1923 b; Novopokrovsky & Skaskin, 1925; Lobik & Dahlstrem, 

1936; Yen, 1937). Christensen (1926) found that a high temperature (28° C.) 

favoured the infection of sorghum by head smut. 

Hahne (1926) gives these figures for the two bunts of wheat; minimum 4° C.; 

optimum, 18°-20° C.; maximum, 36° C. Speaking generally, a low temperature 

(about 15° C.) favours both germination of bunt spores and infection of the 

host (Lobik & Dahlstrem, 1936; Hungerford, 1922; Faris, 1924 c), but the 

optimum temperature for infection varies with the variety (Feucht, 1932). See 

also Tapke (1948). 

Walker & Wellman (1926) found the optimum temperature for germination 

of chlamydospores of Urocystis cepulae to lie between 13° and 22° C. Infection 

of the host occurred when the soil temperature was as low as 10° C. a point near 

the lower Umit for the germination of onion seed, but early sowing in the state 

of New York helped to control the disease by reason of the relatively low 

(8°-13° C.) temperature of the soil (Felix, 1939). 

Noble (1923) obtained germination of U. agropyri from wheat over a wide 

range of temperature, 5°-32° C, with an optimum at 18° to 24° C. Ling (1940 a) 

obtained similar results with U. occulta from rye, giving the optimum as 15° C, 

(For the effect of temperature on the mode of germination, see pp. 56, 66.) 

(6) Light. For most germination tests spores are placed in dark incubators 

and receive light only when examined. In general, Hght has not been regarded 

as a critical factor for the germination of chlamydospores. Tests in hght and 

darkness have often given similar results (Stakman, 1913; Lobik & Dahlstrem, 

1936; Ling, 1940a; Hulea, 1947). Hahne (1925) workmg with Tilletia and Kaiser 

(1936) with Entyloma obtained bettêr results in light. In the absence of daylight 

Kaiser (1936) stimulated germination by means of a fluorescent dye. 

Ultra-violet Hght retarded both germination and subsequent growth in Ustilago 

nmydis (Landen, 1939). 

(c) Media. See pages 24 and 40. 

The promycelium. The distinctive methods of germination in Ustilago and 

Tilletia were first recognized by Prevost in 1807. Tulasne (1847,1854) described 

and figured the process in several species of Ustilago, demonstrated the fusion of


sporidia, and described more fully the development of primary and secondary 

sporidia in T. caries. The grouping of genera into two families, the Ustila~ 

ginaceae and the Tilletiaoeae, has been foUowed Since Brefeld (1883, 1895) made 

his extensive studies on germination and growth in culture. In the nineteenth 

century Fischer von Waldheim (1869), Wolff (1873), de Bary (1874), Schroeter 

(1877), Woronin (1882), and others greatly increased our knowledge of germination 

and development in a number of species and genera. 

Thegerm-tubeput out by a chlamydospore in the Ustilaginales is typically au 

organ of limited growth, which either branches or cuts off hyaline, thin-walled 

sporidia in a characteristic manner. The term 'promycelium', originally used by 

de Bary (1853), has been widely adopted. Brefeld, linking the group with the 

higher Basidiomycetes, used the term 'hemibasidium'. The spores developing on 

the promycelium have been called promycelial spores (Plowright, 1889), conidia 

(Stevens, 1913), 'endconidia' (Paravicini, 1917), basidiospores (Gwynne 

Vaughan & Barnes, 1927), sporidia (Tulasne, 1854; Wolff, 1873; Woronin, 1882; 

Schroeter, 1877; de Bary, 1874). The adjectives primary, secondary, tertiary 

are used to indicate sequence of development. BuUer (1933), from his study of 

the interesting method of discharge of allantoid sporidia in T. carries, proposed 

changes in terminology in order to bring the group more into line with Hymenomycetes. 

It would be difficult to apply this logically throughout the Ustilaginales, 

and the writers prefer a simpler terminology which can be used for all 

species. While parallels can, admittedly, be drawn between the Ustilaginales 

and the Hymenomycetes, the smut fungi constitute a specialized and distinctive 

group with some unique characters. In contrast to the almost rigid standardization 

of the zygote (the chlamydospore), gametic production is both varied and 

plastic. Gametes are not recognized by form, but by behaviour, and copulation 

can occur in diverse ways. Moreover the gametophyte, Mid sometimes the 

dicaryophyte, multiply readily, both in nature and artificially. We have 

decided, therefore, to use the term 'sporidium' for all types of exogenous, thinwaUed 

spores, whether abstricted from the promycelium directly, from subsequent 

growth in culture, or from mycehum in the host. Sporidia may arise by 

budding, they may be slimed off the mycelium, or forcibly discharged from finely 

pointed sterigmata. Segments of the germ-tube which simulate sporidia but 

remain attached are referred to as promycehal branches. They have been called 

sporidia by some writers. 

The length of the promycelium varies with conditions of growth. The protoplasm 

streams towards the apex, and a cross-wall is formed, separating a densely 

protoplasmic, terminal cell from one containing only a thin layer of cytoplasm. 

The process may be repeated several times, with the result that long promyceHa 

even in Tilletia are septate in the older empty region near the chlamydospore 

(BuUer, 1933). 

The distinction between the Ustilaginaceae and the Tilletiaceae rests chiefly 

on the segmentation or branching of the promycelium, and ori. the position of 

sporidia. In the Ustilaginaceae the promycelium segments often into four, and 

branches or sporidia arise both terminally and laterally. In the Tilletiaceae the 

apex of the promycelium develops a crown of branches of uniform length, which 

are abstricted in some species but in others remain attached and elongate to' 

form mycelium. Details of development are far from uniform even within a

BIOLOGY 21 

genus, and the manner of growth can sometimes be altered by Regulating the 

environment. 

It is now generally accepted that meiosis normally occurs in both families at 

the onset of germination, and that segments of the promycelium and the firstformed 

sporidia are haploid. The dicaryophytic condition arises by the fusion of 

either promycelial cells, sporidia, or hyphae derived from them. Cultural conditions 

affect conjugation, and the absence of fusions in any one species may only 

indicate that the right conditions have not been found. It is clear, however, 

that fusions occur more readily in some species than in others, and that even 

physiologic races differ in this res'pect. 

DEVELOPMENT OF SPOBIDIA ON THE HOST 

In many smut diseases the parasite disappears from view after the initial 

infection, and only becomes visible to the eye when sori have developed and 

chlamydospores are exposed. In a few species, all members of the Tilletiaceae, 

the parasitic mycehum emerges through the stomata or between the epidermal 

cells and develops sporidia, sometimes in such profusion that infected organs 

are powdery with spores. 

The first clear account of this so-called 'conidial stage' was given by Woronin 

(1882). Plants of Trientalis europaea infected by Tuburcinia trientalis produce, 

after the winter rest, shoots which are white on the lower surface. Woronin 

described the sporidiophores, which grow in tufts through the stomata ^nd 

between the cells, as non-septate, thin, and bent in such a way that the terminal 

sporidia lie horizontally. The sporidia are pyriform, 11-15 (j,, hyahne, with 

finely granular protoplasm or a small vacuole. They fall easily and a second 

sporidium is produced, but the method of discharge is unknown. If sown on the 

surface of a leaf, the germ-tube enters and in 12 to 20 days black flecks, the 

young sori, appear. Fusions between sporidia were not observed and the number 

of their nuclei is unknown. 

Kiihn (1883) germinated the spores of a parasite oi Primula, which he named 

Paipalopsis irmischiae, but gave no details as to size or mode of origin of the 

spores. Schroeter (1887), listing this as a doubtful member of the Ustilaginales, 

stated that the parasite passes through the flowering stem into the floral organs, 

forming white powdery spore masses which often fill the whole corolla tube. 

The spore, which ha^ a smooth, COIOUEIQSS epispore, is spherical (3-6 /a), and 

germinates to form a thin germ-tuKe, the tip of which again forms sporidia. It 

is not clear if these Sporidia are like the spores from the corolla tube. Wilson 

(1915), recording the fungus from Kent, referred to large numbers of small 

unicellular spores present as meal-like masses in the open flower, glueing the 

stamens together and partially filling the base of the corolla tube. Viable pollen 

was, also present, and Wilson suggested that insects carry spores with poUen to 

healthy flowers, but inoculation experiments were unsuccessful. Fusions between 

sporidia were observed and, after the passage of one nucleus through the 

connecting bridge, the binucleate sporidium developed one or more germ-tubes. 

It is thought that members of the genus Thecaphora also form sporidia on stamens 

of the host, but no good account of this behaviour has been published (see p. 81, 

and Brett, 1940). 

Sporidia develop freely on the foliage of plants attacked by some species of

22 


Entyloma, and Winter (1881) suggested their connexion with the Ustilaginales. 

Schroeter (1887) described thread-hke sporidia preceding resting spores of 

Entyloma serotinum on Symphytum, and de Bary !(1884) recognized a conidial 

stage oi Entyloma ficariae. Marshall Ward (1887) described the development and 

germination of foliar sporidia of the same species on Ranunculus ficariae, and 

by infection experiments established their relationship to the Entyloma. He 

illustrated fully how the very deHcate, copiously branched, intercellular mycelium 

FIG. 1. Entyloma ficariae and E. calendnlae. Culture of E. ficariae (a), 20 hours on agar, 

derived from one allantoid sporidium, sliming off filiform sporidia. AUantoid sporidia of 

JB. ficariae (b) and E. calendulae from Calendula (c) and Dahlia (d) germinating on agar. 

Half-moon-shaped sporidia of E, calendulae from Calendula (e) and Dahlia (/) germinating 

on agar. g-j. Stages in clamp formation in mycelium of E. calendulae. The culture originated 

in one half-moon-shaped sporidium. 

in the leaf sends pencils of hyphae to the outside and produces uinumerable 

colourless sporidia from their free ends. He regarded as normal the club-shaped 

or long ovoid spores which are sHghtly curved and more pointed at the attachment 

end, and suggested that the long filiform spores are formed under the 

stimulus of excessive moisture (see Figs. 1 a and b, and 20 p). The sporidia 

germinated readily in water and produced, with or without fusion, more sporidia 

of the same type. Sown in dew on the living leaf, stronger germ-tubes, were 

formed and penetration of the leaf followed. A pallid, greenish-white spot developed 

on the infected area in from 13 to 19 days from sowing, during the experimental 

period of May to June. The task still remains of inoculating plants 

with single and paired monosporidial cultures and observing if chlamydospores 

develop. 

In subsequent years sporidial stages were recorded for several additional

BIOLOGY 23 

species of Entyloma, and some taxonomists made the presence and absence of 

sporidia a basis for the division of the genus into two groups (Plowright, 1889; 

CHnton, 1904). Two species, E. matricariae Trail and E. trailii Massee, both on 

Matricaria, were separated on the size of the foKar sporidia (Ciferri, 1928). 

While it is generally assumed that these sporidia carry the fungus from plant to 

plant, few experiments on this means of dispersal have been conducted (see 

p. 106). 

The discovery (BuUer & Vanterpool, 1925; Vanterpool, 1932; Buller, 1933) 

that the allantoid sporidia of Tilletia (Fig. 10/) are violently discharged from the 

stalk led Hanna (1938) to examine the sporidial stages of nine species o£ Entyloma 

and to grow some of them in culture. In five species, E. menispermi, E. australe, 

E. linariae, E. meliloti, and E. ficariae, Hanna found, on the host, sporidia of 

two types, filiform and allantoid (sickle-shaped), which corresponded with those 

figured by Marshall Ward. E. nymphaeae and E. lobeliae were associated only 

with allantoid sporidia, while in E. compositarum and E. polysporum no sporidia 

were discovered. The allantoid type, whether produced on the host or in 

culture, was shot off by the water-drop method, while the filiform type was not 

violently discharged but could be detached by a light touch. In form and size 

this type recalls the sporidia that develop on the promyceUum of some species. 

The allantoid sporidia of three species were stained and found to be 'for the most 

part uninucleate'. They varied in size, even in two cultures isolated from the 

same host (Hanna, 1938, Pig. 1 b and c). 

The allantoid sporidia oiE. ficariae and E. calendulae were studied by Stempel 

(1935), who grew them in culture, and obtained haploid chlamydospores (see 

p. 25). In E. calendulae Stempel found still another type which he described as 

half-moon-shaped. They were larger and wider than the allantoid sporidia and 

carried two nuclei. In culture they gave rise to clamp mycelium (Fig. 1 h) and, 

finally, to normal chlamydospores. These sporidia, which are discharged by the 

water-drop mechanism, have been found recently both in E. calendulae and its 

form dahliae (Sampson, unpubhshed data, see Fig. 1). 

Kaiser (1936), studying E. fergussoni on Myosotis palustris, found filiform 

sporidia (30-40 X1-5-2 ju) on the upper surface and ellipsoidal sporidia (15-20 X 

5-7 fj.) on the lower surface of the leaf. Both types were said to be binucleate. 

Plants of Symphytum, sprayed with a suspension of sporidia in water, gave 

positive results within ten to twenty-one days, and Kaiser concludes that sporidia 

provide an effective means of disseminating the smut of the Boraginaceae. 

Though not well known, it seems hkely that a few species of Doassansia 

resemble Entyloma in their habit of forming sporidia on the host. SetcheU (1892) 

described for D. martm»qâ?ia long, slender sporidia (30x1-5^) which germinated 

in situ to give small bunches of tangled hj^hae. In 1941 a leaf of Sagittaria 

attacked by Doassansia was found to be discharging allantoid sporidia like the 

haploid type found on Calendula (Sampson, unpublished data). 

The foliar sporidia of smuts have been confused at times with Hyphomycetes 

belonging to the genera Cylindrosporium and Bamularia. In Entyloma oenotherae 

on Oenothera lamarkiana the sporidia are described as cyUndrical with a rounded 

apex (9-17 x 3-3-5 /x) and are said to remain in short chains as in species of 

Ramularia (Marchal & Stemon, 1925). Ciferri (1928) also described a species of 

Entyloma which possessed a sporidial stage closely resembling a Ramularia, only

,24 THE BBITISH.SMUT FUNGI 

the presence of chlamydospores making possible the identification of the fungus 

as a smut. Von Hohnel (1924) proposed a new genus, Entylomella (= Cylindrosporum 

Sacc. (non Grev.) p.p.) for the imperfect forms of Entyloma and 

Doassansia, and Ciferri (1928) emended it to include those forms more nearly 

resembling Ramularia?- The characteristics of the proposed genus remain somewhat 

Hi-defined and more information is needed before it can be used for naming 

material from which resting spores are absent. 

GROWTH IN CtrLTtJEE 

The natural home of smuts is the living plant. All members of the group are 

parasites but they readily adopt the saprophytic life under artificial conditions. 

Many species wiU grow on synthetic media but agars containing plant materials 

have been more widely used. The richer media, such as those that contain malt 

extract or oatmeal, are most favourable for chlamydospore formatiori (Kniep, 

1921; Sartoris, 1924). A few experiments have been conducted to discover 

whether accessory growth substances are necessary to smuts living in culture. 

Blumer (1937) and Schopfer (1937), using a synthetic medium including a 

carbohydrate, found that commercial saponin, which contains the growth factor, 

aneurin, had a marked stimulatory effect on Vstilago violacea but other species, 

such as U. maydis, U. nuda, U. hordei, and U. bullata,. were discovered to be 

auxo-autotrophic (Schopfer & Blumer, 1938). Itzerott (1938) found, however, 

that the growth of V. maydis benefited by the addition of an extract of the 

coleoptiles of young maize plants to a synthetic medium containing dextrose. 

Aneurin hastened the development of basidia and mycehum in Tilletia caries 

but did not influence the .earlier phases of germination (Hulea, 1947). 

In cultures of Vstilago profuse budding within the medium is more common 

than sporulation above the surface. In certain species, such as U. maydis, some 

hues are wholly sporidial, producing a glabrous surface, while others develop 

aerial mycelium (see p. 31). MyceHal lines sometimes give rise to branched 

chains of small, oval, hyahne sporidia and produce a colony with a white 

powdery surface (Stakman et al., 1929; Hanna, 1929). Aerial sporidia of a catenulate 

type have been found also in cultures of U. hypodytes (Boss, 1927; Kolk, 

1943), Doassansiopsis horiana (Nisikado & Matsumoto, 1936), and Tolyposporium 

filiferum (Kamat, 1933). In the last-named species, under relatively 

dry conditions, clusters of longer sporidia (8-24 p) developed on short, pointed 

branches (Kamat, 1933). 

Allantoid and half-moon-shaped sporidia are discharged with a droplet oi 

water from the apices of short hyphae growing erect from the surface of the 

medium in cultures of some members of the TUletiaceae. It seems probable that 

they are peculiar to this family (see pp. 83 et seq.). 

The study of a smut in culture is often complicated, not only by the existence 

of physiologic races, but also by heterothallism and the segregation of 

gametophytic characters. A complete picture of the saprophytic behaviour of 

even a physiologic race should embrace the growth of the dicaryophyte as well 

as that of its component haplonts. Much of the early work with smuts was 

carried out with cultures derived from a single chlamydospore or mass isolation. 

It seems, however, that the ideal is more difficult to attain in some species than 

^ See S. J. Hughes, Trans. Brit, mycol. Soc, xxxii, p. 55, 1949.

3036^ 

BIOLOGY 25 

in others. Dickinson (1927), working with the covered smuts of oats and barley, 

found that dicaryophytic mycelium, produced on ag*r by the fusion of appropriate 

haplonts, failed to form a stable growth but reverted to the haploid 

condition. Such a culture would be, at least for a time, a mixture of two biotypes, 

but the suppression of one of them or its loss in transfer might reduce it to 

the state of a monosporidial culture. From other evidence it seems that the 

haplonts derived from a single chlamydospore may produce, in culture, a composite 

growth effect with distinctive characteristics, which wiU persist through 

a number of sub-cultures. A monospore culture usuttUy differs from the component 

monosporidial cultures, because chlamydospores are often heterozygous 

for cultural characters, but one collection (Lll) of Ustilago avenae showed no 

such segregation, the four haplonts derived from a siiigle spore were uniform in 

appearance and closely resembled all monospore cultiires of this race (Sampson 

& Western, 1938). 

Dicaryophytic mycelium is not always unstable cm culture media. Thren 

(1937) succeeded, by the use of a low temperature, in separating the haplonts of 

U. ntida. He grew them singly or in pairs and compared their growth with that 

derived from a single chlamydospore. Dicaryophytic hyphae were wider, their 

growth was stronger, and the resulting colony of a dicaryont had a smooth, 

homogeneous appearance and lacked the radial corrugations which characterized 

both plus and minus haplonts. In exceptional cases dicaryont colonies 

developed sectors of monocaryotic mycehum. In flU examples tested these 

sectors represented the minus haplonts, which could be recognized by their 

weaker growth and by their long radial folds. * \ 

Normally in V. nuda stable dicaryophytic growth is maiatained in culture by 

a regular method of cell division followed by the fusion of haploid cells (diagram 

in Thren, 1941, p. 482). The forms of this smut on wheat and barley are not 

identical in their mode of growth (Thren, 1941). 

Stable dicaryophjrtic growth can also be obtained in species of Entyloma, 

which produce binucleate, half-moon-shaped sporidia on the host (p. 22). These 

germinate to give clamp mycelium, which spreads rather quickly over the agar, 

produces abundant sporidia above the surface, and a niass of submerged chlamydospores. 

Stempell (1935) found that some of these chlamydospores from 

cultures of E. calendulae germinated normally, forming a promycelium with 

terminal sporidia. Others, of later origin, developed a germ-tube which terminated 

in another chlamydospore'or directly gave rise to clamp mycelium. 

Cytological evidence indicated that caryogamy had failed in the abnormal 

spores. Cultures of E. jicariae and E. calendulae, originating from the smaller 

uninucleate sporidia, consisted of thinner mycelium without clamps. They 

developed chlamydospores, but these only formed ordinary mycelium on germination 

and were assumed to be haploid. Only a study of their origin, cytology, 

and mode of germination can decide whether artificially produced chlamydospores 

are haploid or diploid. In outward appearance, except possibly in degree 

of pigmentation, they resemble those found on the host. Sartoris (1924) 

obtamed, in a culture of Ustilago heuffleri from the dogtooth violet, uninucleate 

chlamydospores which had their origin in a binucleate cell. They germinated to 

give a four-celled promycelium with lateral sporidia and appeared to correspond 

in every way with natural spores formed on the living host. D. T. Wang (1984)


observed caryogamy in artificially produced chlamydospores of oat and barley 

smuts but did not germinate them. Fleroff (1923), 'wôrking with two races of 

U. avenae, found that one developed haploid chlamycjospores in culture, while 

the other gave rise to spores which seemed to correspond exactly with those 

found naturally. Records of artificially developed chla,mydospores, made usually 

without reference to their nuclear content or subsequent behaviour, are numerous. 

They have been found in the following species: Tilletia caries (Brefeld, 

1883; Sartoris, 1924; BuUer, 1933), Ustilago maydis (Grass, 1902; Sartoris, 

1924), U. nuda (Sartoris, 1924; Schaffnit, 1926; Rodenhiser, 1926, 1928), 

U. hordei (Sartoris, 1924; Rump, 1926), Urocystis anemones (Kniep, 1921), 

Sphacelotheca reiliana (Potter, 1914), Ustilago crameri (C. S. Wang, 1938). 

Yen (1937) in his study of the Chinese smuts found chlamydospores in cultures 

6f eight species. In some species nuclear fusion was observed during their 

development, but on germination all formed long branched mycelium without 

characteristic sporidia. 

With the discovery of the appropriate technique it seems likely that more 

species of smut could be induced to complete the life-cycle in culture. The production 

of artificial chlamydospores has not yet been employed for the practical 

purpose of getting large quantities of inoculum or for genetical studies. WhUe 

geneticists have of necessity made use of media for the study of gametophytic 

characters, they have found the host a more profitable matrix for the production 

of chlamydospores. It is significant, however, that a race of U. striiformis from 

Poa pratensis readily forms, on potato dextrose agar, chlamydospores which 

germinate normally and can be used successfully to inoculate the host (Leach, 

Lowther, & Ryan, 1946). It seems probable that this race of stripe smut is 

homothaUic. It is so far unique in producing diploid (syncaryotic) vegetative 

mycelium on agar and has no true dicaryophase (Leach & Ryan, 1946).

CYTOLOGY 

THE discovery of nuclei in smuts was delayed by their small size, which also 

accounts for our incomplete picture of their division and behaviour in the lifecycle. 

In many published figures the nuclei are little more than black dots, and 

the magnification is often omitted. Êstimating from Rawitscher's plates, 

which are among the best, it seems that the resting nucleus in the ripe spore of 

Tilletia caries is about 3 X 5 /i in diameter. After 47 hours in water, when in 

preparation for division, the size increases to 5 X 7 /i. Nuclei passing out into the 

promyceUum are considerably smaller, 1-2 jit only, and this may be taken as the 

approximate size of haploid nuclei, up to the moment of fusion in the ripe resting 

spore (Rawitscher, 1922). 

The discovery of this fusion was due to the work of Dangeard (1893, 1894 b) 

who studied sporogenesis and observed the change from the binucleate to the 

uninucleate condition in seven species of smuts. Speaking of Doassansia 

alismatis Dangeard describes the nucleus of the ripe spore as ' nucleole, charge 

de chromatine et reconvert d'une membrane nucleaire, a peine observe-t-on 

quelques fins trabecules de protoplasma qui rayonnent vers la parol; tout le reste 

est forme d'une substance oleagineuse qui donne aux oospores vivantes leur 

aspect blanc et refringent'. Some of the figures in Dangeard's paper suggest 

dividing nuclei. Harper (1899), employing the triple stain, described in the 

phraseology of his day the resting nucleus in a promyceHum of Ustilago 

scabiosae as showing 'a sharply differeritiated, blue stained chromatin net Ijring 

in a clear nuclear sap, a red stained nucleole and a surrounding membrane'. He 

was the first to describe nuclear division in a smut. 'The equatorial plate stage 

is very distinct and shows a sharply pointed bipolar spindle, whose fibres end in 

deep staining granules at the poles. No polar radiations at this stage have been 

observed. The chromosomes are rather densely massed at the equator and are 

probably eight or ten in number.' The figure of U. scabiosae, to which reference is 

made, might be interpreted as an early anaphase showing the separation of 

three bivalents. Two drawings of nuclear division in sporidia of U. violacea show 

chromosomes arranged on a spindle, but again the number cannot be exactly 

stated. Harper's work indicated that the nuclei of the smut fungi divide' in a 

manner similar to those of the higher plants, and showed also that the copulation 

of sporidia was not immediately followed by the fusion of their nuclei. 

Rawitscher (1912, 1914) figured resting nuclei in his papers on the origin of 

the binucleate condition in some cereal smuts, and in later work (1922) dividing 

nuclei with intranuclear spindles and chromosomes. He states that in a ripe 

uninucleate spore of Tilletia caries the nucleus lies near the wall and in it one dr 

perhaps two nuclear bodies can be recognized. After 40 hours in water a muchenlarged 

nucleus is seen in a condition similar to synapsis. The content is very 

refractive and, in addition to the globular large nucleolus, a smaller one may be 

present. The chromatin is found in one, sometimes in two nets at the wall of the 

nucleus (Figs. 2 and 3). Spores fixed some hours later showed the prophase 

(spireme threads), and in some nuclei four stainable bodies could be recognized. 

In material fixed after 46 hours some spores already contained four nuclei, but 

stages of nuclear division are rare. Fig. 7, which shows a nucleus with two


large stainable bodies in addition to the nucleolus, may represent diakinesis. 

The intranuclear spindle is so small and narrow that in many cases the number 

of chromosomes cannot be accurately determined. jIt is possible that the diploid 

number is four. Nuclear divisions continue in the spore until ten to sixteen 

nuclei are present and these finally pass out into the promyceUum and so into 

the sporidia. Helton (1935) discovered that the distribution of nuclei between 

spore and promycelium diifers in two races of T. caries. In Cintractia montagnei 

the diploid nucleus leaves the spore and meiosis occurs in the promycehum. 

Some figures of dividing nuclei in vegetative cells and in promyceHa of 

Ustilago avenae, U. maydis, and Tilletia caries were given by Kharbush (1927, 

1928). The two relatively large chromosomes, seen on the spindle of the first 

division in the promycelium, were accepted as bivalents, those seen in later 

divisions and in cells of the parasitic mycelium as monovalents, and two is suggested 

as the haploid number in smuts. D. T. Wang (1932, 1934) confirmed this 

in the following species: U. nuda, U. hordei, U. violacea, U. longissima, Sphacelotheca 

sorghi, S. cruenta, and Tilletia caries. In her experiments spores were 

germinated at 17° to 20° C. except that a lower temperature was used for 

T. caries. Reduction occurred always at the first division which took place either 

in the chlamydospore or in the promycelium. That segregation is not restricted 

to the first and second divisions of the diploid nucleus, but may even occur in the 

second or third division, is suggested by some genetical data (see p. 36). 

Cytological evidence on this point is meagre, but C. S. Wang (1943), working with 

Ustilago crameri {n = 2) observed four chromosomes at meiosis in promycelia,which 

already contained two or four nuclei, and accepts this as evidence that 

reduction had not been completed in the first division of the zygote. Hiittig 

(1933) suggests that external factors can influence the moment of chromosome 

reduction in some smuts. Yen (1937) has also studied nuclear division in the 

smuts and agrees with previous workers that Tilletia caries has a haploid number 

of two. His conclusions (p. 292) regarding the chromosome number in species of 

Ustilago are somewhat contradictory. Leach & Ryan (1946) failed to distinguish 

chromosomes in a form of U. striiformis which they believe to be homothaUic. 

They estimate that nuclei in the young germ-tube measure 2-3 /x. 

The vacuome and the chondriome of smuts have been studied by Moreau 

(1914), D. T. Wang (1934), and Yen (1937). In the chlamydospore the vacuome 

consists of numerous small vacuoles with dense contents which take up water 

and unite to form larger vacuoles, prior to germination. When growth begins, 

they fragment and pass into the promycelium, and as sporidia are formed, 

minute vacuoles pass into them (D. T. Wang, 1934). Yen (1937), using vital stains, 

demonstrated the presence of metachromatic granules which showed Brownian 

movement in the young vacuoles near the tips of growing hyphae. The chondriome 

was represented in material stained with aniline fuchsin and light green, 

by long, wavy, sometimes branched chondriosonies (chondrioconts) running 

parallel with the long axis of the ceU. They were particularly abundant in the 

cells destined to form spores. D. T. Wang (1934) found that the chondriosomes 

had the form of spherical corpuscles in all the species studied except U. hordei 

where some were filamentous. According to Moreau (1914), who studied the 

chondriome (cytome) in Entyloma ficariae, the chondriosomes were chiefly filamentous 

in the mycelium, corpuscular in the spore.

GENETICS 

INCOMPATIBILITY 

KNIEP'S discovery (1919) of heterothallism in smuts initiated the successful 

application of modern genetical principles to the study of this group. It is now 

an. accepted fact that new races of smuts can be produced by hybridization, 

though it is not yet clear how often this happens in nature or how it may affect 

breediag for resistance in the host. 

The majority of species so far studied are heterothallic (Kniep, 1928) and, in 

some of them, fusion of sporidia is governed by a single pair of allelomorphs. In 

these species, if large numbers of monosporidial lines are tested for compatibility 

(see p. 42), they fall into two equal groups. Any member of group A wiU fuse 

with any member of group B but the hnes within a group are incompatible. As 

Dickinson (1928, 1931) showed, segregation for compatibiUty factors can take 

place at either the first or second division of the diploid nucleus during the 

growth of the promycelium. If it occurs at the first division, the arrangement 

of sporidia will be either A, A, B, B, or B, B, A, A; if, at the second division, four 

types of distribution are possible, A, B, A, B; B, A, B, A; A, B, B, A; and 

B, A, A, B. A gametes can only be distinguished from B by reference to a 

culture arbitrarily taken as the standard. The nuclei carrying A or B factors 

show no polarity, A occurring in the apical segment of the promycelium as often 

as B. This type of segregation (2:2) was first observed by Kniep (1919) in 

Ustilago violacea and later found in U. hordei from oats and barley, U. avenue 

from oats, U. avenae (medians) from barley (Dickinson, 1927,1928,1931;Holton, 

1931 b, 1932; Allison, 1937; Bever, 1945), and U. striiformis from Elymus 

glaucus (Fischer, 1940). 

Segregation of incompatibility factors is not so simple in all species, and 

fusion is probably governed in some by a series of multiple allelomorphs. Thus 

in U. maydis, while the sporidia of one chlamydospore may fall into two equal 

groups, in others segregation ratios may be 4:0;3:1;1:1:2; or 1:1:1:1 (Christensen 

in Stakman et al., 1929, 1931; Hanna, 1929; Bauch, 1932 a). Work with 

V. maydis is complicated by the fact that a few exceptional monosporidial lines 

infect maize and produce galls (Eddins, 1929 a; Sleumer, 1932). Three out of 

31 lines intensively studied by ChristeHsen (in Stakman et al., 1929) were thus 

'solo-pathogenic', but Schmitt (1940) met this peculiarity in only three among 

4,000 monosporidial Unes examined. Unusually large numbers of solo-pathogenic 

lines were derived from the promycelia of crosses between Unes carrying 

factors for lysis (Chilton, 1940,1943). It is thought that irregular meiosis, rather 

than mutation, accounts for the origin and behaviour of solo-pathogenic hnes, 

since segregation for incompatibility factors does occur in subsequent generations. 

Chrisxiensen (1931) obtained three successive crops of chlamydospores in 

which reduction for incompatibiUty failed. In solo-pathogenic lines segregation 

for other factors such as colour and pathogenicity may take place normally and 

mutation is not unknown. Cytological evidence for the abnormal behaviour of 

these lines is lacking. 

Multiple factors for incompatibility h4ve been found also in Sphaceloiheca 

reiliana (Hanna, 1929); S. sorghi (Rodenhiser, 1932, 1934; Isenbeek, 1935;


Tyler, 1938); S. cruenta (Rodenhiser, 1932, 1934); Ustilago longissima (Bauch, 

1931, 1932 b; Kammerling, 1929); Sphacelotheca schweinfurthiana (Bauch, 

1932 c); Tilktia caries and T.foeiida (Flor, 1932 a, 1933). The number of factors, 

not yet known with certainty in any species, usually increases when a vddev 

range of material is examined (Becker, 1936). In Ustilago maydis, a muchstudied 

species, at least 63 factors governing compatibiHty have been detected. 

Factors governing the fusion of gametes are not usually linked with cultural 

or pathogenicity factors (Christensen, in Stakman et al., 1929; Stakman et al., 

1929; Dickinson, 1931; Bauch, 1922, 1927; Alhson, 1937; Rodenhiser, 1934; 

Flor, 1933). Kziiep (1919) found, however, a physiological difference between 

the A and B sporidia of Ustilago violacea (from Dianthus deltoides), one type 

failing on malt agar, while the other flourished on that medium. Thren (1937) 

found that haplonts of U. nuda, designated 'plus', could be distinguished from 

'minus' haplonts by their stronger growth on malt agar, while on potato agar 

the 'plus' type failed to grow. 

The first experiments on compatibility stopped at the initial fusion of sporidia, 

but subsequent work, and especially that on interspecific crosses, suggests that 

fusion is not by itself proof of complete compatibility, which alone leads to 

successful invasion of the host and the maturation of chlamydospores. Fischer 

(1940 a) found, on the evidence of sporidial fusions, a high degree of compatibility 

between Ustilago striiformis from Elymus glaucus and Ustilago bullata from several 

hosts. In some of the successfully paired lines infection hyphae developed in 

great numbers, while in others growth ceased after the fusion of sporidia. 

Cultures of U. striiformis, in the same compatibiUty group, always behaved in 

the same way when paired with different lines of U. bullata. Fischer accepts 

these two types of behaviour as comparable to those discovered by Bauch 

(1932 c) in his intraspecific matings of Sphacelotheca schweinfurthiana. Chlamydospores 

of the hybrid Ustilago striiformis x U. bullata have not yet been obtained, 

but it is not unlikely they would develop on appropriate hosts from lines 

that gave the infection hyphae. 

Races of Ustilago avenue from oats and tall oat grass have no common host. 

Their sporidia are compatible and suitable combinations of monosporidial lines, 

one from each race, produced what appeared to be hybrid chlamydospores on 

wild oats (presumably Avenafatua). Among 16 compatible inter-racial matings 

used to inoculate wild oats, tall oat grass, and Anthony oats {Avena sativa), four 

produced smut on the first host and none on the last two. Chlamydospores only 

developed from the paired lines in which fusion was followed by the growth of 

infection hyphae. These two types of compatibility were not evident in matings 

within the race from tall oat grass, but they were met again when this was crossed 

with races of U. hordei from oats and barley. When Fj chlamydospores from 

wild oats were sown on the three hosts named above, smut was produced on 

Anthony oats showing that segregation for pathogenicity had occurred. The 

mode of inheritance of the two types of compatibihty is not yet known (Holton 

& Fischer, 1941). 

THE GAMETOPHYTE IN CULTTJBE 

Monosporidial colonies of a single species grown on a flat agar surface have 

been found to differ in colour, topography, margin, consistency, rate of gro^vth,

GENETICS • 31 

direction of growth, tendency to sector, response to temperature, and response 

to hydrogen-ion concentration in the medium. Few, if any, of these characters 

are linked, and a species hke Ustilago maydis comprises many hundreds of 

different cultural types (Stakman et al., 1929; Christensen & Rodenhiser, 1940). 

Dickinson (1931) studied the segregation in covered smut of oats, of wide or 

narrow margin, brown, yellow, or cream colour, corrugated or depressed centre, 

dry or moist surface, and rate of growth at pH 5-5. Apart from size of margin, 

which gave a 2:2 ratio, the results suggested that segregation was governed by 

multiple factors. This holds also in other species, and cultural characters are 

not usually Unked either with incompatibility or pathogenicity. They are as a 

rule no guide to the identification of physiologic races (Becker, 1936; Utter, 

1938), nor can they be used to separate closely related species (Kienholz & 

Heald, 1930). 

To be of permanent value, descriptions of growth in culture should be supplemented 

by photographs, coloured if possible. Plates illustrating some cultural 

types have been published for the following species: Ustilago maydis (Stakman 

et al., 1929; Christensen, 1931), U. avenae and U. hordei (kolleri) from oats 

(Dickinson, 1931; Western, 1936; Holton, 1931 b, 1932), U. hordei from barley 

(AUison,1937), U. striiformis (Fischer, 1940a), Sphacelotheca sorghi (Rodenhiser, 

1932, 1934; Tyler, 1938), Sorosporium syntherismae and Sphacelotheca destruens 

(Martin, 1943), Tilletia caries (Kienholz & Heald, 1930). 

The fuUest account of biotypes in any one species is that given by Stakman 

et al. (1929) in their study of mutation in U. maydis. Another gametophytic 

character which has received some study is the degree of sporulation in culture. 

Some monosporidial lines of U. maydis produce abundant sporidia, some are 

entirely mycelial, while others are intermediate (Hanna, 1929; Christensen in 

Stakman el al., 1929, 1931; Stakman ei al., 1929). Stakman (1936) reported on 

the clear-cut segregation of these growth types. Kemkamp (1939), testing such 

lines on a wide range of media, found that strictly sporidial cultures could not 

be induced to form mycelium under any conditions tested. Some intermediates 

produced more sporidia with a higher concentration of sugars and other changes 

in the environment. From a cross between two extreme hnes, segregation ratios 

of 4:0, 3:1,2:2, and 1:2:1, were obtained, indicating that more than two factors 

govern the inheritance of sporidial and mycelial types. Further studies (Kemkamp, 

1942) emphasized the stabiUty of strictly sporidial and strictly mycelial 

lines but both types are rare, virtually all lines of U. maydis being intermediate. 

Intermediates can be shifted to extreme mycelial or extreme sporidial by alterations 

in the environment, but the changes are phenotypic and reversible. The 

addition of poisons and toxic dyes, reduction of oxygen and nutrients, especially 

dextrose, stimulated the growth of myceUum. Sectors of myceUum, which 

sometimes developed in intermediate lines, proved in most examples to be 

phenotypic, not genie, changes. Unsuccessful attempts to cross strictly sporidial 

lines revealed the fact that these are incapable of forming myceUum even in the 

host, but when mated with lines capable of forming hyphae the resulting 

dicaryophytes were pathogenic. 

Popp & Hanna (1935), working with the oat race of U. hordei, germinated 

hybrid chlamydospores from the following combinations of cultural types, 

sporidial X sporidial, hyphal X hyphal, sporidial X hyphal, and studied the


with small chlamydospores and short, ovoid smut balls, while brown peridia were 

associated with larger spores and slender, more elongated sori. 

GEBMINATION OF HYBRID SPQEES 

Kniep (1926), in his pioneer work on heterdthallism, paired appropriate 

sporidial lines from several species of Ustilago. Fusions readily occurred among 

smuts with smooth or echinulate spores, but failed if these species were mated 

with reticulate spored species. Whether the cell fusions were followed by 

nuclear fusions in these so-called interspecific crosses was not then determined, 

but true hybridization in the UstQaginales has been established since. 

Several workers have examined hybrid material of the smuts for evidence of 

heterosis, sterility, or other phenomena commonly revealed by out-crossing. 

Goldschmidt (1928) found in crosses between certain physiologic races of U. 

violacea that promycelia of all hybrids were considerably greater than those of 

the parents. The method of growth was often irregular, the promycelium from 

some hybrids consisting of only one cell. Vaheeduddin (1936 a, 1936 b) noted 

the increased size of promycelia and sporidia in the interspecific hybrid Sphacelotheca 

cruentaxS. reiliana and accepts it as a sign of heterosis. 

Both the number and viability of sporidia may be reduced in crosses. Primary 

sporidia isolated from promycelia of hybrid chlamydospores from Ustilago 

avenaex U. hordei from oats would rarely develop in culture (Holton, 1931 b). 

Martin (1943) recorded a viability of less than 10 per cent, in sporidia derived 

from the hybrid Sorosporium syntherismaexSphacelotheca destruens. Peg-like 

branches, which did not develop either into sporidia or hyphae, were characteristic 

of promyceHa in the interspecific cross S. sorghi x S. cruenta (Rodenhiser, 

1934). Sporidia developed sparsely in 8. sorghixS. reiliana, many promyceUa 

of the hybrid producing hyphal branches in place of sporidia (Tyler & Shumway, 

1935). Some intraspecific crosses of Ustilago maydis behaved in a similar manner 

(Christensen, 1931). In others the promyceHa were gnarled and distorted and 

either autolysed before sporidia developed or gave a few sporidia in an irregular 

manner. Chilton (1943) could find no evidence that lysis in U. maydis was 

caused by an infectious agent and he believes that the explanation for this 

behaviour is genetical. The segregation of one or more factors for lysis was 

demonstrated by crossing appropriate haploid lines (Chilton, 1938, 1943). Lysis 

in certain inbred lines of Sphacelotheca sorghi persisted through two chlamydospore 

generations (Laskaris, 1939, 1941). In both species the tendency to 

germinate abnormally was greater in chlamydospores of unusually large size. 

Another example of lysis, described by Fischer (1940 c) as a haplo-lethal 

deficiency, was found in Ustilago bullata. In certain collections half the monosporidial 

isolates ceased growth after budding off a few sporidia and finally disintegrated; 

the others continued to bud and produced a normal saprophytic 

growth on potato dextrose agar. It is not stated if other media were tried (see 

p. 30). By mating with monosporidial lines of U. hordei and U. avenae Fischer 

showed that the surviving Unes of U. bullata belonged to one compatibility 

group. Since infection of the host could be, induced by chlamydospores from 

these collections of U. bullata, it is concluded that gametes carrying the haplolethal 

deficiency factor were functional in nature, this factor operating only 

against saprophytic growth. This was confirmed by finding infection hyphae

GENETICS 35 

when a few sporidia from lethal and non-lethal lines were mixed on plain agar 

(see Bauch test, p. 42). In a single collection of V. bullata from Festuca idahoensis, 

lysis again occurred in half the isolates, but in this example some of the 

surviving lines were compatible, indicating that the lethal factors were not linked 

with those governing fusion as in the other four collections. 

PATHOGENICITY ' 

The multiplicity of physiologic races within a species is eloquent of the complexity 

of the problem of the inheritance of pathogenicity. That an individual 

chlamydospore from a field collection of U. avenae may be heterozygous for 

pathogenicity factors was clearly shown by Mcolaisen (1934), who infected 

a few selected varieties of oats with paired sporidial lines. To quote one 

example, two sporidial matings from chlamydospore 43/31 produced 100 per 

cent, smut on the variety Lischower, while two other matings from the same 

spore gave negative results on this variety (Nicolaisen, 1934, Table 4). In an 

extensive series of cross-infection experiments conducted with monosporidial 

lines Nicolaisen showed that the factor or factors for pathogenicity carried by 

one monosporidial line might be dominant, recessive, or intermediate according 

to the variety of the host. By crossing, segregates can be obtained which differ 

in virulence from both parents (Nicolaisen, 1934, 1935; Holton, 1936 a; Bever, 

1939). 

Allison (1937) obtained segregation for pathogenicity in the Fj of U. hordei x 

U. avenae (medians) and found that some segregates possessed increased virulence 

on certain barley varieties. The factors for pathogenicity segregate 

independently from those governing compatibility, head, type, and spore wall. 

Christensen (in Stakman et al., 1929) found multiple factors for pathogenicity 

in U. maydis and obtained evidence that they act independently of those governing 

fusion. As in the oat. smuts, a monosporidial Hne may be strongly pathogenic 

when in combination with some compatible lines and weakly pathogenic 

with others. 

Maize inoculated with a mixture of haploids gave a lower degree of infection 

than maize inoculated with single pairs of haploid lines (Kemkamp & Martin, 

1941). Some varieties of wheat were resistant to mixed inocula, though this 

included some highly virulent lines of bunt (Holton & Heald, 1936; Rodenhiser 

& Quisenberry, 1938). No satisfactory explanation of these results is available. 

MUTATION 

It is essential in the application of Mendelial principles to an unexplored 

group of organisms to examine the purity of their gametes. Genetical data on 

smuts, collected since the discovery of heterothallism (Kniep, 1919), rests on the 

assumption that meiosis occurs in the promycelium and that the sporidia 

budded from it are uninucleate, haploid cells. They function as gametes but 

differ from many other sexual cells in that they can be multiplied almost 

indefinitely. Theoretically, uniformity is to be expected in the monosporidial 

cultures derived from single promycelial cell and the colonies should remain 

stable. Variations, at least in some species, are certainly not rare, and it is pertinent 

to ask if all have the same origin. Variants in smuts are sudden, abrupt


changes which persist once they have arisen. It is conceivable that they might 

result from (1) chromosome aberration, (2) heterocaryosis, (3) delayed segregation, 

or (4) mutation. Stakman has discussed their liature in connexion with the 

general problem of variation in fungi (Stakman et al., 1929; Stakman, 1936). 

Too little is known of normal cell division, in the smuts to justify speculation 

on possible irregularities in chromosome behaviour. 'Speaking of heterocaryosis, 

Stakman (1936) concludes that this might possibly explain the origin of some 

variants in cultures of smuts. It is known, for example, in U. maydis, that the 

promyeehum occasionally septates before meiosis. One cell might therefore 

contain two genetically different haploid nuclei either of which may enter the 

first successively produced sporidium. The second sporidium would then differ 

from the first abstricted from a single promyceUal cell. Heterocaryosis cannot, 

however, adequately explain the origin of sector variants which appear in great 

multitude and diversity in some cultures of this and other species (Stakman, 

1936; Tyler, 1938). 

Dickinson (1931) considered that his results with the oat race of U. hordei 

were best explained by supposing that segregation had been extended to the 

third and later divisions of the chlamydospore nucleus. Cultures derived in 

succession from the same promycelial cell, though alike in compatibihty, sometimes 

differed widely in colour, topography, or other aspects of growth in culture. 

More variants were obtained on media relatively rich in nitrogenous compounds. 

Holton (1932), also working with the oat smuts, again found distinct biotypes in 

the cultures he obtained by isolating a number of sporidia from the same segment 

of the promycelium and accepted the variants as evidence of delayed segregation, 

but Western (1936 a) found no evidence of this in-the races of oat smut 

he examined. 

If sectoring in smuts were the result of delayed segregation, it seems probable 

that this would work itself out in time, and that the number of sectors would 

decrease in cultures separated by many nuclear divisions from the first-formed 

sporidium, but this does not appear to happen (Stakman, 1936). The extensive 

and detailed work on U. maydis leads to the conclusion that meiosis is normally 

restricted to the germinating chlamydospore or the promycelium (Christonsen, 

1931; Stakman, 1936) and that sectoring in cultures is the result of mutation 

(Stakman et al., 1935). 

Some of the first records of sectoring in haploid lines of a smut were made by 

Bauch (1925) in U. bullata, but the fullest account of the variants that may result 

in any one species has been given by Stakman and his co-workers for U. maydis 

(Stakman et al., 1929). Some 200 monosporidial fines isolated and studied in 

culture yielded thousands of mutants over a period of two years. Appearing as 

sectors on plate cultures, they often had a wedge or &n-shaped form, but might 

develop as irregular patches. The characters involved were rate of growth, 

direction of growth, surface, margin, lustre, pigmentation, consistency (whether 

sfimy, butyrous, viscid, brittle, powdery, membranous, or coriaceous), relative 

proportion of sporidia and myceUum, size and shape of sporidia, compatibiUty, 

pathogenicity, and tendency to mutate. 

A study of the constancy of some mutant types which arose as sectors from 

a single monosporidial line of U. maydis was made by Stakman, Tyler, & Hafstad 

(1933). During repeated transfers over a period of four to five years, 14 variant

GENETICS 37 

lines retained their distinctive features. Moreover, inoculations into maize made 

in 1932 with several pairs of compatible lines produced infection results similar 

to those obtained four years previously, showing that not only growth characters 

but also pathogenicity had remained constant. 

Characters that arise by mutation segregate after hybridization, like other 

characters in the smuts. This was specifically shown by the study of crosses 

involving an easily recognizable white mutant which had appeared as a sector 

in a brownish-tinged vinaceous line of U. maydis. Mated with compatible brown 

or black lines and inoculated into maize, chlamydospores were produced and 

germinated. In nearly every case some of the monosporidial colonies isolated 

were white like the white mutant. From all the chlamydospores examined 83 

white or nearly white segregates were isolated. An attempt was made to produce 

an albino race of the maize smut, 417 matings from 39 of the whitest lines being 

inoculated into maize. Large galls developed in which dicaryophytic mycehum 

was found, but no chlamydospores were present. Even mass inoculations, using 

a number of the hnes together, failed to yield spores. It seems that in the white 

lines factors for the fuU development of the zygote are missing (Stakman et al., 

1943). 

The close study of variation in U. maydis, conducted for a period of years, led 

to the view that the tendency to mutate was due to the presence of genetic 

factors, that there was sometimes a clear-cut segregation for mutability and 

constancy, and that by suitable breeding the tendency towards mutabiUty or 

constancy could be increased. For experimental proof a cross was used which 

showed definite and relatively simple segregation for five pairs of characters: 

compatibility (plus and minus), brown and white, mycelial and sporidial, rough 

and smooth, constant and variable. Twenty-five monosporidial lines were 

isolated in succession from each of the four primary sporidia on the promycelium. 

All those derived from numbers 1 and 2 were alike and aU those from 3 and 4 

were ahke, showing that segregation was complete before the primary sporidia 

were cut off. In the colonies derived from sporidia 1 and 2 no sectoring occurred, 

whereas 360 variants appeared in the cultures derived from sporidia 3 and 4. 

Breeding was carried a step farther by appropriate matings, constant X constant, 

and variable X variable, among F2 lines. One constant x constant cross yielded 

all constant progeny, in others segregation for variability occurred. All F5 segregates 

from a series of variable X variable crosses were variable. An F5 hue was 

back-crossed to an F4 variable line and the 34 segregates were all highly variable. 

It is evident that in U. maydis mutabihty and constancy are due to genetic 

factors. An indefinite number of biotypes can be obtained by isolating mutants 

from sectors in mutable hnes and by crossing. In this work at least 5,000 distinct 

biotypes were studied, but this did not cover all the segregates and mutants that 

appeared (Stakman et al., 1943). 

As in other fungi, the rate of mutation is affected by the culture medium. In 

early experiments with U. maydis no mutants were observed on sugar media, 

or on sugar media with magnesium sulphate or phosphates. Only one appeared 

on plain water agar, a few on peptone dextrose agar, and a number on sugar 

media plus nitrates (Stakman et al., 1929). Schmitt (1940) grew 20 monosporidial 

lines in duplicate on 6 media. The smallest number of sectors (68) 

developed on Difco maize meal agar and the largest number (107) on Carter's


medium, which is relatively rich in dextrose and contains also peptone and 

nitrates. Stock cultures were grown on modified Czapek agar because on it the 

mutation rate was low while growth was reasonably good. A relatively low 

temperature (under 18° C.) is desirable since it keeps sectoring at a minimum. 

Ultra-violet radiation, X-rays, and short exposures to temperatures near the 

thermal death-point failed to increase the rate of mutation (Schmitt, 1940). 

X-radiation also failed to affect the mutation rate in monosporidial lines of 

V. hordei (Rodenhiser & Maxwell, 1941). In a constant diploid fine mutation 

was induced by the addition of certain chemicals, such as Hthium chloride, to the 

medium (Stakman et al., 1943). A constant haploid line frequently mutated on 

a medium containing arsenic (Petty, 1942). 

Another species prone to mutation in culture is Sphacelotheca sorghi (Ficke & 

Johnston, 1930; Rodenhiser, 1934; Isenbeck, 1935). The fullest study of 

variants, illustrated by photographs, was made by Tyler (1938). On malt agar 

and plain sugar media plus nutrient salts the mutation rate was higher than on 

potato dextrose, plain sugar, or peptone agar. Fourteen lines remained culturally 

constant on potato dextrose agar for over a year. 

Sectors affecting colour, topography, type of margin, and direction and rate 

of growth were isolated from Ustilago sphaerogena, U. crameri, U. neglecta, 

Sphacelotheca destruens, and Sorosporium syntherismae by Martin & Kemkamp 

(1941). In some isolates potato dextrose, in others malt agar, favoured mutation.

TECHNIQUE 

COLLECTION AND EXAMINATION OF HEBBABITJM MATERIAL 

MOST smuts make very satisfactory herbarium specimens, and material a 

hundred years old frequently yields as much information on macroscopic and 

microscopic examination as does a recent collection. It is, however, very necessary 

that collections for preservation should be made with care, and that attention 

should be paid to the conditions of storage. 

A specimen should be typical, adequate in amount, and, whenever possible, 

show both immature and mature sori. It should be accompanied by details of 

the locahty, date of coUeotion, and the name or names of the collector and the 

person making the identification. Particular care should be taken to ensure that 

the host plant is identified correctly, and it is a useful practice to include with the 

specimen material of the uninfected host when this would enable an identification 

to be subsequently confirmed or revised. 

Dried specimens of smuts are, in addition to the usual hazards, particularly 

liable to destruction by a pest of herbaria, Cartodera filiom. This small beetle 

feeds on the sori and deposits faeces consisting of columns of chlamydospores 

which, though Uttle changed in appearance, are usually dead (Vanderwalle, 

1932; Gordon, 1938). It is very important that material should be thoroughly 

dry and free from insects before being put into the collection or much valuable 

material may be spoilt. In some large herbaria it is a routine practice to fumigate 

all specimens with hydrocyanic acid gas before they are 'laid in'. For smaU 

collections, to sprinkle flake naphthalene in the folders is a worth-while precaution, 

and paradichlorbenzene keeps the herbarium beetle at bay. Both these 

chemicals must be often renewed as vaporization is rapid. 

When examining herbarium specimens, the gross structure and arrangement 

of the sori can be most easily determined by means of a low-power binocular 

microscope'and by making any necessary dissections with mounted needles. It 

is usually not necessary to soak the material in water or to treat it in any otherway. 

Spores for microscopical examination may be mounted in water, but a more 

satisfactory technique is to mount them in lactic acid or lactophenol. Addition 

of a stain is advantageous when examining sporidia but is usually not necessary 

for chlamydospores. If lactophenol is employed for mounting chlamydospores, 

supplementary mounts should be made in water, the lower refractive iadex of 

which sometimes makes it easier to observe the details of spore ornamentation. 

The reticulate chlamydospores of Tilletia decipiens, for example, appear to be 

25 per cent, larger in water than in lactophenol because the exospore is invisible 

in the latter medium. 

Very small differences in spore size are rarely of significance for delimiting 

species, and the measurement of large numbers of spores from one collection 

(which frequently means from one sorus or even from one preparation) is not 

advocated. The measurement of fewer spores from as many different collections 

as possible gives a much better idea of the spore size characteristic of a species. 

It is not possible in routine work to measure individual spores to an accuracy 

greater than the nearest 0-5 /x and no additional information is given by express-

40 THE BRITISH SMUT FTJNai 

ing the average spore size to several places of decimals. It was the practice when 

examining the large number of collections, on which the systematic part of this 

monograph is based, to measure ia each mount ten Ispores, the largest and the 

smallest seen in several fields and the remainder at random. 

HAEVESTING, STOBAGE, AND GERMINATION OF CHLAMYDOSFORES 

To obtain a good yield of viable chlamydospores, they must be allowed to 

reach full maturity on the living plant. Premature dispersal from exposed 

sori can be prevented by covering them with parchment bags like those used 

for the exclusion of pollen. Chlamydospores in dusty sori are separated from 

plant tissue by passing through a series of sieves from 20 to 60 mesh, or in submerged 

sori by macerating infected organs in water and straining through cheese 

cloth (Fischer & Holton, 1943). A high-speed blender is useful for macerating 

leaves with embedded sori hke those of stripe smut (Andrus, 1941; Kreitlow, 

1945). 

Dry, sieved spores of exceptionally long-lived smuts can retain their viability 

for years in loosely stoppered jars under ordinary laboratory conditions, but a 

temperature of 5°-10° C. is preferable, and care should be taken to protect 

them from the depredations of the herbarium beetle mentioned above. 

Many species of smut will germinate when the spores are ripe for dispersal, 

others are improved by drying indoors for a few days, while some require an 

after-ripening period of weeks or even months (see p. 18). This period can be 

shortened by treatments appropriate to the species. Thus incubation on moist 

filter-paper at 35° C. reduced the period from 197 to 30 days in Ustilago striiformis 

(Kreitlow, 1945). Soaking spores in water before putting them to germinate 

was effective for the dwarf bunt of wheat (Holton, 1943), and for the stripe 

smut of wheat and forage grasses (Noble, 1923-; Fischer & Holton, 1943). 

Spores need oxygen for germination (Platz, 1928) and are often better floating 

than submerged, but carbon dioxide in concentrations up to 15 per cent, may 

have a stimulatory effect (Platz, Durrell, & Howe, 1927). Germination may also 

be stimulated by adding fragments of fresh plant tissue to the water or by 

employing a medium of expressed sap from wheat seedlings at a concentration 

of 1 in 10,000 (Noble, 1924; Griffiths, 1924; Platz, DurreU, & Howe, 1927). 

73enzaldehyde, sahcylaldehyde, acetone, ether, chloroform, nitrogenous salts, 

and organic acids have been used to stimulate germination (Noble, 1923, 1924; 

Davis, 1924; Hahne, 1925; Rabien, 1927; Enomoto, 1934; Stakman, Cassell, 

& Moore, 1934). 

The rate and mode of germination are affected by temperature (see p. 19) 

and media. A moderate temperature (20°-22° C.) suits many species, but for 

some, such as Tilletia caries, a lower temperature (18° C.) gives better results, 

while a higher temperature (25°-30° C.) is preferable for a sub-tropical species 

like Ustilago maydis. Germination may be delayed and atypical at temperatures 

which are lower than the optimum for a particular species. The most suitable 

temperature for the germination of chlamydospores is not necessarily ideal for 

the infection of the host. 

Growth wiU often start on distilled water but may not proceed farther than 

the germ-tube. Rich media usually encourage vigorous sporulation, which may

TECHNIQUE 41 

be undesirable. Weak agar media made with tap-water, dilute Knop solution 

or 1 per cent, malt are.employed when it is desired to isolate individual sporidia 

in series from single promycelia of Ustilago species. 

Sterihzation of chlamydospores can be effected by soaking them for 24 hours 

or longer in 1 per cent, copper sulphate solution (Stakman et al., 1929). 

MEDIA FOR GROWTH IN CULTURE 

Smuts will grow on many standard media used for fungi, but slight changes 

in composition alter the appearance of the colony. For tte comparison of 

several monosporidial lines cultures are made in dupUcate or triplicate on one 

batch of the medium, the same quantity of agar being poured into each dish. 

Potato glucose and potato sucrose agars have been widely used for the study of 

gametophytic characters (see p. 30). 

In descriptive work shades of colour are matched by standard plates such as 

Ridgway's. Photographs are useful to record features not easily described and 

cultures are usually in good condition for this after about 40 days. To avoid 

disturbing reflections liffthe circle of agar bodily from the dish and place it on 

a sheet of cardboard. 

To maintain stock cultures in an active condition they should be transferred 

every four weeks. Potato glucose agar (1 per cent.) and a modified form of 

Czapek agar have been used for U. maydis. The second medium has the merit 

of lowering the rate of mutation (see p. 37). Meat extract agar (1 per cent.) was 

used for stock cultures of the oat smuts by Sampson & Western (1938). 

Smuts attacking grasses have not yet been widely cultured. Fischer (1940) 

found that U. striiformis wiU tolerate a relatively high concentration and makes 

good growth on agar containing 8 per cent, dextrose, 4 per cent, malt extract, 

and 1 per cent, peptone. 

No infallible technique can be given for inducing the development of chlamydospores 

in artificial culture (see p. 25). Species of Entyloma form them readily 

in a few weeks on potato dextrose agar. Cultures may be started by fastening 

portions of fresh, infected leaves to the hds of .Petri dishes, allowing the sporidia 

to fall, as discharged, on the surface of clear filtered agar, and selecting those 

colonies that originate in the larger, allantoid, binucleate sporidia (see p. 22). 

Chlamydospore formation is long delayed in some species, occurring in Tilletia 

caries only after three months on oatmeal and Leonian agars (BuUer, 1933). 

Schmitt (1940) tried many media to induce the formation of chlamydospores in 

U. maydis without success. 

PREPARATION OF MONOSPORIDIAL CULTURES 

For genetical analysis it is necessary to isolate a series of single sporidia in a 

particular order from the promycelium of one chlamydospore. Dickinson (1926) 

described an apparatus designed to move a finely pointed glass needle over a 

small field in three planes, and to drag small cells, from 30 to 20 /n down to the 

Hmits of microscopic vision, to a chosen part of the field while under observation. 

Haima (1928) constructed a similar isolator from parts of apparatus commonly 

used in a laboratory and employed it for the preparation of monosporidial 

cultures of Ustilago maydis and Sphacelotheca reiliana. A single chlamydospore


is taken up on the tip of a dry needle (Hanna, 1924) and placed on a drop 

of sterile 1 per cent, malt agar in the centre of a cover slip, which is then 

inverted over a van Tieghem cell 25 mm. high. The bell, which can be cut from 

a block of paraffin wax, has an opening at one side to admit a glass needle prepared 

from tubing 3 mm. in diameter, the pointed tip of which is about 15 ja in 

diameter and bent at a right angle. When the spore has germiaated and the 

sporidia are full size (8 X 2 jit in U. maydis), the needle is moved up untU its point 

touches the Hquid film immediately below the sporidium to be isolated. By 

the turn of a screw the needle is lowered slightly, and by a movement of the 

mechanical stage the sporidium can be drawn in a cone of liquid away from the 

chlamydospore. After pausing a moment, the needle is lowered and the sporidium 

leaves the agar and remains on the point of the needle. It can then be 

placed on a fresh drop of agar on a new cover slip, temporarily put in the 

position of the first cover slip, and the same procedure is followed with the next 

. sporidium. 

Dickinson (1933) has described, with diagrams, this and other methods of 

monospore isolation, including the separation of h3rphal tips by microscissors 

prepared from razor blades, a technique which might be useful for the isolation 

of haplonts in those smuts which do not form sporidia readily on the promycelia 

or separate into haploid cells at low (L° or 2° C.) temperatures (Lange de la 

Camp, 1936; Thren, 1937). 

TESTS FOR THE COMPATIBILITY OF MONOSPOEIDIAL LINES 

Fusion of sporidia. The oldest method adopted by Kniep (1919), and many 

others, is to pair monosporidial cultures on agar and to record the presence 

or absence of fusions. Cultures should be young and actively budding when 

tested. Tyler (1938) grew stock cultures of Sphacelotheca sorghi on potato dextrose 

agar and for the tests transferred sporidia to drops of sligEtly alkaline 

malt agar (3 per cent, malt, 2 per cent, agar) incubated at 27° C. Early stages 

of fusion can be detected under the microscope after 24 hours,; later a long 

straight hypha guides the eye to the point of fusion., Numbers of sporidia fail 

to fuse even in compatible lines, and experience is needed in interpreting results. 

Media should be low in nutrients (distilled water or 1 per cent, malt extract) and 

the temperature 20°-24° C. for sporidial fusion in U. maydis (Bowman, 1946). 

Bauch test. This was used successfully for U. violacea, U. maydis, and U. 

scorzonerae (Bauch 1927, 1932 a), S. sorghi (Tyler, 1938), and U. striiformis 

(Fischer, 1940 a), but Holton (1932) and Western (1936 b) found it unreHable 

for the two oat smuts. The test depends upon the fact that in certain species 

the cultures derived from compatible lines develop white aerial mycelium (the 

Suchfdden of Bauch) which contrasts sharply with the glabrous surface of monosporidial 

or paired incompatible cultures. Other cultural characters are sometimes 

useful. Haploid colonies of U. nuda belonging to different compatibility 

groups develop a Ught streak at the zone of contact on potato dextrose agar 

(Lange de la Camp, 1936). 

Formation of chlamydospores in the host. A drawback to this method is the 

length of time that must elapse before results can be expected, but by manipulating 

conditions of growth two or more generations of the host can be growii

TECHNIQUE 43 

in one season (see p. 46). Different metliods of inoculating the host are given 

below. Chlamydospore formation on maize is said to be the only reliable test 

for compatibility in U. maydis (Stakman et al., 1943) and most workers use it 

to confirm other tests which stop before reaching this point in the life-cycle. 

Colour changes in the host. These can be used in some species to shorten the 

experimental period since they denote compatibility before sporulation takes 

place. Plants of sorghum inoculated by the hypodermic method with compatible 

lines of S. sorghi develop chlorotic spots in four to six days (Rodenhiser, 1932; 

Tyler & Shumway, 1935; Tyler, 1938). The presence of anthocyanin in the 

epidermal cells of Golden Bantam sweet com is correlated with the presence of 

dicaryophytic mycelium of U. maydis and S. reiliana (Hanna, 1929; Christensen, 

1931). 

INFECTION OF THE HOST 

The following methods of bringing about infection, which have been worked 

out for the cereal smuts, can be adapted for other species when the natural seat 

of infection is known. 

Seedling infection, (a) Dusting dry grain with dry sieved chlamydospores. This 

method works well with bunt of wheat provided the spores are viable ^.nd the 

grain is germinated at a temperature of 5°-15° C. For maximum infection, 

100 gm. of seed are shaken with 0-5 gm. of bunt spores. K these are well distributed, 

about 36,000 to 150,000 spores will adhere to a single grain (Heald, 192L'; 

Heald & Boyle, 1923). The depth of sowing should be about If in., the soil 

50 per cent, water saturated with a reaction of pH 5-5-7-5 (Rodenhiser & ^ 

Taylor, 1940). Other useful details concerning the glasshouse culture of wheat, 

oats, and barley, where high smut infection is desired, are given by the American 

Phytopathological Society, 1944 (see also Faris, 1924 a; Feucht, 1932; Ling, 

1941). ^ 

To get good results with oats, it is necessary to remove the pales before dusting 

the grain with spores; This can be done with a tapering, blunt-tipped scalpel. 

Each sample of shelled grain, coated with spores, is either sown in sand taving 

a moisture content of 20 per cent, saturation, or spaced out on moist filter-paper, 

covered with an additional sheet, and made into rolls. Both methods give 

100 per cent, infection with susceptible varieties if a temperature of 20°- 

22° C. is maintained during the first three days of germination. Subsequently 

the seedlings are transplanted to soil (Sampson, 1929; Sampson & Western, 

1938). In a similar technique with wheat bunt spores are allowed to germinate 

at 10° C. on rags used in seed-testiag seven to ten days before wheat, soaked in 

distilled water for 18 hours, is added. The rag-doll is kept for another ten to 

fourteen days at the same temperature, and the seedlings are transplanted to soil 

when the shoots are not more than 30 mm. long (Livingston & Kneen, 1944). 

The removal of pales from barley by hand (Tisdale, 1923) is laborious and 

may lower the percentage germination. Scarification between sandpaper 

(Aamodt & Johnston, 1935) and soaking in sulphuric acid cause injury (Briggs, 

1927 ; Johnston, 1934; Woodward & Tingey, 1941). 

The following wet methods of inoculation can be used with grain in the husk. 

(6) Spore-suspension method. A spore-suspension is made by shaking 1 gm. 

of spores in 1 litre of water. Seed is shaken in this for ^ minute and then allowed

44 THE BBITISH SMUT FUNGI 

to soak for 15 minutes. The suspension is decanted and the vials are inverted 

over clean blotting-paper to absorb aU free water. The samples of grain are then 

packed in a tightly covered tin box lined with moist blotting-paper and incubated 

for 24 hours at 20° C. They are transferred to envelopes which are left 

wide open for two to three days until the seed is dry, t^hen it should be sown 

in relatively dry soU at a temperature of about 15° C. (Leukel, 1936). This 

method, used effectively for Ustilago hordei (Tapke, 1935 b, 1937 b) and for U. 

avenae (nigra) (Tapke, 1937a), gave better results than the dry method, whether 

seedlings were kept for two to four weeks in a glasshouse or grown entirely in the 

field. The deeper-seated inoculum resulting from the spore-suspension method is 

probably more resistant to cold (Tapke, 1938, 1940). 

(c) Partial-vacuum method applied to grain in the husk. This method was used 

by Zade (1928), Haaring (1930), and Western (1937) for oats, and by Alhson 

(1937) and Tapke & Bever (1942) for barley. It is quicker and more effective 

than dusting the shelled grain of barley and is less likely to lead to contamination 

of physiologic races by air dispersal (Leukel, Stanton, & Stevens, 1938). 

One hundred grains of each variety are placed in test-tubes containing 10 ml. 

of a suspension of chlamydospores and evacuated in a desiccator attached to a 

motor vacuum pump for 20 minutes. The sample is allowed to dry for 12 hours, 

stored at 2° C. for 24 hours, and then sown. This technique can also be used for 

inoculations carried out with suspensions of appropriate sporidial lines (Allison, 

1937). It has been used successfully with spores and sporidia of U. bullata for 

the inoculation of species of Brcmius, Agropyron, Elymus, Hordeum, and other 

genera (Fischer, 1940 b) and for species of Urocystis on cereals and forage grasses 

(Fischer & Holton, 1943). The inoculated seed is sown while stiU wet in pots of 

soU in a glasshouse. 

(d) The infection of wheat by paired monosporidial lines of hunt. A fragment of 

mycelium from each of the two lines to be combined is placed near the edge of a 

Petri dish containing potato' dextrose agar. The dish is turned on edge so that 

sporidia, as they are discharged, may fall on the agar and start new colonies. 

The culture is then inverted over surface-sterilized wheat grains lying in the Hd 

of a dish lined with moist filter-paper and incubated at 10° C. for ten to fourteen 

days. The seedlings thus receive sporidia from the two lines during their growth 

and are subsequently transplanted to soil at about 15° C. and allowed to mature 

(Flor, 1932 a; BuUer, 1933; Hanna, 1934; Holton, 1938 b). 

Flower infection, (a) Use of finely pointed forceps. Spores after removal from 

the flower head are passed through a 40-mesh sieve. They may be held conveniently 

in a capsule secured to the thumb by means of a ring, thus leaving the 

thumb and fingers free to hold the inflorescence (Tapke, 1935 a). The glumes of 

wheat are forced apart when anthesis has begun and the spores are placed on the 

exposed ovary (Hanna, 1937). To open the closely interlocking pales of barley 

causes injury and Tapke (1935) found it better to pierce the centre of one of the 

pales with the forceps and to insert the spores on the stigma. This yielded plump 

seed which could be sterihzed in formalin solution (1 in 320) without injury. It 

is important to keep the temperature and humidity relatively high (over 30 per 

cent.) for some days after inoculation (Tapke, 1931). 

(&) Use of a dry spray. A small sprayer with finely pointed nozzle and a device 

for holding and pumping it with the same hand was used to inoculate wheat and

TECHNIQUE 45 

barley with loose smut at HaUe, Germany, and elsewhere (Tiemann, 1925; 

Seiffert, 1926; Piekenbrock, 1927 ; Grevel, 1930; Zeiner, 1932; Nahmmaoher, 

1932; Radelescu, 1935 b; Roemer, Fuchs, & Isenbeck, 1937). One drawback to 

its use is the danger of introducing between the pales excessive numbers of spores 

which lead to a high death-rate among plants grown from inoculated seed. To 

obviate this, the inoculum is diluted with 95-9 per cent, of dead spores, kiUed 

with ether or by exposure to dry heat at 150° C. for several hours (Thren, 1938). 

(c) Partial vacuum method applied to cereals in flower. A suspension of spores 

of Ustilago nuda is made by shaking two medium-sized smutted heads in 100 ml. 

of water in a conical flask. An apparatus was designed by Moore (1936) for 

bringing the suspension into direct contact with ears of growing wheat or barley. 

A partial vacuum is created by the aid of a large automobUe pump with an 

inverted plunger-leather, and air withdrawn from the florets is replaced by the 

suspension of spores. Oort (1939, 1940) found that, with slight modifications, 

four heads could be treated at one time. Vanderwalle (1945), using a rotary 

vacuum pump, inoculated 180 ears per hour and obtained up to 98 per cent, of 

smut in many lines of barley which showed only slight smut in ordinary culture. 

Atkins (1943) found that four heads gave ample seed for testing the resistance 

of a variety to loose smut. 

The optimum period for inoculation is at mid-anthesis and lasts for a few days 

only. The most efiective concentrations of spores in the suspension are 1 gm. 

for wheat smut and 0-1 gm. per litre for barley smut. The winter hardiness of 

plants raised from seed inoculated by this method is only 10 to 20 per cent, 

below normal. Heads of uniform maturity should be selected for inoculation, 

but even so results are sometimes inconsistent (Middleton & Chapman, 1941). 

{d) Use of a hypodermic needle. A suspension of chlamydospores in 1 per cent, 

glucose solution held in a rubber bulb of 10 ml. capacity is injected by means of 

a 1-in. 25-gauge hypodermic needle into each floret of a spike of barley a day or 

two after the exsertion of the inflorescence. Thirty to forty heads can be inoculated 

in one hour (Poehlman, 1945, 1947). See also Bever, 1947. 

Shoot infection. The hypodermic injection of maize and other cereals. Monosporidial 

lines of U. maydis are grown separately in a solution of 2 per cent, 

dextrose and 1 per cent, malt syrup and allowed to develop for two to three 

weeks before inoculations are made. They are then strained through cheesecloth 

to remove the largest clumps of sohdjuaterial. Cultures for test are mixed 

just before inoculation and the inoculum is injected into plants by means of a 

hypodermic syringe as near to the growing-point as possible. Controls are 

inoculated in the same manner with sterile nutrient solution (Tisdale & Johnston, 

1926; Stakman & Christensen, 1927 ; Stakman et al, 1929; Hanna, 1929; Platz, 

1929). 

Maize plants inoculated wben one week old produce gaUs in three to four 

weeks at a glasshouse temperature of 27°-32° C. and it is possible to grow ten 

generations of chlamydospores of U. maydis within a year (Schmitt, 1940). 

Artificial inoculation will cause infection in some lines of maize resistant to smut 

in the field (Grifliths, 1928; Griffiths & Humphrey, 1929; Platz, 1929). 

Higher infection results if the sporidia are suspended in a fluid having a 

low surface tension. Bavis (1935) obtained good results with a 1 per cent, fish 

oil-soap-carrot decoction having a surface tension of 34-0 dynes per sq. cm.


Wilkinson & Kent (1945) used 0-7 per cent, triethanolamine oleate to reduce the 

surface tension. 

The development of galls in artificially inoculated maize may be inhibited 

by certain bacteria antibiotic to smuts in culture (Johnson, 1931; Bamberg, 

1931). Modifications of the hypodermic injection method have been used for 

bunt of wheat, the loose smuts of wheat and barley, and loose kernel smut of 

sorghum (Fans & Reed, 1925; Milan, 1928 ;.Bodine & Durrell, 1930; Lange de la 

Camp, 1936, 1940). Suspensions of germinating chlamydospores, or mixed 

sporidia from appropriate cultures, form the inoculum which must be inserted 

near meristematic tissue. Chlamydospores of U. striiformis, injected as near as 

possible to the apex of shoots of Poa pratensis, gave good infection, and the 

method is likely to be useful in breeding for resistance to stripe smut (Leach, 

Lowther, & Ryan, 1946). 

The use of low temperatures and artificial illumination to extend the season for 

experimental work on smuts deserves further study, since the results are somewhat 

conflicting. Lengthening the period of light gave a marked increase in the 

percentage bunt in two varieties of spring wheat (Rodenhiser & Taylor, 1940) and 

caused a breakdown in the resistance of another variety to some races of bunt 

(Rodenhiser & Taylor, 1943). A small increase in the amount of smut on Dakold 

rye occurred under long day conditions (Ling, 1941), but artificial illumination 

failed to alter the degree of infection by smut on oats (Reed, 1938). Snell (1938) 

found that early varieties of summer wheat could be tested for bunt resistance 

in six weeks by maintaining a temperature ofl6°-17° C. during germination, 

and 20° C. during subsequent growth and constant (day and night) illumination. 

VemaUzed winter wheat may give a lower bunt infection than the control seed 

(NemUenko, 1935; Lasser, 1938). Marquis wheat artificially inoculated with 

loose smut gave the same incidence of disease when vernalized and not-vernalized 

(Hanna, 1936). Bever (1947) used vernalized seed and grew two experimental 

crops of wheat in one year in his work with loose smut. 

CONTROL 

(a) To determine the smut spore load on cereal seed. Forty gm. of seed are 

placed in a 500-ml. Erlenmeyer flask to which 60 ml. of distilled water containing 

0-1 per cent, of a proprietary wetting agent are added. The flask is then 

shaken vigorously 30 times, taking care to overturn thoroughly the seeds in the 

flask. Ten ml. of the washings are immediately poured into a centrifuge tube, 

centrifuged for four minutes at 2,400 r.p.m., and the supernatant liquid is then 

siphoned off to within 0-3 ml. To this residue is added 0-2 ml. of a 4 per cent, 

gelatine solution maintained at 45° C, making a total of 0-5 ml. of spore suspensions. 

The spores are dispersed by stirring and a loopful is withdrawn quickly 

and placed on a special slide and immediately covered with a cover glass. If 

smut spores are numerous, count eight microscopic fields, if scarce, eight swaths, 

across the central square of the slide. In order to compute the spore load of the 

grain sample, the counts are compared with standards prepared from artificially 

smutted grain samples carrying a range of known spore loads (Cherewick, 1944; 

•BusseU, 1946). 

(6) Seed treatments. Historical reviews have been given by Woolman & 

Humphrey (1924), Sampson & Davies (1925), Koehler (1935), Dillon Weston

TECHNIQUE 47 

(1939), Holton & Heald (1941), and Buttress & Dennis (1947). Holton & Heald 

(1941) give references to over 200 different substances which have been tested 

for the control of bunt. They also review in some detail the laboratory method 

first introduced by Gassner (1923) for determining the chemotherapeutical 

index of fungicides. 

Seed treatment when infection comes from spores carried on the seed. Formaldehyde. 

Grain is sprinkled with a solution made by mixing one part of 40 per cent, 

formaldehyde (formalin) in 320 parts of water and covered for two to four hours 

before it is spread out to dry. From one to two gallons of the solution is required 

to moisten four imperial bushels of grain. Injury to germination sometimes 

follows, especially in wheat if the pericarp lying over the embryo is cracked 

(Hurd, 1921). Grain should be sown within a few days of treatment (Moore, 

1945; Dillon Weston & Taylor, 1948). This method is particularly useful for 

small lots of grain to be used in laboratory experiments requiring smut-free 

seed. If the seed is to be reinoculated, it is washed in running water for 30 

minutes before drying. • Dusts are now preferred for treating grain in bulk. 

Dusts. Copper carbonate applied usually at the rate of two ounces per bushel 

is effective for the control of wheat bunt provided the grain is not too heavily 

contaminated with spores. It is less effective than organo-mercury compounds 

for other seed-borne diseases of cereals, and has been superseded by proprietary 

products which are sold under trade names such as Uspulun, Semesan, TUlantin, 

Ceresan, Agrosan, &c. The ingredients of these dressings vary widely (Dillon 

Weston & Booer, 1935; Martin, 1940) and under a scheme initiated in 1943 

those tested and approved by the Ministry of Agriculture bear a special diamondshaped 

mark (Dillon Weston & Taylor, 1948). 

To treat small samples of any cereal with either copper carbonate or one of the 

organo-mercury dusts it is only necessary to shake the grain with some of the 

powder and to remove the excess by sieving, but for treatment on a larger scale 

special machines must be used. These vary from hand-rotated chums to more 

elaborate power-driven machines (Holton & Heald, 1941; Moore, 1945; Dillon 

Weston & Taylor, 1948). Organo-mercury dusts are poisonous and should not 

be inhaled or handled with wet hands. In the slurry method of treating seed 

flying dust is eliminated. The fungicide, in a wettable form, is applied to the 

seed in a heavy suspension which leaves only 0-5 to 1 -0 per cent, of moisture on 

the seed and this soon evaporates (Leukel, 1948). In Britain some growers make 

a practice of applying an organo-mercury dust to seed oats, wheat, and barley 

before dispatch. Treated grain can be stored for months in a dry, cool, and wellventUated 

place and the chemicals are said, to deter rodents. Injury does not 

follow unless the seed is damp when treated and excess adheres to the seed or if 

seed has been mechanically injured in thrashing. Seeds may be killed outright 

or grow with abnormally thickened and much-stunted shoots and roots (DiUon 

Weston & Brett, 1944; Moore, 1945; Hoppe, 1948). Organo-mercury dusts owe 

some of their popularity to the fact that they exert a fungicidal action against 

some other pathogenic fungi such as Helminthosporium avenae and tend to 

promote good estabhshment in the field (Sampson & Davies, 1925, 1926; 

Muskett & Cairns, 1932; Moore, 1945). They have been recommended for the 

control of Ustilago bullata in forage grasses which are liable to suffer injury from 

formaldehyde (Moorwood, 1935; Fischer, 1942).


8eed treatment when there is mycelium in the embryo. Hot water. Wheat grain 

is soaked in cold water for four hours, drained for a few minutes, and submerged 

in warm water (52°-54° C.) for ten minutes^ It is then quickly spread 

in a thin layer to dry. For barley, the grain, after soaking, is plunged in water 

at 49° C. for five minutes and'then steeped for ten, minutes in water at 51° C. 

If the temperature is allowed to rise above 55° C. the grain may be damaged 

(Moore, 1945). Automatic machines for this treatment have been designed and 

some authors prefer a longer soaking (say, six hours) at a lower temperature 

(43° C.) (Jones, 1939). The injury to germination and growth which may foUow 

even careful treatment depends largely on the condition of the pericarp and this 

varies in each lot of seed (Tapke, 1924). 

Modifications of this method which make direct use of solar energy have been 

devised in India. No thermometer is necessary. Grain is soaked in water from 

8 a.m. to 12 noon and exposed in a thin layer to the sun from noon to 4 p.m. The 

best months for treatment in the Punjab plains, where the method has been 

widely used, are Mayand June, when the temperature in sunshine reaches 131°F. 

The treated grain can be stored without deterioration and complete control of 

smut was obtained when untreated samples gave 5-12 per cent, of smut 

(Luthra & Sattar, 1934; Luthra, 1941). 

The hot-water treatment is applicable to other smut diseases transmitted by 

infected seed or other organs of the plant. Bulbs of the grape hyacinth carrying 

mycelium of V. vaillantii held for one hour in water at 110° F. yielded smut-free 

flowers in the following year (A. Smith in litt., 1947). 

Seed treatment when infection comes from the soil. In Britain the only soUbotne 

smut disease for which control is practised is onion smut. The soU remains 

contaminated for some years, and in view of the serious nature of the disease the 

wisest plan is to avoid planting onions or related crops in ground infested by 

Urocystis cepulae. Where this is not practicable the best method is to apply 

formaHn to the soil. After sowing the seed and before covering it with soil, 

formalin (40 per cent.) solution (one pint in 16 gals, of water) is trickled into the 

drill. This quantity wiU suf&ce for 800 yds. of drill. If the soil is unduly wet, 

a stronger solution (up to two pints) can be used with safety (Minist. Agric. & 

Fish. Advisory Leaflet 261). 

This method gives only partial control but it is more effective than organomercury 

dusts (Gibbs, Bayliss, & Blackmore, 1941). Experiments have been 

made also with organic sulphur dusts such as thiosan, arasan, and tersan. The 

results are conflicting, but on the whole these substances are less effective than 

the standard formahn drip method (Miller & McWhorter, 1945; Nelson, 1946). 

Attempts have been made to combine the fungicide with an excipient such as 

feldspar, which is used in conjunction with methyl ceUulose solution to coat the 

seed. Pelleted seed, which is larger and more uniform in shape, can be sown with 

greater precision and thinning is less laborious, but no method yet devised gives 

complete control of smut (Gorenz & Walker, 1947; Linn & NewhaU, 1948). 

FIXATIVES 

Flemming's weaker solution (Harper, 1899; Paravicini 1917; Bhzzard 

1926; Seyfert, 1927; Kniep, 1921; Hanna, 1929; C. S. Wang, 1943) Bouin's,

TECHNIQUE 49 

Allen's, modification of Bouin's (Seyfert, 1927; Evans, 1933, 1937), and 

Nawaschin's (D. T. Wang, 1934; Western, 1936 b) fixatives have been used for 

smuts. A method for demonstrating nuclei in the promycelium first used by 

Kniep (1921) has been adopted with only slight modifications. The following 

details are taken from Hanna (1929). A thin film of 1 per cent, malt agar is 

spread over a sHde and spores are dusted on the surface with a camel's-hair brush. 

The slides are inverted over glass rods in a Petri dish containing a few drops of 

distilled water. At the desired stage of germination the material is fixed in 

Flemming's weaker fluid (15 minutes). The fixative is removed by adding a few 

drops of distilled water and sucking up the excess liquid with filter-paper. To 

avoid washing off the spores during staining the sHdes are passed through a bath 

of ether and then into a 0-2 per cent, solution of collodion made up with equal 

parts of alcohol and ether. Others (Harper, 1899) have germiaated the spores in 

beerwort in a watch glass, and used egg albumen to fix them to the shde. The 

liquid, which should be turbid with germinating spores, is taken up in a fine 

capillary tube and discharged into a larger droplet of the fixative. The spores 

settle on the film of egg albumen, and the hquid is allowed to evaporate, but not 

to dry out completely, before the shde is passed on to the alcohols. The fixative 

is not washed out. 

For a study of the cytoplasm D. T. Wang (1934) found the best fixative was 

le Regaud, consisting of 3 per cent, potassium bichromate (four parts) and 40 per 

cent, commercial formalin (one part). 

STAINS 

Harper (1899) used the triple stain^ for nuclei in the promycehum, but 

found a 1 per cent, solution of methyl green better for staining nuclei in spores 

already in possession of a thick wall. Most workers since Harper have used 

Heidenhain's haematoxylon. No recognized technique exists for treating the 

nuclei of smuts with a quick-acting fixative followed immediately by acetocarmine 

or similar dye, as in the method used for pollen and macerated tissue. In 

preliminary tests at Aberystwyth dividing nuclei in the promycelia of U. hordei 

were stained red by lacmoid,^ and this type of reagent deserves further trial for 

the nuclei of smuts. 

Metachromatic granules in the vacuome have been demonstrated by means of' 

neutral red, cresyl blue, and Delafield's haematoxylon. AniUne fuchsin, with a 

counter-stain of light green, stained the chondriosomes bright red in material 

fixed in Meves reagent (Yen, 1937). 

For detailed observations on parasitic mycelium sections of plant tissue 

should be 3-5 /x. Triple and Heidenhain's were used by Blizzard (1926), safranin 

and fast green by Evans (1933) for Urocystis cepulae, thionin and orange G for 

Ustilago may Ms by Walters (1934). 

The general distribution of mycelium in the host can be demonstrated in hand 

sections of material fixed in 70 per cent, alcohol and stained by lactophenol 

cotton blue or in microtome sections, 10-12 /^t, by aniline gentian violet wjth a 

counter-stain of Bismarck brown. Take the slides from 70 per cent, alcohol and 

^ For stains and fixatives see Plant Microtechnique, Johansen. McGraw-Hill, 1940. 

^ See The Handling o/ Chromosomes, C. D. Darlington & L. F. La Cour. Allen and Unwin, 

1942. 165 pp. 

D

gQ THE BRITISH SMUT FUNGI 

flood with a saturated solution of Bismarck brown in 70 per cent, alcohol. After 

seven minutes wash with 70 per cent, alcohol until only a faint brown colour 

remains. Flood with aniline gentian violet and leave fpr ten minutes. This stain 

should be freshly prepared, and for this reason the Isoloid' stains supplied by 

Messrs. Burroughs & Welcome Co. are useful. Drain off the violet stain and 

leave the slide in Gram's iodine solution for five to ten minutes. Remove surplus 

stain with absolute alcohol and wash in clove oil until violet is left only in the 

nuclei of the host and in myceHum. Wash in xylol and mount in Canada balsam. 

Mycelium stained deeply by this method shows up well in microphotographs. 

The staining capacity of hyphae varies with their age and it is not possible to get 

the optimum staining of old and young mycelium in the same section. Woolman 

(1930) found the mycelium of bunt to be Gram negative at the point of entry, 

Gram positive in later phases of growth. 

A quick method for the detection of mycelium in embryos of barley and wheat. 

Embryos, previously separated from the endosperm, are treated for several 

hours in a solution of hydrochloric acid (one part concentrated acid to three 

parts of water) containing 5 per cent, potassium chlorate, and then transferred 

to alcoholic caustic potash (20 per cent.). This bleaches and softens the tissue. 

After rapid neutrahzation with acetic acid the embryos are stained with aniline 

blue and crushed under the cover sHp. The myceHum can be seen among the 

dissociated cells of the host (Larose & Vanderwalle, 1939). Simmonds (1946) 

gives full details for separating and microtoming (10 [i) large numbers of embryos 

in order to compute percentage infection in a sample of seed. From 50 per cent, 

alcohol the slides are placed in Harris's haematoxylon for half an hour, washed 

in 50 per cent, alcohol, taken down to water, and stained in 5 per cent, aqueous 

solution of Congo red for three hours. 

Bismarck brown can be used to impart a golden-brown colour to hyaline 

promycelia and sporidia destined to be photographed. AUow most of the water 

to evaporate before adding absolute alcohol as a fixative. After drying leave for 

20 minutes in the stain, drain off excess, and mount in 50 per cent, glycerine 

(McAlpine, 1910). 

The development of spines on the chlamydospores of U. maydis was studied 

by Hutchins & Lutman (1938). Sections of material fixed in Allen's modification 

of Bouin's fixative are transferred to water and then to a satui-ated solution of 

orseiUine BB solution (about 1 gm. of orseilline in 30 ml. of 3 per cent, acetic 

acid) for 24 hours. Alcohol (50 per cent.) is then run quickly over the shde to 

remove the excess stain and the sections are placed in a saturated solution 

(1 gm. of aniline blue in 100 ml. of 3 per cent, acetic acid) for 24 hours. The 

sections are dehydrated quickly by flushing with absolute alcohol, immersed in 

xylol, and mounted in balsam. The exospore of young spores is dark red, while 

the minute spines are a brilhant red in contrast to the blue gelatinous covering 

of the spore Anlagen. In older spores the spines are grey and finally brown.

CLASSIFICATION 

THE morphological characters, on which descriptions of the Ustilaginales are 

based, are few and relatively simple. The size and ornamentation of the spores 

(chlamydospores) and the structure of the sorus are of paramount importance 

for differentiating species on morphological grounds, and from this standpoint 

smuts are among the most, convenient fungi with which to work. The usefulness 

of herbarium material, when carefully preserved, does not deteriorate, and so the 

identity of successive collections is easUy checked and the exchange of material 

between different workers greatly faciUtated. Final proof that a species belongs 

to the Ustilaginales, and the determination of which of the two families (and 

frequently also the genus) in which a specimen should be classified depends, 

however, on the course of events at spore germination. The spores of herbarium 

specimens, after a longer or shorter time, lose their abUity to germinate and the 

spores of fresh material may germinate with difficulty, so that many species have 

been proposed, and often correctly proposed, by analogy. One object of giving, 

whenever possible, details of the behaviour at germination and the conditions 

under which this event occurs after the usual specific descriptions in the 

systematic treatment of the British smuts is to draw attention to the need for 

further studies on this phenomenon. 

What constitutes sufficient grounds for the differentiation of a species varies 

from one group of organisms to another. In general, two tendencies may be 

observed among students of fungi. Morphological or biological characters may 

be emphasized. Among smuts, as in other groups of parasitic fungi, the second 

attitude has been commonly adopted, and many species have been proposed 

from a consideration of differences in parasitic abUity towards a series of plants. 

Hence the identity of the host becomes of primary importance for the identification 

of the parasite, although not infrequently biometrical studies reveal small 

differences in spore-size of other characters between morphologically similar 

'species' from different host plants. 

Butler (1929) reviewed with pertinent illustrations the criteria for the definition 

of species among fungi, and Ciferri (1932) expressed his views on the same 

subject with special reference to the smuts. Both these authors agreed that, in 

general, the most useful course is to defiiie-species by morphological characters 

and to reserve physiological and biological characters for the definition of groupings 

of subspecific rank, and this has been adopted as a guiding principle for 

the present work. Our attitude to the taxonomy of the British smuts has been 

conservative. We have made as few alterations as possible in both groupings 

and names, and whenever there is any doubt or the evidence appears to be 

inadequate no change has been made. Certain of the changes advocated call for 

comment as they affect smuts of economic importance. 

Cunningham (1924) and Rodenhiser (1926) each proposed the consohdation 

of the loose smut of wheat {Ustilago tritici) and the loose smut of barley {U. 

nvda) as a single species, and more recently this view has been supported by 

Fischer (1943). These two smuts are morphologically aUke and only differ in 

their pathogenicity. They may be compared with the specialized races of black 

rust (Puccinia graminis) which attack wheat and oats, and they should, it is felt. 

|V»-EG^


be united as one species for which, under the International Rules of Nomenclature, 

the name U. nuda must be adopted. For similar reasons Fischer has 

been followed in uniting the covered smuts of oats (USkolhri) and barley (U. 

hordei) as one species, U. hordei, and the claim to specific rank of the race of 

U. avenae on tall oat grass (U. perennans) is not admitted. The logic of these 

changes may not appeal to plant pathologists—^neither may the degrading of the 

dahlia smut (Entyloma dahliae) as a form of-B. calendulae, the species into which 

all the forms attacking Compositae have been united—but it is the pathologists 

themselves who have provided the precedent by their skilful treatment of such 

a difficult species complex as Puccinia graminis.


MOST of the large number of specimens on which the following account of the 

smut fungi of the British Isles is based will be found in the herbaria of the Royal 

Botanic Gardens, Kew [Herb. Kew.], the British Museum (Natural History) 

[Herb. B.M.], and the Commonwealth Mycological Institute [Herb. I.M.I.]. 

Other material examined is in the herbarium of the Ministry of Agriculture's 

Plant Pathology Laboratory, Harpenden [Herb. Path. Lab.], the Plowright and 

Grove sections of the herbarium of Birmingham University, and the comprehensive 

series of East Anglian smuts in the herbarium of Mr. E. A. Ellis. 

Whenever necessary and possible, sufficient specimens from Europe and other 

parts of the world were examined in order to establish the identity of the British 

material but, with one or two exceptions, the descriptions are based on collections 

made in these islands. 

The specific names have been carefully scrutinized. The full references to 

places of pubUcation are only given to establish the names adopted and for most 

species the synonymy is limited to names which have been used in this country. 

References to names for which the year only is given, and additional synonyms, 

may be found by consulting such standard works as those by Clinton (1904), 

Liro (1924, 1938), and Ciferri (1938). 

The time of occurrence is derived from the dates of collection of the specimens 

exaniined and for many species this period could probably be extended. 

The detailed distribution of most British smuts is uncertain. The twenty 

species here designated as 'widespread' occur in England and/or Wales, Scotland, 

and Ireland. Sampson (1940) compiled the published records for most species. 

The names of indigenous host plants are those recommended in the Check-List 

of British Vascular Plants (reprinted from J. Ecology, xxx, pp. 308-47, 1946). 

With the exception of Ustilago, the species have been arranged under the 

generic name in alphabetic order. 

USTILAGINAL^S Tulasne, 

Ann. Sci. nat., Bot., Ser. 3, vii, p. 73, 1847 

Mycelium inconspicuous, intra- then, usually, intercellular, systemic or localized 

at the point of infection. Sori conspicuous, generally forming exposed, 

powdery or agglutinated and usually dark-coloured spore masses at definite 

places on the host, especially in the flowers or inflorescence but frequently in the 

leaves and stems. Spores (chlamydospores) fight to dark in colour, smooth or 

variously ornamented, 4-35 /x diam., single, in twos, or in larger aggregates 

('balls') consisting of spores only or of spores and sterile cells. Sporidia 

(conidia) rarely formed on the surface of the host. Spore germination by a promycelium 

bearing lateral or terminal sporidia (basidiospores) which are frequently 

able to make saprophytic growth under natural conditions or in culture. 

Parasitic on plants, especiaUy the Gramineae and Cyperaceae. 

This Order has 33 genera arranged in two Families, the Ustilaginaceae and 

the TiUetiaceae. Two additional genera of palm-leaf parasites comprise the 

Graphiolaceae, a Famfly of somewhat uncertain relationship, which is frequently


included in the Ustilaginales. Representatives of 13 genera have been reported 

in the British Isles. 

Kerj to Families i 

a. Palm-Ieaf parasites . . . . . . • i • • Graphiolaceae 

a. Not palm-leaf parasites . . . . . . . ' . . . . b 

b. Promyceliiim transversely septate, sporidia lateral . . . Ustilaginaceae 

b. Promycelium non-septate, sporidia terminal . . • . . Tilletiaceae 

Key to Oenera 

of the Ustilaginaceae and Tilletiaceae reported in the British Isles 

Spores single . . . . . . . . . . . . b 

Spores in groups . . . . . . . . . . . . i 

b. Sori embedded in host tissue at maturity . . . . . . . c 

b. Sori not embedded in host tissue . . . . . . . . e 

Sori in swellings on roots, on Juncus . . . . . Entorrhiza p. 87 

(if on Eleocharis (Scirpus), see Ustilago marina, p. 75) 

Sori in leaves and stems . . . . . . . . . . d 

d. Spores dark in colour . . . . . . Melanotaenium p. 100 

d. Spores hyaline or light in colour . . . . . Entyloma p. 102 

Sori dusty at maturity . . . . . . . . . . . f 

Sori agglutinated at matiu-ity, on Cyperaceeie . . . . . Ointractia p. 78 

f. Sorus-covering a false membrane of fungus cells, on Polygonaceae 

Sphacelotheca p. 76 

f. Sorus-covering, if present, of host tissue . . . . . . . g 

Spores intermixed with sterile hyphal threads 

Spores not intermixed with sterile hyphal threads 

h. Spores large, usually 15-30 /i. diam. . 

h. Spores small to medium, usually 4^18 /i diam. 

Spores in twos, on Veronica . . . . 

Spores in balls . . . . . . 

j. Spore balls embedded in host tissue at maturity 

j. Spore balls not embedded in host tissue at maturity 

Spore balls having a cortex of sterilo cells, on aquatic plants 

Spore baUs without a cortex of sterile cells, on Primulaceae 

1. Spore balls having a cortex of sterile cells 

1. Spore balls without a cortex of sterile cells 

USTILAGINACEAE Schroeter, 

Krypt. Flor. Schles., iii (1), p. 266, 1887 

Tjrpe: Ustilago (Persoon) Roussel, 1806. 

Farysia p. 75 

. h 

Tilletia p. 81 

Ustilago p. 54 

Schroeteria p. 88 

j . 

. k 

1 

Doassansia p. 109 

Tuburcinia p. 90 

. Urocystia p. 92 

Thecaphora p. 80 

Spores usually exposed at maturity as a dusty or, less frequently, agglutinated 

spore mass. Spore germination by a septate promycelium bearing lateral 

sporidia or branches (see p. 20). 

USTILAGO (Persoon) Roussel, 

Flor. Calv., p. 47, 1806 

Type: Ustilago segetum Pers. on Gramineae, France.. 

Synonym: Ustilagidium'SAtTherg, 1895. 

Sori in various parts of the host, especially the inflorescence. Spore mass 

powdery, usually dark in colour. Spores single, small to medium, usually 

4-18 fj. diam. Spore germination, see p. 20. 

Differs from Tilletia in the methods of spore formation (see p. 15) and germination.

FIG. 2. Spore geimination in Ustilago. a. U. bistortarum. x 3S0 (Brefeld, 1895); 6. U. grandis. 

X400 (Brefeld. 1883); c. U. tragopogonis-pratensis. x460 (Tulasne, 1854); d. U. kiiehneana. 

X350 (Brefeld, 1883); e. U.vaillantii. x 1,200 (Schroeter, 1877);/. U. Imgissima. (Bauch, 

1923); g. U. hypodytes (as V. spegazzini and its var. agrestis). X 800 (Fischer & Hirschhom, 

1945 b); h. U. striiformis. X 350 and x 735 (Osner, 1916); i. U. bullata. x 400 (Brefeld, 1883); 

j. U. scabiosae. (Harper, 1899).

gg THE BRITISH SMUT FUNGI 

* Spores smooth or granular^ 

Ustilago longissima (Sow. ex Schlecht.) Meyen ^ 

\Uredo longissima Sowerby, Engl. Fungi., tab. 139, 17,99] 

Caeoma longissimum Schlechtendal, Flor. berol., ii, p. 129, 1824. 

Ustilago longissima (Sow. ex Schlecht.) Meyen, Pflanzen-Pathdlogie, p. 124,1841. 

Sort in the leaves as raised, dark, longitudinal streaks up to 1 mm. diam. and a 

few mm. to the length of the leaf long; the epidermal sorus covering, usually the 

upper, rupturing at maturity. Spore muss powdery, brown, dispersing to leave 

empty furrows in the leaf. Spores globose to sub-globose or more irregular, pale 

yellow-brown, apparently smooth, but under an oil immersion objective rough 

or granular, 4-6 ju, diam. 

On Glyceria maxima, and 0. fluitans. 

April-Oct. Widespread. Common. 

Exsiccati: on 0. maxima, Cooke, Fungi Brit. Exsicc., i, 55 B; ii, 71; Vize, Fungi 

Brit., 33; Vize, Micro. Fungi Brit., 568; on O. fluitans, Cooke, ibid., i, 55 A. 

Spore germination. The characteristic method of germination was described and 

figured by Fischer von Waldheim (1869), Brefeld (1883), and Plowright (1889), 

and recorded by several other workers (see Liro, 1924, p. 413). It is peculiar in 

that the promyceHum is very short (3-4 fx), scarcely projectiag from the spore, 

and cuts off apically a succession of sporidia. These grow rapidly in the nutrient 

solution, become septate, branch, and form more sporidia. Fusions occur and 

as the medium becomes exhausted sporidial production is replaced by mycelial 

growth. Paravicini (1917) observed the binucleate condition of mycelial cells 

following the fusion of sporidia. Hiittig (1931) claims that the longissima vaeihod 

of germination can be induced in Ustilago avewae by a low temperature (0° C.) and 

that U. longissima will form a four-celled promycelium (U. violacea type) at 35° C. 

Bauch (1923, 1930) and Kammerling (1929) studied incompatibility factors in 

U. longissima and in its variety macrospora. Four haploid nuclei are formed by 

the division of the nucleus in the chlamydospore, and two nuclei, -syhich usually 

differ in the factors that govern fusion, pass into the first sporidium. Consequently 

the uninucleate progeny of this sporidium will fuse inter se. Subsequent 

sporidia cut off from the promycelium carry only one haploid nucleus and their 

descendants will not fuse (see Fig. 2/). Fusion in U. longissima is governed by 

two pairs of allelomorphic genes. Normal fusion leading to the development of 

strong Suchfdden only occurs when the haplonts differ in both factors. If they 

have one factor in common a peculiar tangle of hyphae is formed and growth in 

culture is recognizably distinct (Bauch, 1930). 

Infection of host probably occurs through tiller buds (see Liro, 1924, p. 415). 

Ustilago hjTiodytes (Schlecht.) Fr. Stem Smut of Grasses 

Caeoma hypodytes Schlechtendal, Flor. berol., ii, p. 129, 1824. 

Ustilago hypodytes (Schlecht.) Fries, Systema, iii, p. 518, 1832. 

Sori in the stems, surrounding the internodes, when fully developed extending 

' The species of Ustilago have been grouped according to whether the spores are smooth 

or granular (see above), verrucose or echinulate (p. 60), or reticulate (p. 69), and they are 

arranged in increasing spore size within each group.

THE BRITISH SMUT FUJJGI 57 

from one node to the next and frequently aflFecting several successive intemodes 

or the entire stem (Plate I, Fig. 5), no special covering membrane but at first 

protected by the leaf sheaths; occasionally in the spiltelets. Spore mass powdery, 

dark brown, weathering away to leave the culm bare. Spores spherical to ovoid, 

sometimes more irregular, not infrequently, especially in some collections with 

a rather inconspicuous transparent cap at each pole, yellow-brown, smooth, 

4-7 (av. 4-5-5-0 ;LI) diam.i 

On Agropyron acutum, A. caninum, A. juncewm, A. pungens, A. repens 

Ammophila arenaria, Bromus carinatus, B. erectus, Elymus arenarius, Festuca 

gigantea, Trisetum flavescens. 

June-Sept. Widespread. Common. 

Exsiccati: Cooke, Fungi Brit. Exsic, i, 56; ii, 433; Vize, Fungi Brit., 35. Sydow, 

Dstilagineen, 10; Vestergren, Micromycetes rar. select.^ 1595. 

Spore germination. Several workers refer to the difficulty of germinating spores 

of this species (Fischer von Waldheim, 1869; Plowright, 1889; Viennot-Bourgin, 

1937; Bond, 1940). Winter (1876) figured a septate promycelium with one sporidium 

or a. TeMiveiy long Bierigma^ while BreMd (1^83) and Boss (1927}foand 

that the spores produced only a richly branched mycelium. Fischer & Hirschhom 

(1945 b) have photographed the germination of stem smut from 

several American forage grasses (Fig. 2 g). The proniyceUa become septate and 

put out protuberances which usually develop into branches. Occasionally (see 

Fig. 2gr (lower fig.), from Agropyron spicatum) these branches end in a sporidium, 

thus confirming some of the older conflicting records. In cultures branches grow 

above the medium and form chains of aerial sporidla (Boss, 1927; Bomhovd, 

1936; Kolk, 1943; Fischer & Hu-schhorn, 1945 b). Bornhovd paired 20 monosporidial 

cultures ^d failed to observe hyphal fusion, though the presence of 

coarser hyphae (Siichfaden) in old cultures suggested that fusion had occurred. 

Fischer & Hirschhom (1945 b) record fusions between detached sporidia. 

Infection of the host. The inoculation experiments of Bomhovd (1936) and Bond 

(1940) were inconclusive. Fischer (1945) successfully infected mature plants of 

Elymus canadeîsis; Agropyron trachycaulum, and A. cristatum. The plants were 

clipped back in August to about five in., sprayed with a suspension of spores, and 

kept moist for 48 hours. The smut did not sporulate until two or three years 

after inoculation. The failure of other methods of inoculation, namely, blossominfection 

and seed-contamination, showed that this ^mut is not seed-borne. 

The morphology and growth of the sterile leafy culms replacing normal 

inflorescences on infected plants of Bromus erectus £(,nd Elymus arenarius have 

been described by Feucht (1930) and Bond (1940). Infection is systemic and a 

perennial mycelium exists in the rhizome. In diseased plants the shoot follows 

a continuous development in contrast to the periodic growth of healthy rhizomes. 

Viennot-Bourgin (1937) has described the changes in anatomy induced 

in the host by this smut. 

^ This description was written before the publication of the paper by Fischer & Hirschhom 

(1945 b), in which V. hypodytes is considered to embrjice four species and one variety 

separable into two groups characterized by species whose spores possess or lack hyaline 

bipolar areas or appendages. After a re-examination of the JBritish material and a study of 

other collections from Europe and North America, it was decided to make no change at 

present in the taxonomy and nomenclature of this smut.


Ustilago hordei (Pers.) Lagerh. Covered Smut of Barley and Oats 

[Beticularia segetum BuUiard, 1791, P-p.] 

Uredo segetum subsp. hordei Persoon, Synopsis, p. 224, 1801. 

Uredo carbo de Candolle, 1815 [nov. nom. for U. segetum] p.p. 

Ustilago segetum (Pers.) Ditmar, 1817 [as ' U. segetum Link'] p.p. 

Ustilago carbo (DC.) Tulasne, 1847, p.p. 

Ustilago hordei (Pers.) Lagerheim, Mitt, badischen bat. Ver., p. 70 (March) 1889.' 

Ustilago avenae var. levis KeUerman & Swingle, 1890. 

Ustilago kolleri WiUe, 1893. 

Ustilago levis (Kellerm. & Swing.) Magnus, 1894. 

Sori in the spikelets replacing the ovaries and more or less of the tissues within 

the glumes. Spore mass firm, brown- or purpUsh-black, partly (or rarely completely) 

hidden by the glumes. Spores spherical to subspherical, pale yellow or 

greenish-brown, lighter in colour on one side than the other, smooth, 7-11 

(av. 8-5-9-0) fj, diam. 

On barley (Hordeum) and oats (Avena) causing Covered Smut. 

July-Sept. Widespread. Common. 

Spore germination has been studied by Fischer von Waldheim (1869), Kellerman 

& Swingle (1890), Brefeld (1895), Herzberg (1895), McAlpine (1910), Paravicini 

(1917), and others (see Liro, 1924). Stakman (1913), using a-race from barley, 

found that some spores germinated on water in 6^ hours and nearly all in 

24 hours. The growth of promycelia and sporidia follows the same plan as 

U. avenae (see p. 61). 

Infection of the host occurs during germination from spores lying on the surface of 

the grain or between the pales and the caryopsis. See p. 43. 

Racial specialization. Jacqzewski (1925) reported on the natural occurrence of 

U. hordei on rye in Siberia, and in the United States it occurs on Agropyron 

cristatum and Elymus glaucus jepsoni. Fischer (1939 a), using paired monosporidial 

cultures of covered smut from these hosts, produced infection on 

two varieties of barley and on the following grasses: Agropyron caninum, E. 

canadensis, E. glaucus jepsoni, E. sibiricus, Hordeum nodosum, and Sitanion 

jubatum. This race was physiologically distinct from covered smut of oats. 

Faris (1924 b) gives a table showing the infection of four differential varieties 

of barley by five physiologic races. Rodenhiser (1928), dealing mainly with 

cultural races, found that two differed also in pathogenicity. Aamodt & Johnston 

(1935) reported on two physiologic races at Alberta. Semeniuk (1940) in the 

same State detected four physiologic races in 1935-7 with an unexplained change 

in pathogenicity in 1938. Allison (1937) found that 27 out of 28 collections of 

covered smut could be differentiated on six varieties of barley, the type of 

infection varying with the race. Tapke (1937 b) distinguished eight races (including 

those of Faris) on five varieties of spring barley. Odessa was susceptible to 

all races. Later, 13 races were differentiated on eight varieties (Tapke, 1945, 

Table 1). New races were obtained by screening certain collections. Apart 

from pathogenicity, races differed in the size of colour of the chlamydospores, 

relative smoothness of the walls, degree of compactness of the heads, and mode

THE BRITISH SMUT FUKGI 59 

of exsertion. The most promising variety for breeding for resistance was 

Pannier C. 1. 1330. A change in pathogenicity attributed to hybridization 

resulted from the inoculation of Odessa with a mixture of two races of smut 

(Tapke, 1944). 

UstUago vaillantii Tul. 

Ustilago vaillantii Tulasne, Ann. Sci. not., Bot., Ser. 3, vii, p. 90, 1847. 

Sori in the anthers and, less frequently, the ovaries. Spore mass powdery, 

brownish-black. Spores globose, irregularly globose, or somewhat elongated, 

pale greenish-yeUow, smooth or slightly granular, 6-12 X 6-9 /x. 

On Chionodoxal uciliae, Muscari botryoides, M. cyaneo-violaceum, Scilla bifolia, 

S. verna. 

April. Widespread. 

Spore germination. Figures of germination made by Schroeter (1877), Brefeld 

(1883), Schellenberg (1911), Massee (1914), and Davie & Wilson (1914) suggest a 

similarity between this species and U. longissima (see p. 56). According to 

Schroeter (1877) a long eUiptical cell (16-18x3-5^ yu) arises on a short stem 

(3-5 X 2 /i) from which it is soon released; subsequently it becomes septate and 

cuts off sporidia directly or on short sterigmata. Additional sporidia (sometimes 

12 X 3, usually 4-6 X 2 /n) may develop from the promycelium (Fig. 2 e). Spores 

retain their viability for at least three months after being dried (Massee, 1914). 

Paravicini (1917) confirmed this method of germination in material from Scilla 

bifolia, observed fusions between sporidia, and figured nuclei. 

Infection of the host. The fungus is systemic and passes from the parent to newly 

formed bulbs. It wUl also infect young Scilla seedlings (Massee, 1914). 

Racial specialization. Ciferri (1938) distinguishes the form on S. bifolia as 

U. scillae Cif. 

Ustilago grandis Fr. Reed Smut 

Ustilago grandis Fries, Systema, iii, p. 518, 1832. 

Erysibe typhoides Wallroth, 1833, fide de Toni in Sacc. Syll., 1888. 

Ustilago typhoides (Wallr.) Berkeley & Broome, 1850 [Notices of British Fungi, 

No. 480]. 

Sori in the culms as raised, brown, longitudinal streaks, sometimes completely 

surrounding the culm and extending from one node to the next, at first covered 

by the epidermis (Plate I, Fig. 4). Spore mass powdery, brownish-black, 

weathering away to leave the culm bare. Spores globose or somewhat elongated, 

pale brown, smooth (or, under an oil immersion objective, granular) 10-12 X 

7-10 ;x. 

On Phragmites communis. 

July-Oct. Cambridgeshire [Herb. Kew]; Norfolk [Herb. I.M.I. 17263] 

Spore germination. Kiihn (1877) described germination, noting a tendency for 

the promycelia to separate from the spore before producing sporidia. Brefeld 

(1883), who found that spores would germinate in autumn and remain viable


until spring, described the promycelia as three- to several-celled, with numerous 

almost rod-like sporidia which became septate in nutrient solutions, budding o£f 

sporidia in the same manner as the promycelia (Fig. 2 b). Fusions (clampconnexions) 

occurred between promycelial cells. Bauch (1925), working with 

four different collections, found certain race peculiarities. In one sample sporidia 

fused readily, showing simple heterothallism, while sporidial cultures from other 

collections soon lost their capacity to unite. Whereas the promycelium was 

normally four-ceUed, spores were observed which had two bicellular promycelia. 

Ustilago omithogali (Schm. & Kunze) Magn. 

Uredo omithogali Schmidt & Kunze, Deutschl. Schwamme, p. 5, 1819. 

Ustilago omithogali (Schm. & Kunze) Magnus, Hedwigia, xiv, p. 19, 1875. 

Sori ia the leaves and pedicels forming raised, elongated blisters 1-0-10 mm. long, 

each at first covered by a layer of host tissue which later ruptures. Spore mass 

granular, purphsh-brown. Spores globose, subglobose, or ovoid, not infrequently 

somewhat angled as a result of mutual pressure, smooth, 12-19 (av. 15-0) /i • 

diam. 

On Gagea lutea. 

The only British collection [Herb. I.M.I. 32334] is that by W. G. Bramley, 

Tadcaster, Yorks., April, 1928 (see Mason, 1928). 

Spore germination. Cocconi (1889) germinated spores from Gagea arvensis in 

water and in a filtered extract of leaves from the host plants. Elliptical sporidia 

developed terminally and laterally on the septate promycelia. Fusions between 

cells of the promycelium and between sporidia were observed. 

** Spores verrucose or echinulate 

Ustilago avenae (Pers.) Rostr. Loose Smut of Oats 

[Reticularia segetum BuUiard, 1791, p.p.] 

Uredo segetum subsp. avenae Persoon, Synopsis, p. 224, 1801. 

Uredo carbo de Candolle, 1815 [nov. nom. for U. segetum], p.p. 

Uredo segetum e. decipiens Wallroth, 1815, fide Liro, 1924, p.p. 

Ustilago segetum (Pers.) Ditmar, 1817 [as ' U. segetum Link'], p.p. 

Erysibe vera holci-avenacei Wallroth, 1833, fide Ciferri, 1938. 


Ustilago avenae Jensen, 1889 [nomen nudum]. 

Ustilago avenae (Pers.) Rostrup, Overs. K. Danske Vid. Selsk. Forh. 1890, p. 13, 

1890. 

Ustilago perennans Rostrup, 1890, fide Fischer, 1943. 

Ustilago decipiens (Wallr.) Liro, 1924. 

Ustilago nigra Tapke, 1932, fide Fischer, 1943. 

Ustilago holci-avenacei (Wallr.) Ciferri, 1938. 

Sori in the spikelets replacing the ovaries and more or less the glumes (Plate I, 

Fig. 1); occasionally in the leaves. Spore mass firm then powdery, dark greenishbrown. 

Spores spherical to subspherical, pale greenish-brown and lighter in 

colour on one side than the other, minutely echinulate (echinulations especially

THE BRITISH SMUT FUNGI 61 

noticeable on the lighter side) or, occasionally, apparently smooth, 4-8 (av. 

6-0-6-5) /x diam. 

On oats {Avena), causing Loose Smut, and Arrhenatherum elatius. 


Exsiccati: Cooke, Fungi Brit. Exsicc, ii, 430. 

Spore germination was figured by Tulasne (1847), Kiihn (1858), Fischer von 

Waldheim (1869), Brefeld (1883), and others (see Lire, 1924). Herzberg (1895) 

and Stakman (1913) studied germination on different media and at varied 

temperatures. On water at 22° C. germination begins in ten hours or under with 

the emergence of one or two promycelia from a single spore. Fully grown 

promyceUa are one to three septate, and the sporidia, cut off from the apex and 

from the septa, are oval to elongate (2 X 4-7 X 7 /i). Fusions occur readUy between 

cells of the promycehum. or between abstricted sporidia. On nutrient media 

sporidial production is more abundant and more prolonged and the sporidia tend 

to be larger and subglobose (5x9 /x) (Stakman, 1913). 

Infection of the host takes place at germination from chlamydospores which 

have drifted between the pales at anthesis and produced resting myceUum on the 

inner surface of the pales and on the pericarp, or from spores lying on or within 

the pales which germinate only when the seed is sown. The relative significance 

of the two methods in nature is a matter of debate (Zade, 1922, 1924, 1939; 

Arland, 1924; Gage, 1927; Sampson, 1929; McKay, 1936). 

Bacial specialization in the oat smuts. It is convenient to consider together the 

two species, Ustilago avenae and the. oat race of U. hordei (U. kolleri), since most 

reports on physiologic speciaUzation cover both types of smut. Evidence of 

racial specialization was suppUed by Reed (1924,1925 a, 1927) who numbered and 

described eleven races of U. avenae and five of U. hordei (as U. kolleri) (Reed, 

1930). Some races originated in collections from countries outside the United 

States, notably U. avenae, race fi, and U. kolleri, race 4, from England and 

U. avenae, race 7, and U. kolleri, rslce 2, from Wales. These and some other races 

were described by Sampson (1925, 1928, 1929). The behaviour of six spore collections 

was studied over a ten-year period, three remained stable whUe others 

were changed by screening on selected oat varieties. Evidence was presented for 

the heterozygosity of certain collections (Sampson & Western, 1938). Leitzke 

(1937) inoculated an oat variety with a mixture of two races and obtained a 

distinct race, already known in nature, but presumably originating in his 

experiment by hybridization within the host. 

Further search revealed new races in the United States (Reed & Stanton, 

1932, 1936) and in 1940 Reed tabulated the source and behaviour of 29 races of 

U. avenae, differentiated on 17 oat varieties, and 14 races of U. hordei differentiated 

on ten varieties. Nine species of Avena were examined and in all species 

a variety was found susceptible to at least one race of smut. A. barbata was 

susceptible to all races and A. sativa, var. Canadian, to nearly all races of both 

species of smut. The results with aU races were remarkably constant over a 

number of years. 

Racial speciaUzation has not been completely surveyed in Britain but Radchffe 

(1940) analysed 120 field collections using a seedling reaction based on the

62 


progress of invading mycelium, as well as spore development in the mature 

plant. He detected seven races of V. avenae and five of U. hordei (as U. kolleri)^ 

three of which were identical with races isolated fijom field samples 15 years 

earher (Sampson, 1925,1929). Two races, GlofU. hordei and L 11 of C/. avenae^ 

showed identical pathogenicity to a wide range ofl hosts. Race L 16 of U. 

avenae was peculiar in producing the symptoms of covered smut upon many 

varieties. Oats belonging to the potato and sprig groups oiA. saliva (Marquand, 

1922) were susceptible to 11 races of smut, a fact which can be correlated with the 

well-known tendency for crops of these old varieties to be heavily smutted (Stapledon, 

1921). U. avenae is more common in Britain on oats than U. hordei, only 

23 among 120 collections belonged to the smooth-spored species (Radcliffe, 1940). 

In all the trials certain varieties stand out as resistant, notably Markton, 

Navarro, Victoria, and Black Mesdag, but none is immune from all races 

(Coffman et al., 1931; Radelescu, 1935 a; Murphy, Stanton, & CofFman, 1942). 

Black Mesdag can be infected by at least four races of U. hordei (Reed & Stanton, 

1936; Reed, 1940) and by one or more races of U. avenae (Roemer, Fuchs, & 

Isenbeck, 1937; Vaughan, 1938). Markton, at first regarded as immune (Stanton, 

Shepherd, & Gaines, 1924), may be slightly infected by some races of 

U. hordei (Smith & Bressman, 1931), but it is classed with Navarro and Victoria 

as a valuable parent in breeding work, (Stanton, 1933; Murphy, Stanton, & 

Coffman, 1942). Fulton, a resistant selection from the cross ]?ulghum XMarkton, 

is now known to be susceptible to a new race of U. avenae (Hansing, 

Heyne, & Melchers, 1945). 

That resistance to smut is usually dominant in oat crosses was shown by 

Humphreys & Coffman (1937) from a study of F^ and by others of Fg and Fg 

generations. Resistance is governed by one, two, or three pairs of factors 

according to the varieties crossed (Barney, 1924; Gaines, 1925; Rosenstiel, 

1929; Garber, Giddings, & Hoover, 1929; Schattenberg, 1934; Stanton, Reed, 

& Coffman, 1934; Austin & Robertson, 1936; Reed, 1925-40; Reed & Stanton, 

1925-37). Resistance to covered^smut is apparently recessive in the cross 

Danish Island x Monarch (Reed & Stanton, 1937). Inheritance to the two smuts 

is usually independent (Reed, 1931-5; Reed & Stanton, 1937-8), but crosses 

involving the resistant variety Black Mesdag show parallel results suggesting 

that the same factors, or closely Unked factors, are responsible for resistance to 

both smuts (Reed, 1934). 

Black Loose Smut of barley, U. avenae (U. nigra, see Fischer, 1943). 

This seedling-infecting smut, at first confused with U. nuda, has been known 

since 1914 (Johnson, 1914; Tisdale & Tapke, 1924; Tapke, 1932; Ruttle, 1934; 

Tapke, 1935 a; Moore & Allison, 1935 b; Leukel, 1936). It has a wide distribution 

in the United States (Moore & Allison, 1935 b) and in a recent survey 209 among 

500 collections of loose smut of barley belonged to this species (Tapke, 1943). 

It is easily distinguished from U. nuda by the abundance of sporidial growth on 

2 per cent, potato dextrose agar (Tapke, 1941). 

Fischer (1939 a) inoculated a number of grasses with paired monosporidial 

cultures of U. nigra and produced infection on Elymus canadensis, Hordeum 

Twdosum, and Sitanion jubatum. Tapke (1943 b) records Hordeum 'pusillum as a 

host of U. nigra, race 4.


Evidence of racial speciaKzation in this smut was given by Tapke (1936) and 

Josephson (1942). Tapke (1943 a) examined 168 collections and distinguished 

seven races. Race 4, which was most frequent, gave the same reactions on barleyvarieties 

as U. hordei, race 6. Races of U. hordei and U. avenae f. nigra readily 

hybridize and give rise to new forms (Bever, 1942, 1945). 

Ustilago nuda (Jens.) Rostr. Loose Smut of Wheat and Barley 

Vredo segetum subsp. tritici Persoon, 1801. 

Uredo carbo de CandoUe, 1815 [nov. nom. for U. segetum], p.p. 

Ustilago segetum (Pers.) Ditmar, 1817 [as ' U. segetum Link'], p.p. 


Ustilago segetum var. hordei f. nuda Jensen, Om Kornsortenes Brand, p. 61,1888. 

Ustilago segetum var. nuda Jensen, J. Roy. agric. Soc, Ser. 2, xxiv, p. 406,1888. 

Ustilago nuda (Jens.) Rostrup. Tidsskr. Landakon., viii, p. 745, 1889. 

Ustilago tritici (Pers.) Rostrup, (March) 1890. 

Ustilago tritici (Pers.) Jensen in Kellerman & Swingle, ©© 

(June) 1890. ^^ © 

Ustilago nuda (Jens.) Kellerman & Swingle, (June) 1890. y^Q 3 xjstilago nuda 

„ . . ,1 ., , , . , . ,T^, T -r-.. £M from wheat. Spores. 

8ori m the spikelets replacmg the ovaries (Plate I, lig. 2). x500. 

Spore mass firm, then powdery, dark greenish- or blackbrown, 

blowing away at maturity to leave the rachis bare. Spores spherical to 

subspherical or sometimes more irregular, pale yeUow-brown, lighter in colour on 

one side than the other, minutely echinulate, 5-9 (av. 6-5-7-0) fi diam. (Fig. 3). 

On wheat (Triticum) and barley (Hordium) causing Loose Smut. 

June-Aug. Widespread. Common. 

Exsiccati: Cooke, Fungi Brit. Exsicc., ii, 428. 

Spore germination. Brefeld (1888,1895), Kellerman & Swingle (1890), and others, 

(see Liro, 1924) described the non-sporidial type of germination characteristic 

of this smut. The chlamydospores are short-lived (see p. 18) and even fresh 

samples do not often give such high germination as U. avenae and U. hordei. 

According to Stakman (1913) spores from wheat begin to germinate on water in 

14-17 hours. A promycelium, usually only one, issues from the Hght-coloured 

area of the spore, branches after 24 hours, and forms either knee-joint fusions' 

between adjacent cells or connecting bridges between branches of the same 

promycelium or promycelia of near-by spores. Free promyceHa, detached 

segments, and sporidia are normally absent in this species, but on sugar solution 

the promycelium of the barley smut sometimes breaks up to form free segments 

(Stakman, 1913) and low temperatures also tend to promote fragmentation (see 

p. 42). After fusion the infection hyphae which grow out do not differ from 

other branches of the promycehum. 

Infection of the host. Experiments, substantiated by microscopic examination, 

established that the loose smut of wheat and barley gains entrance through the 

young ovary, passes to the growing-point of the embryo, and lies dormant until 

the seed germinates (Maddox, 1895,1897 ; Brefeld, 1903; Hecke, 1904; Freeman 

& Johnson, 1909). The progress of mycehum from the integuments to the

64 THE BBITISH SMUT FUNGI 

embryo sac and the invasion of all parts of the embryo except the roots and 

young leaf primordia was described by Lang (1909, 1917 b). Mycelium is viable 

in the seed for at least three years. Certain field conditions, such as deep sowing 

(4r-5 cm.), may deter the fungus from reaching the inflorescence (Tiemann, 1925). 

Resistant varieties of wheat may produce some viable seed on infected plants 

and there is evidence that such seed carries mycelium derived directly from that 

in the axis of the parent (Larose & Vanderwalle, 1939). 

Racial specialization. (1) On wheat. Evidence of physiologic specialization in 

the loose smut of wheat was presented by Tapke (1929), and by Hanna & 

Popp (1932). Hanna (1937) described four races from western Canada, two 

direct from the field and two obtained by screening other collections on selected 

wheat varieties, Grevel (1930), following other workers at Halle, found four 

distinct races among 48 collections from Germany and other countries. 

Radelescu (1935 a) recognized three of Grevel's races on summer wheat in 

Rumania. Oort (1940) found three races on wheat in Holland, aU distinct from 

the loose smut of barley. Many varieties of wheat were resistant both in the field 

and under efiicient methods of inoculation (see p. 45). Bever (1947) distinguished 

11 races among 52 collections from the eastern soft wheat region of 

the United States. 

Marquis, Garnet, Hope, Presto, and Hussar were among the highly resistant 

varieties in America. Resistance to loose smut is dominant in some wheat 

crosses, recessive in others (Tingey & Tollman, 1934; Rudorf & Rosenstiel, 1934). 

The resistance of the Fj is similar in reciprocal crosses, showing that infection of 

hybrids is determined by the nature of the embryo rather than the character of 

floral tissues in the female parent (Larose & Vanderwalle, 1937; Milan, 1939). 

In resistant varieties the fungus penetrates the base of the ovary but does not 

normally invade the embryo (Vanderwalle, 1942), Resistance is apparently not 

correlated with the degree of opening of the glumes at flowering or with sap 

acidity (Tapke, 1929). 

Some wheat varieties which are hypersensitive to certain races of loose smut 

are inhibited in growth, and their leaves may be curled and chlorotic in stripes. 

Death often occurs at the third leaf stage (Oort, 1944, 1947). 

A loose smut, capable of attacking both wheat and rye, has been reported 

from several States of the American Union. Partial destruction of the heads 

is more common in rye than in wheat (Humphrey & Tapke, 1925). A smut, 

indistinguishable from U. nuda, has been recorded on Agropyron sibiricum at 

Washington. The inflorescence was only partially destroyed and spore production 

sparse (Fischer, 1938). 

(2) On barley. Nahmmacher (1932) detected two physiologic races among 45 

collections. Vanderwalle (1932) described early and late forms of loose smut 

which differed also in the degree of infection, the former, under glasshouse conditions, 

producing sori on culms and leaves. Oort (1940) records that the races on 

winter and summer barley in Holland are distinct from each other and from 

loose smut on wheat. 

Many barley varieties, both German and foreign, were tested for resistance 

to loose smut at HaUe (see p. 44). Most of the foreign naked barleys of the 

inaequalis type were highly resistant, spring barleys of the nutans-c type and


winter inaequalis barleys were highly susceptible, while other types of barley 

included both resistant and susceptible varieties (Nahmmacher, 1932). No highly 

resistant varieties of winter or spring barley were found in HoUand (Oort, 1940). 

The inheritance of resistance has been studied both in Germany (Zeiner, 1932; 

Nahmmacher, 1932) and in the United States (Livingston, 1942). Eesistance 

appears to be dominant but not completely so in all crosses, and is sometimes 

controlled by a single factor. Interpretation of results is difficult, since no method 

of inoculation gives 100 per cent, infection in the susceptible varieties, and low 

results probably follow from death in the field of plants carrying smut. The 

infection of the embryo of Fj plants derived from reciprocal crosses between 

susceptible and resistant parents, indicates that hyphae can penetrate the floral 

tissues of plants bearing a dominant factor for resistance (Livingston, 1942). 

TJstilago bistortarum (DC.) Korn. 

Uredo bistortarum a pustulata 

' p marginalis de Candolle, Flor. franc, vi, p. 76, 1815. 

Caeorrut bistortarum (DC. [a]) Link, 1825. 

Caeoma marginak (DC. [jS]) Link, 1825. 

Ustilago marginalis (DC.) LeveiUe, 1848. 

Tilleiia bullata Fuckel, 1869 [nov. nom. for C bistortarum (DC.) Link]. 

Ustilago bistorfurum (DC.) Kornicke, Hedwigia, xvi, p. 38, March, 1877. 

Ustilago pustulata (DC.) Winter, 1880. 

Sori in the leaves either as rounded pustules 2-5 mm. diam. scattered over the 

surface or as a continuous band round the margin, at first covered by the 

epidermal layers. Spore mass powdery, purplish-black. Spores globose, ellipsoidal, 

or angled, pale purple, densely, but minutely, verrucose, 10-16 /x diam. 

On Polygonum bistorta and P. viviparum. 

July-Aug. Scotland (see Trans. Brit, mycol. Soc, xxiv, p. 297, 1940). 

Spore germination. The four-celled promyeeHum is borne on an empty basal cell, 

and the sporidia, which are produced laterally at two only of the septa, fuse in 

pairs while still on the promycelium (Brefeld, 1895) (Fig. 2 a). 

Liro (1924), Ciferri (1938), and others (see sjmonymy above) regard the 

pustulate and marginal forms as distinct species. 

Ustilago bullata Berk. ^ -^ • Ear Smut of Brome Grass 

Ustilago carbo a vulgaris S bromivora Tulasne, 1847, fide G. W. Fischer, 1937. 

Ustilago bullata Berkeley in Hooker, Flora of New Zealand, ii, p. 196,1855. 

Ustilago bromivora (Tul.) Fischer von Waldheim, 1867. 

Cintractia patagonica Cooke & Massee, 1899. 

Ustilago patagonica (Cooke & Massee) Ciferri, 1928. 

Sori in the spikelets replacing the flower parts and sometimes destroying the 

bases of the glumes, each covered by a membrane of host tissue, 4-10 mm, long. 

Spore mass firm then powdery, black. Spores globose, yeUow-brown, generally 

minutely verrucose, sometimes granular or apparently smooth, 8-12 (mostly 

9-10) ju. diam. 

On Bromus maximus, B. mollis, B. madritensis, B. secalimis, and B. unioloides. 

May-Jime. England. Fairly Common.

66 

THE BBITISH SMUT FUNGI 

This species has usually been designated U. bromivora (Tul.) Fisch. v. Waldh., 

but an examination of the type specimen of U. hullata Berk, on Triticum 

(Agropyron) scabrum from New Zealand confirms the aption of Fischer (1937) in 

reducing U. bromivora to a synonym of U. bullata. 

The type of Cintractia patagonica Cooke & Massee, a smut described on 

B. unioloides from Patagonia and subsequently reported in Lincolnshire on the 

same host grown from imported seed, was found to agree with U. bullata. 

Spore germination. Schroeter (1887) described the promycelium as cylindrical, 

spindle-shaped, readily falling away from the spore, becoming septate, and producing 

sporidia from the ends and sides. These, which were usually two-celled 

like the promycelia, gave rise to unicellular sporidia. Brefeld (1883) germinating 

spores from B. secalinus figured fusions between cells of the promyceUum and 

between the unicellular sporidia (Fig. 2 i). Plowright (1889) confirming these 

observations found that spores collected in June germinated freely in September 

and the general experience has been that spores of this species germinate easily. 

McAlpine (1911) also described and figured germination, following Brefeld in 

regarding it as a distinct type. Hiittig (1931) found, however, that the manner of 

growth varied with temperature. At 20° C. two-ceUed sporidia are cut off as 

described by previous workers but at 25° C. a four-celled promyceUum is formed 

with terminal and lateral sporidia (the so-called violacea type see p. 70). Subsequent 

development is characterized by the abundant production of sporidia by 

budding as in U. hordei and U. avenae and scanty mycelial growth (KoBs, 1943). 

Bauch (1925) working with six collections of U. bromivora [V. bullata] noted 

several variations of the method of germination. While some spores produced 

a normal four-ceUed promycelium others developed two promycelia each of 

which was two-ceUed, while others had one three-celled and one one-celled 

promycelium. The sporidia were always unicellular and fusion was governed 

by a single pair of factors. In certain collections neutral strains were discovered 

which could be distinguished from the normal so-called sexual strains by the 

special growth form of the colonies. Hirschhom (1941 b), working with collections 

of spores from species of Hordeum and Bromus, detected slight differences 

in the size and number of promycelial cells which might be diagnostic for 

physiologic races. 

Infection of the host arid racial specialization. Extensive inoculation experiments 

have shown that infection takes place at the seedling stage (Liro, 1924; 

Fischer, 1940 b).. Using 44 collections from 36 species of Agropyron, Bromus, 

Elymus, Festuca, Hordeum, and Sitanion, Fischer (1940 b) detected eight 

physiologic races by their reactions on 14 differential hosts. They include 

the races on Bromus secalinus and B. mollis which Liro (1924) raised to 

specific rank. 

Ustilago maydis (DC.) Corda Maize Smut 

[Lycoperdon zeae Beckmann, 1768.] 

Uredo segetum var. mays-zeae de CandoUe, 1805. 

Uredo maydis de CandoUe, Flor. franc, vi, p. 77, 1815. 

Uredo zeae Sehweinitz, 1822. 

Ustilago zeae Unger, 1836.


Ustilago maydis (DC.) Corda, Icones Fung., v, p. 3, 1842. 

Vstilago mays-zeae Magnus, 1895. 

Sori in the inflorescence and other aerial parts of the host as irregular sweUings less 

than 1 cm. to more than 10 cm. in length, at first limited by a white or cream membrane 

of host and fungus tissue. Spore mass powdery, very dark sepia. Spores 

globose or sub-globose to ellipsoidal, epispore bluntly echinulate, 8-12 fi diam. 

On Zea mays. 

Occasionally recorded in southern England. 

Exsiccati: Cooke, Fung. Brit. Exsicc., i, 433; ii, 431. 

Spore germination, which has been described by Brefeld (1895) and a number of 

other workers, takes place in nutrient solution at any time of the year. Terminal 

and lateral uninucleate sporidia are borne on a four-celled promycehum, 

singly or in simple or branched chains. Sporidial fusion occurs only under certain 

conditions (see p. 42). 

Infection of the host. Brefeld (1895) first demonstrated the localized infection of 

maize by U. maydis in contrast to the systemic infection of several other cereal 

smuts. The fungus can penetrate any part of the plant where the tissue is 

meristematic. Walter (1934) described the direct penetration of the epidermal 

wall and found that infection might arise either from the promycelium or from 

germinating sporidia. Chlamydospores and sporidia are distributed by wind 

and are very resistant to low temperature and to desiccation. The smut can ^ 

multiply and live for some time as a saprophyte in soil (Piemeisel, 1917). 

Chlamydospores retained viabihty in pure sand for eight years (Kornfeld, 1937) 

and were not always destroyed by silage (Perlet, 1938). In the United States dry 

weather conditions are most conducive to infection (Immer & Christensen, 1928). 

Racial specialization. Ustilago maydis, a heterothalhc species, comprises an 

indefinite number of biotypes differing in pathogenicity and other characters 

(Christensen, 1931; Christensen et al., 1929; Hirschhorn & Hirschhom, 1939). 

Isolations from a single smut gall differed in their reactions on inbred fines of 

maize under artificial methods of inoculation (Eddins, 1929 a), but collections of 

smut spores from separate geographical areas were often aHke in pathogenicity 

when tested on selfed fines of maize under field conditions. Eesistance and suseeptibUity 

are governed by genetic factors. Flint varieties are more susceptible than 

dent varieties (Hayes et al., 1924), but rpsistailt selections can be found in most 

types of maize, and breeding for resistance offers the most promising method of 

control (Immer & Christensen, 1925; Immer, 1927; Immer & Christensen, 1931; 

Christensen & Johnson, 1935). 

Ustilago striiformis (Westend.) Niessl Stripe Smut of Grasses 

Ustilago salvei Berkeley & Broome, 1850.^ 

' Berkeley & Broome (Notices of British Fungi, No. 482) described V. salvei on Dactylia 

glomerata collected by Rev. T. Salwey, St. Martin's, Guernsey. De Toni {Sacc. Syll., va, 

p. 485, 1888) listed U. salvei as a synonym of U. striiformis, and Liro (1922) used the name 

for a smut on D. glomerata which he considered to be distinct from V. striiformis. Examination 

of the Berkeley and Broome type in Herb. Kew. shows the host to be Holcus lanatus 

and the fungus to be V. striiformis. As the niles stand at present XJ. salvei Berk. & Br. 

appears to be the valid name for the fungus now widely known as V. striiformis, but we agree 

with Stevenson (Plant Dis. Beptr, xxx, p. 53,1946) in not advocating the adoption of the 

former name.

68 THE BRITISH SMTJT FUNGI 

Uredo striaeformis Westendorp, Bull. Acad. roy. Bdg.j xviii, p. 406, 1852. 

Ustilago striaeformis (Westend.) Niessl, Hedtoigia, xv, p. 1, 1876. 

Tilletia de baryana Fischer von Waldheim, 1867, fide ê Toni, 1888. 

Tilletia striaeformis (Westend.) Saccardo, 1877 [as 'T. striaeformis (Westend.) 

Niessl']. 

Sori in the leaves forming longitudinal raised streaks at first covered by the 

epidermis which ruptures to expose the spores, the leaves spHtting into ribbons 

(Plate I, Kg. 3); rarely in the stems and inflorescences. Spore mass powdery, 

dark brown. Spores spherical to ellipsoidal, yellow-brown, echinulate, 9-14 

(av. 10-5-11-5) /i diam. - v 

On Arrhenatherum elatiiis, Dactylis glomerata, Deschampsia caespitosa, Festuca 

ovina, F. rubra, Holcus lanatus, H. mollis, Lolium perenne, Phalaris arundinacea, 

Phleum pratense, and Poa pratensis. 

May-Sept. Widespread. • Common. 

Exsiccati: Cooke, Fungi. Brit. Exsicc, i, 57; Vize, Fungi Brit., 133; Vize, Micro. 

Fungi Brit., 222. 

Spore germination. Spores of this species do not always germinate readily (see 

p. 18). Clinton (1900) germinated the spores, but the first clear figures of germination 

were those of Osner (1916) who obtained the best results with spores 

from Agrostis sp. Many media were tried, but the character of the medium did 

not affect the number of spores germinating or the method of growth. The 

promycelia became septate as the protoplasm collected towards the tips. 

Irregular branching often occurred without fusions, but some spores were found 

with simple, septate promycelia having clarnp-connexions between the cells 

(Fig. 2 h). Davis (1924) obtained somewhat similar results with spores from 

timothy, bent, and cocksfoot, the promycelia branching in a manner resembling 

U. nuda. Typical sporidia were rarely produced, but under some conditions 

short, uninucleate fragments did separate from the promycehum. Kreitlow 

(1943 a) figured branched promycelia in a form collected on Agrostis. Fischer 

(1940 a) collected a new race (f, hordei) on Agropyron paucijiorum and Elymus 

glaucus which germinated without a rest period, developed two or three promycelia 

from each spore, and budded off eUiptical sporidia which fused on nutrient 

agar. They were compatible with appropriate sporidia of U. bullata. Branched 

promycelia developed from chlamydospores of the form from Poa pratensis and 

gave rise on agar, to two types of colony, one breaking up into fragments, the 

other mycelial. Some cultures of each type developed chlamydospores and these, 

though slightly abnormal in size and shape, germinated like those from the host 

(Leach, Lowther, & Ryan, 1946; Leach & Ryan, 1946). See also Thirumalachar 

& Dickson, 1947. 

Infection of the host occurs through the young coleoptile and tiller buds. Contaminated 

seed of Poa pratensis gave only a low percentage (0 to 3 per cent.) of 

infection but high figures were obtained by sowing seed in inoculated soil and 

by injecting chlamydospores into the stem near the growing point. The disease 

was slow to develop; in some plants 300 days elapsed before sori appeared. 

Experiments showed that inoculum can persist in the soil under greenhouse 

conditions for 256 days (Leach, Lowther, & Ryan, 1946). Liro (1924) using spore

THE BRITISH SMUT FUlJGI 69 

material from AlopexMrus pratensis, Deschampsia caespitosa, and Dactylis 

glomerata infected the hosts named by sowing contaminated seed. Negative 

results were obtained with other grasses. Davis (1926) showed that stripe smut 

infects Phleum pratense at the seedling stage. The disease wiU persist for several 

years in perennial grasses, but infected plants tend to die under adverse conditions 

such as drought (Leach, Lowther, & Ryan, 1946). 

Bacial specialization. This species has been variously subdivided by Liro (1924), 

Ciferri (1938), Fischer (1940 a), and other workers an(i in this country it has been 

confused with the closely related but possibly distinct U. macrospora (q.v.). A 

stripe smut with larger spores (14-17 n) on Phalaris has been distinguished as 

U. echinata Schroet. but the one British collection (Sridge of Dun, Angus, coll. 

R. W. G. Dennis, 26.vii.43, Herb. Kew.) of stripe smut of this host examined does 

not differ morphologically from U. striiformis. 

Ustilago macrospora Desm. 

Ustilago macrospora Desmazieres, PI. Crypt, franc. No. 2127, 1850. 

Differs from TJ. striiformis (q.v.) in the spores \\rhich are spherical to ellipsoidal 

but frequently somewhat elongated or angular, yeUow-hrown, coarseJj 

echinulate or verrucose to papillate, at times somewhat reticulate or striate, 

11-18 (av. 13-5-14-5) [j. diam. 

On Agropyron repens, A. junceum, Bromus erectus, and Calamagrostis canescetis. 

May-Aug. England (Norfolk, Surrey), Guernsey, S(>otland. 

The first British record is by V. J. Chapman (Tratis. Norf. Nonvich Nat. Sac, 

xiii, p. 302, 1932) on A. junceum, Scolt Head, Norfolk [Herb. Kew.]. 

Spore germination. Unknown. 

Racial specialization. It is doubtful if the stripe smut of Calamagrostis distinguished 

as U. calamagrostis (Fuckel) Clinton is a morphologically distinct species. 

The one British collection (Wheatfen Broad, Norfolk, coU. E. A. ElHs, 9.vu.44, 

Herb. I.M.I. 32329) on C. canescens does not differ from U. macrospora from 

other grasses in this country. 

*** Spores reticulate 

Ustilago vinosa Tul. 

Uredo vinosa Berkeley in litt. to Tulasne [nom. nud.]. 

Ustilago vinosa Tulasne, Ann. Sci. nat., Bot., Ser. 3, vii, p. 96,1847. 

Sori involving the flower parts within the perianth, which is frequently inflated. 

Spore mass powdery, pinkish purple. Spores globose to sub-globose, tinted 

violet, delicately reticulate (reticulations 1-0 fi or slightly less in diam.), 6-10 

(mostly 7-8) n diam. [Type specimen in Herb. Kew.] 

On Oxyria digyna. 

July. England (Cumber!.), Scotland (Forfarshire). Uncommon. 

Spore germination. Sporidia develop from a four-celled promycelium, bud, and 

fuse readily in nutrient solution (Brefeld, 1883). 

Infection of the host. Unknown. Mycelium is said to be perennial in the root 

stock (Schellenberg, 1911).


Ustilago violacea (Pers.) Fuckel 

Uredo violacea Persoon \pisp. Meih. Fung., p. 57, 1797] ex Persoon, Synopsis, 

p. 225, 1801. ' 

Farinaria stellariae Sowerby, 1803, fide Fries, 1832. , 

Uredo antherarum de CandoUe, 1815 [nov. nom. for U\ violacea Pers.]. 

Ustilago antherarum (DC.) Fries, 1832. 

Ustilago violacea (Pers.) Fuckel, Symb. mycol., p. 39, 1869 [as '(Pers.) Tul.']. 

8ori in the anthers (Plate II, Fig. 2). Spore mass powdery, pinkish purple. Spores 

spherical or sub-spherical to elUpsoidal, tinted pa-le violet or almost hyahne, 

delicately reticulate (reticulations about 1 fj. diain.) 5-12 (av. 7-8) /A diam. 

On Cerastium viscosum, Cucubalus baccifer, Dianthtts caryophyllus (cultivated 

carnation). Lychnis flos-cuculi, Melandrium album, M. dioicum, Silene acaulis, 

S. alsine, S. cucubalus, S. maritima, S. otites, Stellaria graminea, and S. holostea. 

May to October (and at other times on carnations under glass). Widespread. 

Common. 

Exsiccati: Cooke, Fungi. Brit. Exsicc, ii, 427; Vize, Fungi Brit., 34; Vize, 

Micro. Fungi Brit., 569. 

Spore germination. Spores of this species germinate easily when fresh and remain 

viable for some time. Tulasne (1847) described the septate promycelium 

which falls somewhat easily from the spore. Schroeter (1877) described the 

sporidia from the smut on Dianthus carthusianorum as elliptic, often flattened on 

one side, 4x2-3 /x. Fischer von Waldheim (1869), Brefeld (1883), and Schellenberg 

(1911) also figured germination and it has been accepted as a type which 

like U. avenae readily produces a four-celled promycelium with sporidia sprouting 

from each cell. PlowTight (1889) germinated spores of the form known as 

U. major on Silene otites and Liro (1924) described fusion between sporidia in 

the form on Silene vulgaris [S. cucubalus]. According to Harper (1899) who 

studied nuclear division in the sporidia, one nucleus may remain in the spore 

and a second or third promycelium develop after the first has fallen off. Fusions 

readily occur in cultures several days old between appropriate cells of the promycelium, 

between these and sporidia, or among the sporidia and their progeny. 

Paravieini (1917) also figured fusions of uniaucleate sporidia. The classic work 

of Kniep (1919, 1928) which established heterothalHsm in the Ustilaginales was 

conducted on this species (see p. 29). 

Infection of the host. The fungus can infect the plant through seedlings, underground 

shoots, and axOlary buds (Hecke, 1907,1926; Werth, 1913; Zfilig, 1921; 

Liro, 1924). It is apparently not carried by the seed as in loose smut of wheat, 

but if spores are sown on the ovaries of healthy flowers the fungus will invade the 

plant and a few months later the newly formed blossoms haye infected anthers. 

When female plants are attacked, the flower develops on a longer floral axis and 

has a cylindrical calyx more like that of the male. Stamens which would 

normally remain rudimentary develop and contain chlamydospores as on infected 

male plants (Werth, 1913, Fig. 1). 

Racial specialization. ZilHg (1921) recognized eight physiologic races of anther 

smut and showed that the fungus would not pass between two such closely 

related hosts as Melandrium album and M. dioicum. Liro (1924) tabulated the


results of many infection experiments and gave specific rank to eleven forms of 

anther smut on members of Caryophyllaceae (see also CSferri, 1938). 

The anther smut of Silene otites has been distinguished as U. major Schroet. on 

account of its larger spores, but as the spore size (8-10 /x) in the one British 

collection (Vize, Micro. Fungi Brit., 569) examined on this host fell within the 

range of variation shown by collections from other hosts of the same and different 

genera, this distinction is not made here. 

Ustilago scabiosae (Sow.) Winter 

Farinaria scabiosae Sowerby, Engl. Fungi, Tab. 396, Fig. 2, 1803. 

Ustilago scabiosae (Sow.) Winter, Hedwigia, xix, p. 159, 1880. 

Sori in the anthers. Spore mass powdery. Honey Colour (Ridgway), filling the 

florets and giving the flower heads a dusty appearance. Spores globose to subglobose, 

tinted pale yellow, wall about 2 [j, thick, epispore hyaline, reticulate 

(reticulations up to 1-0 jn diam.), 8-11 [i diam. 

On Knautia arvensis. 

July-Aug. Widespread. • Fairly Common. 

Exsiccati: Vize, Fungi Brit., 566 (as U. flosculorum var. succissae). 

Spore germination. Germination has been figured by Fischer von Waldheim 

(1869), Schroeter (1877), Brefeld (1883), Plowright (1889), and Harper (1899) 

(Fig. 2 j). According to Schroeter (1877) the triseptate promyceUa (16-20 X 5-6) fj. 

produced shortly ovate sporidia which tended to become round (about 6 /ii) later. 

PromyceUa often feU away from the spores. Budding in nutrient solution was 

described as particularly profuse by Brefeld (1883) and the sporidia were nearly 

spherical (4-5 X 4 /x). Harper (1899) described the passage of the chlamydospore 

nucleus into the promycelium and its division when the promycelium has attained 

one-third of its mature length. Paravicini (1917) figured the fusion of sporidia. 

Infection of the host. Experiments by Liro (1924) suggest that seedKngs and 

underground parts of mature plants can be invaded by this smut. 

Ustilago succisae Magn. 

Ustilago succisae P. Magnus, Hedwigia, xiv, p. 17, 1875. 

Sori in the anthers. Spore mass granular to powdery, white or cream. Spores 

globose to sub-globose, colourless, wall 2^7i thick, epispore hyaline, reticulate 

(reticulations up to 1-0 /x diam.), 11-14 fi diam. 

On Succisa pratensis. 

Aug.-Oct. Widespread. Common. 

Spore germination. Magnus (1875) observed germination in September and 

December. Sporidia were budded oif terminally and laterally from the fourcelled 

promyceUa at first singly and later in groups of three. Budding occurred 

before and after the sporidia became detached. Fusions were not observed. 

Ustilago flosculorum (DC.) Fr. 

Uredo flosculorum de CandoUe, Flor. franc, vi, p. 79, 1815. 

Ustilago flosculorum (DC.) Fries, Systema, iii, p. 518, 1832. 

Sori in the anthers. Spore mass powdery. Brown Vinaceous (Ridgway). Spores


glotose to sub-globose or ovoid, light brown tinged with violet, wall 2 [J, thick. 

Epispore hyaline or tinted, reticulate (reticulations l'5-2-0 IJ. diam.), 12-16 ft 

diam. 

On Knautia arvensis. ' , 

July. England (Yorks.), Scotland (Fife): Uncommon. 

Spore germination. Unknown. Some of the records for U: scabiosae may refer to 

this species. 

Ustilago utriculosa (Nees) Tul. 

Caeoma utriculosa Nees, Syst. Pilze, i, p. 14, 1817. 

Ustilago utriculosa (Nees) Tulasne, Ann. Sci. nat., Bot., Ser. 3, vii, p. 102, 1847. 

Sori in the flowers inflating the ovaries and involving the filaments of the 

stamens, about 2-3 mm. long. Spore mass powdery, 

brownish violet. Spores globose to sub-globose, violet 

when fresh, brownish violet when dry, with prominent 

reticulations (2 to 3-4 /Lt wide, 1-5-2 y. deep), 

11-14/^ diam. (Fig. 4:b). 

On Polygonum lapathifolium and Polygonum sp. 

Aug .-Sept. Yorks. 

Exsiccati: Vize, Micro. Fungi, 132. 

This species is similar to U. anomala (q.v.).with 

FIG. 4. o. Ustilago anomala. '^^^^^ i* has been confused. It appears to be of less 

Spores from type collection, frequent Occurrence in Great Britain than 17. anomala. 

x500. 6. U. utriculosa. 

Spores. x500. Spore germination. The four-celled promycehum bears 

apical and lateral sporidia which produce secondary 

sporidia by budding or germ-tubes. No sporidial or hyphal fusions were observed 

by Brefeld (1895) or by Fischer & Hirschhorn (1945 a), but Liro (1924, p. 208) 

who germinated spores of this species and of U. anomala records the fusion of 

sporidia still attached to the promycelium. Infection of the host occurs at the 

seedling stage. 

Physiologic races. The net-spored smuts attacking species of Polygonum can be 

subdivided into physiologic races some of which diifer slightly in size of spore. 

Several races have been given specific rank (Liro, 1924; Ciferri, 1938). 

Ustilago anomala Kunze 

Ustilago anomala J. Kunze, Fungi select, exsicc, No. 23, 1875. 

Similar to U. utriculosa (q.v.) from which it differs in the globose, sub-globose, 

or ovoid spores having more delicate reticulations (up to 2 /x wide, about 1 ft 

deep) (Fig. 4 a). 

On Polygonum convolvulus, P. hydropiper, and P. persicaria. 

Aug.-Oct. Widespread. Fairly common. 

Spore germination has been described by Schroeter (1877) and Brefeld (1895). 

Germination occurs in the spring after overwintering when sporidia are produced 

on a four-celled promycelium. The sporidia after fusing in pairs become 

detached from the promycehum and then produce germ-tubes or, in nutrient 

splution, bud off secondary sporidia to give yeast-like colonies.


TTstilago tragopogonis-pratensis (Pers.) Roussel 

[Uredo tragopogi Persoon, 1797.] 

Uredo tragopogi pratensis Persoon, Synopsis, p. 225, 1801. 

Ustilago tragopogi pratensis Roussel, Flor. Calvados, p. 47, 1806. 

Uredo receptaculorum de CandoIIe, 1808, p.p. 

Uredo receptaculorum tragopogi de Candolle, 1815, fide de CandoUe, 1815. 

Ustilago receptaculorum (DC.) Fries, 1832. 

Ustilago tragopogi de Toni, 1888 [as '(Pers.) Schroet.']. 

Sori in the inflorescence destroying the florets. Spore mass powdery, dark 

purple. Spores globose or sub-globose to slightly elongated, pale violet, delicately 

reticulate (reticulations 1-2 /i diam.), 12-14 /A diam. 

On Tragopogon pratensis and T. porrifolius (salsify). 

May-June. Widespread. 

Exsiccati: Cooke, Fungi. Brit. Exsicc., i, 59; ii, 434; Vize, Fungi Brit., 134. 

Spore germination has been figured by Tulasne (1854) (Fig. 2 c), de Bary (1866), 

Fischer von Waldheim (1869), and Brefeld (1883). The sporidia arising from the 

four-ceUed promycelium are long, almost rod-shaped, 14-24 X 2-5-4-5 /i (Fischer 

von Waldheim), 18-22 x 2-5-3 /x (Liro, 1924). They usually bend so that the long 

axis is parallel with the promycelium and fuse readily either before or after 

detachment. Paravicini (1917) figured the fusion of eUiptical uninucleate 

sporidia. Tulasne (1854) germinated the nearly related small spored species on 

Scorzonera. The sporidia were very small and oblong and budded profusely. 

Fusions were not observed. Brefeld (1883) agreed with Tulasne but Paravicini 

(1917) claims to have found fusions in old cultures. 

Infection of the host. Liro (1924) showed experimentally that this smut is seedborne. 

He failed to get conclusive evidence on the exact mode of transmission 

but suggests that flower infection may occur as in loose smut of wheat. 

Ustilago kuebneana Wolff 

Ustilago kuhneana Wolff, Bot. Zeit., xxxu, p. 815, 1874. 

Sori in the inflated ovaries or anthers; itt-'the stems, especially the upper 

branches of the inflorescence, as spot-like or elongated blisters which burst to 

give spore-filled lesions; less frequently, in the leaves. Spore mass powdery, 

pinkish purple. Spores spherical, pale yellow or yellowish brown tinged with 

purple, reticulate, 12-20 (av. 13-16 or occasionally more) /x diam. 

On Eumex acetosa, B. acetosella, and B. crispus. 

June-Sept. England, Scotland. Fairly Common. 

Exsiccati: Cooke, Fungi Brit. Exsicc., ii, 436. 

Spore germination. Wolff (1874 b) germinated the spores on water and obtained 

a three or four-celled promycelium with lemon-shaped sporidia which were not 

seen to fuse. Brefeld (1883) figured the sporidia in whorls at each septum. In 

nutrient solution they budded profusely and fusions were observed.

FIG. 5. Spore germination in Farysia, Sphacelotheca, Cintractia, and Thecaphora. 

o. F. oUvacea. (Yen, 1938); 6. S. hydropiperis. X 300 (Brefeld, 1895); c. C. siibinclusa. x 300 

(Brefeld, 1895); d. O. carieis. X 150 (Brefeld, 1895); e. C. karii. x225 (PohjakalUo, 1935); 

/. T. deformans (as T. lathyri). x 150 (Brefeld, 1883); g. T. seminis-convolvuli (as T. hyalma). 

X520 (Woronin, 1882).


Species incertae sedis 

Ustilago maxina Dur. d. Maisonn. 

Ustilago marina Durieu de Maisonneuve in Tulasne, Ann. Sci. nat., Bot., Ser. 5, 

V, p. 134, 1886. 

8


Yen (1938) obtained germination in 12 hours in sterile water, carrot juice, and 

beerwort. Sporidia were normally budded off'directly from the spore. Sometimes 

a longer tube was formed which became detached, divided into two cells, 

and budded off sporidia (Fig. 4 a). The method of growth is said to be identical 

with that of U. longissima var. macrospora as described by Bauch (1923). 

SPHACELOTHEOA de Bary, 

Vergl Morph. Biol. Pilze, p. 187, 1884. 

Type: Sphacelotheca hydropiperis (Schum.) de Bary on Polygonum hydropiper. 

Synonym: Bndothlaspis Sorokin, 1890. 

Sori in the inflorescence, frequently confined to the ovaries, each Umited by a 

definite false membrane of colourless, sterile, fungus cells. (Spore mass powdery, 

dark in colour, surrounding a central columella (usually of host tissue). Spores 

single. Spore germination, see below. 

Sphacelotheca destraens (Schlecht.) Stev. & A. G. Johns. Millet Smut 

Caeoma destruens Schlechtendal, Flor. berol., ii, p. 130, 1830. 

Uredo segetum var. panici-miliacea Persoon, 1801. 

Ustilago panici-miliacea (Pers.) Winter, 1884'. 

Sphacelotheca panici-miliacea (Pers.) Bubak, 1912. 

Sphacelotheca destruens (Schlecht.) Stevenson & A. G. Johnson, Phytopathology, 

xxxiv, p. 613, 1944. 

Sori destroying the inflorescence, 7-5 cm. long, at first covered by a whitish 

membrane of fungus tissue which ruptures irregularly to expose the spore mass 

which is traversed longitudinally by numerous strands of host vascular tissue. 

Spore mass powdery, dark brown. Spores globose to sub-globose, light brown, 

apparently smooth but under oil immersion obscurely punctate, 7-11 ja diam. 

On Panicum miliaceum. 

Billing, Northants., Sept. 1944, E. F. Hurt (Herb. Path. Lab. No. 164). 

Spore germination. The spores germinate in autumn and in spring of the following 

year. Some were viable in collections eight years old. On water they formed 

a four-celled promyceHum with fusions between adjacent and distant cells. On 

nutrient solution sporidia (10-15 X 3-5 /a) were budded off from the promycelium, 

while in older cultures sporidia germinated and formed aerial mycelium and 

chains of aerial sporidia (Brefeld, 1883). Vasey (1918) obtained abundant 

sporidia from spores germinating in water. On nutrient agar at room temperature 

ovoid to elliptical sporidia were produced on a four-celled promycelium 

(Fischer & Hirschhom, 1945 a). 

Infection of the host takes place on germination of the seed before the seedlings 

are three in. high (Vasey, 1918). This is confirmed by the fact that the smut can 

be controlled by seed treatments (Yatz3niina, 1927). 

Sphacelotheca hydropiperis (Schum.) de Bary 

Uredo hydropiperis Schumacher, Enum. A. Saell., ii, p. 234, 1803. 

Ustilago candollei Tulasne, 1847, p.p.

" TJSE BRITISH SMUT FUNGI 77 

Ustilago hydropiperis (Schum.) Schroeter, 1877. 

Sphacelotheca hydropiperis (Schum.) de Bary, Vergl. Morph. Biol. Pilze, p. 187, 

1884. 

Sori in the flowers, replacing the ovaries and projecting from the perianths, 

each covered by a greyish false memljrane of globose to ^~. 

polygonal, hyaline or slightly tinted cells, mostly 8-14 but /^ SiU) 

up to 24 ju, diam., which disintegrates from the apex to 

expose the spores. Spore mass powdery, purplish black, 

surrounding an unbranched central columella which re- pjQ. 7. Sphacelotheca 

mains after the spores have been dispersed. Spores globose, hydropiperis. Spores. 

purplish, apparently smooth but when examined under an 

oil immersion objective seen to be abundantly verrucose, 10-14 fi diam. (Fig. 7). 

On Polygonum hydropiper. 

Sept.-Oct. Widespread. Common. 

Exsiccati: Cooke, Fungi Brit, exsicc., i, 58 (as U. utriculosa), 59; ii, 72; Vize, 

Micro. Fungi, 134. 

Spore germination. Schroeter (1887) described, but did not figure, germination. 

The promycelium became four-celled and formed eUiptical sporidia, which fused 

in pairs at the base. Brefeld (1895) figured germination of the same type but 

without the fusion of sporidia (Fig. 5 6). Boss (1927) also failed to find fusions. 

Infection of the host. Liro (1924) sowed, in the autumn, seeds of several species of 

Polygonum together with spores of this species. They were left covered with a 

thin layer of soil in the open until the following year. P. hydropiperis gave the 

highest infection in all experiments but P. persicaria and several other species 

were readily infected. Some species of Polygonum were immune. (See Liro, 

1924, p. 141.) 

Sphacelotheca inflorescentiae (Trel.) Jaap 

Uredo bistortarum y ustilaginea de Candolle, 1816 fide Liro, 1921. 

Ustilago bistortarum (DC.) Korn. var. inflorescentiae Trelease in Harriman 

Alaska Exped., Crypt. Bot., v, p. 35, 1904. 

Ustilago inflorescentiae (Trel.) Maire, July-Aug., 1907. 

Sphacelotheca polygoni-vivipari Schellenberg, Oct., 1907 [nom. nov. for U. 

bistortarum var. inflorescentiae]. • 

Sphacelotheca inflorescentiae (Trel.) Jaap, Ann. mycol., Berl., v, p. 194, 1908. 

Ustilago ustilaginea (DC.) Liro, 1921. 

Sphacelotheca ustilaginea (DC.) Ciferri, 1938. 

Sori in the bulbils of the inflorescence. Spore mass granular, purpUsh black, 

surrounding a short columefla of host tissue. Spores globose to ellipsoidal, violet 

to brownish violet, distinctly but minutely and densely verrucose, 11-16 /x diam. 

On Polygonum viviparum. 

Scotland: Ben Lui (June, 1914) and Ben Ledi (June, 1921), Perthshire (Malcolm 

Wilson, Trans. Brit, mycol., Soc, ix, p. 143, 1924). 

Spore germination,. Schellenberg (1907) has described and figured the germination. 

The promycelium has three to five cross-walls, seldom more, on which


ovoid sporidia are borne at the apex and at the septa-. The basal cell of the 

promycelium becomes empty. Conjugation between sporidia was not observed 

but they were seen to bud off secondary sporidia. I 

Infection of the host probably takes place through the bulbils (ScheUenberg, 

1907). '' 

It is rather doubtful whether this smut, which shows affinities to S. hydropiperis 

and Ustilago bistortarum, should be treated as a distinct species. The 

spores of the Ben Lui material differ from those of S. hydropiperis in being 

clearly verrucose without resort to an oil immersion objective but the presence 

of a false membrane within the covering of host tissue could not be established. 

Fischer & Hirschhorn (1945 a) list U. bistortarum var. injiorescentiae as a 

synonym of S. hydropiperis. Through the kindness of Dr. L. Zundel, a fragment 

of the type specimen of U. bistortarum var. inflorescentiae [Herb. I.M.I. 19826] 

was obtained. It has clearly verrucose spores. 

CniTEACTiA Comu, 

Ann. Sci. nat., Bot., Ser. 6, xv, p. 279, 1883. 

Type: Cintractia axicola (Berk.) Cornu on Fimbristylis annua var. diphylla. 

North America. 

Synonym: Anthracoidea Brefeld, 1895. 

Sori in various parts of the host, especially the ovaries. Spore mass agglutinated, 

black, surrounding a central columella of host tissue. Spore development centripetal. 

Spores single, medium or large in size. Spore germination see p. 79. . 

Usually on Cyperaceae. 

Cintractia caricis (Pers.) Magn. 

Uredo caricis Persoon, Synopsis, p. 225, 1801. 

Farinaria carbonaria Sowerby, 1803. 

Uredo urceolorum de CandoUe, 1815 [nov. nom. for U. caricis Pers.]. 

Caeoma urceolorum (DC.) Schlechtendal, 1824. 

Ustilago caricis (Pers.) Unger, 1836. 

Ustilago urceolorum (DC.) Tulasne, 1847. 

Anthracoidea carycis (Pers.) Brefeld, 1895. 

Cintractia caricis (Pers.) Magnus, Abh. bot. Ver. Brandenb., xxxvii, p. 78, 1896. 

Scyri in the spikelets replacing the ovaries, usually partly hidden by the glumes, 

globose or somewhat elongated, about 2-3 mm. diam., 

each covered by a thin grey false membrane which soon 

disintegrates. Spore mass firmly agglutinated, sometimes 

becoming powdery, black, weathering away to 

expose a central columella of host tissue. Spores round, 

oval, or polygonal in surface view, navicular in side 

^"'•Spore^*'^>f500^"*''^' êw, sometimes attached to the remains of semigelatinized 

hyphae, dark brown, frequently almost 

opaque, smooth or granular to distinctly but very minutely verrucose, 14-24 /tt 

diam. (Fig. 8).

THE BKITISH SMUT FUNGI 79 

On Carex arenaria, G. bigelowii, C. capilUtris, C.fiacca, C. nigra, C.panicea, and 

C. pulicaris [Plowright (1889) also gives C. praecox [G. caryophyllea], G. stdlatula 

[G. echinata], G. dioica,, G. pseudocyperus, and C. hirta]; Ehynchospora 

alba; Scirpus caespitosus. 

June-Sept. Widespread. 

Exsiccati: (as Ustilago urceolorum) Cooke, Fungi Brit. Exsicc., i, 541 (on Scirpus 

caespitosus (see Sadler, Trans. Proc. Edinh. hot. Soc, xi, p. 469, 1873); Vize, 

Micro. Fungi Brit., 131 (on Garex flacca). 

Spore germination. Brefeld (1895) obtained germination in spring'from spores 

which had been lying in damp soil since the previous season. The relatively 

thick promycelium became empty and septate in the older part, branched above 

the surface of the water and cut off oval sporidia which fell off and germinated 

to form mycelium (Fig. 5 d). 

A number of different species of Gintractia have been distinguished on Garex 

(seeLiro, 1938) and the forms on Ehynchospora and Scirpus are sometimes 

designated G. montagnei (Tul.) Magn. and C. scirpi (Kiihn) Schellenb., respectively. 

Of the British collections examined, only those of G. subinclusa (see 

below), with its coarsely warted spores, could invariably be distinguished morphologically 

from G. caricis. 

Cintraetia subinclusa (Korn.) Magn. 

Ustilago subinclusa Kornicke, Hedwigia, xiii, p. 159, 1874. 

Anthracoidea subinclusa (Korn.) Brefeld, 1895. 

Gintractia subinclusa (Korn.) Magnus, Abh. bot. Ver. Brandenb., xxxvii, p. 79, 

1896. 

Sori in the spikelets replacing the ovaries, partly hidden by the glumes, globose, 

3-4 mm. diam., each at first covered by a thin grey false membrane. Spore mass 

agglutinated, black, surrounding a central columella of host tissue. Spores 

globose, ellipsoidal, or somewhat elongated, dark brown with hyahne to tinted 

coarse wart-like projections, 12-20 ju. diam. 

On Garex riparia. -'* * 

Warwicks., Bradnocks Marsh (June, 1920), Hampton-in-Arden (June, 1922), 

near Tanworth Grove (see J. Bot., Lond., Ix, p. 168, 1922); Norfolk. 

Exsiccati: Berkeley, Brit. Fungi, 114 (as Uredo urceolorum). 

Spore germination is, according to Brefeld (1895), very similar to that of G. 

caricis, but the sporidia tend to be produced singly or in twos at the tips of the 

promycehal branches rather than in twos or threes (Fig. 5 c) as in C. caricis. 

Pohjakallio (1935) described the germination in G. karii Liro from Garex 

brunnescens (Pers.) Pon. The promycelia were often dilated at the apex and the 

sporidia developed on short sterigmata (Fig. 5 e). Gintractia pratensis Sydow 

from Garex recurva Huds. was studied by Cocconi (1893). Sporidia were lateral 

on a simple promycelium and budded in the medium.


THECAPHOEA Fingerhuth, 

Linnaea, x, p. 230, 1836 

Type: Themphora hyalina Fingerli. [= T. seminis-convolvuli] on Convolvulus 

sepium, Europe. 

Synonym: PoiMlosporium Dietel, 1897. 

Sori frequently in the inflorescence. Spore mass powdery. Spore balls composed 

of few to numerous rather permanently united spores. Spores yellowish to 

reddish, adjacent sides flat and smooth, free surfaces rounded and variously 

ornamented. Spore germination, see below. ' 

Thecapbora deformans Tul. 

Thecaphora deformans Durier & Montagne ex Tulasne, Ann. Sci. nat., Bot., Ser. 3, 

vii, p. 110, 1847. 

Thecaphora lathyri Kiihn, 1873, fide Clinton, 1904. 

Sori in the seeds. Spore mass granular, reddish brown. Spore halls globose to 

ellipsoidal, reddish brown, rather permanent, 20-60 p, diam., each composed of 

five to more than 20 spores. Spores globose or variously angled, contiguous 

surfaces flat and smooth, free surfaces rounded and coarsely verrucose, 10-18 [i 

diam. ^ 

On Lathyrus pratensis. 

Scotland: Edinburgh, Sept., 1923, M. Drummond (WUson, Tran^. Brit, mycol. 

Soc, ix, p. 144, 1924, as T. lathyri); Drem, E. Lothian, Aug., 1929, Malcolm 

Wilson. 

Spore germination. Brefeld (1883) found the spores of this species, which he 

studied as T. lathyri, to be viable throughout the year. After three weeks septate 

promyceUa, emerging from the water, produced terminal cylindrical sporidia, 

15-25 X 3-5 fji, which gave rise in nutrient media to a richly branched mycelium 

bearing sporidia on small sporidiophores (Fig. 5/). 

CHnton (1904) concluded that there is'no reliable basis for distinguishing 

T. lathyri and other species described in legumes from T.. deformans and an 

examination of representative material has confirmed this conclusion. T. deformans 

differs from T. seminis-convolvuli in the larger spore balls composed of 

more numerous spores. 

Thecaphora seminis-convolvuli (Duby) Liro 

Uredo seminis-convolvuli Duby, Bot. gall., ii, p. 901, 1830. 

Thecaphora hyalina Fingerhuth, 1836. 

Thecaphora seminis-convolvuli (Duby) Liro, Die Ustilagineen Finnlands, p. 59, 

1935. 

Sori in the seeds. Spore mass granular, reddish brown. Spore balls irregularly 

globose, 10-30 fj. diam., each composed of 3-10 spores. Spores globose, contiguous 

surfaces flat and smooth, free surfaces rounded and coarsely verrucose, 

pale yellow, 12-16 (occasionally up to 20) fi diam. (Fig. 8). 

On Convolvulus arvensis, Calystegia sepium, G. soldanella. 

Aug.-Sept. Norfolk, Devon, Wilts. Uncommon.


Exsiccati: Cooke, Fungi. Brit. Exsicc., i, 313; Vize, Micro. Fungi Brit., 45. 

References have been made to a so-called 'conidial' stage of this smut 

(Tulasne, 1866; Rostrup, 1898; and others; see Liro, 1938, p. 319). Anthers of 

infected flowers are described as sessile, white or dirty yellow, and covered with 

oval, hyaline, unicellular spores. It is suggested 

that Oloeosporium antherarum Oud. 

on Calystegia sepium may be the sporidial {'\'-''l 'h •il^Jk"^ 

state of a Thecaphora (Oudemans, 1898). *•....• *• 

Spore germination. Woronin (1882) obtained ^ "^ 

germination during October and November j,^^ g Thecaphora seminis-convolvnli. 

in two to two and a half weeks using freshly Spore ball. a. Surface view; 6. optical 

harvested spores from G. arvensis. Older section. x500 

spores gave negative results. The promyceUum grew out through a smooth, 

round, germ pore in the exosporium, became septate, and developed thin branches 

some of which met and fused in pairs (Fig. 5g). A long hypha grew out from 

the place of fusion. 

Thecaphora trailii Cooke 

Thecaphora trailii Cooke, Orevilha, xi, p. 155, 1883. 

Poikilosporium trailii (Cooke) Vestergren, 1902. 

Sari in the inflorescence. Spore mass powdery, purplish brown. Spore balls 

irregularly globose, 18-35 [i diam., each composed of 2-8 spores. Spores hemispherical 

or three-sided, contiguous sides flat and smooth, free surface rounded ^ 

and with reticulations which appear as warts at the circumference, pale yellow, 

10-17 /x diam. [Based on the type specimen in Herb. Kew.] 

On Carduus heterophyllus. 

Scotland, Braemar, Aug., 1883, J. W. H. Trail (Cooke,,toe. cit.). 


TILLETIACEAB Schroeter, 

Krypt. Flor. Schles., iii (1), p. 276, 1887 

Type: Tilletia Tulasne, Ann. Sci. nat., Bot., Ser. 3, pp. 112-13, 1847. 

Spores exposed at maturity as a powdery^Spore mass or permanently embedded 

in the host tissues. Spore germination by a non-septate promycelium bearing a 

group of terminal sporidia or branches (see p. 20). 

TILLETIA Tulasne, 

Ann. Sci. nat., Bot., Ser. 3, vii, pp. 112-13, 1847. 

Type: Tilletia caries (DC.) Tul. on Triticum vulgare, Europe. 

Sari usually in the ovaries, less frequently in the leaves. Spore mass powdery. 

Spores single, medium to large, usually 15-30 fi diam., variously ornamented, 

frequently intermixed with sterile or immature spores. 

Spore germination, see p, 83. 

Differs from Ustilago in the methods of spore formation (see p. 16) and 

germination.

FIG. 10. Spoie germination in Tilletia and Melanotaenium. a. T. decipiens. x 350 (Brefeld, 

1895); 6. M. cingens. x 350 (Brefeld, 1895); c. M. endogenum. Spores and mycelium, x 520 

(Woronin, 1882); d. M. cingens. X 520 (Woronin, 1882); e. T. caries, x 660 (Buller, 1933); 

/. T. caries. Discharge of allantoid sporidia. X 767 (Buller, 1933).


Tilletia caries (DC.) Tul. Wheat Bunt 

[Lycoperdon tritici Bjerkander, 1775.] 

Uredo caries de Candolle, Flor. franc, vi, p. 78, 1815. 

Tilletia caries (DC.) Tulasne, Ann. Sci. nat., Bot., Ser. 3, vii, p. 113, 1847. 

Tilletia tritici (Bjerk.) WolflF, 1874. 

{Fusisporium inosculans Berkeley, J. hort. Soc, ii, p. 114, 1847 is based on the 

secondary sporidia of T. caries.) 

Sori in the ovaries filling the grain with spores, partly hidden by the glumes, 

4-7 mm. long. Spore mass powdery, dark brown to black, foetid when crushed. 

Sterile cells (intermixed with spores) globose, hyaline, 

smooth or indistinctly reticulate, 12-17 /x diam. Spores 

globose to sub-globose, pale brown, reticulate (reticulations 

2-4 (mostly 2-5-3-5) /x wide, 0-5-1-0 /x deep), 14-20 fj. 

diam. (Fig. 11). 

On Wheat (Triticum) and Rye (Secale) causing Bunt KiQ. 11. Tilletia caries. 

July-Aug. England; less common in Scotland. Spores, x 500. 

Exsiccati: Cooke, Fungi Brit. Exsicc, i, 53; ii, 429; Vize, Micro. Fungi, 130. 

Bunt of rye, which has only been recorded twice in this country (Salop., 

1917, Cambs., 1929, fide 'Moore, W. C, 1943, p. 10), was included in Tilletia 

separata Massee (1899) and is sometimes distinguished as T. secalis (Corda) 

Kiihn. 

Spore germination. Prevost (1807) first figured germination, showing promycelia 

with thin, terminal sporidia and the later formed allantoid sporidia. 

Berkeley (1847) discovered the fusion in pairs of the fihform sporidia and this 

was confirmed by Tulasne (1854), Fischer von Waldheim (1869), Kiihn (1858), 

Wolff (1874 a), Brefeld (1883, 1888), Plowright (1889), and others. The filiform 

sporidia, which arise as protuberances at the apex of the promycelium as soon 

as it reaches the air, are 8-12 in number, septate, and 80-100 î in length. The 

apex of the promycelium remains tuberculated after the sporidia have fallen 

(Fig. 10 e). The allantoid sporidia, which develop on short pointed sterigmata, 

from filiform sporidia or from mycelium (Fig. 10/) are forcibly discharged (see 

p. 23). In the related dwarf bunt (see p. 85) branched promyceUa are common 

and tlie terminal filiform sporidia arp verj? numerous as in species of Neovossia. 

Hulea (1947) made a detailed study of spore germination in some species of 

Tilletia on wheat in Rumania. 

Infection of the host occurs at the seedhng stage (Prevost, 1807; Kiihn, 1858). 

The progress of mycehum in the host has been described by Lang (1912) and 

Woolman (1930) (see p. 13). Factors influencing infection are surveyed in 

detail by Holton & Heald (1941). 

Racial specialization. Infection of genera other than Triticum. Aegilops cylindrica 

(Vavilov, .1918) and A. ventricosa (Gaiidineau, 1932; Reichert, 1931) have 

been infected experimentally by Tilletia caries. Twenty-one other species of 

Aegilops were immune from the races of bunt used by Reichert. 

Agropyron cristatum, A.pauciflorum, A. subsecundum, A. inerme, A. spicatum, 

A. trichophorum, Hordeum nodosum, and Sitanion jubatum were infected


artificially by Fischer (1936 a, 1939 b) using a mixture of several virulent races of 

T. caries and T. foetida. T. caries has been found on A. cristatum under field 

conditions in the State of Washington. Infected plants ire markedly stunted 

and predisposed to winter injury. Both T. caries and T. foetida can overwinter 

in perennial grasses but tend to disappear in time. ' | 

Rye-grasses were inoculated with a mixture of T. carie^ and T. foetida and 

bunt balls with smooth chlamydospores Uke T. foetida developed on Lolium 

multijlorum and on L. perenne (Bressman, 1932 a). 

Rye is susceptible to some races of both T. caries and T. foetida from wheat 

(Gaines & Stevenson, 1922, 1923; Schafer, 1923; Ducomet, 1927; Lobik, 1930 

Bressman, 1931; DiUon Weston, 1932; Nieves, 1933, 1935). Volkart (1939) 

accepts bunt of rye as a distinct species, T. secalis, on grounds of larger chlamydospores 

but most workers regard it as a race of T. caries. 

Infection of species of Triticum. Bressman (1932 b) found susceptible varieties 

in all classes of wheat irrespective of chromosome number. Among 13 species of 

Triticum tested for resistance to buht, T. vulgare is the most susceptible and 

T. timococcum, an experimentally produced amphidiploid (Kostoff, 1938), one 

of the most resistant (Holton & Heald, 1941), T. timopheevi (C.I. 11802) is 

resistant to each of the 31 races of bunt recognized in the United States 

(Rodenhiser & Holton, 1945) and has beeu'Used for breeding (Kostoff, 1938; 

Shands, 1941), 

Physiologic races. Evidence of racial specialization in Tilletia caries and T. 

foetens has been obtained in the United States (Rodenhiser & Stakman, 1927; 

Reed, 1928a; Gaines, 1928; Heald & Gaines, 1930; Holton, 1930-31; Bressman, 

1931,1932 b; Smith, 1932 b; Flor, 1933; Gaines & Smith, 1933; Melehers, 1934; 

Holton & Heald, 1936; Rodenhiser & Holton, 1937); in Bulgaria (Atanasoff, 

1929); in Palestine (Reichert, 1930 a, 1930 b); in Canada (Aamodt, 1931); in 

Great Britain (Dillon Weston, 1932); in Germany (Roemer & BarthoUy, 1933); 

in Argentine (Nieves, 1933,1935); in Rumania (Savelescu & Sandu-Ville, 1939); 

and in Australia (Churchward, 1938 a). Holton & Heald (1941) compiled tables 

showing the number of races recorded and the different systems used in their 

classification. The totals, 73 races of T. caries and 66 of T. foetida, doubtless 

include duplicates, since no standardized international method of identifying 

and describing races has been used. 

The most complete study of racial specialization in bunt has been made by 

Rodenhiser & Holton who have now distinguished 16 races of T. caries and 15 

races of T. foetida. The reactions of the differential hosts to these 31 races are 

given in table I of the latest paper which shows also the source of their material 

(Rodenhiser & Holton, 1937; Holton, 1938 a; Holton & Rodenhiser, 1942; 

Rodenhiser & Holton, 1945). 

Physiologic races tend to be regional in distribution, their location depending 

largely on the "varieties of wheat grown in a particular area (Holton, 1947), but 

interchange of seed and dispersal of inoculum by wind alter in time the relative 

prevalence of races (Holton, 1930, 1931; Holton & Suneson, 1942; Hansing & 

Melehers, 1945). Races Til {T. caries) and L8 (T. foetida) have recently assumed 

greater importance in areas where Ridit and Oro have replaced older commercial 

varieties of wheat (Rodenhiser & Holton, 1945). 

Races differ, not only in pathogenicity, but also in the size and shape of the


bunt balls, the size, reticulations, colour, and germination of the chlamydospores, 

nuclear behaviour, cultural characters, and in their effect on height and^tUlering 

of the host (Bressman (1931), Smith (1932 b), Holton (1933), Young (1935), 

Mitra (1935), Holton & Heald (1936), Savelescu & Sandu Ville (1939), Spangenberg 

& Gutner (1936), Gassner (1938), Hanna (1932), Kienholz & Heald (1930), 

Flor (1933), Becker (1936), Melchers (1934), Churchward (1938 a), Rodenhiser & 

Holton (1937). 

The name dwarf bunt (Young, 1935) has been given to a variety of T. caries 

which causes excessive dwarfing and tillering of infected plants and produces 

small, relatively hard balls of spores. These have prominent reticulations, 

germinate only after prolonged soaking (or at 5° C, see Lowther, 1948), and give 

atypical promycelia (see p. 83) (Holton, 1943), Dwarf bunt is largely soilborne 

and attacks only autumn-so^vn wheat in the United States (Bamberg, 

1941; Holton & Suneson, 1943; Blodgett, 1944). It is suppressed if grown with 

T. caries and T. foetida on the same plant (Bamberg et al., 1947). 

Tilletia indica Mitra (1931,1935, 1937) is only distinguished from T. caries by 

the size of spore—which is said to be nearly double that of T. caries. At first it 

was said to be odourless and to cause only partial swelling of the host, but this 

was corrected later. 

Varietal resistance. The world-wide search for varieties of wheat immune from 

bunt (reviewed in Holton & Heald, 1941) brought to Ught certain highly resistant 

varieties used in genetical studies by the workers named: Turkey (Gaines, 1920, 

1925 a; Gaines & Singleton, 1926); Hohenheimer (Gaines & Smith, 1933); Hussar, 

Martin, White Odessa, Banner Berkeley, Turkey, Sherman, Oro (Briggs, 1926- 

40; Schlehuber, 1938; Wismer, 1934; Bryan, 1937; Stanford, 1941); Albit 

(Bressman & Harris, 1933; Schlehuber, 1933, 1935); Florence (Churchward, 

1931, 1932, 1938 b); Garnet (Kildufif, 1933); and Hope (Smith, W. K., 1933; 

Clark et al., 1933; Bryan, 1937; Churchward, 1938 b). Certain varieties, such as 

Hope, resistant when spring-sown, are susceptible if sown in the autumn (Smith, 

W. K., 1932 a, 1933). The main genetical results of crosses between resistant and 

susceptible varieties are presented in tabular form by Holton & Heald (1941). 

The most clear-cut evidence of segregation involving only one or two main 

factors was obtained when the inoculum consisted of a single physiologic race of 

bunt (Briggs, 1926-40; Churchward, 1931-58). Three major factors for resistance, 

designated M (Martin), H (Hussar), and T (Turkey) with linkage between 

T and M were recognized by Briggs (1940). Some varieties of wheat carry 

modifying factors (Briggs, 1929, 1930 c). Resistance is dominant, incompletely 

dominant, or recessive according to the cross. Although a single factor for 

resistance does not govern the reaction to all forms of bunt, one factor may 

function for a group of three or more races (Bressman & Harris, 1933; Smith, 

W. K., 1933; Gaines & Smith, 1933). The reaction to certain races of the two 

species of Tilletia is controlled by the same gene (Gaines & Smith, 1933; Schlehuber, 

1935). In a cross between White Odessa and a Turkey X Florence selection, 

with two races of bunt in the inoculum, resistance was apparently governed 

by six genes (Schlehuber, 1938). A mixture of physiologic races is often used in 

practical plant-breeding (Martin, 1936). Holton & Heald (1936) recommend that 

the number be limited to ten, since more may dilute the inoculum with a decHne

86 THE BEITISH SMUT FUNGI 

in the degree of infection (Fittschen, 1939). The value of the back-cross method 

of breeding bunt-resistant wheats is discussed by Briggs (1930 a, 1935 b). 

I 

Tilletia decipiens (Pers.) Korn. 

Uredo segetum e decipiens Persoon, Synopsis, p. 225, 180,1. 

Uredo decipiens a graminum Strauss, 1810. I 

Uredo sphaerococca Rabenhorst, 1844, fide Komicke, 1877. 

Tilletia sphaerococca (Rabenh.) Fischer von Waldheim, 1867. 

Tilletia decipiens (Pers.) Komicke, Hedwigia, xvi, p. 30, 1877. 

Tilletia separata Massee, 1899, p.p., fide Massee, 1899. 

Sari in the ovaries filHng the grata with spores, partly hidden by the glumes, 

about 1 mm. long. Spore mass powdery, dark brown, foetid. Spores globose to 

sub-globose, brown, reticulate (reticulations somewhat irregular, 3-5 [J, wide, 

2-4 (mostly 2-5-3-5) fj, deep), 26-32 ^ diam. 

On Agrostis canina, A. stolonifera, A. tenuis. 

Sept. Widespread. 

Infected plants are stunted, and dwarfed plants of A. tenuis were at one 

time known as A. pumila L., see W. R. PhUlipson (J. Bat., Land., Ixxiii, pp. 

70-2, 1935, J. Linn. Sac., Bot., U, pp. 84, 89, 100, 193) who states that infected 

plants sometimes recover and revert to their normal habit. 

Spore germination. Brefeld (1895) germinated spores three years old. The 

promycelial branches six to ten in number and septate like those of T. caries, 

fuse in pairs and, still in situ, give rise to sickle-shaped sporidia. In Brefeld's 

figures these are seen germinating, without falling, to form long hyphae 

(Fig. 10 a). 

Tilletia hold (Westend.) Schroet. 

Polycystis hold Westendorp, Bull. Acad. roy. Belg., Ser. 2, xi, p. 660, 1861. 

Tilletia hold (Westend.) Schroeter, in Cohn, Beitrag. Biol.Ppinz.,u,j). 365,1877. 

Tilletia rauwenhoffii Fischer von Waldheim, 1887 [nov. nom. for P. hold Westend.] 

Sori in the ovaries filling the inflated grain with spores, partly hidden by the 

glumes, 2-3 mm. long. Spore mass powdery, brownish black, slightly foetid. 

Spores globose to sub-globose, brown, reticulate (reticulations 4-6 ix wide, 2-3 ju. 

deep), 22-28 /x diam. 

On Holcus lanatus and H. mollis. 


First recorded for the British Isles as T. rauwenhoffii on H. mollis, ra. Doncaster, 

17 July 1891, by Plowright (1891, 1899) {Qdnrs' Chron., Ser. 3, iv, 

p. 374, 1891; Trans. Brit, mycol. Sac, i, 60, 1899). 


Tilletia lolii Auers. 

Tilletia lolii Auerswald in IQotzsch-Rabenhorst, Herb. viv. myc, No. 1899,1854. 

Sori in the ovaries filling the, inflated grain with spores, partly hidden by the 

glumes, 5-7 mm. long. Spore mass powdery, brown, foetid when fresh. Spores

THE BEITISH SMUT FUNGI 87 

globose to sub-globose, light brown, reticulate (reticulations 2-4 JJ, wide, 2-3 /A 

deep), 18-22 fi diam. 

On Lolium temulentum, L. multiflorum, L. perenne, and L. remotum. 

Welsh Plant Breeding Station, Aberystwyth. Introduced in seed of L. temulentum 

from Portugal and infected the four species of Lolium named, in a pot 

.experiment in 1937-8 (Sampson & Western, 1941). 

Spore germination was figured by Kiihn (1858). The sporidia at the end of the 

promycelium are shorter and wider than those of T. caries. Fusions of filiform 

sporidia and the development of allantoid sporidia were shown. 

Infection of the host occurs at the seedling stage (Sampson & Western, 1941). 

Tilletia menieri Har. & Pat. 

Tilletia menieri Hariot & Patouillard, Bull. Soc. mycol. Fr., xx, p. 61, 1904. 

Sori in the ovaries filling the inflated grain with spores, partly hidden by the 

glumes, 3-4 mm. long. Spore mass powdery, brownish black. Spores globose to 

sub-globose, light brown, reticulate (reticulations 2-^ fj, wide, 1-5-3-0 /A deep), 

20-26 fx. diam. 

On Phalaris arundinacea. 

August. Ireland (Antrim) (see A. L. Smith, Trans. Brit, mycol. Soc., iii, p. 374, 

1911); England (Suffolk, Northumberland); Scotland. 


ENTOEEHIZA C. Weber, 

Bot. Zeit., xlii, p. 378, 1884 

Type: Entorrhiza cypericola (Magnus) Weber on Cyperus flavescens, Germany. 

Sori in swellings of the living roots of Cyperus and Juncus. Spores single, 

thick-waUed. Spore germination by one or more germ tubes on which small 

sicklei-shaped sporidia are developed. 

Magnus (Verh. bot. Vereins Brandenburg, xx, p. 53, 1878) described a smut 

causing swelhngs on the roots of Cyperus flavescens which he referred to the 

genus Schinzia Naeg. as S. cypericola Magn. Because of the doubtful nature of 

Schinzia, a genus erected by Naegeli {Linnea, xvi, p. 281, 1842) for two uncertain 

species found in 7ns roots, Webert|1884) proposed a new genus Entorrhiza 

based on E. cypericola (Magn.) Weber. Weber, however, united smuts from root 

swellings of C. flavescens and Junxyus bufonius as E. cypericola and his observations 

on the biology were made on material from the second host. Subsequently, 

Magnus (1888) showed that the smut on C. flavescens (which has finely reticulate 

or punctate spores) differs from that on J. bufonius^ (which has coarsely warted 

spores) and proposed the name Schinzia aschersoniana Magnus {foe. cit., p. 103) 

for the latter. Lagerheim in Aug., 1888, and de Toni in Oct., 1888 {Sacc. Syll., 

vii, p. 497), independently made the combination Entorrhiza aschersoniana. 

This confusion has been reflected in the nomenclature adopted by different 

authors for these smuts. 

No British specimen has been examined. It is clear from the pubhshed records 

that E. aschersonia on J. bufonius has been collected in Scotland but the species 

involved in certain records on other species of Juncus is less certain.


Entorrhiza aschersoniana (Magn.) Lagerh. 

Schinzia aschersoniana P. Magnus, Ber. deutsch. hot. Oes.. vi, p. 103, 1888.. 

Entorrhiza aschersoniana (Ka,^.) Lagerheim, Hedioigia, xxvii, p. 261, (Aug.) 

1888. I 

Bori in swellings of the roots, 3 mm. diam. and up to l' cm. long. Spcn-e mass 

cream-coloured, then light- brown, granular. Spores elliptical, thick-walled,yellow-brown, 

coarsely verrucose, 17-20 X15-17/x 

. (Fig. 12). [No British material examined.] 

Sporidia sickle-shaped, 5-10 X-2-3 fi. 

On Juncus bufonius, nr. Aberdeen, Scotland (Trail, 

Scot. Naturalist, N.S., vi, p. 241, 1884; Ann. Scot. nat. 

Hist., No. 47, p. 188,1903). 

FIG. 12. Entorrhiza ascher- This, or allied species, have also been reported 

Spores. X500. (Rabenh., ^^ '^• squarrosus and J. uligmosus, nr. Glasgow 

Fungi Europ. 3902.) (Cameron, Proc. Trans, nat. Hist. Soc. Glasgow, N.S., i, 

p. 299, 1886, as E. cypericola), and on J. articukitus 

(Trail (1903) loc. cit., as E. digitata; Schwartz (1910), as E. cypericola) but in 

the absence of specimens the identity of the species involved must remain in 

doubt. 

Spore germination is not weU known. Weber (1884) germinated spores which had 

been overwintered in moist sand out of doors in water at 10° C. during February, 

and stated that in nature germination occurs in early May. The spores formed 

one to four septate hyphae from the apices of which solitary sickle-shaped 

sporidia developed. Brefeld (1912), who doubted the relationship between 

Entorrhiza and the Ustilaginales, stated that on germination richly branched 

hyphae produced long, pointed conidia in basipetal succession on sterigmata as 

in Acrostalagmus. The conidia germinated and repeated the process. Schwartz 

(1910) who made observations on the development of the chlamydospores was 

unable to induce them to germinate. 

ScHEOETEEiA Winter, 

Rabenh. Krypt. Flor., i (1), p. 117, 1881 

Type: Schroeteria delastrina (Tul.) Winter on Veronicapraecox, Poictiers, France. 

Synonym: Oeminella Schroeter, 1869 [non Turpin]. 

Sori in the seed capsules of species of Veronica. Spore mass dark coloured. 

Spores in pairs. Spore germination, see p. 89. 

Schroeteria delastrina (Tul.) Wint. 

Thecaphora delastrina Tulasne, Ann. Sci. nat.„Bot.,SGv. 3, p. 108, 1847. 

Geminella delastrina (Tul.) Schroeter, 1869. 

Schroeteria delastrina (Tul.) Winter, Rabenh. Krypt. Flor., i (1), p. 117, 1881. 

Sori in the seed capsules. Spore mass granular, at first grey-green, later dark 

grey. Spores in twos, or, less frequently, single, globose when single, flattened 

on side of contact when one of a pair, tinted grey-green, thin-walled, verrucose, 

9-12 /i diam. (Fig. 14).


FIG. 13. Spoie geimination in Schioeteria. a. S. delastrina. x200 (Brefeld, 1883); 

6. S. delastrinaT X 340 (Cocooni, 1898). 

On Veronica arvensis. 

Norfolk (Fakenham, June, 1889, Plowright, Trans. Brit, mycol. Soc, i, p. 60, 

1899; BrundaU, 21 June, 1945, E. A. Ellis); Oxon. (Peppard Common, May, 

1943, L. E. Hawker, ibid, xxvii, p. 48,1944 [Herb. I.M.I. 32336]). 

Spore germination. Schroeter (1877) germinated spores from Veronica arvensis. 

Only one of the paired spores produced a germ-tube. Three days after sowing 

this was 2-5 /x thick and about five times the diameter of 

the spore in length, septate, and usually branched. Eggshaped 

sporidia (5-6 X 3 ft) were formed at the end of the 

promycelium. Brefeld (1883) illustrated the germiuation of 

12 pairs of spores (from Veronica arvensis or V. triphyllosl). 

Sometimes both spores germinated. The promycelia were 

septate, relatively long, of uniform thickness, and nearly 

spherical sporidia developed in a chain from the apex 

(Fig. 13 a). Winter (1876) figured a promycelium with one 

short side branch and one longer, septate ^filament bearing 

FIG. 14. Schroeteria 

delastrina. Spores. 

X500. 

three apical branches. Cocconi (1898) investigated the form (described as 

var. reticulata) on Veronica praecox. In some spores the germ-tube formed a 

much-branched mycelium, in others round, sporidia developed basipetaUy in 

chains on a simple or forked promyceUum. One spore was figured with a 

terminal crown of short branches as described by Winter (Fig. 13 6). 

The related Schroeteria decaisneana from Veronica hederifolia was described 

and figured by Schroeter (1877). A peculiar feature of this species was the flaskshaped 

promycelium (width 3-4 /u. at base) from the neck of which developed a 

succession of globular sporidia (2-5-3 /x). These sometimes remained in a chain 

of four to seven. Their subsequent behaviour was not determined.


TuBURCiNiA Fries em. Woronin, 

Abh. Senck. Nat. Ges., xii, 359-591, 1882 

Type: Tvburcinia trientalis Berk. & Br. on Trientalik europaea, Scotland. 

Synonym: Ginanniella Ciferri, 1938. • 

Sori usually in the stems and leaves, and rather permanently embedded in the 

host tissue. Spore balls composed of a number of firmly united fertile spores 

only. Sporidia sometimes produced in the host plant before spore development. 

Liro (1922) monographed the genus Urocystia as Tuburcinia Fr. but a 

proposal has been made for the conservation of the name Urocystis, see p. 92. 

Tubuicinia piimulicola (Magn.) Bref. 

Urocystis primulicola P. Magnus, Verh. bot. Ver. Brandenburg, xx, p. 53, 1878. 

Tuburciniaprimulicola (Magn.) Brefeld, Untersuch. Ges. Mykol., xii, p. 180,1895 

[as 'Rostrup']. 

Paepalopsis irmischiae Kiihn is considered to be the stat. eonid. 

Sori in the ovaries. Spore mass brown-black, powdery. Spore balls globose or 

somewhat elongated, dark brown, 30-60 X 20^5 /J.. Spores globose to ovate, dark 

brown, wall about 2 [J, thick, smooth, 10-15 ^ diam. Sporidia (in ovaries and 

anthers of young flowers) globose or elongated, hyaline, smooth, 4-12 X 4-6 [i. 

On Primula farinosa and P. vulgaris. 

March, July-Aug. England, Scotland. Uncommon. 

Spore germination has been described and figured by Pirotta (1881), Plowright 

(1889) (Pig. 15 c), Brefeld (1895) (Fig. 15 d), and Cocconi (1890). The promyceUa 

produce terminally one to four short cylindrical sporidia which fuse in situ or 

after abscission and give' rise to secondary sporidia. Under some conditions 

promycelia form only simple or branched hyphae. Germination, occurs immediately 

the spores are ripe (Kiihn, 1892). 

Infection of the host. Kiihn (1892) inoculated in May young plants of Primula 

vulgaris with germinating sporidia {Paipalopsis irmischiae), kept them for 

several days in a moist atmosphere, then in a cold glasshouse. In April of the 

following year first sporidia, then chlamydospores, developed on the flowers of 

inoculated plants. 

Tuburcinia trientalis Berk. & Br. 

Tuburcinia trientalis Berkeley & Broome, Ann. Mag. nat. Hist., Ser. 2, ii, p. 464, 

1850 [Notices of British Fungi No. 488]. 

Sorosporium trientalis (Berk. & Br.) Cooke, 1877 [as 'Sorosporium trientalis 

Woron.']. 

Ginanniella trientalis (Berk. & Br.) Ciferri, 1938. 

Ascomyces trientalis Berkeley, Outlines of British Fungology, p. 376, 1860 [stat. 

conid.]. 

Sori in the leaves and stems forming bhster-like swellings. Spore mass granular, 

black. Spore balls irregularly rounded or elongated, opaque, black, 30-90 /x 

diam., each consisting of a large number (25-100) of firmly united spores. 

Spores globose to polygonal, dark yellowish-brown, smooth, 11-18 /x diam.

FIG. 15. Spore geimination in Taboicinia and Doassansia. o. T.trientalis. x 520 and x620 

(Woronjn, 1882); 6. T. trientalis. Foliar sporidia. x320 and X520 (Woronin, 1882); c. T. 

primulicola. x475 and x500 (Plowright, 1889); d. T. primulicola. X 350 (Brefeld, 1895); 

6. D. alismatis. X 1000 (Setchell, 1892);/. D. sagittariae. x 350 (Brefeld, 1895).


(Fig. 16). Sporidia on the host in spring and early summer as white patches on 

the stems, in autumn on the undersides of the leaves, pear-shaped or elliptical, 

7_l4x4-5ft(Fig. 15 6). 

On Trientalis europaea. 

May-Oct. Scotland. 

Exsiccati: Vize, Fungi Brit., 136; Phillips, Elvell. Brit., 50 (as A. trientalis). 

Spore germination. Woronin (1882) germinated fresh spores during September- 

October from plants subject to moist weather conditions. 

Attempts at other times of the year failed. 

Germinating spores were found on the leaves and 

stems and on material kept under a watch glass. 

As many as 20 promycelia originated in succession 

from one spore ball. The promycelium issued 

through a round hole in the exosporium. The 

length varied with conditions and the promyeelial 

branches developed better in Ught than in darkness. 

fusion one of the pair developed a sporidimn. 

Unpaired branches also formed sporidia and fusions sometimes occurred 

between sporidia which had fallen off (Fig. 15 a). 

Infection of the host. Woronin (1882) placed geriiiinating spores on young healthy 

shoots of Trientalis europaea, covered with a thiu layer of soil and left over the 

winter. In spring the shoots grew above the soil and carried sporidia of the smut. 

UBOCYSTIS Rabenhorst, 

Herb. Viv. Myc, ii. No. 393, 1856. 

Type: Urocystis occulta (Wallr.) E-abenh. on Secale cereale, Europe. 

Synonym: Polycystis Leveille, 1846. 

Sori usually in the leaves and stems. Spore mass usually powdery. Spore balls 

composed of one to several permanently united fertile spores-more or less completely 

surrounded by a cortex of colourless or tinted sterile cells. Spores 

generally dark in colour. Spore germination, see pp. 94-100. 

This genus was monographed by Liro (1922) as Tuburcinia but to avoid 

changes in the names of major plant pathogens conservation of Urocystis 

Rabenh. against Tuburcinia Fr. has been proposed (see Trans. Brit. mycol.Soc, 

xxiii, p. 214,1939, and Phytopathology, xxx, p. 453, 1940). 

Urocystis agtopyri (Preuss) Schroet. Stripe Smut of Wheat. 

Uredo agropyri Preuss in Sturm, Deutschl. Fhr., vi, p. 1, 1848. 

Urocystis agropyri (Preuss) Schroeter, Abh. Schles. Ges., naturw. Abth. 1869-72, 

p. 7, 1869. 

Urocystis tritici Kornieke, 1877, fide G. W. Fischer, 1943. 

Tvhurcinia agropyri (Preuss) Liro, 1922. 

Tuburcinia tritici (Komicke) Lire, 1922. 

Sori in the leaves as elongated blisters parallel with the veins, at first beneath 

the epidermis which ruptures to expose the spores, the leaves splitting into

FIG. 17. Spore germination in Urocystis. a. U. violae. x 350 (Brefeld, 1895); 6. V. violae. 

X 1,000 (Paravicini, 1917); c. U. anemones, x 1,000 (Paravioini, 1917); d. U.fischeri. x 500 

(Plowright, 1889); e. V. occulta. (Stakman et at, 1934).


ribbons. Spore mass powdery, black. Spore halls irregularly globose, 14-26 jti 

diam., each composed of one or two (occasionally three) spores completely surrounded 

by a layer of yeUowish-tinted sterile cellsl mostly 7-10 /i diam., but 

frequently rather disorganized to give a ridged effect. Spores irregularly globose, 

reddish-brown, smooth, 12-14 (rarely up to 16) fj. diam. 

On Agropyron pungens, A. repens, Arrhenatherum\elatius. 

May-June. England (Surrey), Scotland. 

Spore germination of the smut on grasses is unknown. Spore balls from wheat 

germinate on water in three to five days, producing a short thick promycehum 

with an apical cluster of three to five or more hyahne cylindrical sporidia 

(Fischer & Hirschhorn, 1945 a). 

Infection of the host occurs at the seedhng stage. The fungus persists for several 

years in perennial grasses (Fischer & Holton, 1943). Underground buds of 

Agropyron repens were infected experimentally but not those of Carex, Phleum, 

Poa, or Agrostis species (Liro, 1938). 

Racial specialization. The following species of grasses in the United States are 

more or less susceptible to the stripe smut of wheat: Agropyron caninum, A. 

dasystachyum, A. desertorum, A. inerme, A. repens, A. semicostatum, A. spicatum, 

A. trachycaulum, Elymus canadensis, E. glaucus, E. triticoides, and Hordeum 

jubatum var. caespitosum. Rye appears to be immune but one variety of wheat 

(KanredxHard Federation C.I. 10092) is slightly susceptible to Urocystis 

agropyri from grasses. Three out of four collections of spores from grasses were 

physiologically distinct (Fischer & Holton, 1943). In South Africa and in 

Australia the stripe smut from wheat failed to infect grasses (Verwoerd, 1929; 

Jarrett, 1932). 

Two physiologic races of the wheat stripe smut were distinguished by their 

reactions on certain Oro X Federation selections (Holton & Johnson, 1943), and 

12 races were recognized in China where varietal resistance and its mode of 

inheritance have been studied (Shen, 1934; Yu, Hwang, & Tsiang, 1936; Yu, 

Wang, & Fang, 1945). Work on the resistance of wheat varieties to stripe smut 

has also been done in Australia (Pridham & Dwyer, 1930; Limbourn, 1931; 

Jarrett, 1932.; Millikan & Sims, 1937), in South Africa (Verwoerd, 1929), and in 

the United States (Tisdale, Duncan, & Leighty, 1923). 

Urocystis anemones (Pers.) Winter Anemone Smut 

Uredo anemones Persoon, Synopsis meth. Fung., p. 233, 1801. 

Gaeoma pompholygodes Schlechtendal, 1826, fide Saccardo, 1886. 

Polycystis pompholygodes (Schlecht.) LeveiUe, 1846. 

Polycystis anemones (Pers.) LeveiUe, 1847. 

Urocystis pompholygodes (Schlecht.) Rabenhorst, 1864. 

Urocystis anemones (Pers.) Winter in Rabenh. Krypt. Flor., i (1), p. 123,1881. 

Tuburcinia anemones (Pers.) Liro, 1922. 

Sori in the leaves and stems as blister-like swellings beneath the epidermis which 

ruptures to expose the spores. Spore mass powdery, black. Spore balls irregular, 

16-32 fi diam., each composed of one spore (occasionally two or three) partially 

surrounded by yellowish sterile cells, 6-14 fx. diam., which not infrequently


separate from the central spore. Spores globose, angular, or somewhat elongated, 

dark brown, smooth, 12-26 (mostly 14^18) y, diam. 

On Anemone nemorosa, A. pulsatilla, cultivated Anemones, and Ranunculus 

repens. Malcolm Wilson {Trans. Brit, mycol. Soc, xii, p. 115) has also recorded 

B. ficaria and Trollius europaeus as hosts in Scotland. 

April-Sept. Widespread. Common. 

Exsiccati: Berkeley, Fungi Brit. 236 [as Uredo pompfiolygodes]; Vize, Fungi Brit. 

36 [as Urocystis pompholygodes]; Microfungi Brit. 40 [as Urocystis pompholygodes]; 

Cooke, Fungi Brit. Exsicc. i, 79 [as Polycystis pompholygodes]; ii, 148 

[as Urocystis pompholygodes}. 

Spore germination. Fischer von Waldheim (1867) and Plowright (1889) obtained 

similar results in regard to germination. The latter found that spores immersed 

for 48 hours in water in November and December produced promyceUa which, 

growing up into the air, developed three or four sporidia (10-14 x 3-3-5 fj,). Enlarging 

and becoming vacuolate, these sometimes attained a size of 22 X 4 ju.. 

Fusion between sporidia was observed by Plowright. Liro (1938) confirmed these 

results, noting the shortness of the promycelia and observing fusions between 

sporidia which finally became septate. Paravicini (1917) found that the sporidia, 

while still on the promycehum, were uninucleate (Fig. 17 c)., Fusions were not 

observed but in old cultures some cells had two nuclei. The binucleate condition 

appeared to arise by the fusion of two neighbouring cells but his figures are not 

convincing. ' 

Infection of the host. Plowright (1889) placed sporidia on leaves of Ranunculus 

repens in December and obtained sori at the same point in February. He con- 

' eludes that infection is localized, not systemic. Markova (1927) found the spores 

capable of germination as soon as they were formed and any young part of the 

plant could be infected throughout the year. He established the existence of 

three physiologic races, f. cassubici on Ranunculus cassvhicus, f. repentis on 

R. acris, R. repens, and six other species of Ranunculus, and f. anemones on 

Anemone nemorosa and A. ranunculoides. He failed to infect R. ficaria, R. 

flammula, R. lingua, R. sderatus, and Trollius europaeus. Liro (1938) has given 

specific rank to the races on Anemone, Trollius, Ranunculus ficaria, and some 

other members of the Ranunculaceae. 

Urocystis cepolae Frost , ^ - Onion Smut 

Urocystis cepulae Frost, Ann. Rep. Sec. Mass. St. Bd. Agric, xxiv, p. 175,1877. 

Urocystis colchici (Schlecht.) Rabenh. var. cepulae M. C. Cooke, 1877. 

Tuhurcinia cepulae (Frost) Liro, 1922. ' 

Sori in the leaves as isolated pustules or as elongated dark streaks beneath the 

epidermis which later ruptures (Plate II, Fig. 3). Spore mass powdery, dark 

brown. Spore halls spherical to elhpsoidal, 14-22 fi diam., each composed of a 

single spore surrounded by a layer of spherical to ellipsoidal yellowish to subhyaline 

sterile cells, 4-6 /i diam. Spores spherical to ellipsoidal, reddish brown, 

smooth, 11-14 fi. diam. 

On Allium cepa (cultivated onion); also A. porrum (leek) and A. vineale (Moore, 

1943, 1948). 

April, May, Nov. England, Scotland.


Spore germination. Spores germinate as soon as they are ripe at an optimum 

temperature of 13° to 22° C. (Walker & WeUman, 1926). Thaxter (1890) first 

observed germination. Anderson (1921) described fiow the promycelium remained 

short and hemispherical, while from it arose a whorl of branches which 

grew indefinitely to form myceUum. Older parts of the mycehum became empty, 

the protoplasm collecting in the growing tips. The cells tended to separate and 

detached fragments started new growth in culture. BHzzard (1926) confirmed 

these results. He described the promyceHum as a spherical vesicle about 6-10 /i 

diam. From it arose four to eight branches of variable length which continued 

growth and produced in 12 to 18 hours on onion decoction agar a dense weft of 

myceUum. Fusions were not observed and no sporidia developed. All cells of 

the hyphae developing from the promyceUum were uninucleate and remained so 

during the saprophytic life. Parasitic mycehum consisted at first of uninucleate 

cells but binucleate segments were seen in the young sorus, and before sporogenesis 

all the cells contained two nuclei. 

Infection of the host occurs through the cotyledon before the emergence of the 

first leaf at soil temperatures between 10° and 27° C. (Walker & Jones, 1921; 

Szembel, 1926). No resistant varieties of onion of commercial value are known 

but a fertile amphidiploid, obtained by crossing Allium cepa with the resistant 

species A. fistulosum, may be useful ,in breeding resistant types (Walker, 

Jones, & Clarke, 1944). The fungus survived in soil for 20 years (Moore, 1948). 

Urocystis colchici (Schlecht.) Rabenh. 

Caeoma colchici Schlechtendal, Linnaea, i, p. 241, 1826. 

Uredo colchici Link, Handbuch, iii, p. 435, 1883. 

Polycystis pompholygodes (Schlecht.) LeveUle, 1846 p.p. 

Polycystis colchici Tulasne, 1847. 

Urocystis colchici (Schlecht.) Rabenhorst, Fung. Eur., No. 396, 1861. 

Tuburcinia colchici (Schlecht.) Liro, 1922. 

Sori in the leaves as bhster-hke swellings parallel with the veins, 0-5-1-0 mm. 

wide, 2-10 or more mm. long, at first beneath the epidermis which later ruptures 

to expose the spores. Spore mass powdery, dark brown. Spore halls globose to 

irregular, 14-34 x 14-22 ju., each composed of one or two (rarely three or four) 

spores surrounded by a layer of yellowish, ovoid, sterile cells, 7-10 /x diam. 

Spores globose or angled to somewhat elongated, flattened on side of contact, 

reddish-brown, smooth, 12-16 /u. diam. 

On Colchicum autumnale. Also recorded on imported bulbs of Colchicum sp. 

and Bulbocodium vernum {Bull. Minist. Agric, Land., 79, p. 109, 1934). 

June. Wilts. Uncommon. 

Exsiccati: Berkeley, Brit. Fungi, 309 [as Uredo colchici^ 


Urocystis eranthidis (Passerini) Ainsworth & Sampson, comb. nov. 

Polycystis anemones var. eranthidiaVa.&serixxi, Erb. Critt. Ital., Ser. 2, No. 549,1871. 

Urocystis pompholygodes var. eranthidis (Pass.) Passerini, 1877. 

Tuburcinia eranthidis (Pass.) Liro, 1922 [as 'T. eranthis'].


8ori in the leaves and petioles as blister-like swellings beneath the epidermis 

which ruptures to expose the spores. Spore mass powdery, black. Spore balls 

globose to somewhat ellipsoidal, 20-40 ja diam., each composed of one spore (or 

occasionally two) completely surrounded by a layer of yellowish-tinted, somewhat 

elongated, sterile cells, 8-12 fj, diam. Spores globose, dark brown, smooth, 

13-18 fi diam. 

On Eranthis hyemalis. 

April-May. Norfolk, Dorset, Cambs. 


Urocystis filipendulae (Tul.) Schroet. 

Polycystis filipendulae Tulasne, Ann. Sci. not., Sot., Ser. 4, ii, p. 163, 1854. 

Urocystis filipendulae (Tul.) Schroeter, Die Brand- und Bostpilze Schlesiens, p. 7, 

1870. 

Tuburcinia filipendulae (Tul.) Liro, 1922. 

Sori in the petioles and mid-ribs of the radical leaves, irregular, finally erumpent, 

up to 44 mm. long. Spore mass powdery, black. Spore balls variable, each composed 

of one to seven spores surrounded, by irregular sub-globose, brown, sterile 

cells, up to 12 /idiam. Spores rounder angular, brown, punctate, 15-25 X10-15 [JL. 

On Filipendula liexapetala. 

Damford Down, Salisbury, May, 1897, Mr. Tatum (Plowright, Trans. Brit, 

mycol. Soc, i, p. 60, 1899). ^ 

Spore germination. Schroeter (1877) germinated spores, collected two months 

previously, in distilled water. The short promycelium produced terminally a 

tuft of five or six long cylindrical branches about equal in length to the diameter 

of the spore. Brefeld (1883) confirmed these results with spores that had lain 

for a year in moist soil. The promycehal branches developed mycehum without 

fusion. 

Urocystis flscheri K6m. 

Urocystis fi^cheri Komicke, Hedwigia, xvi, p. 34, 1879. 

Tuburcinia fischeri (Kom.) Liro, 1922. 

Sori in the leaves as elongated blisteTs parallel with the veins, at first beneath 

the epidermis which ruptures to expose the spores. Spore mass powdery, black. 

Spore balls irregularly globose, 20-35 jn diam., each composed of one to two 

(occasionally three to four) spores completely surrounded by a layer of yellowishtinted, 

sterile cells, 8-14 /j. diam. ^Spores rounded, dark reddish-brown, 14-16 ju. 

diam. ' 

On Carex flacca. 

June. England (Dorset [Herb, Path. Lab. 12]), Scotland (Forfarshire), 

Spore germination. Plowright (1889) germinated the spores after a considerable 

period of soaking in water. He remarked on the length of the promycelium and 

on the size and number of the sporidia, as many as eight occurring on one promycelium. 

No reference was made to fusions (Fig, 17 d). 

' G


Tlrocystis gladiolicola Ainsworth Gladiolus Smut 

Urocystis gladiolicola Ainsworth, Trans. Brit, mycol. Sdc, xxxii, p. 257, 1950. 

Sori in the leaves, as dark brown blisters paraUelwith the jvêins, 1 mm. to several 

cm. in length, the epidermis rupturing to expose the spores, and in the corms. 

Spore mass powdery, dark brown. Spore balls globose, 154-28 ft diam., each composed 

of one or two spores completely surrounded by a rstther irregular layer of 

colourless sterile cells, 6-10 [i diam. Spores globose or sU'ghtly angled, reddishbro%vn, 

12-18 ju. diam. 

On cultivated Gladiolus. 

June, Dec. Somerset, Cornwall. 


The fungus on which W. G. Smith based Urocystis gladioli W. G. Sm. was a 

species of Papulaspora (see Ainsworth, 1950). 

Urocystis hepaticae-trilobae (DC.) Ainsworth & Sampson, comb. nov. 

Uredo ranunculacearum 8 hepaticae-trilobae De CandoUe, Flor. franc, vi, p. 75, 

1815. 

Tuburcinia hepaticae-trilobae (DC.) Liro, 1922. 

Sori in the leaves as blister-like swellings beneath the epidermis which ruptures 

to expose the spores. Spore mass powdery, black. Spore balls rather irregular, 

21-52 n diam., each composed of one to seven (usually three to five) spores 

partially surrounded by yellowish-tinted, sterile cells, 10-13 /ix diam. Spores 

globose, angular or somewhat elongated, dark brown, smooth, 14-19 JJ. diam. 

On Hepatica pennsylvanica, Kew Gardens, 1890 [as Urocystis pompholygodesi, 

[Herb. Kew.]. 

Infection of the Iwst. Markova (1927) found that spores from Hepatica triloba 

would not infect Trollius europaeus, Anemone spp., or Ranunculus spp. 

Urocystis junci Lagerh. 

Urocystis junci Lagerheim, genuina Lagerheim, Botaniska Notiser 1888, p. 210. 

Tuburcinia junci (Lagerh.) Liro, 1922. 

Sori inside the lower parts of the stems which finally rupture. Spore mass 

powdery, brownish black. Spore balls globose to rather irregular, 20-50 fi diam., 

each composed of one to four (occasionally up to eight or more) spores, completely 

surrounded by a layer of smooth, elUpsoidal, yellowish cells 7-10 X 3-5 /x. 

Spores globose to ellipsoidal, yellowish, smooth, 12-16 n diam. 

On Juncus acutus. 

Burnfen Broad, Norfolk, 2.viii.l945, E. A. Ellis {Trans. Norf. Norwich Nat. Soc., 

xvi, p, 175, 1946 [Herb. I.M.I. 582]). 


Urocystis occulta (Walk.) Rabenh. Stripe Smut of Rye 

Erysibe occulta Wallroth, Flor. Crypt. Qerm., ii, p. 212, 1833. 

Uredo parallela Berkeley, 1836. 

Polycystis parallela (Berk.) Fries, 1849. 

Polycystis occulta (Wallr.) Schlechtendal, 1852.


Urocystis occulta (Wallr.) Rabenhorst in Klotzsch, Herb. viv. myc, ii, No. 393, 

1856. 

Urocystis parallela (Berk.) Fischer von Waldheim, 1870. 

Tufmrcinia occulta (Wallr.) Lire, 1922. 

Sori in the leaves, culms, and inflorescence as very long, dark, linear blisters 

parallel with the veins, at first covered by the epidermis which later ruptures to 

expose the spores. Spore mass powdery, dark reddish-brown. Spore halls globose 

to somewhat elongated, 15-26 /A long, each composed of one or two (rarely three 

or four) spores, completely or, frequently, incompletely surrounded by a layer of 

hyaline or tinted sterile cells, 5-10 /x, diam. Spores globose or angled, flattened 

on side of contact, reddish-brown, smooth, 12-16 fi diam. (Fig. 18). 

On Secale cereale (rye) causing Stripe Smut. 

June. England. Uncommon. 

(Spore germination. Germination has been described and figured by Kiihn (1858), 

Wolf (1873), Brefeld (1883), and more recently by 

Ling (1940 a) and Stakman, Cassell, & Moore (1934). 

According to the last-named, spores germinated best 

after soaking for 16 hours in water to which benzaldehyde 

had been added (three parts in 2,000,000), 

and a temperature of 24° C. favoured development. 

The promycelia varied in length and septation, the 

longest consisting of ten to fifteen cells with protoplasm '°" gpores^'^xôo! 

only in the apical one. Fusion between the promyceUal 

branches occurred at the base, apex, or by H -shaped connexions in the 

middle, but a study of nuclear behaviour suggested that the dicaryophase can 

be initiated not only by fusion but, rarely, by the direct passage of two nuclei 

from the promycelium into one of its branches or by the union of two cells in 

fairly long hyphae (Fig. 17 e). 

Infection of the host during germination of the seed, first demonstrated by Wolff 

(1873, 1874 a), has been confirmed by many workers. 

Racial specialization. Agropyron caninum, A. inernie, Elymus canadensis, and 

E. triticoides were infected by stripe smut from rye while wheat was immune 

(Fischer & Holton, 1943). 

Urocystis sorosporioides Kom. 

Urocystis sorosporioides Kornicke in Fuckel, Symb. mycol.,Nachtr., iii, p. 10,1876. 

Tuburcinia sorosporioides (Korn.) Liro, 1922. 

Sori in the leaves as blister-like swellings beneath the epidermis which finally 

ruptures; less frequently in the petioles and stems. Spore mass powdery, black. 

Spore balls spherical to ellipsoidal, dark brown, opaque, 26-38 /i diam., each 

composed of three to seven spores completely surrounded by somewhat elongated, 

yellowish, sterile cells, 8-10 fi diam. Spores sub-globose, usually angled 

by mutual pressure, brown, smooth, 10-14 jx diam. 

On Thalictrum mimis and its var. inaritima. 

June. England (Lanes.), Scotland (Aberdeens.). Eare. 

Spore germination. Unknown.


Urocystis violae (Sow.) Fisch. v. Waldh. Smut of Violets 

Granuluria violae Sowerby, English Fungi, t. 440, 1815. 

Polycystis violae (Sow.) Berkeley & Broome, 1850. 

Urocystis violae (Sow.) Fischer von Waldheim, Bull. Soc. Nât. Moscow, xl, p. 258, 

1867. 

Tuburcinia violae (Sow.) Liro, 1922. i 

Sori in the petioles, veins, and upper parts of the root stock as large elongated 

swellings which distort the attacked parts. Spore mass powdery, dark brown. 

Spore balls rather irregular, globose to elongated, 26-68 /A long, each composed of 

four to eight spores covered by a (frequently disorganized) layer of yellowish 

sterile cells, 6-10 JJ. diam. Spores sub-globose, ellipsoidal, or polyhedral, reddish 

brown, smooth, 8-16 ja diam. 

On Viola odorata, V. reichenbachiana, V. riviniana, and cultivated violets. 

Feb., July, Nov. Widespread. Common. 

Exsiccati: Cooke, Fungi Brit. Exsicc, i, 78; Vize, Micro. Fungi, 137,. 

Spore germination. Germination was obtained by Kiihn (1876), PrilUeux (1880), 

Dangeard (1894 a), Brefeld (1895), and Schellenberg (1911). Brefeld figured 

several promycelia of varying age from one spore ball. Five or six short fusiform 

branches developed at the apex of the promycelium and each produced on a thin 

sterigma a long oval sporidium (Fig. 17 a). A similar result was obtained by 

Paravicini (1917) who also showed fusion of fallen sporidia (Fig. 17 b). Rawitscher 

(1922) described the development of seven to eight uninucleate sporidia 

which fused in pairs. 

MEiANOTAENrcTM de Bary, 

Bot. Zeit., xxxii, p. 105, 1874. 

Type: Melanotaenium endogenum (Ung.) de Bary on Galium mollugo, Europe. 

Sori in the stems, leaves, and roots giving rise to extensive black or grejrish 

areas, permanently embedded in the host tissue. Spore mass never powdery. 

Spores single, dark in colour. Sporidia not observed on host plant. Spore germination, 

see below. 

An account of this genus has been given by Beer (1920). 

Melanotaenium cingens (Beck) Magn. 

Ustilago cingens Beck, Oster. bot. Zeitschr., xxxi, p. 313, 1881. 

Melanotaenium caulium Schroeter, 1887, fide Magnus, 1892. 

Cintractia cingens (Beck) de Toni, 1888 [as 'Gintractial cingens'^ 

Melanotaenium cingens (Beck) Magnus, Oster. bot. Zeitschr., xlii, p. 40, 1892, 

Sori in the stems and leaves, covered by a layer of host tissue which disintegrates 

to expose the spores. Spore mass firm to somewhat granular, black. Spores 

rather irregular, globose to sub-globose, polygonal or ellipsoidal, dark brown, 

almost opaque, smooth, 13-18x10-16 ja. 

On Linaria vulgaris. 

July-Aug. N. Wales: Glyndyfrdwy, nr. Langollen, C. T. Green {Trans. Brit, 

mycol. Soc, ii, p. 6, 1903); Prestatyn; Cambs, [Herb. Kew.]. 

Spore germination. Brefeld (1883) figured germination showing very short

30390 


promycelia, basal fusions between the promycelial branches, and the growth of 

these to form'hyphae (Fig. 10 b, d). Juel (1894) also figured germination noting 

the short promyceUa (15 /x) with three or four terminal branches, but he did not 

observe fusions. Some of the branches formed long septate hyphae (diameter 

2 fi) and small, somewhat bent sporidia (9 x 3 ja). In nutrient solution derived 

from dung the apical branches of the promycelium formed a bunch of sterile 

filaments. Viennot-Bourgin (1937), using a filtrate of soil and compost, germinated 

spores from plants of Linaria striata which had been exposed to the 

weather until April. The promycelia (70-130 /x.) were thin and flexuous with one 

or two slender apical branches (20-30 X 3 ft) which bore at the tip thin slightly 

acuminate sporidia (9-18 X 3-5 fi) on rudimentary stalks. l^^. 

Melanotaenium endogenum (Unger) de Bary 

Protomyces eridogenus Unger, Die Exantheme der Pflanzen, pp. 342, 419, 183: 

Protomyces galii Nees von Esenbeck, 1837, fide de Toni, 1888. 

Melanotaenium endogenum (Unger) de Bary, Bot. Zeit., xxxii, p. 106, 1874. 

Entyloma endogenum (Unger) Wiinsche, 1877. 

Sori in the stems and leaves blackening the stunted shoots of the infected plants, 

covered by the epidermis of the host. Spore mass firmly agglutinated, black. 

Spores rather irregular, globose, sub-globose, polygonal 

or elhpsoidal, dark brown, almost opaque, 

16-22 X12-20 ja (Figs. 19, 10 c). 

On Qalium verum. 

Scotland, Aberdeen (see Trail, Scot. Nat., vii (N.S. i), 

p. 243, 1884), St. Fagans, Aberdeens. (A. Smith, 

July, 1932, Herb. Kew.); Newcastle-on-Tyne (A. W. 

Bartlett, 1938, Herb. I.M.I. 32325); Guernsey (E. A. 

Ellis, July, 1939, Herb. I.M.I. 32326); Cambs. Fio-19- Melanotaenium endogenum. 

Spores. x500. 

Spore germination. Woronin (1882) germinated, in 

October and November, spores collected at the end of June. The epispore spht 

and the endospore grew out as a blunt, cylindrical germ-tube which often 

branched, but only one branch developed further, forming a promycelium 

•\vith four to seven apical branches which fused at the tip or at the base. After 

fusion some of these developed septate mycelium but no sporidia were observed. 

Melanotaenium hypogaeum (Tul.) ScheUenb. 

Ustilago hypogaea Tulasne, Fung, hypog., p. 196, 1851. 

Melanotaenium hypogaeum (Tul.) ScheUenberg, Die Brandpilze der Schweiz, 

p. 108, 1911. 

Sori in the root stock. Spore mass compact, black, intersected by white fibres. 

Spores rounded or rounded polygonal, dark brown, smooth, contents very 

oleaginous, 20-24 x 14r-20/x. [n.v., after Phillips & Plowright.] 

On Linaria spuria. 

Freshwater, Isle of Wight, 1869, John Lowe (see Phillips & Plowright, Orevillea, 

xiii, p. 52, 1884). 

Spore germination. Unknown.

102 THE BKITISH SMUT FUNGI 

Melanotaenium lamii Beer 

Melanotaenium lamii Beer, Trans. Brit, mycol. Soc, vi, p. 337, (Sept.) 1920. 

Melanotaenium lamii Sydow, Ann. mycol., Berl., xviii, pi 156, (April) 1921. 

Sari in the undergroxind stems as blister-like swellings! or as tuberous bodies 

8-5-9-0 mm. diam. (Plate II, Fig. 1); affected buds are much more swoUen. 

Spore mass firm, black. Spores spherical to oval, dark brown, thick-waUed, 

smooth, 17-20 [J. diam. 

On Lamium album. 

Chalfont, Stroud, Glos., early summer 1918 and again in 1919, W. F. Drew 

(Beer, loc. cit.); Lacey Green, Bucks., 11 Feb. 1948, K. Sampson (Herb. Kew.). 

Spore germination and infection of the host are unknown. Viennot-Bourgin (1937) 

has described the development and anatomy of galls produced by this species 

on Linaria spuria and by M. cingens on L. striata. 

ENTYLOMA de Bary, 

Bot. Zeit., xxxii, p. 101, 1874. 

Type: Entyloma microsporum (Ung.) Schroet. [E. ungerianum de Bary] on 

Banunculus repent, Germany. 

Synonym: Bhamphosora D.D. Cunningham, 1887. 

Sori usually in the leaves, generally giving rise to discoloured areas, permanently 

embedded in the host tissue. Spores single, hyahne or pale in colour. Sporidia 

not infrequent on the host plant as a result of spore germination in situ or on 

mycelium protruding through the stomata. 

Spore germination, see pp. 104-8. 

Entyloma achilleae Magn. 

Entyloma achilleae P. Magnus, Abh. naturh. Ges. Niirnberg, xiii, p. 8, 1900. 

Sori in the leaves. Spores globose, colourless, 10-12/A diam. [Sporidia on the host 

one-, rarely two- to four-celled, hyaline, 6-25 by 3-5-5-5fi; fide Liro (1938)]. 

On Achillea millefolium. 

Isle of Bute, Aug., 1907, D. A. Boyd (A. L. Smith, Trans. Brit, mycol. Soc, iii, 

p. 122, 1909 [Herb. B.M.]). 

Entyloma calendulae (Oudem.) de Bary 

Protomyces calendulae Oudemans, Archiv. Neerl. Sci. Exact, nat., viii, p. 384, 

1873. 

Entyloma calendulae (Oudem.) de Bary, Bot. Zeit., xxxii, p. 102, 1874. 

Sori in the leaves as circular spots, 1 •0-5-0 mm. or more diam., first pale, then 

brown. Spores globose to polygonal, almost hyaline to pale yellow, smooth, 

9-14 /x diam. Sporidia, see p. 22. 

On Calendula officinalis and (fide Beaumont, Bep. Plant Path., Seale Hayne 

agric. Coll., x, p. 39; xi, p. 54; xiii, p. 39) cultivated Calendula. 

March-Dec. Cornwall, Kent, Norfolk, Suffolk. 

Spore germination. De Bary (1874) described and figured the germination of

FIG. 20. Spore geimination in Entyloma. a. E. ficariae. Foliar sporidia and mycelium 

(Marshall Ward, 1887); b. E. microsporum. x600 (de Bary, 1874); c. B. magnusii. x520 

(Woronin, 1882); d. E. calendulae (Kaiser, 1936).


fresh material. Three to eight short, cylindrical branches developed at the apex 

of the promyceUum, fused in pairs and grew out iw, situ to form very long, 

slender, spindle-shaped sporidia. Paravicini (1917) foxmd that the short and 

rather broad promycelial branches fused after abstriction, and one nucleus 

passed through the bridge. Kaiser (1936) confirmed de Bauy's observations and 

demonstrated the binucleate condition of the sporidia which developed from the 

fused promycelial branches. Some branches grew out directly to form mycelium, 

others, unpaired, cut off uninucleated sporidia (Fig. 20 d). In rare cases two 

promycelia developed from one chlamydospore. Above and below the optimum 

temperature (8°-12° C.) the number of promycelial branches was reduced. 

Infection of the host. The infection of young leaves occurs throughout the 

summer, presumably from foliar sporidia and germinating chlamydospores, and 

in spring from chlamydospores which have overwintered in old parts of the 

plant. De Bary (1874) observed light flecks nine days after germinating 

chlamydospores had been placed on leaves of Calendula officinalis. 

Entyloma calendulae (Oudem.) de Bary f. bellidis (Kreiger) Ainsworth & 

Sampson, comb, no v. 

Entyloma bellidis Kreiger, Hedwigia, xxxv, p. (144), 1896. 

Sori in the leaves. Spores as E. calendulae. {Sporidia on the host needle-shaped, 

colourless, 20-45 X1-5 ft, fide Liro (1938).] 

On Bellis perennis. St. Fergus, Aberdeenshire, Dec, 1932, A. Smith [Herb. 

Kew.]. 


Entyloma calendulae (Oudem.) de Bary f. dahliae (Sydow) Viegas 

Dahlia Smut 

Entyloma dahliae Sydow, 1912. 

Entyloma calendulae (Oudem.) de Bary f. dahliae (Sydow) Viegas, Bragantia, iv, 

p. 748, 1944. 

Sori in the leaves as circular to elliptical spots up to 1 cm. diam., sometimes' 

confluent, at first pale, later brown and giving rise to dead areas (Plate II, Fig. 4). 

Spores as E. calendulae. Sporidia, see below and p. 22 (Fig. 1 f). 

On cultivated DahUas. 

Aug.-Oct. Widespread. Common. 

Spore germination has been observed by Pape (1926), Pethybridge (1928), and 

Green (1932). Pape figured the promycelium with an apical crown of branches 

which fuse in pairs, apparently at their apices, and produce long, needle-shaped 

sporidia, 60 X 1-0 /i. Green described the sporidia as needle-like (45-75 x 2-0 fx), 

sometimes slightly curved, aseptate, with one end pointed and the other somewhat 

blunt, marking its point of attachment to the sporidiophore. Infection 

experiments were negative. 

Entyloma calendulae (Oudem.) de Bary f. hieracii Sehroet. 

Entyloma calendulae (Oudem.) de Bary f. hieracii Schroeter, Cohn Beitr. Biol. 

PJlanz., ii, p. 439, 1876. 

Entyloma hieracii Sydow, 1919.


Sori in the leaves. Spores as E. calevdulae. Sporidia not reported on the host. 

On Hieracium vulgaium and (fide Plowright, 1889) H. murorum. 

Autumn. Scotland (nr. Aberdeen). 


Entyloma chrysosplenii (B. & Br.) Schroet. 

Protomyces chrysosplenii Berkeley & Broome, Ann. Mag. nat. Hist., Ser. 4, xv, 

p. 36, 1875. [Notices of British Fungi No. 1472.] 

Entyloma chrysosplenii (B. & Br.) Sehroeter in Cohn, Beitr. Biol. PJlanz., ii, 

p. 372, 1877. 

Sori in the leaves as thickened, whitish spots, 2-6 mm. diam. Spores globose or 

shortly ellipsoidal, colourless, smooth, 10-12 fx, diam. [n.v., after Plowright.] 

On Chrysosplenium oppositifolium. 

June-Sept. Scotland (New PitsUgo [type locaUty]; Birks of Fiadhom [Keith, 

Scot. Naturalist, iv, p. 348, 1878]). 

There is no type specimen in the Berkeley herbarium in Herb. Kew. and no 

British specimens have been traced. 

Spore germination. According to Maire (1900) the spore germinates while still in 

the leaf and produces at the apex of the promycelium two to four oblong, 

cylindrical sporidia, 15-16x2-5-3 /x. 

Entyloma eryngii (Corda) de Bary 

Physoderma eryngii Corda, Icones Fungorum, in, p. 3, t. 1., 18. 

ErUyloma eryngii (Corda) de Bary, Bat. Zeit., p. 105, 1874. 

Sori in the leaves as fawn-coloured, raised, spots, 1-3 mm. diam. Spores 

globose, or shghtly angular, epispore 1/x thick, smooth, hyaUne to yeUow-brown, 

8-10 /i diam. 

On Eryngium maritimum. 

Stevenston, Ayrshire, D. A. Boyd, Sept. 1908 [Herb. B.M.]. 

Spore germination. De Bary (1874) described and figured germination. The 

promycelium bears four (sometimes five or six) terminal branches which fuse in 

pairs either at the apex or the base, and finally grow out to form mycehum. 

Sporidia were not seen. / 

Entyloma fergussoni (B. & Br.) Plowr. 

Protomyces fergussoni Berkeley & Broome; Ann. Mag. nxit. Hist., Ser. 4, xv, p. 36, 

1875. [Notices of British Fungi No. 1473.] 

Entyloma canescens Sehroeter, 1877. 

Entyloma fergussoni (B. & Br.) Plowright, British Ured.


Spore germination. Schroeter (1877) states that spores from Myosotis stricta and. 

M. hispidus germinated easily soon after they were ripe and formed, as in 

Entyloma microsporum, long, spindle-shaped sporidia 26-^:0 X 2-2-3 fi. Old ilecks 

on the leaves were thickly covered with beds of sporiciia. Kaiser (1936) sawspores 

germinating in the tissues of the host but he was unable to germinate 

chlamydospores of this species under artificial condition^. He suggests that the 

two types of sporidia found in nature ion the leaf are mainly responsible for 

dissemination of the disease, that they can overwinter and infect new plants in 

the spring (see p. 23). The best method for transmitting the disease was to 

spray plants with water containing dry or fresh infected material broken into 

small fragments. A suspension of sporidia gave particularly good results. The 

technique used did not completely exclude the possibility of chlamydospores 

being present in the suspension. The incubation period was 21 days. In E. 

serotinum on Symphytum sp. Schroeter (1887) refers to the thread-like 

sporidia (26-40 X 2-2-3 [x.) that precede the spores making young flecks pure 

white. 

Physiologic specialization. Infection experiments, using sporidial suspensions 

from various hosts, showed that the forms of E. fergtissoni on Myosotis, Symphytum, 

Borago, Mertensia, and Pulmonaria are biologically distinct. Measurements 

of chlamydospores and sporidia from' these genera of host plants agreed 

closely and Kaiser (1936) unites the forms as one species indicating the forms by 

trinomials as recommended by Ciferri (1932). 

Entyloma ficariae (Berk.) Fiseh. v. Waldh. 

Cylindrosporium ficariae Berkeley, Brit. Fungi, No. 212, 1837. [Notices of 

British Fungi, No. 135, 1838.] Stat, conid. [in 1875 Berkeley & Broome 

(Notices of British Eungi, No. 1471) reported chlamydospores in the type 

specimen]. 

Fusidium ranunculi Bonorden, 1851. Stat, conid. 

Gloeosporium ficariae (Berk.) Cooke, 1871. Stat, conid. 

Entyloma ungerianum f. ficariae Winter, Bahenh. Fungi Europ.,'No. 1873,1874. 

[C. ficariat Berk, cited as conidial state.] 

Entyloma ungerianum f. ficariae von Thiimen, Mycoth. Univ., No. 219, 1876. 

[Collected by G. Winter and probably the same as Babenh. Fungi Europ., 

No. 1873.] 

Entyloma ficariae (Thvim.) Fischer von Waldheim, Bull. Soc. Nat. Moscow., 

hi, p. 309, 1877. 

Entyloma ranunculi (Bon.) Schroeter, 1877, 

Cylindrosporium ranunculi (Bon.) Saccardo, 1878. Stat, conid. 

Entylomella ficariae (Berk.) v. Hohnel in Wese, Ann. mycol, 

Berl., xxii, p. 191, 1924. Stat, conid. 

Sori as circular spots on the leaves, at first yellowish (or 

FiG.21. Entyloma whitish due to sporidia), 2-5 mm. diam. (Plate II, Fig. 5). 

ficariae. Spores. Spores globose to sub-globose, pale brown, wall 1-2 fj. thick, 

^ • smooth, 10-14 fi diam. (Fig. 21). Sporidia on the host fusiform, 

thread-like, or ellipsoidal, hyaline, mostly 30-45 X about 2-0 /x (Figs. 16 and 20a), 

as whitish growths on both sides of the leaves (see p. 22).

On Ranunculus ficariae and B. scleratus. 

THE BEITISH SMUT FUNGI 107 

April-May. Widespread. Common. 

Exsiccati: Berkeley, Brit. Fungi, 212; Cooke, Fungi Brit. Exsicc., i, 533. 

Spore germination. Marshall Ward (1887) states that after some months in the 

dormant condition the spores put out promycelia from which sporidia are developed 

which seem to behave like those on the leaves. 

Entyloma fuscum Schroet. 

Entyloma fuscum Schroeter in Cohn, Beitr. Biol. Pflanz., ii, p. 373, 1877. 

Sari in the leaves, forming roundish yellow spots. Spores globose or polygonal, 

colourless then brown, 10-16 /oi diam. Sporidia on the host, on the undersides of 

the leaves, cylindrical, curved, attenuated towards the base, simple or septate, 

hyaline, 10-20 X 3-0/x. 

On Papaver rhoeas. 

North Wootton, Norfolk, July, 1882 (Phillips & Plowright, Grevillea, xiii, p. 52, 

1884) [Herb. B.M.]; Wisley, Surrey, May, 1930, J. Ramsbottom [Herb. B.M.]. 

Both the British collections have been identified as E. bicohr Zopf [E. bicolor 

Stromeyer] a species near to or identical with E. fuscum from which it is said to 

differ by having spores 23 X12-17 jx instead of 11-16 /n diam. Plowright (1889) 

gives the spore size as 20-23 X15-18 ju, but as the spore size of the two specimens 

examined is rather less than this they have been tentatively referred to E. 

fuscum. 

Spore germination. Schroeter (1877) described how the hght flecks on the basal 

leaves of Papaver in spring became covered, under moist conditions, with thin 

white tufts resembling Ramularia. Sections of the leaf showed tufts of promycelia 

passing between the guard cells and bearing apically five to eight sporidia, 

at first cylindrical, later long, spindle-shaped, almost thread-like in form, 

like those on Myosotis (see p. 106). 

Entyloma helosciadii Magn. 

Entyloma helosciadii Magnus, Hedwigia, xxi, j).^ 129, 1882. Stat, conid. 

Cylindrosporium helosciadii repentis Magnus, Abh. bat. Ver. Brandenburg, xxxv, 

p. 68, 1893. 

Entylomella helosciadii repentis (Magn.) von Hohnel in Weese, Ann. mycol., Berl., 

xxii, pp. 193-4, 1924. 

Sori in the leaves as discoloured spots which become necrotic, frequently 

covered, especially on the underside, by a white sporidial growth. Spores 

spherical to elhpsoidal, thin-walled, hyaline to dark yellow, 5-12 fi diam. 

Sporidia on the host cylindrical with shghtly tapered ends to oval, hyaline, 

9-14 X about 3-0/i. 

On Apium nodiflorum. 

June-Oct. Eire, Co. Dublin [Herb. I.M.I. 32305] and Tipperary (first recorded 

by O'Connor, Sci. Proc. roy. Dublin Soc, N.S., xxi, p. 395, 1936, where host is 

given in error as Sium erectum); England (Wilts.).

108 THE BKITISH SMUT FUNGI 


In some of the material examined Protomyces macrosporus Ung, (see Plowright 

(1889) p. 300) was also present. ' 

Entyloma henningsianum Syd. 

Entyloma henningsianum Sydow, Hedwigia, xxxix, p. 123; 1900. 

Sori in the leaves forming scattered orbicular spots, 4-8 mm. diam., pale yellow, 

becoming brownish. Spores globose or globose-angular, yellowish-hyaline, 

epispore about 2 ft thick, smooth, 9-15 /x. 

On Samolus valerandi. 

Dubh Loch, Inveraray, Argyllshire, Sept., 1907, D. A. Boyd (A. L. Smith & Rea, 

Trans. Brit, mycol. Soc, iii, p. 34, 1908 [Herb. B.M.]). 


Entyloma matiicaxiae Eostr. 

- Entylxyma matricariae Rostiup in Thumen, Mycoth. univ.. No. 2223,1884. 

Entyloma matricariae Trail in Plowright, 1889. 

Entyloma trailii Massee, 1891 [nom. nov. for E. matricariae Trail apud Plowr.]. 

Sori in the leaves, when mature as discrete brown spots or affecting all surfaces 

of the leaf segments, and, less frequently, the stems. Spores globose or polygonal, 

thin-walled, hyaUne to dark yeUow, smooth, 10-12 fi diam. Sporidia on the host, 

in mature and maturing sori, filiform, hyaline, one- to four-celled, 6-25 X 2-3 fx. 

On Matricaria inodora. 

Aug.-Sept. Scotland (Orkneys, Aberdeens., Argylls.). 


Entyloma microsporum (Ung.) Schroet. 

Protomyces microsporus Unger, Die Exantheme der Pflanzen, p. 343, 1833. 

Entyloma ungerianum de Bary, 1874 [nom. nov. for P. microsporus Ung.]. 

Entyloma microsporum Schroeter in Rabenh. Fungi Europ., No. 1872, 1874. 

Stat, conid. 

Gylindrosporium ranunculi var. microsporum D. Saccardo, 1904. 

Entylomella microspora (D. Sacc.) Ciferri, 1938. 

Sori in the leaves and petioles as round or fusiform yellowish-brown swellings. 

Spores globose or irregular, pale yellowish brown, epispore formed of several 

layers, 2-6 /x thick, smooth, 12-21 X10-18 /LI. Sporidia on the host fusiform, 

hyaline, 12-18x2-5/n. 

On Eanunculus repens, R. acris. 

Sept.-Oct. England (Yorks.), Scotland. 

Spore germination. De Bary (1874) obtained germination in 24 hours by placing 

spores from a fresh, ripe sorus in water in a moderately warm room. Spores 

dried for three months also germinated. Four to eight (usually six or seven) 

terminal branches developed simultaneously on the promycelium with apical or 

basal fusion. Sometimes the branches grew out to form mycelium, sometimes 

they gave rise to long, thin, slightly bent sporidia (Fig. 20 b).


Infection of the. host. Characteristic flecks developed in 11 to 14 days after 

inoculating leaves of R. repens with germinating chlamydospores (de Bary, 

1874). 

DoASSANSiA Cornu, 

Ann. Sci. nat.. Bat., Ser. 6, xv, p. 285, 1883. 

Type; Doassansia alismatia (Nees) Cornu on Alisma plantago, Europe. 

Synonyms: SetchelUa Magnus, 1895. 

Doassansiopsis (Setch.) Dietel, 1897, p.p. 

Sari usually in the leaves of aquatic plants or of plants in moist situations; 

rather permanently embedded in the host tissue. Spore balls each composed of 

a sterile cortical layer and a central mass of fertile spores which in some species 

surround a central core of sterile cells or hyphae. Spores light-coloured, thinwalled, 

smooth. Spore germination, see below. 

Setchell (1892) in his monograph of the genus distinguished three sub-genera: 

Eudoassansia, for forms such as D. sagittariae and D. alismatis, in which the 

centre of the spore ball is composed of spores only; Doassansiopsis, for forms 

such as D. martianoffiana, in which the spores surround a core of parenchymatous 

tissue; and Pseudodoassansia in which the spores enclose an irregular 

mass of hyphae. 

Doassansia alismatis (Nees) Cornu 

Sclerotium alismatis Nees in Fries, Systema, ii, p. 257, 1822. 

Perisporium alismatis Fries, ibid., iii, p. 252, 1829. 

Doassansia alismatis (Nees) Comu, Ann. Sci. nat., Bot., Ser. 6, xv, p. 285,1883. 

Sphaeria alismatis Currey, Trans. Linn. Soc., Lond., xxii, p. 334, 1859 fide 

SeteheU [but see Grove, Coelomycetes, i, p. 53, 1935]. 

Sphaeropsis alismatis (Currey) Cooke, 1867. 

Phyllosticta curreyi Saccardo, Syll. Fung., iii, p. 60, 1884 [nov. nom. for S. alismatis']. 

Cylindrosporium alismacearum Saccardo, p.p., fide Grove, 1937. 

Sori in the leaves as yellowish to brownish circular spots up to 1 cm. diam. and 

as larger irregular areas on which the embedded spore balls form numerous 

minute elevations. Spore balls more or less spherical, dark reddish-brown, 

130-200 [I diam., each composed of a distinct cortical layer of radially elongated 

cells (10-20x5-12 /x) surrounding a central mass of spores. Spores globose or 

somewhat angled, tinted yellowish, smooth, 10-12 /j, diam. 

On Alisma plantago-aquatica. 

July-Oct. England (Suffolk), Scotland. 

Exsiccati: Cooke, Fungi Brit. Exsicc, i, 431 (as Sphaeropsis alismatis). 

Spore germination. Comu (1883) found that the spores germinated easily in 

water forming a crown of sporidia which were at first fusiform, elongated and 

diverging, later almost thread-like. Brefeld (1895) so figured germination. 

SetcheU (1892) who germinated fresh spores in July to August and dried 

material in October to March, described the process in some detail. The promycehum 

was long, slender (40-50 X 3-4 jti) with five to seven fusiform sporidia


(20-28 X 2 /i) at the apex. Septation occurred as the protoplasm passed to the 

apex and a short stump of the promyceUum separated after the sporidia had 

become detached (see Fig. 15 e). The sporidia conjugatedlin pairs at the base. 

Germ-tubes developed from the apex of one or both sporidia or from the base. 

Unconjugated sporidia did not germinate but sometimes the promyceUum gave 

rise directly to mycelium. No secondary sporidia were observed. Grove (1937) 

assumes that Cylindrosporium alismacearum Sacc. represents the sporidia produced 

on promycelia from spores of Doassansia alismatis germinating in sihi. 

This may be so, but it is possible that this Doassansia sometimes develops sporidia 

directly from parasitic mycelium (see p. 23). 

Doassansia limosellae (Kunze) Schroet. 

Protomyces limoseUae Kunze, Rabenh. Fungi Eur., No. 1694 (1873). 

Entyloma limosellae (Kunze) Winter, 1884. 

Doassansia limosellae (Kunze) Schroeter, Die Pilze Schles., iii, p. 287, 1887. 

Burrillia limosellae (Kunze) Liro, 1920. 

Sori in the leaves and leaf stalks on both surfaces of which the embedded spore 

balls form numerous, irregularly scattered, brown then black elevations, at first 

beneath the epidermis, later erumpent. Spore balls oval or globose, brown, 

50-150 [I diam., each composed of a central mass of spores enclosed by what 

appears to be partly disorganized brown hyphae. Spores globose to oval, pale 

brown, smooth, 9-11 fi diam. 

On Limosella aquatica. 

Earlswood Reservoir, Warwickshire, on dried-up mud, W. B. Grove, Oct., 1921 

(see J. Bot., Lond., Ix, p. 169, 1922), and Oct., 1929 [Herb. Grove in Herb. 

Univ. Birmingham]. 

As can be seen from the synonymy, there is some doubt regarding the generic 

position of this smut which was excluded from Doassansia by Setchell (1892). 

Pending the examination of fresh material, the name used is that under which 

the fungus was first recorded for this country by Grove {loc. cit.). 

Spore germination. Brefeld (1895), who was only able to germinate spores in 

nutrient solution, described the spore germination as being very similar to that 

of D. sagittariae. Grove (Joe. cit.) observed spores on the host in a state of active 

germination and reported conjugation of the primary sporidia in pairs and the 

presence of great numbers of elongated secondary sporidia. 

Doassansia martianoffiana (Thiim.) Schroet. 

Protomyces martianoffianus Thiimen, Bull. Soc. imp. Nat. Moscou, liii, p. 207, 

1878. 

Doassansia martianoffiana (Thiim.) Schroeter, Die Pilze Schles., iii, p. 287, 1887. 

Doassansiopsis martianoffiana (Thiim.) Dietel, 1897. 

Sori in the undersides of the leaves as round or irregular yellowish spots on 

which the embedded spores baUs form numerous minute elevations. Spore balls 

sub-globose, brownish, 120-160 /x diam., each consisting of a cortical layer within 

which is a layer of spores enclosing a central mass of parenchymatous cells. 

Spores sub-globose or shghtly elongated, pale yellow, smooth, 8-12 /x diam.

THE BKITISH SMUT FUNGI 111 

[Sporidia on the liost, on blunt hyphae protruding from the stomata, long, 

slender, 30 X1 -5 fi. They apparently germinate in position and give rise to small 

bunches of tangled hyphae (Setchell, 1892,1894).] 

On Potamogeton sp. 

Ayrshire, Ardrossan, Aug., 1911, D. A. Boyd (Trans. Brit, mycol. Soc., iv, p. 185, 

1912) and West Kilbride, July, 1914, D. A, Boyd [Herb. Kew.]. 


Doassansia sagittaiiae (Westend.) C. Fisch 

Uredo sagittariae Westendorp., Herb, crypt. Belg., No. 1177, 1857. 

Physoderma sagittariae Fuckel, 1865. 

Protomyces sagittariae (Fuckel) Fuckel, 1869. 

Aecidiwm incarceratum Berkeley & Broome, 1875 [Notices of British Fungi, 

No. 1469]. 

Doassansia sagittariae (Westend.) C. Fisch, Ber. dtsch. hot. Ges., ii, p. 405, 1884. 

Sori in the leaves as yellowish brown spots 5-10 mm. diam. on which the embedded 

spore balls form numerous minute elevations. Spore balls more or less 

spherical, pale yellow-brown, 50-80 fi diam., each composed of a distinct cortical 

layer of rather irregularly arranged sterile cells, 12-18 fj. diam., and a central 

mass of spores. Spores globose to angular, tinted yellow, smooth, 8-12 [j. diam. 

On Sagittaria sagittifolia. 

Summer. England. Uncommon. 

Exsiccati: Vize, Micro. Fungi Brit. 50 (as Protomyces sagittariae); Rabenhorst, 

Fungi Europ., No. 1492 (as Aecidium incarceratum; some specimens of this 

exsiccata are leaves of Alisma plantago presumably infected by D. olsiTnatis). 

Spore germirmtion. Fisch (1884) obtained germination in spring and early 

summer. The sporidia are inserted at unequal distances on the markedly conical 

tip of the promycelium. They were not observed to conjugate but, rarely, 

fusions took place between secondary sporidia. This was confirmed by Brefeld 

(1895) who germinated over-wintered spores (Fig. 15/) and found that sporidia 

were viable after three months. Infection takes place throughout the summer, 

first from overwintered spores and then from sporidia. Infected leaves are 

always raised above the surface of the water. 

Type: GrapUola Poit., 1824. 

GRAPHIOLACEAE 

Sori in the leaves of palms, erumpent, single or in groups in a compact black 

peridium. Sporidia ('spores') produced laterally in whorls at the septa of sporogenous 

hyphae (equivalent to chains of chlamydospores) arising from the base 

of the sorus. 

GEAPHIOLA Poiteau, 

Ann. Sci. nat. iii, p. 473, 1824 

Ty^: Graphiola phoenicis Poit. on date-palm [Phoenix dactylifera], Paris, 

France. 

Sori single, each with an inner thin-walled, colourless, peridium and fascicles of


protruding sterile hyphae intermixed with the sporogenous hyphae. Sporidia 

globose to elliptical. Sporidial germination by a filamentous mycelium or by the 

formation of fusiform secondary spores. 

Graphiola phoenicis Poit. , Palm Smut 

Oraphiola phoenicis Poiteau, Ann. Sci. nat. iii, 473, 1824 [G. phoenicis (Moug.) 

de Toni [as '(Moug.) Poit.'] {PRacidium phoenicis Mougeot, 1821) is a later 

homonym]. 

Sari in the leaves, erumpent, rounded, 1-1-5 mm. wide, 0-5 mm. high, each with 

a hard black outer wall surrounding a thin colourless membrane, at first closed, 

then with an apical opening through which fascicles of yellowish hyphae protrude 

2 mm. or more. Sporidial mass yqUowish, granular. Sporidia globose to 

elliptical, colourless, smooth, 3-6 /x diam. 

On date-palm (Phoenix dactylifera) in greenhouses. 

Eccsiccati: Vize, Fungi Brit., 171; Fungi exsicc. Select, ex Herb. M. C. Cooke, on 

palms, Kew Gardens, April, 1855. 

DOUBTFUL AND EXCLUDED SPECIES 

Doassansia comari (Berk. & White) de Toni & Massee {Protomyces comari Berk. 

& White) = Physoderma comari (Berk. & White) Lagerh. See Sampson 

(1940). 

Melanotaenimn ari (Cooke) Lagerh. [Protomyces ari Cooke (Grevillea, i, p. 7, 

1872) on leaves of Arum maculatum, Chichester) has frequently been accepted 

as a smut but an examination of the type specimen and other European 

material in Herb. Kew. supports the opinion expressed by Beer (1920) that 

this species does not belong to the UstUaginales. The thick-walled spores are 

possibly oospores. 

Sorosporiom scabies (Berk.) Fisch. v. Waldh. (Tuburcinia scabies Berk.) = 

Spongospora subterranea (Wallr.) Lagerh. 

Sphacelotheca reiliana (Kiihn) Clinton on maize was compiled by Cooke (1906) 

but no British record has been traced. 

Tilletia berkeleyi Massee (1899) on Triticum vulgare, King's Cliffe, Northants. 

(Rev. M. J. Berkeley). The type specimen, which has no spores, gives no clue 

to this very doubtful species. 

Tilletia sphagni Nawaschin in capsules oi Sphagnum papillosum Lindb., Blelham 

Tarn, nr. Ambleside, Westmorland, 24 March 1948 (D. Walker, 1948), is of 

doubtful affinity. 

Tolyposporium montiae (Rostr.) Rostr. (Sorosporium montiae Rostr.) which was 

recorded on Montia fontana. West Kilbride, Ayrshire (D. A. Boyd) by Wakefield 

& Dennis {Trans. Brit, mycol. Soc, xxix, p. 145, 1946) is of doubtful 

affinity and does not, it is felt, justify the introduction of either Tolyposporium 

or Sorosporium into the British list. 

IlstilagO caidui Fisch. v. Wald. on Carduus was recorded by Cooke (1878) and 

Plowright (1889). No British specimen has been traced but there is a record 

on Girsium paltistre (F. A. Mason, Naturalist, 1921, p. 349). 

Ustilago cucumis A. B. Grifiiths, zooglea threads in root nodules of Cucumis 

sativa.


Ustilago ficuum Eeichardt on figs, Plowright (1889), p. 85 (footnote) is a species 

of Aspergillus, probably of the A. niger series, fide Thom & Raper, Manual 

of the Aspergilli, 1945. 

Ustilago grammica Berk. & Br. on Aira aquatica, Oxton, Notts., is probably a 

species of Pirostoma and the host may be Olyceria aquatica. See Sampson 

(1940). 

Ustilago phoenicis Corda on dates, Plowright (1889) p. 85 (footnote) = Aspergilliis 

phoenicis (Corda) Thom. 

UstUago rudolphi Tul. was recorded on Dianthu^ deltoides in a Norwich garden 

by Southwell {Gfrevillea, x, p. 67, 1881) and described by Plowright (1889) as 

Sorosporium saponariae Rudolphi. The description does not agree with 

S. saponariae, which is confined to Saponaria, and in the absence of a 

specimen the identity of the fungus recorded on D. deltoides must remain in 

doubt. 

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114 THE BKITISH SMUT KTTNGI 

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INDEX 

to generic and specific names of smuts (italics) and to British hosts (romans) 

Bold face page number indicates description, asterisk {*) a figure. 

Achillea miUefolium 

Entyloma achilleae, 102 

Aecidium incarceratum B. & Br., Ill 

Agropyron 

Vrocystis agropyri, 94 

Vstilago hypodytes, 57 

— macrospora, 69 

Agrostia 

Tilletia decipiens, 86 

Alisma plantago-aquatica 

Doassansia alismatis, 109 

Alliimi 

Vrocystis cepulae, 95 

Ammophila arenaria 


Anemone 

Vrocystis anemones, 94 

Anthracoidea Bref., 78 

— carycis (Pers.) Bref., 78 

— suhinclusa (Kom.) Bref., 79 

Apimn nodiflorum 

Entyloma helosciadii, 107 

Arrhenatherum elatius 

Vrocystis agropyri, 94 

Vstilago avenae, 61 

— striiformis, 68 

Ascomyces trientatis Berk., 90, 92 

Avena 

Vstilago avenae, 61 

— hordei, 58 

Barley, see Hordeum 

Bellis perennis 

Entyloma calendulae f. belUdis, 104 

Bromus 

Vstilago bullata, 65 

— hypodytes, 57 

— macrospora, 69 

Bulbocodium vernum 

Vrocystis colchici, 96 

Burrillia limosellae (Kunze) Liro, 110 

Caeoma bistortarum (DC.) Link, 65 

— colchici Schlecht., 96 

— destruens Schlecht., 76 

— hypodytes Schlecht., 56 

— longissimum Schlecht., 56 

— marginale (DC.) Link, 65 

• —pompholygodes Schlecht., 94 

— urceolorum (DC.) Schlecht., 78 

— utriculosa Nees, 72 

Calamagrostis canescens 

Vstilago macrospora, 69 

Calendula 

Entyloma calendulae, 102 

Calystegia 

Thecaphora seminis-convolvuli, 80 

Carduus heterophyllus 

Thecaphora trailii, 81 

Carex 

Cintractia caricis, 79 

— suhinclusa, 79 

Parysia olivacea, 75 

Vrofystis fischeri, 97 

Carnation, see Dianthus caryophyllus 

Cerastium viscosum 

Vstilago violacea, 70 

Chionodoxa luciliae 

Vstilago vaillantii, 59 

Chrysosplenium oppositifolium 

Entyloma chrysosplenii, 105 

CINTRACTIA Comu, 78 

Cintractia axicola (Berk.) Cornu, 78 

— caricis (Pers.) Magn., 74*, 78* 

— cingens (Beck) de Toni, 100 

— karii Liro, 74,* 79 

— montagnei (Tul.) Magn., 28, 79 

— patagonica Cooke & Massee, 65, 66 

— pratensis Syd., 79 

— scirpi (Kuhn) Schellenb., 79 

•— suhinclusa (Kom.) Magn,, 74,* 79 

Cirsium 

Vstilago cardui, 112 

Colchicum 

Vrocystis colchici, 96 

Convolvulus arvensis 

Thecaphora seminis-convolvuli, 80 

Cucubalus baccifer 


Cylindrosporium alismacearum Sacc, 109, 

110 

— ficariae Berk., 106 

— helosciadii repentis Magn., 107 

— ranunculi (Bon.) Sacc, 106 

var. microsporum D. Sacc, 108 

Dactylis glomerata 

Vstilago striiformis, 68 

Dahlia 

Entyloma calendulae f. dahliae, 104 

Deschampaia caespitosa 


Dianthus caryophyllus 


— deltoides 

^Vstilago rudolphi', 113 

DOASSANSIA Comu, 109 

Doassansia alismatis (Nees) Comu, 18, 27, 

91,* 109, 111 

— comari (Berk. & White) de Toni & Massee, 

112 

— deformans Setch., 17 

— limosellae (Kunze) Schroet., 110 

— martianoffiana (Thum.) Schroet., 23, 110 

— obscura Setch., 18 

•— occulta (Hoffm.) Diet., 18 

— sagittariae (Westend.) Pisch, 18, 91,* 

109, 110, 111 

Doassansiopsis (Setch.) Diet., 109 

— horiana (P. Henn.) Shen, 24 

— martianoffiana (Thiim.) Diet., 23, 110 

Elateromyces Bubak, 75 

— olivaceus (DC.) Bubak, 75 

Eleocharis parvula 

Vstilago marina, 75 

Elymus arenarius 

Vstilago hypodytes, 57

134 

Endoihlaspis Sorok., 76 

ENTORRHIZA Weber, 87 

Entorrhiza aschersoniana (Magn.) Lagerh., 

87, 88* 

— cypericola (Magn.) Weber, 87, 88 

— digitata Lagerh., 88 

ENTYLOMA de Bary, 102 

Entyloma achilleae Magn., 102 

— azistrale Speg., 23 

— bellidis Kreiger, 104 

— bicolor Stromeyer, 107 

^^calendulae (Oudetn.) de Bary, 12, 22,* 

23. 25, 102, 103* 

f.6eHia!»s (Kreiger) Ainsw.& Samps.,104 

f. dahliae (Syd.) Viegas, 12, 18, 22,* 

23, 52, 104 

f. hieracii Sohroet., 104 

— canescens Sohroet., 105 

— chrysoaplenii (B. & Br.) Sohroet., 105 

— compositarum Farl., 23 

— endogenum (Ung.) Wiinche, 101 

— eryngii (Corda) de Bary, 105 

—fergussoni (B. & Br.) Plowr., 105 

—ficariae (B. & Br.) F. v. Waldh., 22,* 23, 

25, 28, 103,* 106* 

—ftiscum Schroet., 107 

— helosciadii Magn., 107 

—• henningsianum Syd., 108 

— hieracii Syd., 104 

—• limosellae (Kunze) Wint., 110 

— linariae Sohroet., 23 

— lobeliae Farl., 23 

— magnusii Woron., 103* 

— matricariae Rostr., 23, 108 

Trail, 108 

— meliloH, Mo Alp., 23 

— menispermi Farl. & Trel., 23 

— microsporum (ting.) Sohroet., 102, 103,* 

106, 108 

— nympheae (D. Cunn.) Setch., 16, 23 

— oenoiherae Marohal & Stemon, 23 

— polysporum (Peck) Farl., 23 

— ranunculi (Bon.) Sohroet., 106 

— serotinum Sohroet., 22, 106 

— trailii Massee, 23, 108 

— ungerianum de Bary, 102, 108 

f. flcariae Wint., 106 

Entylomella flcariae (Berk.) Hohn., 106 

— hehsciadii-repentis (Magn.) Hohn., 107 

— microspora (D. Saoc.) Cif., 108 

Eranthis hiemalis 

Vrocystis eranthidis, 97 

Eryngiinn maritimum 

Entyloma eryngii, 105 

Erysibe occulta Walh., 98 

— typhoides Wallr., 59 

— vera holci-avenacei Wallr., 60 

Farinaria carbonaria Sow., 78 

— scabiosae Sow., 71 

— stellariae Sow., 70 

FARYSIA Raoib., 75 

Farysia caricis (DC.) Lire, 75 

—javanica Raoib., 75 

— olivacea (DC.) Syd., 74,* 75* 

Festuoa 


— striiformis, 68 

Filipendula hexapetala 

Vrocystis filipendulae, 97 

Fusidium ranunculi Bon., 106 

Fusisporium inosculans Berk., 83 

INDEX 

Gagea lutea 

Vstilago omithogali, 60 

Galium verum • 

Melanotaenium endogenum, 101 

Oeminella Sohroet., 881 

— delastrina (,Tul.) Sohroet., 88 

Qinanniella Cif., 90 

— trientalis (B. & Br.)]Cif., 90 

Gladiolus 

Vrocystis gladiolicold, 98 

Oloeosporium antherarum Oudem., 81 

—flcariae. (Berk.) Cooke, 106 

Glyoeria 

Vstilago longissima, 56 

Granularia violae Sow., 100 

ORAPHIOLA Poit., Ill 

Graphiola pkoenicis Poit., 17, 111 

Hepatiea pennsylvaniea 

Vrocystis hepaticae-trilobae, 98 

Hieraoium 

Entyloma calendulae f. hieracii, 105 

Holous 

Tilletia hold, 86 


Hordeum 

Vstilago hordei, 58 

— nuda, 63 

Junous 

Entorrhiza aschersoniana, 88 

Vrocystis junci, 98 

Knautia arvensis * 

Vstilago flosculorum, 72 

— sc(Aiosae„ 71 

Lamium albiun 

Melanotaenium lamii, 102 

Lathyrus pratensis 

Thecaphora deformans, 80 

Leek, see Alhvun 

LimoseUa aquatioa 

Doassansia limosellae, 110 

Linaria spuria 

Melanotaenium hypogaeum, 101 

— vulgaris 

Melanotaenium cingens, 100 

Lolium 

Tilletia lolii, 87 


Lychnis flos-cuouli 


Lycoperdon tritici Bjerk., 83 

Maize, see Zea mays 

Matricaria inodora 

Entyloma matricariae, 108 

Melandrium 


MELANOTAENIVM de Bary, 100 

Melanotaenium ari (Cooke) Lagerh., 112 

— caulium Sohroet., 100 

— cingens (Berk.) Magn., 82* 

— endogenum (Ung.) deBary, 82,* 100,101* 

— hypogaeum (Tul.) Sohellenb., 101 

— lamii Beer, 15, 102 

Syd., 102 

Montia fontana 

Tolyposporium montiae, 112

Muscari 

Ustilago vaillantii, 59 

Myosotis 

Entyloma fergussoni, 105 

Oats, see Avena 

Onion, see AUiuni' 

Oxyria digyna 

Ustilago vinosa, 69 

INDEX 

Paipalopsis irmischae Kiihn, 21, 90 

Panieum miliaceum 

Sphacelotheca destruens, 76 

Papaver rhoeas 

Entyloma fuscum, 107 

Perisporium alismatis Fr., 109 

Phacidium phoenicis Moug., 112 

Phalaris arvindinaeea 

Tilletia menieri, 87 

Ustilago striiformis, 68 

Phleum pratense 


Phoenix dactylifera 

Graphiola phoenicis, 112 

Phragmites communis 

Ustilago grandis, 59 

Phyllosticta curreyi Sacc, 109 

Physoderma comari (Berk. & White) Lagerh., 

112 

— eryngii Corda, 105 

— sagittariae Fuckel, 111 

Poa pratensis 


Poikilosporium Diet, 80 

— trailii (Cooke) Vesterg., 81 

Polycystis anemones (Pers.) L6v., 94 

var. eranthidia Pass., 96 

— colchici Tul., 96 

—filipendulae Tul., 97 

— hohi Westend., 86 

— occulta (Wallr.) Schlecht., 98 

— parallela (Berk.) Fr., 98 

— pompholygodes (Schlecht.) Lev., 94, 95, 96 

— violae (Sow.) B. & Br., 100 

Polygonum 

Sphacelotheca hydropiperis, 77 

— inflorescentiae, 77 

Ustilago anomala, 72 

— histortarum, 65 

— vtriculosa, 72 

Potamogeton 

Doassansia martianoffiana, 110 * 

Primula 

TvJburcinia primulicola, 90 

Protomyces ari Cooke, 112 9 

— calendulas Oudem., 102 

— canescens B. & Br., 105 

— chrysosplenii B. & Br., 105 

— comari Berk. & White, 112 

— endogenus TJng., 101 

•— gain Nees, 101 

— limoseUae Kunze, 110 

— microsporus XJng., 108 

— martianoffiana (Thiim.) Schroet., 110 

— sagittariae (Fuckel) Fuckel, 111 

Ranunculus 

Entyloma ficariae, 107 

— microsporum, 108 

Urocystis anemones, 95 

Beticularia segetum BuU., 58, 60 

Rhamphospora D.D. Cimn., 102 

Rhynchospora alba 

Cintractia caricis 78 

Rumex 

Ustilago kuehneana, 73 

Rye, see Secale 

135 

Sagittaria sagittifolia 

Doassansia sagittariae. 111 

Samolus valerandi 

Entyloma henningsianum, 108 

Schinzia aschersoniana Magn., 87, 88 

— cypericola Magn., 87 

80HB0ETERIA Wint., 88 

Schroeteria decaisneana (Bond.) de Toni, 89 

— delastrina (Tul.) Wint., 88, 89* 

var. reticulata Cocconi, 89* 

Scilla 

Ustilago vaillantii, 59 

Scirpus caespitosus 

Gintractia caricis, 79 

Sclerotium alismatis Fr., 109 

Secale 

Tilletia caries, 83 

Urocystis occulta, 99 

Setchellia Magn., 109 

Silene 

Ustilago violacea, 70 

Sorosporium montiae Rostr., 112 

— sapononoe Rudolphi, 113 

— scabies (Berk.) F. v. Waldh., 112 

— syntherismae, 31, 33, 34, 38 

— trientalis (B. & Br.) Cooke, 90 

SPHACELOTHECA de Bary, 76 

Sphacelotheca cruenta, 28, 30, 32, 33, 34 

— destruens (Schlecht.) Stevenson & A. G. 

Johns, 31, 33, 34, 38, 76 

— hydropiperis (Schmn.) de Bary, 74,* 76, 

77,* 78 

— inflorescentiae (Trel.) Jaap, 77 

— panici-milacea (Pers.) Bubak, 76 

— pologoni-vivipari Sohellenb., 77 

— reiliana (Kiihn) Clint., 15, 26, 29, 32, 33, 

34, 41, 43, 112 

— schweinfurthiana (Thiim.) Sacc, 30 

— sorghi (Link) Clint., 18, 28, 29, 31, 32, 

33, 34, 38, 42, 43 

— ustilaginea (DC.) Cif., 77 

Sphaeria alismatis Currey, 109 

Sphaeropsis alismatis (Currey) Cooke, 109 

Sphagnum, papillosum 

.--fOîlletia sphagni, 112 

Spongospora subterranea (Wallr.) Lagerh., 

112 

Stellaria 

/ Ustilago violacea, 70 

Succisa pratensis 

Ustilago succisae, 71 

Thalictrum minus 

Urocystis sorosporioides, 99 

THECAPHORA Fingerh., 80 

Thecaphora deformans Tul., 74,* 80 

— delastrina Tul., 88 

— hyalina Fingerh., 80 

— lathyri Kiihn, 80 

— seminis-convolvuli (Duby) Lire, 74,* 80, 

81* 

— trailii Cooke, 81 

TILLETIA Tul., 81 

Tilletia herheleyi Massee, 112 

— bullata Fuckel, 65

136 

TiUetia caries (DC.) Tul., 10, 11, 13, 18, 20, 

24, 26, 27, 28, 30, 31, 32, 40, 41, 81, 

82,* 83,* 84, 85 

— de baryana F. v. Waldh., 68 

— decipiens (Pers.) Komicke, 15, 39, 82,* 86 

—foetida (Wallr.) Liro, 11, 13, 18, 30, 32, 

84 

— holci (Westend.) Sohroet., 86 

•— indica Mitra, 85 

•— lolii Auers, 86 

— menieri Har. & Pat., 87 

— rauwenhoffii F. v. Waldh., 86 

— secalis (Corda) Kuhn, 83, 84 

— separata Massee, 83, 86 

— sphaerococca (Rabenh.) F. v. Waldh., 86 

— sphagni Nawasch., 112 

— striaeformis (Westend.) Sacc, (58 

— tritici (Bjerk.) Wolff, 83 

— tumefaciens Syd., 15 

Tolyposporium fiUferum Busse, 24 

— montiae (Bostr.) Rostr., 112 

Tragopogon 

Vstilago tragopogonis-pratensis, 73 

Trientalis europea 

Tuburcinia trientalis, 92 

Trisetum flavescens 


Tritieum ' 

TiUetia caries, 83 

Ustilago nuda, 63 

TroUius europaeiis 

Urocystis anemones, 95 

TVBVRGINIA Fr. em. Woron., 90, 92 

Tuburcinia agropyri (Preuss) Liro, 92 

— anemones (Pers.) Liro, 94 

— cepulae (Frost) Liro, 95 

— colchici (Sehlecht.) Liro, 96 

— eranthidis (Pass.) Liro, 96 

—filipendulae (Tul.) Liro, 97 

•—fischeri (Komicke) Liro, 97 

— hepaticae-trilobae (DC.) Liro, 98 

—junci (Lagerh.) Liro, 98 

— occulta (WaUr.) Liro, 99 

— primulicola (Magn.) Bref., 90, 91* 

•—scabies Berk., 112 

— sorosporioides (Komicke) Liro, 99 

— trientalis B. & Bh, 21, 90, 91,* 92* 

— tritici (Kornieke) Liro, 92 

•—violae (Sow.) Liro, 99 

Uredo agropyri Preuss, 92 

— anemones Pers., 94 

— antherarum DC, 70 

— bistortarum a pustulata DC, 65 

P marginalis DC, 65 

y ustilaginea DC, 77 

— carbo DC, 58, 60, 63 

— caricis Pers., 78 

— caries DC, 83 

— colchici Link, 96 

— decipiens a graminum Strauss, 86 • 

—flosculorum DC, 71 

— hydropiperis Schum., 76 

— longissima Sow., 56 

— maydis DC, 66 

— olivacea DC, 75 

— omithogali Schm. & Kunze, 60 

— parallela Berk., 98 

— pompholygodes Berk., 95 

— ranunculacearum S hepaticae-trilobae DC, 

98 , 

— receptaculorum DC, 73 

INDEX 

Uredo receptaculorum tragopogi DC, 73 

— sagittariae Westend., Ill 

— segeturn snhsp. avenae Pers., 60 

-T f. caricis Pers,, *75 

€ decipiens Pers., 86 

subsp. hordei Pers., 58 

var. mays-zeae DC, 66 

var. panici-miliacea Pers., 76 

subsp. tritici Pers., 63 

— seminis-convolvuli Duby; 80 

— sphaerococca Rabenh., 86 

— striaeformis Westend., 68 

— tragopogi Pers., 73 

pratensis Pers., 73 

— urceolorum DC, 78, 79 

Pers., 78 

— vinosa Berk., 69 

— violacea Pers., 70 

— zeae Schwein., 66 

UEOCYSTIS Rabenh., 90, 92 

Urocystis agropyri (Preuss) Sohroet., 11, 19, 

92, 94 

— anemones (Pers.) Wint., 18, 26, 93,* 94 

— cepulae Frost, 11, 13, 16, 17, 19, 48, 49, 

95 

— colchici (Sehlecht.) Rabenh., 96 

var. cepulae Cooke, 95 

— eranthidis (Pass.) Ainsw. & Samps., 96 

—filipendulae (Tul.) Schroet., 97 

—fischeri Komicke, 93,* 97 

— gladioli W. G. Sm., 98 

— gladiolicola Ainsw., 12, 98 

— hepaticae-trilobae (DC) Ainsw. & Samps., 

98 

—junci Lagerh., 98 

— occuUa (Wallr.) Rabenh., 11, 17, 19, 92, 

93,* 98, 99* 

— parallela (Berk.) F. v. Waldh., 99 

— pompholygodes (Pers.) Rabenh., 94, 95, 98 

var. eranthidis (Pass.) Pass., 96 

— primulicola Magn., 90 

— sorosporioides Komicke, 99 

•—tritici Komicke, 11, 19, 92; and see V. 

agropyri 

— violae (Sow.) F. v. Waldh., 12, 17, 93,* 

100 

Ustilagidium Herzb., 54 

USTILAGO (Pers.) Rous., 54 

Ustilago anomala Kunze, 72* 

— antherarum (DC) Fr., 70 

— avenae Jens., 60 

(Pers.) Rostr., 10, 11, 13, 18, 25, 28, 

29, 30, 31, 32, 33, 34, 35, 44, 52, 56, 58, 

60, 63, 66 

var. levis Kellerm. & Swing., 58 

f. nigra Tapke, 63 

— bistortarum (DC) Komicke, 55,* 65, 78 

var. inflorescentiae Trel., 77, 78 

— bullata'BeTk., 10, 18, 24, 30, 34, 36, 44, 47, 

55,* 65, 68 

— calamagrostidis (Fuokel) Clint., 69 

— candollei Tul., 76 

— carbo (DC) Tul., 58, 60, 63 

a. vulgaris 8 bromivora Tul., 65 

— cardui F. v. Waldh., 112 

— caricis (Pers.) XJng., 78 

— cingens Beck, 100 

— crameri Kornieke apud Fuokel, 19, 26, 

28, 38 

— cucumis Griff., 112 

— decipiens (Walh.) Liro, 60 

— echinata Sohroet., 69

Ustilago ficuum Reich., 113 

—flpsculorum (DC.) Fr., 71 

var. succissae Vize, 71 

— grammica B. & Br., 113 

— grandis Fr. 65,* 59 

— heufleuri Fuckel, 16, 25 

— holci-avenacei (Wallr.) Cif., 60 

— hordei (Pers.) Lagerh., 11, 15, 18, 19, 24, 

26, 28, 29, 30, 31, 32, 33, 34, 35, 36, 38, 

44, 49, 52, 58, 61, 63, 66 

— hydropiperis (Schum.) Schroet., 77 

— hypodytes (Schlecht.) Fr., 15, 24, 55,* 56 

—-hypogea Tul,, 101 

•—inflorescentiae (Trel.) Maire, 77 

— kolleri Wille, 58; and see V. hordei 

— kuehneana Wolff, 55,* 73 

— levis (KeUerm. & Swing.) Magn. 58 

— longissima (Schlecht.) Meyen, 28, 30, 33, 

55,* 56, 69, 75 

var. macrospora Davis, 33, 66 

— macrospora Desm., 69 

— major Schroet., 70, 71 

— marina Dur% d. Maisson., 75 

— maydis (DC.) Corda 10, 13, 14, 16, 19, 24, 

26, 28, 29, 30, 31, 34, 35, 36, 37, 40, 

41, 42, 43, 46, 49, 50, 66, 67 

— mays-zeae Magn., 67 

— medians, see U. avenae 

•— neglecta Niessl, 38 

— nigra Tapke, 43, 60, 62; and see U. avenae 

— nuda (Jens.) Rostr., 11, 13, 14, 24, 25, 26, 

28, 30, 42, 45, 51, 62, 63,* 68 

— oUvacea (DO.) Tul., 75 

— ornithogali (Schm. & Kunze) Magn., 60 

— panici-miliacea (Pers.) Wint., 76 

— patagonica (Cooke & Massee) Cif., 65 

•— perennans Rostr., 33, 52, 60; and see U. 

avenae 

— phoenicis Corda, 113 

— pustulata (DC.) Wint., 66 

— receptaculorum (DC.) Fr., 73 

INDEX 137 

Ustilago rudolphi Tul., 113 

— salvei B. & Br., 67 

— scabiosae (Sow.) Wint., 27, 55,* 71 

— scillae Cif., 59 

— scorzonerae Schroet., 42 

— segetum (Pers.) Dittm., 54, 58, 60, 63 

var. hordei f, nuda Jens., 63 

var. nuda Jens., 63 

— spegazzini Hirsch. var. agrestis (Syd.) 

Fischer & Hirsch., 55* 

— sphaerogena Burrill, 38 

— striiformis (Westend.) Niessl, 18, 19, 26, 

28, 29, 30, 31, 40, 41, 42, 46, 55,* 67, 68 

f. hordei Fischer, 68 

— subinclusa Korn., 79 

— succisae Magn., 71 

— tragopogi de Toni, 73 

— tragopogonis-pratensis (Pers.) Rous , 65 * 

73 

— tritici (Pers.) Rostr., 63; and see V. nuda 

— typhoides (Wallr.) B. & Br., 69 

— urcelorum (DC.) Tul., 78, 79 

— ustilaginea (DC.) Liro, 77 

— utriculosa (Nees) Tul., 72*, 77 

— vaillantii Tul., 14, 16, 48, 55,* 59 

— vinosa Tul., 69 

— violacea (Pers.) Fuckel, 12,14, 24, 27, 28, 

29, 30, 34, 42, 56, 70 

— vuijckii Oudem. & Beyer, 16 

— zeae (Beckm.) Unger, 66 

Veronica arvensis 

Schroeteria delastrina, 89 

Viola 

Vrocystis violae, 100 

Wheat, see Triticum 

Zea mays 

Ustilago maydis, 67

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