Fungal Diversity (2014) 67:21–125
DOI 10.1007/s13225-014-0298-1
One stop shop: backbones trees for important phytopathogenic
genera: I (2014)
Kevin D. Hyde & R. Henrik Nilsson & S. Aisyah Alias & Hiran A. Ariyawansa &
Jaime E. Blair & Lei Cai & Arthur W. A. M. de Cock & Asha J. Dissanayake &
Sally L. Glockling & Ishani D. Goonasekara & Michał Gorczak & Matthias Hahn &
Ruvishika S. Jayawardena & Jan A. L. van Kan & Matthew H. Laurence &
C. André Lévesque & Xinghong Li & Jian-Kui Liu & Sajeewa S. N. Maharachchikumbura &
Dimuthu S. Manamgoda & Frank N. Martin & Eric H. C. McKenzie &
Alistair R. McTaggart & Peter E. Mortimer & Prakash V. R. Nair & Julia Pawłowska &
Tara L. Rintoul & Roger G. Shivas & Christoffel F. J. Spies & Brett A. Summerell &
Paul W. J. Taylor & Razak B. Terhem & Dhanushka Udayanga & Niloofar Vaghefi &
Grit Walther & Mateusz Wilk & Marta Wrzosek & Jian-Chu Xu & JiYe Yan & Nan Zhou
Received: 6 June 2014 / Accepted: 16 July 2014 / Published online: 17 September 2014
# The Author(s) 2014. This article is published with open access at Springerlink.com
Abstract Many fungi are pathogenic on plants and cause
significant damage in agriculture and forestry. They are
also part of the natural ecosystem and may play a role in
regulating plant numbers/density. Morphological identification and analysis of plant pathogenic fungi, while important, is often hampered by the scarcity of discriminatory taxonomic characters and the endophytic or inconspicuous nature of these fungi. Molecular (DNA sequence) data for plant pathogenic fungi have emerged as
key information for diagnostic and classification studies,
although hampered in part by non-standard laboratory
practices and analytical methods. To facilitate current
and future research, this study provides phylogenetic synopses for 25 groups of plant pathogenic fungi in the
Ascomycota, Basidiomycota, Mucormycotina (Fungi),
and Oomycota, using recent molecular data, up-to-date
names, and the latest taxonomic insights. Lineagespecific laboratory protocols together with advice on their
application, as well as general observations, are also provided. We hope to maintain updated backbone trees of
these fungal lineages over time and to publish them jointly as new data emerge. Researchers of plant pathogenic
fungi not covered by the present study are invited to join
this future effort. Bipolaris, Botryosphaeriaceae,
K. D. Hyde (*) : P. E. Mortimer : J.<C. Xu
Key Laboratory for Plant Diversity and Biogeography of East Asia,
Kunming Institute of Botany, Chinese Academy of Sciences,
Kunming 650201, People’s Republic of China
e-mail: kdhyde3@gmail.com
R. H. Nilsson
Department of Biological and Environmental Sciences, University of
Gothenburg, Box 461, 405 30 Göteborg, Sweden
K. D. Hyde : P. E. Mortimer : J.<C. Xu
World Agroforestry Centre, East Asia Node, Heilongtan,
Kunming 650201, People’s Republic of China
K. D. Hyde : H. A. Ariyawansa : A. J. Dissanayake :
I. D. Goonasekara : R. S. Jayawardena : J.<K. Liu :
S. S. N. Maharachchikumbura : D. S. Manamgoda : D. Udayanga
Institute of Excellence in Fungal Research, and School of Science,
Mae Fah Luang University, Chiang Rai 57100, Thailand
K. D. Hyde
Botany and Microbiology Department, College of Science, King
Saud University, Riyadh 1145, Saudi Arabia
K. D. Hyde : S. A. Alias : S. S. N. Maharachchikumbura
Institute of Ocean and Earth Sciences (IOES), C308, Institute of
Postgraduate Studies Building, University of Malaya,
50603 Kuala Lumpur, Malaysia
J. E. Blair
Department of Biology, Franklin & Marshall College,
Lancaster, PA, USA
L. Cai : N. Zhou
State Key Laboratory of Mycology, Institute of Microbiology,
Chinese Academy of Sciences, Beijing 100101
People’s Republic of China
22
Botryosphaeria, Botrytis, Choanephora, Colletotrichum,
Curvularia, Diaporthe, Diplodia, Dothiorella, Fusarium,
Gilbertella, Lasiodiplodia, Mucor, Neofusicoccum,
Pestalotiopsis, Phyllosticta, Phytophthora, Puccinia,
Pyrenophora, Pythium, Rhizopus, Stagonosporopsis,
Ustilago and Verticillium are dealt with in this paper.
Keywords Ascomycota . Basidiomycota . Endophytes .
Mucormycotina . Molecular identification . Oomycota . Plant
pathogens . Protozoa
Contents and contributors (main contributors underlined)
1. Bipolaris–DS Manamgoda, KD Hyde
2. Botryosphaeriaceae–AJ Dissanayake, JK Liu, JY Yan, XH
Li, KD Hyde
3. Botryosphaeria–AJ Dissanayake, JK Liu, JY Yan, XH
Li, KD Hyde
4. Botrytis–RB Terhem, M Hahn, JAL van Kan
5. Choanephora–J Pawłowska, G Walther, M Wilk, M
Gorczak, M Wrzosek
6. Colletotrichum–RS Jayawardena, DS Manamgoda, L Cai,
XH Li, JY Yan, KD Hyde
7. Curvularia–DS Manamgoda, KD Hyde
Fungal Diversity (2014) 67:21–125
8. Diaporthe–AJ Dissanayake, D Udayanga, JY Yan,
XH Li, KD Hyde
9. Diplodia AJ Dissanayake, JK Liu, JY Yan, XH Li, KD
Hyde
10. Dothiorella JK Liu, KD Hyde
11. Fusarium–B Summerell, MH Laurence
12. Gilbertella–J Pawłowska, G Walther, M Wilk, M
Gorczak, M Wrzosek
13. Lasiodiplodia JK Liu, KD Hyde
14. Mucor–J Pawłowska, G Walther, M Wilk, M Gorczak, M
Wrzosek
15. Neofusicoccum AJ Dissanayake, JK Liu, JY Yan, XH Li,
KD Hyde
16. Pestalotiopsis–SSN Maharachchikumbura SA Alias KD
Hyde
17. Phyllosticta–N Zhou, L Cai
18. Phytophthora–F Martin, JE Blair
19. Puccinia–AR McTaggart, RG Shivas
20. Pyrenophora–HA Ariyawansa, KD Hyde
21. Pythium–CFJ Spies, TL Rintoul, AWAM de Cock, SL
Glockling, CA Lévesque
22. Rhizopus–M Gorczak, G Walther, J Pawłowska, M
Wilk, M Wrzosek
23. Stagonosporopsis–N Vaghefi, PWJ Taylor
24. Ustilago–AR McTaggart, RG Shivas
25. Verticillium–PWJ Taylor, PVR Nair
A. W. A. M. de Cock
CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8,
3584CT Utrecht, The Netherlands
F. N. Martin
United States Department of Agriculture, Agriculture Research
Service, Salinas, CA, USA
A. J. Dissanayake : R. S. Jayawardena : X. Li : J. Yan
Beijing Academy of Agriculture and Forestry Sciences, Institute of
Plant and Environment Protection, No. 9 of
Shuguanghuayuanzhonglu, Haidian District, Beijing 100097,
People’s Republic of China
E. H. C. McKenzie
Landcare Research, Private Bag, 92170 Auckland, New Zealand
S. L. Glockling
135 Brodrick Road, Eastbourne BN22 9RA, East Sussex, UK
M. Gorczak : J. Pawłowska : M. Wrzosek
Department of Plant Systematics and Geography, Faculty of Biology,
University of Warsaw, Al. Ujazdowskie 4, 00-478, Warsaw, Poland
M. Hahn
Department of Biology, TU Kaiserslautern,
Erwin-Schrödinger-Straße, 67663 Kaiserslautern, Germany
J. A. L. van Kan : R. B. Terhem
Laboratory of Phytopathology, Wageningen University,
Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
C. A. Lévesque : T. L. Rintoul : C. F. J. Spies
Agriculture and Agri-Food Canada, Central Experimental Farm,
Ottawa, ON, Canada
M. H. Laurence : B. A. Summerell
Royal Botanic Gardens and Domain Trust, Mrs Macquaries Rd,
Sydney, New South Wales 2000, Australia
P. V. R. Nair : P. W. J. Taylor : N. Vaghefi
Faculty of Veterinary and Agricultural Sciences, The University of
Melbourne, Parkville, Victoria 3010, Australia
A. R. McTaggart : R. G. Shivas
Department of Agriculture, Fisheries and Forestry, Ecosciences
Precinct, Dutton Park, Queensland 4102, Australia
R. B. Terhem
Department of Forest Management, Faculty of Forestry, Universiti
Putra Malaysia, 43400 Serdang, Malaysia
G. Walther
Leibniz-Institute for Natural Product Research and Infection
Biology–Hans-Knöll-Institute, Jena Microbial Resource Collection,
Jena, Germany
G. Walther
Institute of Microbiology, Department of Microbiology and
Molecular Biology, University of Jena, Jena, Germany
M. Wilk
Inter-Faculty Interdisciplinary Doctoral Studies in Natural
Sciences and Mathematics, University of Warsaw, Warsaw,
Poland
Fungal Diversity (2014) 67:21–125
Introduction
Fungi form a large and heterogeneous eukaryotic kingdom
with an estimated 1.5 million extant species. While all fungi
are heterotrophic, a wide range of nutritional strategies is
known in the kingdom. Most of the ca. 100,000 described
species of fungi are associated with plants through interactions
including symbiosis, endophytism, saprotrophy and parasitism (Stajich et al. 2009; Delaye et al. 2013; Persoh 2013;
Hyde et al. 2013b). As plant parasites, fungi can cause significant economic loss with far-reaching social implications and
consequences in agriculture, forestry and natural ecosystems
(Fisher et al. 2012). They are also part of the natural ecosystem
and play an important role in regulation of species (Hantsch
et al. 2014).
The study of plant pathogenic fungi–their systematics,
biology, and biological control–has a long and rich history
(Udayanga et al. 2011; Maharachchikumbura et al. 2011;
Manamgoda et al. 2011). The inconspicuous nature of most
fungi makes their study difficult. For example, there are
typically few discriminatory morphological characters, which
often makes precise field- or laboratory-based identification
problematic. Morphological characters that vary with the
choice of host or environmental conditions form an additional,
serious concern. Many species are difficult or impossible to
keep alive in culture, which excludes them from physiological
and often molecular tests that are available. The formation of
sexual fruiting bodies is rarely observed in many plant pathogenic fungi, which has hampered their integration in the
fungal tree of life, resulting in the proliferation of polyphyletic
asexual genera. The biology of most plant pathogenic fungi
remains poorly understood.
The last 25 years have witnessed the emergence of molecular data (DNA sequences) as a source of high fidelity information that has revolutionised mycology (Nilsson et al. 2014).
DNA sequences offer a means by which to examine and
compare fungi, independent of morphological plasticity, cultivability, and host-pathogen interactions. Since integration of
molecular data in the study of plant pathogenic fungi in the
early 1990s, there has been a much deeper understanding of
the ecology, distribution, and systematics of plant pathogenic
fungi (Bridge et al. 2005; Wingfield et al. 2012; Udayanga
et al. 2013; Manamgoda et al. 2013). The use of molecular
data in diagnostics and systematic studies is not without
pitfalls and shortcomings that researchers must consider
(Kang et al. 2010; Ko et al. 2011; Hyde et al. 2013a).
Synonyms, homonyms, asexual-sexual relationships, ambiguous and misidentified specimens are rife in the plant pathology literature and public databases of DNA sequences, which
posses an enormous challenge for the unwary. Equally challenging is the large number of unidentified and seemingly
unidentifiable fungi and fungal sequences isolated from plants
(Kõljalg et al. 2013; Unterseher et al. 2013). Certain plant
23
pathogenic fungi require specialized extraction and PCR
primers/protocols in order to amplify their DNA.
Furthermore, the same genetic markers that give unparalleled
phylogenetic resolution in some fungi may give none whatsoever in others. Many plant pathology studies focus on single
species of fungi, and recent revisions or synopses at the
generic or higher levels are lacking for the majority of plant
pathogenic fungi.
The present study seeks to facilitate present and future
studies of plant pathogenic fungi by providing phylogenetic
backbone trees for as many groups of fungi as our expertise
allowed. Our ambition is to synthesize all recent molecular
data, recommendations on correct names, type material, geo/
ecological observations, literature, and lineage-specific laboratory advice into a comprehensive, uniform molecular treatise for some of the largest and most widely encountered
lineages of plant pathogenic fungi.
Material and methods
The phylogenetic analyses were performed based on up to
date ex-type, ex-epitype or otherwise authentic sequence data
available in GenBank as a concerted effort of the multiple
contributors listed in authors section. By authentic sequence
data we refer to those sequences used for names that are
considered by the current working groups with the support
of reliable publications in each genus as representative for
each species. Sequences for the genes and genetic markers
recommended for each genus were selected based on the
current publications and have commonly been used for each
of the genera (Table 1). The single gene sequence alignments
were initially aligned with Clustal X and improved in
MAFFTv. 7.017 (Katoh et al. 2002). Individual alignments
were then concatenated and used to construct the backbone
trees of each pathogenic genus listed. The phylogenetic analyses were performed for maximum parsimony in PAUP v.
4.0b10 (Swofford 2002), maximum likelihood in RAxML
7.4.2 Black Box or RAxMl GUI (Stamatakis 2006;
Stamatakis et al. 2008), PhyML 3.0 (Guindon et al. 2010) or
Bayesian inference in MrBayes v. 3.1.2 (Huelsenbeck and
Ronquist 2001) as specified in the legend of each phylogenetic tree. The trees used to represent each genus were analyzed
by multiple contributors based on the selection of genes in
given publications under each description.
Backbone tree for important phytopathogens
Condensed synopses are provided for 25 important plant
pathogenic group or genera. Each synopsis includes notes on
background, species identifications and numbers, molecular
phylogeny, recommended genetic markers, tables of species
24
Table 1 Gene regions and primers
Genus
Gene regions
ITS5
GPD1
ITS5
LROR
NS1
728F
BT2A
ITS4
GPD2
ITS4
LR5
NS4
986R
BT2B
White et al. 1990
Berbee et al. 1999
White et al. (1990)
Vilgalys and Hester (1990)
White et al. (1990)
Carbone and Kohn (1999)
Glass and Donaldson (1995)
ITS
LSU
SSU
TEF
β- tubulin
RPB2
HSP60
GPDH
NEP1
NEP2
ITS
ITS
GPDH
CHS-1
HIS3
ACT
β- tubulin
ApMat
ITS
ITS5
LROR
NS1
728F
BT2A
RPB2for+
HSP60for+
G3PDHfor+
NEP1(−207)for, NEP1for
NEP2(−200)for, NEP2forD, NEP2forE, NEP2forF
V9G
ITS1-F
GDF
CHS-79F
CYLH3F
ACT-512F
T1
AM-F
ITS5
ITS4
LR5
NS4
986R
BT2B
RPB2rev+
HSP60rev+
G3PDHrev+
NEP1revA, NEP1revB, NEP1(+1124)rev
NEP2(+1124)rev, NEP2revD, NEP2revE
LR3
ITS4
GDR
CHS-345R
CYLH3R
ACT783R
T2
AM-R
ITS4
White et al. (1990)
Vilgalys and Hester (1990)
White et al. (1990)
Carbone and Kohn (1999)
Glass and Donaldson (1995)
Staats et al. (2005)
Staats et al. (2005)
Staats et al. (2005)
Staats et al. (2007a, b)
Staats et al. (2007a, b)
de Hoog and Gerrits Van den Ende (1998)
Gardes and Bruns (1993)
Templeton et al. 1992
Carbone and Kohn (1999)
Crous et al. 2004
Carbone and Kohn (1999)
O’Donnell and Cigelnik 1997
Silva et al. (2012)
White et al. 1990
Choanephora
Colletotrichum
Curvularia
Diaporthe
GPDH
GPD1
GPD2
Berbee et al. 1999
ITS
TEF
β- tubulin
CAL
HIS
ITS
ITS5
728F
BT2A
228F
CYLH3F
ITS5
ITS4
986R
BT2B
737R
CYLH3R
ITS4
White et al. (1990)
Carbone and Kohn (1999)
Glass and Donaldson (1995)
Carbone and Kohn (1999)
Crous et al. 2004
White et al. (1990)
Diplodia
Fungal Diversity (2014) 67:21–125
Reverse
ITS
GPDH
Botryosphaeriaceae ITS
LSU
SSU
TEF
β- tubulin
Botrytis
Reference
Forward
Bipolaris
Botryosphaeria
Primers
Genus
Dothiorella
Fusarium
Gilbertella
Lasiodiplodia
Mucor
Neofusicoccum
Pestalotiopsis
Phyllosticta
Phytophthora
Puccinia
Gene regions
Primers
Reference
Forward
Reverse
TEF
β- tubulin
ITS
TEF
RPB1
RPB2
ITS
ITS
TEF
β- tubulin
LSU
728F
BT2A
ITS5
728F
5F2 and 7cF
Fa and F5
V9G:
ITS5
728F
BT2A
NL1
986R
BT2B
ITS4
986R
7cR and 11aR
G2R and F7
LR3
ITS4
986R
BT2B
1492R
ITS
LSU
ITS5
LROR
ITS4
LR5
SSU
TEF
β- tubulin
ITS
TEF
β-tubulin
NS1
728F
BT2A
ITS5
526F
BT2A
NS4
986R
BT2B
ITS4
1567R
BT2B
ITS
ACT
TEF
GPDH
LSU
β-tubulin
ITS1
ACT512F
EF1–728F
GDF1
LROR-O (LSUFint)
Btub_F1
ITS4
ACT783R
EF1–786R
Gpd2–LM
LR6-O (LSURint)
Btub_R1A
White et al. (1990)
Carbone and Kohn (1999)
Glass and Donaldson (1995)
White et al. 1990
Rehner 2001
Glass and Donaldson 1995; O’Donnell
and Cigelnik 1997
White et al. 1990
Carbone and Kohn 1999
Carbone and Kohn 1999
Myllys et al. 2002; Guerber et al. 2003
Blair et al. (2008)
Blair et al. (2008)
cox2
nad9
rps10
LSU
SSU
ITS
FM35
Nad9-F
Prv9-F
Rust 2INV
NS1
ITS5-u
Phy10b
Nad9-R
Prv9-R
LR6
Rust 18SR
ITS4
Martin et al. (2014)
Blair et al. (2008)
Blair et al. (2008)
Aime (2006), Vilgalys and Hester (1990)
White et al. (1990), Aime (2006)
Pfunder et al. (2001); White et al. (1990)
Carbone and Kohn (1999)
Glass and Donaldson (1995)
White et al. (1990)
Carbone and Kohn (1999)
Reeb et al. 2004
O’Donnell et al. 2010
de Hoog and Gerrits Van den Ende 1998
White et al. (1990)
Carbone and Kohn (1999)
Glass and Donaldson (1995)
O’Donnel (1993)
Vilgalys and Hester 1990
White et al. (1990)
Vilgalys and Hester (1990)
Fungal Diversity (2014) 67:21–125
Table 1 (continued)
25
26
Table 1 (continued)
Genus
Gene regions
Primers
Reference
Forward
Reverse
ITS
LSU
GPDH
5.8S, ITS2, LSU
SSU, ITS1, 5.8S
cox2
ITS5
LROR
GDF
Oom-up5.8S01
NS1
COX2F, FM35, FM82
ITS4
LR5
GDR
Un-lo28S1220
Oom-lo5.8S47
COX2R, FM78_Pyt, FM52, FM83, Oom-cox1-lev-lo
β-tubulin
BtubF1A, Oom-Btub-up-415
Rhizopus
Stagonosporopsis
ITS
ITS
SSU
LSU
CAL
ACT
β-tubulin
V9G
V9G/ITS1
NS1
LROR
CAL-228F
ACT-512F
BT2Fd
Oom-Btub-lo-1401, BT-R2 (5′- CTTGATGTTG
TTNGGRATCCACTC-3′)
LR3
ITS4
NS4
LR7
CAL-737R /CAL2Rd
ACT-783R
BT4R
de Hoog and Gerrits Van den Ende 1998
V9G, de Hoog and Gerrits Van den Ende 1998
White et al. 1990
Rehner and Samuels 1994; Vilgalys and Hester 1990
Carbone and Kohn (1999), Quaedvlieg et al. (2011)
Carbone and Kohn (1999)
Woudenberg et al. (2009)
Ustilago
ITS
LSU
ITS
TEF
ACT
ITS1F
LROR
ITS1-F
VEFf
VActF
ITS4
LR7
ITS4
VEFr
VActR
Gardes and Bruns (1993), White et al. (1990)
Vilgalys and Hester (1990)
Gardes and Bruns (1993), White et al. (1990)
Inderbitzin et al. (2011b)
Inderbitzin et al. (2011b)
GPDH
TS
VGPDf2
VTs3f
VGPDr
VTs3r
Inderbitzin et al. (2011b)
Inderbitzin et al. (2011b)
Pyrenophora
Pythium
Verticillium
White et al. 1990
Vilgalys and Hester (1990)
Templeton et al. 1992
Man in ’t Veld et al. (2002), Bala et al. (2010a)
White et al. (1990), Man in ’t Veld et al. (2002)
Hudspeth et al. (2000), Martin (2000), Martin and
Tooley (2003b), Robideau et al. (2011),
Eggertson (2012)
Bilodeau et al. (2007), Blair et al. (2008), this study
Fungal Diversity (2014) 67:21–125
Fungal Diversity (2014) 67:21–125
and the latest phylogenetic trees. We have not been able to
include all important phytopathogenic genera (e.g. Alternaria,
powdery mildews), but intend to update or add these in future
publications. Interested parties should contact the corresponding author.
Bipolaris
Background
The genus Bipolaris belongs to the family Pleosporaceae
of the Pleosporales in Dothideomycetes (Ascomycota).
Bipolaris was introduced by Shoemaker (1959) and typified with B. maydis. Bipolaris species are pathogens,
saprobes or endophytes mostly associated with grasses
including cultivated cereals. Some species are important
plant pathogens. The Bengal famine in 1943 was caused
by B. oryzae and caused 90 % of crop losses in India as well
as the loss of 1.5 million human lives (Scheffer 1997). In
the 1970s, around 19 million metric tons of wheat were
destroyed in the USA due to southern corn leaf blight
caused by B. maydis. Bipolaris sorokiniana causes southern leaf blotch, seedling blight and crown rot. Bipolaris
sorokiniana was confirmed as the most economically important foliar pathogen in warm areas by the conference
“Wheat for the national warm areas” held in Brazil in 1990.
Bipolaris species have also been recorded from other plant
families such as Alliaceae, Anacardiaceae, Araceae,
Euphorbiaceae, Fabaceae, Malvaceae, Rutaceae and
Zingiberaceae (Manamgoda et al. 2011).
Species identification and numbers
Bipolaris species were formerly described in
Helminthosporium, however, species associated with grasses
were morphologically distinct from H. velutinum, the type
species (Luttrell 1963; Ellis 1971; Alcorn 1988). In several
taxonomic refinements, these graminicolous
Helminthosporium species were segregated into four genera;
Bipolaris, Curvularia, Drechslera and Exserohilum
(Sivanesan 1987). Later Subramanian and Jain (1966) placed
all Bipolaris species in Drechslera, but this transfer was not
accepted by later authors (Sivanesan 1987; Alcorn 1988).
After molecular data became available, Drechslera was
shown to be a phylogenetically different genus from
Bipolaris (Berbee et al. 1999). The sexual state of Bipolaris
is Cochliobolus (Drechsler 1934). Cochliobolus is the older
name but conservation of the name Bipolaris over
Cochliobolus has been proposed to avoid numerous name
changes and Bipolaris is the most common name among plant
pathologists (Manamgoda et al. 2012a; Rossman et al. 2013).
27
Morphology-based classification of Bipolaris species is
challenging as the asexual state has overlapping conidia and
conidiophore dimensions (Sivanesan 1987). A few Bipolaris
species are known to be host-specific, while most of the other
species are generalists (Manamgoda et al. 2011). However,
some of the host-specific species are known only from limited
collections. Therefore, the information on host-specificity
may change with further collections. Interspecific compatibility can be observed between some taxa. For example, successful hybridization leading to ascospore production has
been reported between B. zeicola and B. victoriae (Nelson
1960a, b) as well as between B. maydis and B. oryzae (Alcorn
1988). However, the latter species are definitively distinct
phylogenetic species and also they are commonly recorded
pathogens, causing different symptoms on their respective
hosts. Identification of Bipolaris species using morphological
and biological species concepts is not always correct and it is
essential to use molecular tools in identifying species. Lack of
DNA sequences from type material/ex-type cultures (or other
authentic material) in public sequence databases is a problematic issue regarding the molecular identification of the
Bipolaris species (Nilsson et al. 2014). Currently there are
118 Bipolaris names listed in Index Fungorum (2014), but
nine of them do not belong to this genus based on phylogenetic evidence.
Molecular phylogeny
The first phylogenetic analysis for Bipolaris with its sister
genus Curvularia was carried out by Berbee et al. (1999)
and Goh et al. (1998) using a combined ITS and GPDH
analysis. These studies showed that Bipolaris species
cluster in two clades. Combined ITS, GPDH, EF and LSU
phylogenetic analysis for Bipolaris and Curvularia by
Manamgoda et al. (2012a) showed that Bipolaris and
Curvularia cluster into two major clades. Nine Bipolaris
species clustered with the generic type, Curvularia lunata
Boedijn, while other species of Bipolaris clustered with the
generic type, Bipolaris maydis. Accordingly, the nine
Bipolaris species were moved to Curvularia, and
Bipolaris was maintained as a distinct genus based on the
generic type and those species that clustered with it. In this
section we provide a backbone tree (Table 2, Fig. 1) for
Bipolaris using combined ITS and GPDH sequence data.
Recommended genetic markers
GPDH is the best single genetic marker for the genus
Bipolaris (Manamgoda et al. 2012a). Combined ITS, EF and
GPDH can resolve almost all species of Bipolaris currently
known from sequence data (Manamgoda et al. 2012a).
28
Fungal Diversity (2014) 67:21–125
Table 2 Bipolaris. Details of the isolates used in the phylogenetic tree
Species
Isolate
Host
GenBank accession number
ITS
GPDH
Bipolaris chloridis
B. cynodontis
B. drechsleri
B. drechsleri
B. eleusines
B. luttrellii
B. maydis
B. melinidis
B. microlenae
B. oryzae
B. oryzae
B. peregianensis
B. sorghicola
B. sorokiniana
CBS 242.77*
ICMP 6128*
CBS 136207
CBS 136208
8749C*
14643-1*
C5*
BRIP 12898
CBS 280.91
MFLUCC 100694*
MFLUCC 100716
BRIP 12970
MAFF511378*
ICMP 6233a
Chloris gayana
Cynodon dactylon
Microstegium vimineum
Microstegium vimineum
Eleusine indica
Dactyloctenium aegyptium
Zea mays
Melinis minutiflora
Microlaena stipoides
Oryza sativa
O. sativa
Cynodon dactylon
Sorghum sudanense
Lolium perenne
JN192372
JX256412
KF500530
KF500532
AF081451
AF071350
AF071325
JN601035
JN601032
JX256413
JX256415
JN601034
AF071332
JX256418
JN600961
JX276427
KF500533
KF500535
AF081405
AF081402
AF081380
JN600972
JN600974
JX276428
JX276429
JN600977
AF081387
B. urochloae
B. victoriae
Curvularia lunata
DAOM 171970*
CBS 174.57*
CBS 730.96
Urochloa panicoides
Avena sativa
Unknown
AF071334
JN601027
JX256429
AF081389
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
Fig. 1 Phylogram generated
from parsimony analysis based on
combined ITS and GPDH
sequenced data of Bipolaris.
Bootstrap support values greater
than 50 % are indicated above the
nodes. The ex-type (ex-epitype)
and voucher strains are in bold.
The tree is rooted with Curvularia
lunata
JX276441
TEF
JX266581
JN601017
JX266582
JX266584
JN601022
JN601005
JX266596
Fungal Diversity (2014) 67:21–125
Botryosphaeriaceae
The family Botryosphaeriaceae is classified in the order
Botryosphaeriales of the Dothideomycetes (Ascomycota).
Members of the fungal family Botryosphaeriaceae were described in the 1820’s as species of Sphaeria (Fr.) (Crous et al.
2006; Schoch et al. 2006). There have subsequently been
various treatments of the family. von Arx and Müller (1954)
included 15 genera, but later reduced it to 14 genera (von Arx
and Müller 1975). Barr (1987) included only nine genera,
which are mostly different from those of von Arx and
Müller (1954). Hawksworth et al. (1995) listed five genera.
Lumbsch and Huhndorf (2010) included 11 genera, while
Hyde et al. (2011) and Wijayawardene et al. (2012) listed 16
genera. Liu et al. (2012) included 17 genera in the family
based on molecular data and examination of generic types.
Species of Botryosphaeriaceae range in habit from saprobic to
parasitic or endophytic (Smith et al. 1996; Denman et al.
2000; Phillips et al. 2006; Slippers and Wingfield 2007;
Huang et al. 2008; Pérez et al. 2010; Ghimire et al. 2011;
González and Tello 2011). Members are cosmopolitan in
distribution and occur on a wide range of monocotyledonous,
dicotyledonous and gymnosperm hosts; on woody branches,
herbaceous leaves, stems and culms of grasses; and on twigs
and in the thalli of lichens (Barr 1987; Denman et al. 2000;
Mohali et al. 2007; Lazzizera et al. 2008; Marincowitz et al.
2008).
Species identification and numbers
Currently, more than 2,000 species names are linked to
Botryosphaeriaceae, including sexual and asexual states of
Diplodia, Botryosphaeria, Fusicoccum, Dothiorella,
Lasiodiplodia and Sphaeropsis. Identification to genus and
species is presently undergoing major revision and it is likely
that many older names will not be used in modern treatments.
Identification of species in Botryosphaeria, Diplodia,
Dothiorella, Lasiodiplodia and Neofusicoccum are dealt separately under this family entry.
Molecular phylogeny
Recent advances in DNA-based molecular techniques have
begun to provide efficient tools to characterize the presence
and identity of species of the Botryosphaeriaceae (Slippers
and Wingfield 2007). Studies applying these tools are revealing significantly greater diversity on some hosts than was
previously realized. Recent studies on the taxonomy of
Botryosphaeria have employed molecular methods to reveal
phylogenetic relationships among species (Jacobs and Rehner
1998) and to resolve species complexes (Denman et al. 2003;
Alves et al. 2004; Phillips et al. 2005). Two major clades
corresponding to species with Diplodia and Fusicoccum
29
asexual morphs were revealed based on ITS phylogenies
(Jacobs and Rehner 1998; Denman et al. 2003). Later studies,
including additional species and a larger suite of genetic
markers, supported this grouping (Zhou and Stanosz 2001;
Alves et al. 2004; Slippers et al. 2004d). Lasiodiplodia has
been treated as a distinct genus from Diplodia by many
authors due to its distinct phylogeny (usually ITS or EF-1α)
and morphology (striated or smooth conidia and presence or
absence of pseudoparaphyses). Pavlic et al. (2004) employed
morphological and phylogenetic data to separate
Lasiodiplodia from Diplodia. The value of the introndominated sequences of the ITS, β-tubulin and TEF markers
(on which most previous studies were based) to infer phylogenetic relationships across the diversity of the genus is,
however, unclear. The more conserved mtSSU data have, for
example, suggested that B. dothidea and B. corticis (Demaree
and Wilcox) are unrelated to Fusicoccum (Zhou and Stanosz
2001) even though they are typically assigned to this genus.
Most taxonomic studies on Botryosphaeriaceae using molecular data have employed ITS rDNA phylogenies, but this
single marker can underestimate the species diversity among
closely related or cryptic species. Multiple gene sequence
concordance phylogenies have therefore been applied to identify cryptic or previously overlooked species of
Botryosphaeriaceae (Slippers et al. 2004a, b, c; Burgess
et al. 2005; Phillips et al. 2005). As the elongation fctor 1alpha (TEF) gene is consistently more variable than the ITS
rDNA region in these fungi, most commonly data from TEF
have been combined with ITS sequence data. Unfortunately
no single genetic region is sufficient to distinguish all species,
because not all single nucleotide polymorphisms (SNPs) represent restriction sites, especially between some closely related species.
The Botryosphaeriaceae has been separated into numerous
distinct genera (Crous et al. 2006; Liu et al. 2012). A natural
classification is needed for a more stable and accurate taxonomic framework and this will strongly influence the understanding of the ecology of the Botryosphaeriaceae. In this part
we provide a tree to the genera of Botryosphaeriaceae (Table
3, Fig. 2) and deal with the important genera Botryosphaeria,
Diplodia, Dothiorella, Lasiodiplodia and Neofusicoccum in
the following parts.
Recommended genetic markers
&
&
LSU, SSU, β-tubulin and ITS–generic level
TEF–species level
LSU has been shown to be suitable for distinguishing
many ascomycetes at the generic level due to its relatively
conserved nature (Crous et al. 2006; Schoch et al. 2006;
Hibbett et al. 2007). The study of Liu et al. (2012) suggested that the combined TEF and β- tubulin gene
30
Fungal Diversity (2014) 67:21–125
Table 3 Botryosphaeriaceae. Details of the isolates used in the phylogenetic tree
Species
Isolate
ITS
β- tubulin
TEF
SSU
LSU
Barriopsis fusca
B. iraniana
Botryobambusa fusicoccum
Botryosphaeria agaves
B. corticis
B. dothidea
B. fusispora
Cophinforma eucalypti
Diplodia corticola
D. cupressi
D. mutila
Dothiorella iberica
D. sarmentorum
D. thailandica
Endomelanconiopsis endophytica
E. microspora
Lasiodiplodia crassispora
CBS 174.26*
IRAN1448C*
MFLUCC 11-0143*
MFLUCC 11-0125*
CBS 119047*
CMW 8000*
MFLUCC 10-0098*
MFLUCC 11-0425*
CBS 112549*
CBS 168.87*
CBS 112553*
CBS 115041*
IMI 63581b*
MFLUCC11-0438*
CBS 120397*
CBS 353.97*
CBS 118741*
EU673330
KF766150
JX646792
JX646791
DQ299245
AY236949
JX646789
JX646800
AY259100
DQ458893
AY259093
AY573202
AY573212
JX646796
KF766164
KF766165
DQ103550
EU673109
KF766127
–
JX646841
EU673107
AY236927
JX646839
JX646848
DQ458853
DQ458861
DQ458850
EU673096
EU673102
JX646844
KF766131
–
EU673133
EU673296
FJ919652
JX646857
JX646856
EU017539
AY236898
JX646854
JX646865
AY573227
DQ458878
AY573219
AY573222
AY573235
JX646861
EU683637
EU683636
EU673303
EU673182
KF766231
JX646826
JX646825
EU673175
EU673173
JX646823
JX646833
EU673206
EU673209
EU673213
EU673155
EU673158
JX646829
KF766249
KF766250
EU673190
DQ377857
KF766318
JX646809
JX646808
EU673244
AY928047
JX646806
JX646817
AY928051
EU673263
AY928049
AY928053
AY928052
JX646813
EU683629
KF766330
DQ377901
L. gonubiensis
L. parva
L. pseudotheobromae
L. theobromae
Macrophomina phaseolina
Neodeightonia palmicola
N. phoenicum
N. subglobosa
Neofusicoccum luteum
N. mangiferae
N. parvum
Neoscytalidium dimidiatum
CBS 115812*
CBS 494.78*
CBS 116459*
CBS 164.96*
CBS 227.33*
MFLUCC 10-0822*
CBS 122528*
MFLUCC11-0163*
CBS 110299*
CBS 118532*
CMW 9081*
DQ458892
EF622084
EF622077
AY640255
KF766195
HQ199221
EU673340
JX646794
AY259091
AY615186
AY236943
DQ458860
EU673114
EU673111
EU673110
–
–
EU673116
JX646842
DQ458848
AY615173
AY236917
DQ458877
EF622064
EF622057
AY640258
KF766422
–
EU673309
JX646859
AY573217
DQ093220
AY236888
EU673193
EU673201
EU673199
EU673196
KF766281
HQ199223
EU673205
–
EU673148
EU673154
EU673151
DQ377902
EU673258
EU673256
EU673253
KF766364
HQ199222
EU673261
JX646811
AY928043
DQ377921
AY928045
N. hyalinum
N. novaehollandiae
Phaeobotryon mamane
Pseudofusicoccum adansoniae
P. ardesiacum
P. kimberleyense
P. stromaticum
IP127881
CBS145.78*
WAC 12691*
CPC 12440*
WAC 12689*
CMW 26159*
CMW 26156*
CMW13434*
AF258603
KF531816
EF585543
EU673332
EF585534
KF766221
KF766222
KF766223
FM211167
KF531796
–
EU673121
–
–
–
EU673094
EU144063
KF531795
EF585574
EU673298
EF585567
EU144075
EU144072
KF766437
AF258603
KF531815
–
EU673184
–
KF766307
KF766308
KF766309
DQ377925
DQ377922
EF585548
EU673248
EF585554
KF766387
KF766388
KF766389
Spencermartinsia viticola
Sphaeropsis citrigena
S. eucalypticola
S. porosa
S. visci
Tiarosporella graminis var. karoo
T. tritici
T. urbis-rosarum
Melanops tulasnei
CBS 117009*
ICMP 16812*
CBS 133993*
CBS 110496*
CBS 186.97*
CBS 118718
CBS 118719*
CMW 36479*
CBS 116805*
AY905554
EU673328
JX646802
AY343379
EU673325
KF531828
KF531830
JQ239408
FJ824769
EU673104
EU673140
JX646850
EU673130
EU673128
KF531808
KF531810
JQ239382
–
AY905559
EU673294
JX646867
AY343340
EU673293
KF531807
KF531809
JQ239395
KF766423
EU673165
EU673180
JX646835
EU673179
EU673178
KF531827
KF531829
–
KF766474
DQ377873
EU673246
JX646819
DQ377894
DQ377868
DQ377939
DQ377941
JQ239421
KF766365
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
Fungal Diversity (2014) 67:21–125
31
Fig. 2 Phylogram generated
from parsimony analysis based on
combined SSU, LSU, TEF, βtubulin and ITS sequence data of
Botryosphaeriaceae. Parsimony
bootstrap support values greater
than 50 % and Bayesian posterior
probabilities greater than 0.5 are
indicated above the nodes. The
ex-type (ex-epitype) and voucher
strains are in bold. The scale bar
indicates ten changes. The tree is
rooted with Melanops tulasnei
CBS 116805
analysis is best for delimiting genera of
Botryosphaeriaceae. It has also been recommended that
the RPB2 gene should be considered in similar combined
analyses of genus and species levels of
Botryosphaeriaceae (Pavlic et al. 2009a, b).
Botryosphaeria
Background
The genus Botryosphaeria (Botryosphaeriaceae) was introduced by Cesati and de Notaris (1863), amended by Saccardo
(1877), and is based on the type species Botryosphaeria
dothidea (Barr 1972; Slippers et al. 2004c). Species in
Botryosphaeria were described largely on the basis of the
morphology of their ascomata and host associations, and this
has led to a proliferation of names. von Arx and Müller (1954)
examined 183 taxa of Botryosphaeriales and reduced them to
11 species, with extensive synonymies under B. dothidea and
B. quercuum, together with nine new combinations. In later
studies these synonymies were not always accepted
(Shoemaker 1964; Sivanesan 1984; Slippers et al. 2004a).
Slippers et al. (2004b) epitypified the type species
Botryosphaeria dothidea based on morphology and phylogeny
(combined ITS, TEF and β-tubulin analysis) and this enabled a
better resolution of species. Species of Botryosphaeria occur on
a wide range of monocotyledonous, dicotyledonous and gymnosperm hosts, on woody branches, herbaceous leaves and
grasses (Barr 1987). The life styles may be saprobic, parasitic
and endophytic (Smith et al. 1996; Denman et al. 2000), and
species can cause die-back and canker diseases of numerous
woody hosts (von Arx 1987). Species in the genus
Botryosphaeria have hyaline to dark ascospores, multiloculate
ascomata, and a wide range of asexual morphs that typically
lack a mucoid sheath and apical appendage.
Species identification and numbers
More than 18 asexual genera have been associated with
Botryosphaeria. A phylogenetic study based on part of the
28S ribosomal DNA gene together with morphological characters revealed that Botryosphaeria comprises several distinct
lineages, each comprising individual genera (Crous et al.
2006). In that study, only B. dothidea and B. corticis were
retained in Botryosphaeria, while most species were reduced
32
Fungal Diversity (2014) 67:21–125
to synonymy under Diplodia (conidia mostly ovoid,
pigmented, thick-walled), or Fusicoccum (conidia mostly
fusoid, hyaline, thin-walled). Studies have also linked
Botryosphaeria to species with pigmented, septate ascospores
and Dothiorella asexual morphs, or Fusicoccum asexual
morphs with Dichomera synanamorphs. More recently
B. agaves (which has been epitypified), B. fusispora (Liu
et al. 2012), and B. schariffi (Abdollahzadeh et al. 2013) were
described in the genus Botryosphaeria, while B. fabicerciana
was illustrated from Eucalyptus sp. in southern China (Chen
et al. 2011). Phylogenetically, B. fabicerciana is closely related to B. corticis, B. dothidea, B schariffi and B. ramosa. The
present phylogenetic analysis was performed based on up to
date holotype or ex-epitype sequence data available in
GenBank (Table 4).
Molecular phylogeny
Recent studies on the taxonomy of Botryosphaeria have
employed molecular methods to reveal phylogenetic relationships among species (Jacobs and Rehner 1998) and to resolve
species complexes (Smith and Stanosz 2001; Phillips et al.
2002, 2005; Denman et al. 2003; Alves et al. 2004; Slippers
et al. 2004c). Studies including additional species and a larger
suite of DNA-based markers supported this grouping (Zhou
and Stanosz 2001; Alves et al. 2004; Slippers et al. 2004c).
Based on combined ITS and TEF sequence data seven species
are currently recognised in Botryosphaeria (Phillips et al.
2013). The phylogenetic tree constructed with holotype or
ex-epitype sequences is presented in Fig. 3.
Botrytis
Background
Recommended genetic markers
&
&
Fig. 3 Phylogram generated from parsimony analysis based on combined ITS, TEF, β- tubulin, LSU and SSU sequenced data of
Botryosphaeria. Parsimony bootstrap support values greater than 50 %
and Bayesian posterior probabilities greater than 0.5 are indicated near the
nodes. The ex-type (ex-epitype) and voucher strains are in bold. The tree
is rooted with Macrophomina phaseolina CBS 227.33
Erected by Micheli in 1729, the genus Botrytis is one of the
first described genera of fungi. Persoon (1801) designated five
LSU, SSU and ITS–generic level
β-tubulin and TEF–species level
Table 4 Botryosphaeria. Details of the ex-type and voucher isolates used in the phylogenetic tree
Species
Botryosphaeria agaves
B. corticis
B. dothidea
B. fabicerciana
B. fusispora
B. ramose
B. scharifii
Macrophomina phaseolina
Isolate
CBS 133992*
CBS 119047*
CBS 115476*
CBS 127193*
MFLUCC 10-0098*
CBS 122069*
CBS 124703*
CBS 227.33*
Type strains and voucher stains are bolded
GenBank accession numbers
SSU
ITS
LSU
TEF
β-tubulin
JX646825
EU673175
EU673173
N/A
JX646823
N/A
N/A
KF531823
JX646825
DQ299245
AY236949
HQ332197
JX646789
EU144055
JQ772020
KF531825
JX646808
EU673244
AY928047
N/A
JX646806
N/A
N/A
DQ377906
JX646856
EU017539
AY236898
HQ332213
JX646854
EU144070
JQ772057
KF531804
JX646841
EU673107
AY236927
N/A
JX646839
N/A
N/A
KF531806
Fungal Diversity (2014) 67:21–125
species under the binomial system of Linnaeus, validated the
genus, and included one of Micheli’s species, B. cinerea, so
named by Von Haller (1771). The genus name refers to the
structure of the macroconidia, which rise and form clusters
with the shape of grape bunches: ‘botryose’. Botrytis is the
asexual stage of Botryotinia. The Botrytis community has in
its recent meeting (Italy, 23–28 June 2013) unanimously
recommended the exclusive use of the asexual name Botrytis
over Botryotinia, the name of the sexual stage, since Botrytis
is historically the oldest name and it is commonly used by
plant pathologists, breeders and growers. In line with this
recommendation, a list of generic names of fungi for protection under the International Code of Nomenclature has included this genus under the name Botrytis and not Botryotinia
(Kirk et al. 2013). We therefore follow this recommendation
in this paper and use Botrytis. Species of the genus Botrytis
infect >250 host species, including major greenhouse and field
crops such as tomato, grape, strawberry, onion and ornamentals such as rose, lily, and tulip (Staats et al. 2005). Most
Botrytis species are necrotrophic pathogens that (are able to)
kill the host tissue during infection. Interestingly, an endophytic species (B. deweyae) has recently been discovered,
which under appropriate conditions can cause ‘spring sickness’ in ornamental Hemerocallis (daylily) hybrids (GrantDownton et al. 2014). Botrytis cinerea is the best-studied
species in the genus (Williamson et al. 2007) and was recently
elected as the second most important plant pathogenic fungal
species (Dean et al. 2012).
In the asexual state, Botrytis produces different tissues
including mycelia, macroconidia, microconidia, and sclerotia.
Macroconidia are ellipsoidal to obovoid shape and rise from
conidiophore branches into botryose clusters. They are pale
brown and range in size from 9–23×8–15 μm. Microconidia
are more sphaerical and much smaller than macroconidia
(about 1 μm), and function as male spermatia (Groves and
Loveland 1953; Faretra et al. 1988; Beever and Parkes 1993;
Fukumori et al. 2004). Sclerotia are irregularly hemispherical,
convex and normally have a concave surface. They are usually
black, with sizes ranging between 1 and 10 mm (Whetzel
1945), and function as survival structures during winter and
serve as maternal parent in the production of apothecia.
The sexual state forms fruiting bodies called apothecia: a
cup- or open saucer-shaped ascoma at the top of a stalk, that
acts as a platform to discharge ascospores from the ascus.
Botrytis apothecia vary in size depending on the species,
between 1 and 25 mm high and 1–6 mm diam. (Hennebert
and Groves 1963; Bergquist and Lorbeer 1972). Apothecia are
brown and become darker when mature (Hennebert and
Groves 1963; Bergquist and Lorbeer 1972; Faretra and
Antonacci 1987). Generally multiple apothecia can develop
on a single sclerotium. Mature apothecia normally can be
observed 2 months after fertilization (Faretra et al. 1988;
Hennebert and Groves 1963; Van Der Vlugt-Bergmans et al.
33
1993). In the genus Botrytis, both homothallic and heterothallic
reproductive lifestyles have been reported. Homothallic (selffertile) species can undergo sexual reproduction and form
apothecia and generate progeny in the absence of a mating
partner, e.g. B. porri and B. globosa (Buchwald 1953; Elliott
1964). By contrast, heterothallic (self-sterile, self-incompatible) species require isolates with compatible mating types in
order to complete the sexual cycle. B. cinerea is considered a
typical heterothallic fungus (Elliott 1964; Faretra et al. 1988).
Mating is controlled by the mating type locus with two alleles,
MAT1-1 and MAT1-2 (Faretra et al. 1988), each carrying two
distinct, non-homologous genes (Amselem et al. 2011).
Species identification and numbers
Approximately half of the Botrytis species are named after the
host that they are derived from (listed in Table 5). One hybrid
species, B. allii which originated from hybridization between
B. byssoidea and B. aclada (Nielsen and Yohalem 2001;
Yohalem et al. 2003) could not be placed in the phylogeny
(Staats et al. 2005) and was omitted from Table 3. The genus
Botrytis predominantly comprises narrow host range pathogens that infect a single, or a few (often related) host species.
There are two exceptions to this rule: B. cinerea can infect
m or e t h a n 2 0 0 h o s t s pe c i e s ( J a r v i s 1 9 7 7 ) , a n d
B. pseudocinerea has been isolated from several unrelated
host species (Fournier et al. 2005; Leroch et al. 2013).
The taxonomic classification and nomenclature in Botrytis
have rarely been comprehensively reviewed. Morphological
descriptions of most species have been published in the 19th
and first half of the 20th century in separate papers, many of
which are not easily accessible. The most recent taxonomic
compilation of the genus is in a monograph by Jarvis (1977),
which also lists ~25 excluded or doubtful species, and briefly
describes the historical debates between mycologists and the
confusion in classification of Botrytis species. Morphological
features were often inadequate to distinguish species and the
variability among isolates of the same species further complicated the situation (Jarvis 1977). Recent studies have identified B. cinerea and B. pseudocinerea as species that are very
similar in morphology, yet recognized as distinct taxa that
diverged several million years ago (Walker et al. 2011).
Even more puzzling, the morphology and narrow host range
of B. fabae separate this species clearly from B. cinerea and
B. pseudocinerea, but phylogenetic studies revealed it to be a
sister species of B. cinerea (see below). These examples
illustrate the limitations of morphological characters for
Botrytis species identification.
Molecular phylogeny
Holst-Jensen et al. (1998) were the first to use nuclear ribosomal ITS sequences to infer a phylogeny of the family
34
Fungal Diversity (2014) 67:21–125
Table 5 Botrytis. Details of the isolates used in the phylogenetic tree
Species
Isolate
Host
GenBank accession numbers
RPB2
HSP60
G3DPDH
NEP1
NEP2
Botrytis aclada
B. byssoidea
B. calthae
B. cinerea
B. caroliniana
B. convoluta
B. croci
B. deweyae
B. elliptica
B. fabae
B. ficariarum
B. fabiopsis
B. galanthina
B. gladiolorum
MUCL8415
MUCL94
MUCL1089
MUCL87
CB15*
MUCL11595
MUCL436
CBS134649*
BE9714
MUCL98
MUCL376
BC-2*
MUCL435
MUCL3865
Allium spp.
Allium spp.
Caltha palustris
>200 species
Rubus fruticosus
Iris spp.
Crocus spp.
Hemerocallis spp.
Lilium spp.
Vicia spp.
Ficaria verna
Vicia faba
Galanthus spp.
Gladiolus spp.
AJ745664
AJ745670
AJ745672
AJ745676
JF811590
AJ745680
AJ745681
HG799518
AJ745684
AJ745686
AJ745688
EU514473
AJ745689
AJ745692
AJ716050
AJ716059
AJ716061
AJ716065
JF811587
AJ716069
AJ716070
HG799519
AJ716073
AJ716075
AJ716077
EU514482
AJ716079
AJ716081
AJ704992
AJ704998
AJ705000
AJ705004
JF811584
AJ705008
AJ705009
HG799521
AJ705012
AJ705014
AJ705016
EU519211
AJ705018
AJ705020
AM087059
AM087045
AM087031a
DQ211824a
JF811593
AM087035
AM087047
HG799527
AM087049
DQ211829
AM087056
NA
AM087057
AM087041
AM087087
AM087079
AM087088a
DQ211825a
NA
AM087062
AM087065
HG799520
AM087080
DQ211831
AM087085a
NA
AM087067a
AM087072a
B. globosa
B. hyacinthi
B. narcissicola
B. paeoniae
B. pelargonii
B. polyblastis
B. porri
B. pseudocinerea
B. ranunculi
B. sinoallii
B. sphaerosperma
B. squamosa
B. tulipae
Monilinia fructigena
Sclerotinia sclerotiorum
MUCL444
MUCL442
MUCL2120
MUCL16084
CBS 497.50
CBS287.38
MUCL3234
VD110
CBS178.63
HMAS250008
MUCL21481
MUCL1107
BT9830
9201
484
Allium ursinum
Hyacinthus spp.
Narcissus spp.
Paeonia spp.
Pelargonium spp.
Narcissus spp.
Allium spp.
Vitis vinifera
Ranunculus spp.
Allium spp.
Allium triquetrum
Allium cepa
Tulipa spp.
Stone fruit and pome fruit
>400 species
AJ745693
AJ745696
AJ745697
AJ745700
AJ745662
AJ745702
AJ745704
Unpublished
AJ745706
EU514479
AJ745708
AJ745710
AJ745713
AJ745715
AJ745716
AJ716083
AJ716085
AJ716087
AJ716089
AJ716046
AJ716091
AJ716093
Unpublished
AJ716095
EU514488
AJ716096
AJ716098
AJ716102
AJ716047
AJ716048
AJ705022
AJ705024
AJ705026
AJ705028
AJ704990
AJ705030
AJ705032
Unpublished
AJ705034
EU519217
AJ705035
AJ705037
AJ705041
AJ705043
AJ705044
AM087044a
AM087048
AM087046
AM087033
AM087030
AM087039
AM087060
NA
AM087054
NA
AM087042
AM087052
AM087037
NA
NA
AM087071
AM087066a
AM087078
AM087064a
DQ211834a
AM087074
AM087063
NA
AM087086
NA
AM087068
AM087084
AM087077
NA
NA
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
a
sequences obtained from a different isolate than the one listed in the table.
Sclerotiniaceae, including several members of the genus
Botrytis. The relationships among many Botrytis species
could not be resolved because of the limited number of informative characters, however the study permitted the conclusion
that Botryotinia asexual morphs along with Botrytis sexual
morphs constitute a monophyletic lineage (Holst-Jensen et al.
1998). The phylogeny of the Sclerotiniaceae was further
refined by Andrew et al. (2012) using three protein-coding
genes: calmodulin, glyceraldehyde 3-phosphate dehydrogenase G3PDH and heat shock protein HSP60.
Staats et al. (2005) performed a comprehensive phylogenetic analysis of the genus Botrytis, at that time comprising 22
recognized species and one hybrid. Using three protein-coding
genes (G3PDH, HSP60 and the DNA-dependent RNA polymerase subunit II gene RPB2), they corroborated the
morphological and host plant-based classification of Botrytis
spp. and divided the genus into two (rather widely separated)
clades. Clade I contained species that only infect eudicot
plants, while Clade II contained species that can infect either
eudicotyledonous or monocotyledonous plants. The use of the
same three genes facilitated the discovery of Botrytis sinoallii,
a new species infecting Allium spp., and its distinction from
other Botrytis spp. infecting the same hosts (Zhang et al.
2010b); B. fabiopsis, a new species infecting broad bean, very
distant from B. fabae (Zhang et al. 2010a); and B. caroliniana,
a new species infecting blackberry (Li et al. 2012).
Two genes, encoding phytotoxic proteins NEP1 and NEP2,
were shown to provide higher resolution in distinguishing
species in the genus Botrytis because they seem to be the
subject of higher evolutionary rates than the housekeeping
Fungal Diversity (2014) 67:21–125
genes G3PDH, HSP60 and RPB2 (Staats et al. 2007a). The
NEP1 and NEP2 genes were shown to have evolved under
positive selection which suggested a role of these proteins in
the infection process (Staats et al. 2007a). One might therefore
infer that such genes cannot serve as neutral phylogenetic
markers. Functional analysis in B. cinerea and B. elliptica
using targeted knockout mutants failed to reveal a role of
NEP genes in virulence of these two species (Staats et al.
2007b; Cuesta Arenas et al. 2010), which would lend support
to considering these genes as neutral markers and adequate
tools in phylogeny.
The studies by Staats et al. (2005) revealed incongruence
between the phylogenies of Botrytis spp. and their hosts.
Species infecting the same host clustered in different (sub)
clades, e.g. B. aclada, B. squamosa, B. porri, B. byssoidea
and B. sinoallii all infecting Allium. Conversely, closely related
species can infect very different hosts, e.g. B. elliptica infecting
the monocotyledonous host Lilium and B. ficariarum infecting
the dicotyledonous host Ficaria (Staats et al. 2005). More
recently, similar incongruence has been reported for newly
described species, e.g. B. fabiopsis infecting Vicia faba is very
distant from B. fabae infecting the same host (Zhang et al.
2010a), and B. caroliniana infecting blackberries and strawberries is very distant from B. cinerea (Li et al. 2012).
Recently, Khan et al. (2013) combined data from ITS and
IGS regions with the G3PHD gene, with the aim of improving
Fig. 4 Phylogram generated
from Maximum likelihood
analysis based on combined
sequences of G3PDH, HSP60 and
RPB2 from 28 recognized
Botrytis species. Bootstrap
support values greater than 50 %
are indicated above/below the
nodes. The ex-type (ex-epitype)
and voucher strains are in bold.
The tree is rooted with Monilinia
fructigena and Sclerotinia
sclerotiorum
35
molecular identification of Botrytis species that cause neck rot
disease on onion. ITS and IGS regions were insufficiently
informative to distinguish B. allii and B. byssoidea. The
sequences of ITS and IGS for B. allii and B. byssoidea confirmed that they have a close relationship, but G3PDH sequences of several B. allii isolates were clearly distinct, some
clustering with B. aclada and others clustering with
B. byssoidea (Khan et al. 2013), as might be expected for a
hybrid species.
Sequence analysis of the G3PDH and β-tubulin genes
amplified from herbarium specimens of Botrytis collected
from grey mould-infected apple (deposited in 1932) enabled
O’Gorman et al. (2008) to corroborate the existence of
B. mali, a species that had been published (Ruehle 1931),
but by lack of description was considered doubtful.
Figure 4 shows a maximum likelihood tree of Botrytis spp.,
based on concatenated sequences of parts of the three genes
G3PDH, HSP60 and RPB2 (amplified using primers defined
by Staats et al. (2005). Five species described after publication
of the phylogeny by Staats et al. (2005), i.e. B. caroliniana, B.
deweyae, B. fabiopsis, B. pseudocinerea and B. sinoallii,
clearly cluster within the genus and are genuine Botrytis
species. Botrytis mali could not be included in the tree due
to lack of sequences for the HSP60 and RPB2 genes. Based on
G3PDH and ß-tubulin sequences it would cluster with
B. paeoniae (O’Gorman et al. 2008).
36
The Botrytis cinerea species complex
The Botrytis ‘dicot’ clade I consists of B. cinerea,
B. pelargonii, B. fabae, B. pseudocinerea and B. calthae.
Molecular data do not fully support a separation between
B. pelargonii and B. cinerea (Staats et al. 2005, 2007a;
Plesken et al. 2014), and the existence of B. pelargonii as a
separate species is therefore doubtful. As mentioned above,
B. cinerea and B. pseudocinerea are morphologically very
similar yet phylogenetically more distant from each other than
B. cinerea and B. fabae. All genes tested so far place
B. calthae as most remote to all other clade I species.
Botrytis cinerea not only has a broad host range, but also
shows considerable phenotypic variability in vegetative
growth, conidiation and sclerotium formation (Kerssies et al.
1997; Martinez et al. 2003; Schumacher et al. 2013).
Numerous studies have documented a similar variability in
genotypic characters, such as amplified restriction length
polymorphism, detection of transposable elements and microsatellite heterogeneity. Recently, B. cinerea strains have been
described that produce bikaverin, a reddish pigment. These
strains contain an intact bikaverin biosynthesis gene cluster
(presumably acquired by horizontal gene transfer from
Fusarium), which is partially deleted and nonfunctional in
most non-bikaverin producing B. cinerea strains (Campbell
et al. 2012; Schumacher et al. 2013
A subdivision of B. cinerea into genetically distinct groups
has proved to be difficult. Analysis of the presence or absence
of two types of transposable elements, named Boty (Diolez
et al. 1995) and Flipper (Levis et al. 1997), was adopted as a
tool to divide isolates into four transposon types, Transposa
(isolates having both elements), Vacuma (isolates having neither element), Boty and Flipper (Giraud et al. 1997, 1999).
This classification led to the discovery of B. pseudocinerea,
which is usually Vacuma, but the transposon-based classification turned out to be of limited use since B. cinerea populations appear to consist of mixtures of different transposon
types. Intriguingly, predominance of a certain type appears
to be influenced by the host. While on grapes, strawberries
and tomatoes, Transposa types are predominant, whereas
B. cinerea populations from kiwi and apples are dominated
by Vacuma types (Esterio et al. 2011; Johnston et al. 2013;
Muñoz et al. 2002; Samuel et al. 2012; M. Hahn, unpublished). Reasons for this observation are unknown.
Evidence for genetic differentiation of B. cinerea populations with different host preference was obtained with microsatellite markers. In France, isolates from grapes and blackberries were shown to be divergent, indicating limited gene
flow between populations on these host plants (Fournier and
Giraud 2008). A recent study on grey mould isolates from
fungicide-treated strawberry fields revealed the existence of a
predominant B. cinerea genotype, named group S, that is
closely related to but distinct from the common genotype of
Fungal Diversity (2014) 67:21–125
B. cinerea (Leroch et al. 2013). Sequencing of the highly
polymorphic MRR1 gene revealed that group S isolates show
more than 4 % divergence from B. cinerea strains B05.10 and
T4, which have MRR1 genes with 99.9 % identity. Further
sequencing of HSP60 and NEP2, and of two FUNYBASE
genes that are suitable for phylogenetic studies (Marthey et al.
2008), partially supported the genetic separation of group S
isolates (Johnston et al. 2013; Leroch et al. 2013). Genome
sequencing of several B. cinerea and group S strains, and the
analysis of additional polymorphic genes in isolates collected
from various host plants in different countries, revealed at
least two subclades that could be separated from the common
B. cinerea genotype (Plesken and Hahn, unpublished). In
fungicide-treated strawberry fields group S isolates dominated, whereas grapes were infected almost exclusively by common B. cinerea genotypes. These data, together with those of
putative new endophytic Botrytis taxa that grouped close to
B. cinerea (Shipunov et al. 2008), support the idea that
B. cinerea represents a species complex, comprising genetically and phenotypically distinct groups.
Recommended genetic markers
G3PDH, RPB2 and HSP60—placement within the
Sclerotiniaceae and the ascomycetes
NEP1 and NEP2—for higher resolution within the genus
Botrytis,
The NEP1 and NEP2 genes are under positive selection
(Staats et al. 2007a) and potentially influence interactions with
the host plants. The NEP genes should therefore be used with
caution.
Research is ongoing to identify a set of highly polymorphic
genes that better resolve the phylogeny of taxa in clade I
(Hahn et al., unpublished). It remains to be established whether those gene are equally useful for resolving the clade II
species, and whether universal primers can be designed before
these genes can be employed to infer a comprehensive phylogeny of the entire genus.
Choanephora
Background
The genus Choanephora belongs to family Choanephoraceae
in the order Mucorales (former Zygomycota). The genus was
introduced by Currey (1873) for C. cunninghamii, to replace
the generic name of his newly described species
Cunninghamia infundibulifera, as Cunninghamia already
existed as a genus of conifers. Because the specific epithet
could not be retained, Choanephora cunninghamia remained
invalid, based on the same type as Cunninghamia
infundibulifera. The prop er na me Choanep hora
Fungal Diversity (2014) 67:21–125
infundibulifera was validly published by Saccardo (1891), so
the correct authorship of the species is “(Currey) Sacc.” It is
also the type species of the genus. Choanephora was
monographed by Hesseltine (1953), Milko and Beljakova
(1970) and Kirk (1984). Currently the genus is classified
within the family Choanephoraceae which can be distinguished by the presence of a persistent sporangium wall that
ruptures at preformed sutures. It is furthermore placed in the
subfamily Choanephoroideae, which is characterized by the
presence of apposed suspensors and smooth zygospores
(Hoffmann et al. 2013).
Both species of the genus can grow as saprobes, but they
frequently become plant pathogens causing various leaf and
fruit rots and blights and are commonly reported from a wide
range of plant hosts, including angiosperms (monocotyledons
and dicotyledons) and gymnosperms (Farr and Rossman
2014). Their distribution is worldwide, however, disease development is more common in tropical and subtropical regions characterized by high temperatures and humidity.
Choanephora cucurbitarum is the causal agent of fruit and
blossom rot of various cucurbits, e.g. yellow crookneck
squash (Kucharek and Simone 1983). This species is also
known from crop plants such as green beans (McMillan
1972), garden peas (Oikawa et al. 1986), and okra (El-Sayed
and El-Sajed 2013) and is reported as an agent of wet rot of
Mesembryanthemum crystallinum in hydroponic greenhouse
culture in Japan (Kagiwada et al. 2010). It is very common
during rainy summers in the southeastern United States and
globally in other regions with similar climates. Recently it was
isolated also from cultivated Hyoscyamus muticus in Japan
(Abdel-Motaal et al. 2010) and Withania in India (Saroj et al.
2012). Choanephora often attacks tissues that have been
damaged mechanically by insects or otherwise; plants that
are poorly adapted to a hot humid climate are particularly
prone to infection by the genus. The general appearance of
Choanephora rot is similar to that of blights caused by other
Mucorales representatives. Signs of infections on fruits or
leaves include water-soaked, necrotic lesions, which progress
rapidly under wet conditions. As the fungus begins to produce
spores, affected tissues become dark grey-brown and hairy.
This specific appearance results from the tall sporangiophores
that produce a cluster of brown, one-spored sporangiola at
their tips (Turkensteen 1979).
Species identification and numbers
Although more than ten species (and many varieties) have
been described within this genus, only two species (viz.
C h oa n ep h or a i nf un d i b ul i f e r a a nd C h o an ep h or a
cucurbitarum) were finally recognized in a monograph of
the genus (Kirk 1984). These two species can be distinguished
by shape and ornamentation of indehiscent sporangiola.
C. cucurbitarum produces ellipsoid sporangiola, which are
37
usually distinctly longitudinally striate, whereas
C. infundibulifera forms subglobose to obovoid sporangiola
with usually smooth or faint striate ornamentation. The remaining species were synonymized under these taxa (e.g.
C. mandshurica is currently a synonym of C. cucurbitarum)
or were moved to other genera (e.g. C. persicaria is a synonym of Gilbertella persicaria). Choanephora circinans with
its two varieties (C. circinans var. indica and C. circinans var.
prolifera) were moved by Kirk (1984) to Poitrasia. Poitrasia
was established for those species belonging to the family
Choanephoraceae that do not form dehiscent or indehiscent
sporangiola (Kirk 1984). Although Poitrasia is primarily a
soil-borne genus, it has been isolated from Equisteum arvense
(Rai 1990). Recent molecular studies confirmed the taxonomic position of Poitrasia proposed by Kirk (1984).
Molecular phylogeny
All Choanephora strains available in CBS culture collection
(three strains of C. infundibulifera and five strains of
C. cucurbitarum) have been sequenced for their ITS sequences and included in molecular analysis by Walther et al.
(2013). These studies showed that the universal fungal DNA
barcoding marker–the ITS region (Schoch et al. 2012)–is
sufficient for Choanephora species identification (Table 6,
Fig. 5). Multigene phylogenetic analysis including representatives of this genus was performed by Hoffmann et al. (2013).
Recommended genetic markers
&
&
The internal transcribed spacer (ITS)–generic and species
level
The large and small subunits (LSU and SSU) of nrDNA–
placement within the Mucorales order, higher-level
phylogeny
Table 6 Choanephora. Details of the isolates used in the phylogenetic
tree
Species
Isolate
Host
GenBank no
Choanephora infundibilifera
C. infundibilifera
C. infundibilifera
C. cucurbitarum
C. cucurbitarum
C. cucurbitarum
C. cucurbitarum
C. cucurbitarum
Poitrasia circinans
P. circinans
CBS 153.51
CBS 155.51
CBS 155.58
CBS 445.72
CBS 178.76
CBS 674.93
CBS 120.25
CBS 150.51
CBS 153.58*
CBS 647.70
–
–
–
–
Dead insect
–
–
–
Soil
Soil
JN206236
JN206237
JN206238
JN206234
JN206235
JN206233
JN206231
JN206232
JN206239
JN206240
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher
stains are bolded
38
Fungal Diversity (2014) 67:21–125
Fig. 5 Phylogram generated
from Maximum likelihood
analysis based on ITS sequenced
data of Choanephora. Bootstrap
support values greater than 50 %
are indicated above the nodes.
The ex-type (ex-epitype) and
voucher strains are in bold
&
The partial actin gene (ACT) and the partial translation
elongation factor 1-alpha gene (TEF)–higher-level
phylogeny
Colletotrichum
Background
The genus Colletotrichum was introduced by Corda (1831)
and belongs to the family Glomerellaceae (Glomerellales,
Ascomycota). Colletotrichum is a coelomycetous phytopathogenic genus with a Glomerella sexual state that includes a
number of important pathogens causing diseases of crops and
fruits worldwide (Cai et al. 2009; Cannon et al. 2012; Doyle
et al. 2013). Colletotrichum species have furthermore been
recorded as endophytes in angiosperms, conifers, ferns, lichens and grasses (Hofstetter et al. 2012; Damm et al.
2012b; Cannon et al. 2012; McKenzie et al. 2009; Petrini
et al. 1990; Manamgoda et al. 2013; Tao et al. 2013). This
genus was voted the eighth most important group of plant
pathogenic fungi in the world, based on perceived scientific
and economic importance (Dean et al. 2012). Colletotrichum
species commonly cause anthracnose resulting in sunken necrotic lesions on leaves, stems, flowers and fruits of numerous
hosts, including important crops (Lenne 2002; Waller et al.
2002; Agrios 2005; Cai et al. 2009; Than et al. 2008; Peng
et al. 2012; Doyle et al. 2013). It is therefore important to plant
health disease practitioners, quarantine personnel and plant
breeders to know what species infect which crops (Huang
et al. 2013b; Lima et al. 2013; Giaretta et al. 2010;
Sangeetha and Rawal 2010; Liu et al. 2009a; Akinbode and
Ikotun 2008; Adegbite and Amusa 2008; Peres et al. 2002).
Therefore, having a rigid and stable taxonomy for the identification of Colletotrichum species is a significant practical
concern (Sheno y et al. 2007 ). Identific ation of
Colletotrichum species has been difficult due to the lack of
reliable morphological features and confused, ambiguous species boundaries (Hyde et al. 2009a, b; Cai et al. 2009).
Difficulties in recognising Colletotrichum species has resulted
from having a few and variable morphological characters,
widespread host ranges and pathogenicity, lost specimens or
type specimens in poor condition and incorrectly named sequences in NCBI (Freeman et al. 2000; Du et al. 2005;
Thaung 2008; Crouch et al. 2009a, b; Damm et al. 2009;
Cai et al. 2009).
Colletotrichum species are extensively studied as model
organisms for research in genetics (Cannon et al. 2012). The
pathogenicity genes of C. higginsianum were discovered by
random mutagenesis (Huser et al. 2009). Genomes and
transcriptomes of C. higginsianum and C. graminicola were
studied through the use of two different infection strategies by
O’Connell et al. (2012). Work on the genetics of pathogenicity
in the C. orbiculare species aggregate led to transformation of
pathogenic strains to endophytic forms (Cannon et al. 2012).
Gene manipulation techniques such as Agrobacterium
tumefacien-mediated transformation or protoplast transformation were established (Tsuji et al. 2003). Peroxisome biogenesis genes, PEX6 and PEX13 were identified and their pathogenesis was functionally analyzed (Fujihara et al. 2010). The
importance of the pexophagy factor ATG26 for apressorium
formation was discovered by Asakura et al. (2009). Whole
genomes of C. higginsianum and C. graminicola have been
Fungal Diversity (2014) 67:21–125
sequenced (O’Connell et al. 2012). Correct species identification is essential in plant pathogenic genera. In order to have
effective measures to prevent the unwanted entry of diseases
in to a country, the plant pathologists should be able to name
the Colletotrichum species confidently. Therefore, pathologists need to be able to clarify and identify the species of
Colletotrichum using the wide genetic variation among the
taxa (Cannon et al. 2000).
Species identification and numbers
Colletotrichum species have been traditionally named after
their hosts. The history of naming Colletotrichum species has
been reviewed in several key papers (Cannon et al. 2008,
2012; Hyde et al. 2009a). Cai et al. (2009) outlined the recent
polyphasic protocols for species identification: A total of 25
Colletotrichum species have been epitypified, one has been
neotypified and three have been lectotypified (Cannon et al.
2008; Damm et al. 2009, 2012a, b, 2013; Doyle et al. 2013;
Liu et al. 2011a, b, 2013; Su et al. 2011; Weir and Johnston
2010; Weir et al. 2012). Significant changes to the understanding of Colletotrichum species took place with incorporation of
these polyphasic approaches, especially the use of multimarker phylogenetic analysis, classification and knowledge
of species complexes, as well as epitypifications for many
species (Cai et al. 2009; Cannon et al. 2012; Damm et al.
2012a, b, 2013; Doyle et al. 2013; Su et al. 2011; Weir et al.
2012). Cannon et al. (2012) studied nearly all presently sequenced species in the genus using a six-gene analysis, and
revealed at least nine clades; 119 species previously thought to
be well circumscribed proved to be polyphyletic.
Colletotrichum gloeosporioides (Cannon et al. 2008;
Phoulivong et al. 2010a, b; Weir et al. 2012), C. acutatum
(Marcelino et al. 2008; Shivas and Tan 2009; Damm et al.
2012a), C. boninense (Moriwaki et al. 2003; Yang et al. 2009;
Damm et al. 2012b), C. orbiculare (Damm et al. 2013) form
important species complexes within Colletotrichum and
well-resolved among all the nine clades. Further studies in
the C. gloeosporioides species complex led to identification
of C. murrayae (Peng et al. 2012), C. viniferum (Peng et al.
2013), C. citricola (Huang et al. 2013b), C. fructivorum
(Doyle et al. 2013), C. melanocaulon (Doyle et al. 2013),
C. temperatum (Doyle et al. 2013), C. endophyticta
(Manamgoda et al. 2013) and C. syzygicola (Udayanga
et al. 2013). Tao et al. (2013) introduced seven new species;
four species belonging to the graminicola clade, two species belonging to the spaethianum clade and one singleton
species. Damm et al. (2013) resolved C. orbiculare and
introduced four new species. Crouch (2014) introduced a
new species complex, C. caudatum, with five new species
found on warm-season grasses, characterized by the conidial apex reducing into a filiform appendage. The current
39
numbers of species recognised in the genus are listed in
Table 7.
Molecular phylogeny
Some species such as Colletotrichum gloeosporioides were
defined using ITS sequence data, but the outcome was not
good partially due to prolific misidentification in GenBank
and because ITS does not resolve Colletotrichum species well.
In Colletotrichum, species definitions based on ITS sequence
data, the “universal” DNA barcoding marker for fungal species has proved unsatisfactory (Du et al. 2005; Crouch et al.
2009b; García et al. 2009; Cannon et al. 2012; Doyle et al.
2013; Gunjan et al. 2013). Comparison of a phylogenetic tree
of Colletotrichum species derived from ITS sequence alone
and one generated from multi-marker data confirms that ITS
resolves major clades well, although it does not reflect their
higher-order relationships accurately in all cases (Cannon
et al. 2012). Cannon et al. (2012) suggested that a robust
sequence-based identification system for Colletotrichum species must therefore use an alternative molecular marker or a
combination of markers. Damm et al. (2012a) indicated that
the most diagnostic markers are β-tubulin and GPDH. βtubulin performed marginally better than GPDH due to a
larger overall number of base pair differences, but even so,
some clades differed only by one base pair in the β-tubulin
alignment. As single genes that were used are not efficient to
differentiate the species, Cai et al. (2009) suggested using
multiple markers. Cannon et al. (2012), Weir et al. (2012),
and Damm et al. (2012a, b) used several genetic markers:
actin (act), chitin synthase (chs1 β-tubulin and ITS which
revealed that Colletotrichum comprises nine major clades as
well as a number of small clusters and singleton species. Many
recent studies used multimarker phylogeny including actin
(act), chitin synthase (chs1), β-tubulin, calmodulin (cal),
glyceraldehydes-3-phosphate dehydogenase (gadph), histamine (HIS3), glutamine synthetase (GS), DNA lyase (apn2),
intergenic region of apn2 and MAT1-2-1 genes (ApMat) (Weir
et al. 2012; Damm et al. 2012a, b; Cannon et al. 2012; Peng
et al. 2012; Doyle et al. 2013; Gunjan et al. 2013) to understand the phylogenetic divergence of Colletotrichum species.
There is, however, no agreement among mycologists as to
which genetic markers should be used (Doyle et al. 2013;
Gunjan et al. 2013). Silva et al. (2012) stressed the need to use
‘powerful genes’ such as ApMat and Apn25L. The Apmat
marker provides better resolution as compared to the genetic
markers used by Weir et al. (2012), Silva et al. (2012), Doyle
et al. (2013) and Gunjan et al. (2013). Up to now it has been a
better gene-marker for resolving species within
C. gloeosporioides species complex (Doyle et al. 2013;
Gunjan et al. 2013). Only ITS sequences are available for
several species of Colletotrichum showing the need of sequencing the other important gene regions and those species
40
Fungal Diversity (2014) 67:21–125
Table 7 Colletotrichum. Details of the isolates used in the phylogenetic tree
Species
Isolate
GenBank Accession Number
ApMat
ITS
GPDH
CHS-1
HIS3
ACT
β-tubulin
C. acerbum*
C. acutatum*
C. aenigma*
C. aeschynomenes*
C. agaves
C. alatae*
C. alcorni*
C. alienum*
C. annellatum*
C. anthrisci*
C. aotearoa*
C. asianum*
C. australe*
C. axonopodi
CBS 128530
CBS112996
ICMP 18608
ICMP 17673
CBS 118190
ICMP 17919
IMI 176619
ICMP 12071
CBS 129826
CBS 125334
ICMP 18537
ICMP 18580
CBS116478
IMI 279189
JQ948459
JQ005776
JX010244
JX010176
DQ286221
JX010190
JX076858
JX010251
JQ005222
GU227845
JX010205
FJ972612
JQ948455
EU554086
JQ948790
JQ948677
JX010044
JX009930
–
JX009990
JQ949120
JQ005797
JX009774
JX009799
–
JX009837
JQ949450
JQ005818
–
–
–
–
JQ949780
JQ005839
JX009443
JX009483
–
JX009471
JQ950110
JQ005860
JX010389
JX010392
–
JX010383
–
–
–
–
–
KC888932
JX010028
JQ005309
GU228237
JX010005
JX010053
JQ948786
–
JX009882
JQ005396
GU228335
JX009853
JX009867
JQ949116
–
–
JQ005483
GU228041
–
–
JQ949446
–
JX009572
JQ005570
GU227943
JX009564
JX009584
JQ949776
–
JX010411
JQ005656
GU228139
JX010420
JX010406
JQ950106
–
KC888927
–
–
KC888930
FR718814
–
–
C. baltimorense*
C. beeveri*
C. bletillum*
C. bidentis*
C. boninense*
C. brasiliense*
C. brassicola*
C. brevisporum*
SD11
CBS 128527
CGMCC 3.15117
COAD 1020
CBS 123755
CBS 128501
CBS 101059
BCC 38876
JX076866
JQ005171
JX625178
KF178481
JQ005153
JQ005235
JQ005172
JQ247623
–
JQ005258
KC843506
KF178506
JQ005240
JQ005322
JQ005259
JQ247599
–
JQ005345
–
KF148530
JQ005327
JQ005409
JQ005346
–
JQ005432
–
KF178554
JQ005414
JQ005496
JQ005433
–
JQ005519
KC843542
KF178578
JQ005501
JQ005583
JQ005520
–
JQ005605
JX625207
KF178602
JQ005588
JQ005669
JQ005606
–
–
–
C. brisbanense*
C. carthami*
C. caudasporum*
C. caudatum*
C. cereale
C.chlorophyti*
C. chrysanthemi
Glomerella cingulata
“f.sp. camelliae”
C. circinans*
C. citri*
C. citricola*
C. clidemiae*
C.cliviae*
C.coccodes
C. coccodes
C. colombiense*
C. constrictum*
C. cordylinicola*
C. cosmi*
C. costaricense*
CBS292.67
SAPA100011
CGMCC 3.15106
BPI423339
CBS 129663
IMI 103806
IMI364540
ICMP 10643
JQ948291
AB696998
JX625162
JX076860
JQ005774
GU227894
JQ948273
JX010224
JQ948621
–
KC843512
–
–
GU228286
JQ948603
JX009908
–
JQ948952
–
–
–
JQ005795
GU228384
JQ948934
JX009891
–
JQ949282
–
–
–
JQ005816
GU228090
JQ949264
–
JQ247647
JQ949612
–
KC843526
–
JQ005837
GU227992
JQ949594
JX009540
JQ247635
JQ949942
AB696992
JX625190
–
JQ005858
GU228188
JQ949924
JX010436
–
–
–
–
–
–
–
–
–
CBS 221.81
ZJUC41
SXC151
ICMP 18658
CBS 125375
CBS 369.75
ITCC 6079
CBS 129818
CBS 128504
ICMP 18579
CBS 853.73
CBS 330.75
GU227855
KC293581
KC293576
JX010265
JX519223
JQ005775
–
JQ005174
JQ005238
JX010226
JQ948274
JQ948180
GU228247
KC293741
KC293736
JX009989
GQ856756
HM171673
–
JQ005261
JQ005325
JX009975
JQ948604
JQ948510
GU228345
–
KC293792
JX009877
JX519232
JQ005796
–
JQ005348
JQ005412
JX009864
JQ948935
JQ948841
GU228051
–
–
–
–
JQ005817
–
JQ005435
JQ005499
–
JQ948604
JQ949171
GU227953
KC293621
KC293616
JX009537
JX519240
JQ005838
–
JQ005522
JQ005586
HM470234
JQ949595
JQ949501
GU228149
KC293661
KC293656
JX010438
JX519249
JQ005859
–
JQ005608
JQ005672
JX010440
JQ949925
JQ949831
–
–
–
KC888929
–
–
KC790652
–
–
JQ899274
–
–
C. curcumae*
IMI 288937
GU227893
GU228285
GU228383
GU228089
GU227991
GU228187
–
C. cuscutae*
C. cymbidiicola*
C. dacrycarpi*
IMI 304802
IMI 347923
CBS 130241
JQ948195
JQ005166
JQ005236
JQ948525
JQ005253
JQ005323
JQ948856
JQ005340
JQ005410
JQ949186
JQ005427
JQ005497
JQ949516
JQ005514
JQ005584
JQ949846
JQ005600
JQ005670
–
–
–
–
–
–
Fungal Diversity (2014) 67:21–125
41
Table 7 (continued)
Species
Isolate
GenBank Accession Number
ApMat
ITS
GPDH
CHS-1
HIS3
ACT
β-tubulin
C. dematium*
C. destructivum
C. dianensei*
C.dracaenophilum*
C. duyunensis*
C. echinochloae*
C. eleusines*
C. endomagniferae*
C. endophytica*
C. endophytum*
C. eremochloae*
C. excelsum altitudum*
C. falcatum
C. fioriniae*
C. fructi*
C. fructicola*
C. fructivorum*
CBS 125.25
CBS 149.34
CMM4083
CBS 118199
CGMCC 3.15105
MAFF 511473
MAFF 511155
MFLUCC 14-0563
LC0324
CGMCC 3.15108
CBS 129661
CGMCC 3.15130
CBS 147945
CBS 128517
CBS 346.37
ICMP 18581
Coll1414
GU227819
AJ301942
KC329779
JX519222
JX625160
AB439811
JX519218
KC702994
KC633854
JX625177
JX519220
HM751815
JQ005772
JQ948292
GU227844
JX010165
JX145145
GU228211
–
KC517194
–
KC843515
–
–
KC702955
KC832854
KC843521
–
KC843502
–
JQ948622
GU228236
JX010033
–
GU228309
JQ005785
–
JX519230
–
–
JX519226
KC598113
–
–
JX519228
–
JQ005793
JQ948953
GU228334
JX009866
–
GU228015
JQ005806
–
–
–
–
–
–
–
–
–
–
JQ005814
JQ949283
GU228040
–
–
GU227917
JQ005827
KC517298
JX519238
KC843530
–
JX519234
KC702922
KF306258
KC843533
JX519236
KC843548
JQ005835
JQ949613
GU227942
FJ907426
–
GU228113
JQ005848
KC517254
JX519247
JX625187
–
JX519243
KC702922
–
JX625206
JX519245
JX625211
JQ005856
JQ949943
GU228138
JX010405
JX145196
C. fuscum
CBS 130.57
JQ005762
–
JQ005783
JQ005804
JQ005825
JQ005846
–
–
C. gigasporum*
C. gloeosporioides*
C. godetiae*
C. graminicola*
C. grevilleae*
C. guajave*
C. guizhouensis*
C. hanaui*
C. hemerocallidis*
C. higginsianum
C. hippeastri*
C. horii
C. hsienjenchng
C. incanum*
C. indonesiense*
C. jacksonii*
C. jasiminigenum*
C. johnstonii*
MUCL 44947
CBS 112999
CBS 133.44
CBS 130836
CBS 132879
IMI 350839
CGMCC 3.15112
MAFF 305404
CDLG5
IMI 349063
CBS 125376
ICMP 10492
MAFF 243051
ATCC 64682
CBS 127551
MAFF 305460
MFU 10-0273
CBS 128532
AM982797
JQ005152
JQ948402
JQ005767
KC297078
JQ948270
JX625158
JX519217
JQ400005
JQ005760
JQ005231
GQ329690
AB738855
KC110789
JQ948288
JX519216
HM131513
JQ948444
–
JQ005239
JQ948733
–
KC297010
JQ948600
KC843507
–
JQ400012
–
JQ005318
GQ329681
–
KC110807
JQ948618
–
HM131499
JQ948775
–
JQ005326
JQ949063
JQ005788
KC296987
JQ948931
–
JX519225
JQ399998
JQ005781
JQ005405
JX009752
AB738846
–
JQ948949
JX519224
–
JQ949105
–
JQ005413
JQ949393
JQ005809
KC297056
JQ949261
–
–
–
JQ005802
JQ005492
–
AB738847
KC110798
JQ949279
–
–
JQ949435
–
JQ005500
JQ949723
JQ005830
KC296941
JQ949591
KC843536
–
JQ399991
JQ005823
JQ005579
JX009438
AB738845
KC110825
JQ949609
JX519233
HM131508
JQ949765
FN557442
JQ005587
JQ950053
JQ005851
KC297102
JQ949921
JX625185
JX519242
JQ400019
JQ005844
JQ005665
JX010450
–
KC110816
JQ949939
JX519241
HM153770
JQ950095
–
JQ807843
–
–
–
–
–
–
–
–
–
JQ807840
–
–
–
–
–
–
C. kahawae*
ICMP17816
CORCG6
CBS 198.35
CBS 112989
CBS 109214
CBS 114.14
CBS 144.31
CBS 125337
CBS 172.51
CBS 119444
CBS 109225
JX010231
HM585409
JQ948454
JQ948289
GU227810
JQ948193
JQ005779
GU227829
JQ005765
GU227804
JQ948155
JX010012
HM585391
JQ948785
JQ948619
GU228202
JQ948523
JX546712
GU228221
–
GU228196
JQ948485
JX009813
HM582023
JQ949115
JQ948950
GU228300
JQ948854
JQ005800
GU228319
JQ005786
GU228294
JQ948816
–
–
JQ949445
JQ949280
GU228006
JQ949184
JQ005821
GU228025
JQ005807
GU228000
JQ949146
JX009452
HM581995
JQ949775
JQ949610
GU227908
JQ949514
JQ005842
GU227927
JQ005828
GU227902
JQ949476
JX010444
HM585428
JQ950105
JQ949940
GU228104
JQ949844
JQ005863
GU228123
JQ005849
GU228098
JQ949806
JQ899282
–
–
–
–
–
–
–
–
–
–
C. kartsii*
C. kinghornii*
C. lacticiphilum*
C. lilii
C. limetticola*
C. lindemuthianum*
C. lineola*
C. linicola
C. liriopes*
C. lupini
–
–
KJ155461
–
–
–
–
KJ155453
–
–
–
–
–
–
–
JQ807838
42
Fungal Diversity (2014) 67:21–125
Table 7 (continued)
Species
Isolate
GenBank Accession Number
ApMat
ITS
GPDH
CHS-1
HIS3
ACT
β-tubulin
C. melanocaulon*
C. malvarum*
C. melonis*
C. metake
C. miscanthi*
C. musae*
C. murrayae*
C. navitas*
C. nicholsonii*
C. nigrum*
C. novae-zelandiae*
C. nupharicola*
C. nymphaeae*
C. ochracea*
C. oncidii*
C. orbiculare*
C.orchidophilum*
C. parsonsiae*
Coll131
CBS 527.97
CBS 159.84
NBRC 8974
MAFF 510857
ICMP19119
GZAAS5.09506
CBS 125086
MAFF 511115
CBS 169.49
CBS 128505
ICMP 18187
CBS 515.78
CGMCC 3.15104
CBS 129828
CBS 570.97
CBS 632.80
CBS 128525
–
KF178480
JQ948194
AB738859
JX519221
JX010146
JQ247633
JQ005769
JQ005770
JX546838
JQ005228
JX010187
JQ948197
JX625156
JQ005169
KF178466
JQ948151
JQ005233
–
KF178504
JQ948524
–
–
JX010050
JQ247609
–
–
JX546742
JQ005315
JX009972
JQ948527
KC843513
JQ005256
KF178490
JQ948481
JQ005320
–
KF178529
JQ948855
–
JX519229
JX009896
–
JQ005790
JQ005791
JX546693
JQ005402
JX009835
JQ948858
–
JQ005343
KF178515
JQ948812
JQ005407
–
KF178553
JQ949185
–
–
–
–
JQ005811
JQ005812
JX546791
JQ005489
–
JQ949188
–
JQ005430
KF178539
JQ949142
JQ005494
–
KF178577
JQ949515
–
JX519237
JX009433
JQ247657
JQ005832
JQ005833
JX546646
JQ005576
JX009437
JQ949518
KC843527
JQ005517
KF178563
JQ949472
JQ005581
–
KF178601
JQ949845
–
JX519246
HQ596280
JQ247644
JQ005853
JQ005854
JX546885
JQ005662
JX010398
JQ949848
JX625183
JQ005603
KF178587
JQ949802
JQ005667
C. paspali*
C. paxtonii*
MAFF 305403
IMI 165753
JX519219
JQ948285
–
JQ948615
JX519227
JQ948946
–
JQ949276
JX519235
JQ949606
JX519244
JQ949936
C. petchii*
C.phaseolorum
C. phormii*
C. phyllanthi*
C. proteae
C.pseudoacutatum*
C. psidii
C. pyricola*
C. queenslandium*
C. rhexiae*
C. rhombiforme*
C. rusci*
C. salicis*
C. salsolae*
C. sansevieriae
C. scovillei*
CBS 378.94
CBS 157.36
CBS 118194
CBS 175.67
CBS132882
CBS 436.77
ICMP 19120
CBS 128531
ICMP 1778
Coll 1026
CBS 129953
CBS 119206
CBS 607.94
ICMP 19051
MAFF 239721
CBS 126529
JQ005223
GU227896
JQ948446
JQ005221
KC297079
JQ948480
JX010219
JQ948445
JX010276
JX145128
JQ948457
GU227818
JQ948460
JX010242
AB212991
JQ948267
JQ005310
GU228288
JQ948777
JQ005308
KC297009
JQ948811
JX009967
JQ948776
JX009934
–
JQ948788
GU228210
JQ948791
JX009916
–
JQ948597
JQ005397
GU228386
JQ949107
JQ005395
KC296986
JQ949141
JX009901
JQ949106
JX009899
–
JQ949118
GU228308
JQ949121
JX009863
–
JQ948928
JQ005484
GU228092
JQ949437
JQ005482
KC297045
JQ949471
–
JQ949436
–
–
JQ949448
GU228014
JQ949451
–
–
JQ949258
JQ005571
GU227994
JQ949767
JQ005569
KC296940
JQ949801
JX009515
JQ949766
JX009447
–
JQ949778
GU227916
JQ949781
JX009562
–
JQ949588
JQ005657
GU228190
JQ950097
JQ005655
KC297101
JQ950131
JX010443
JQ950096
JX010414
JX145179
JQ950108
GU228112
JQ950111
JX010403
–
JQ949918
C. siamense*
C. sidae*
C. simmondsii*
C. sloanei*
C. somersetense*
C. spaethianum*
C. spinaceae
C. spinosum*
ICMP 18578
CBS 504.97
CBS 122122
IMI 364297
JAC 11-11
CBS 167.49
CBS 128.57
CBS 515.97
JX010171
KF178472
JQ948276
JQ948287
JX076862
GU227847
GU227847
KF178474
JX009924
KF178497
JQ948606
JQ948617
–
GU228239
GU228239
KF178498
JX009865
KF178521
JQ948937
JQ948948
–
GU228337
GU228337
KF178523
–
KF178545
JQ949267
JQ949278
–
GU228043
GU228043
KF178547
FJ907423
KF178569
JQ949597
JQ949608
–
GU227945
GU227945
KF178571
JX010404
KF178593
JQ949927
JQ949938
–
GU228141
GU228141
KF178595
C. sublineola*
C. syzygicola*
C. tabacum
CBS 131301
DNCL021
CBS 161.53
JQ005771
KF242094
JQ005763
–
KF242156
–
JQ005792
–
JQ005784
JQ005813
–
JQ005805
JQ005834
KF157801
JQ005826
JQ005855
KF254880
JQ005847
JX145313
–
–
–
KC888926
–
–
–
–
–
JX145319
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
KC888928
JX145290
–
–
–
KC888925
–
–
JQ899289
–
–
–
–
–
–
–
–
–
–
Fungal Diversity (2014) 67:21–125
43
Table 7 (continued)
Species
Isolate
GenBank Accession Number
ApMat
ITS
GPDH
CHS-1
HIS3
ACT
β-tubulin
JQ949835
JX218233
KF178594
JX145211
JN050248
JX010447
JX010442
GU228095
JQ005598
GU228106
KF178599
JX010407
JN050246
GU228156
GU228100
JN412813
–
JQ949926
–
–
–
JX145298
–
KC790726
–
–
–
–
–
KC790728
–
–
–
–
KJ623242
–
C. tamarilloi*
C. tanaceti*
C. tebeestii*
C. temperatum*
C. thailandicum*
C. theobromicola
C. ti*
C. tofieldiae
C. torulosum*
C.trichellum
C. trifolii*
C. tropicale*
C.tropicicola*
C. truncatum*
C. verruculosm*
C. viniferum*
C. viniferum
C. walleri*
CBS 129814
CBS 132693
CBS 522.97
Coll883
MFUCC110113
ICMP 18649
ICMP 4832
CBS 495.85
CBS 128544
CBS 217.64
CBS 158.83
ICMP18653
BCC 38877
CBS 151.35
IMI 45525
GZAAS5.08601
GZAAS5.08608
CBS 125472
JQ948184
–
KF178473
JX145159
JN050242
JX010294
JX010269
GU227801
JQ005164
GU227812
KF178478
JX010264
JN050240
GU227862
GU227806
JN412804
–
JQ948275
JQ948514
JX218243
KF178505
–
JN050231
JX010006
JX009952
GU228193
JQ005251
GU228204
KF178502
JX010007
JN050229
GU228254
GU228198
JN412798
–
JQ948605
JQ948845
–
KF178522
–
–
JX009869
JX009898
GU228291
JQ005338
GU228302
KF178527
JX009870
JQ949175
–
KF178546
–
–
–
–
GU227997
JQ005425
GU228008
KF178551
–
GU228352
GU228296
–
–
JQ948936
GU228058
GU228002
–
–
JQ949266
JQ949505
JX218238
KF178570
–
JN050220
JX009444
JX009520
GU227899
JQ005512
GU227910
KF178575
JX009489
JN050218
GU227960
GU227904
JN412795
–
JQ949596
C. xanthorrhoeae*
C. yunnanense*
ICMP 17903
CGMCC AS3.9167
JX010261
EF369490
JX009927
–
JX009823
JX519231
–
–
JX009478
JX519239
JX010448
JX519248
KC790689
–
C. zoysia*
MAFF 238573
JX076871
–
–
–
–
–
–
Ex-Type (ex-epitype) strains are bolded and marked with an * and authentic stains are bolded
were not included in this analysis. Here we present an analysis
using six genetic markers for all the Colletotrichum species that
are accepted (Fig. 6) and for the C. acutatum species complex
(Fig. 7). Figure 8 presents the analysis of C. gloeosporioides
species complex using the apmat gene. The whole genomes of
several species of Colletotrichum have been sequenced, such
that it is now possible to carry out whole-genome analysis, and
compare this with single gene analysis to establish a gene (or
gene combinations) that can really resolve species in the genus.
These marker combinations can resolve the phylogenetic positions of most species in the genus. GPDH
alone can delineate the majority of species. However,
research is ongoing to identify better genetic markers to
resolve the phylogenetic position of many species of
Colletotrichum.
Curvularia
Background
Recommended genetic markers
&
&
&
&
&
ITS alone will not resolve species in the genus, but it can
separate taxa to species complexes. Multigene analysis
using the following genes has been recommended for a
backbone tree for species of Colletotrichum:
GPDH–Glyceraldehyde-3-phosphate dehydrogenase- resolves to species level, more accurate.
β-tubulin–Beta-tubulin resolves to species level
ApMat–Intergenic region of apn2 and MAT1-2-1 genes
can resolve within the C. gloeosporioides complex
GS–glutamine synthetase–CHS-1. HIS3–Histone3 and
ACT–Actin–Placement within the genus and also some
species-level delineation.
Curvularia is a dematiaceous hyphomycete genus in the family Pleosporaceae, Pleosporales, Dothideomycetes
(Ascomycota) (Boedijn 1933). It is typified by C. lunata.
Curvularia species have been recorded as saprobes and also
plant, human and animal pathogens. Bipolaris and Curvularia
species are associated with Cochliobolus sexual states
(Sivanesan 1987). Curvularia species are found as plant pathogens especially associated with the family Poaceae. Species
such as C. lunata, C. tuberculata and C. trifolii cause leaf
spots and leaf blights of some cereal crops such as maize, rice
and horticultural crops such as Bermuda grasses and turf
grasses (de Luna et al. 2002). The most frequent human and
animal pathogens within the genus are C. aeria, C. geniculata,
44
Fig. 6 Phylogram generated from parsimony analysis based on combined ITS, GADPH, CHS-1, ACT, HIS and β- tubulin data of
Colletotrichum. Parsimony bootstrap support values and Bayesian
Fungal Diversity (2014) 67:21–125
posterior probabilities greater than 50 % are indicated above the nodes.
The ex-type (ex-epitype) and voucher strains are in bold. The tree is
rooted with Monilochaetes infuscans CBS 869.96
Fungal Diversity (2014) 67:21–125
Fig. 6 (continued)
45
46
Fungal Diversity (2014) 67:21–125
Fig. 7 Phylogram generated
from parsimony analysis based on
combined ITS, GADPH, CHS-1,
ACT, HIS and β- tubulin
sequenced data of Colletotrichum
acutatum complex. Parsimony
bootstrap support values and
Bayesian posterior probabilities
greater than 50 % are indicated
above the nodes. The ex-type (exepitype) and voucher strains are in
bold. The tree is rooted with
C. orchidophilum
C. lunata, C. inaequalis, C. verrucosa and C. borreriae. These
species cause keratitis, sinusitis, cutaneous and subcutaneous
infections, peritonitis, onychomycosis, endocarditis, endophthalmitis, cerebral phaeohyphomycosis, and allergic
bronchopulmonary as well as disseminated disease (da
Cunha et al. 2013).
Species identification and numbers
Curvularia is morphologically characterized by its dark mycelium, geniculate conidiophores with sympodial, tretic
conidiogenous cells, conidia with smooth to slightly verrucose
wall and several false septa (distosepta). Morphological species identification of Curvularia species is challenging as
many species have morphological similarities and have overlapping conidial dimensions. Most of the clinical isolates and
common plant pathogens of Curvularia are recorded as
C. lunata, which was recently epitypified (Manamgoda et al.
2012a). Following phylogenetic assessments, it was revealed
that most of the sequences named as C. lunata in GenBank are
incorrectly identified (Cai et al. 2011; da Cunha et al. 2013).
Ellis (1971) and Sivanesan (1987) described 37 species in the
genus Curvularia and currently there are 122 species epithets
in Index Fungorum.
Molecular phylogeny
Phylogenetic recognition is crucial for species identification in
Curvularia. Former morphological identifications do not correlate with the phylogeny (Manamgoda et al. 2012a, b).
Combined ITS and GPDH analysis for Curvularia and its
sister genus Bipolaris by Berbee et al. (1999) revealed that some
Bipolaris species cluster within the genus Curvularia.
Curvularia was therefore redefined by Manamgoda et al.
(2012a) based on a combined phylogenetic analysis of ITS,
GPDH, TEF and LSU. Nine Bipolaris species clustering within
Curvularia were transferred and their nomenclature redefined
(Manamgoda et al. 2012a). Lack of ex-type cultures and
epitypifications form limitations for phylogenetic species recognition. In this paper we present a phylogenetic tree with combined ITS and GPDH sequences obtained from available type
material and voucher cultures (Table 8, Fig. 9). This can be used
as a backbone in the identification of Curvularia species.
Recommended genetic markers
&
GPDH is the best single genetic marker for the genus
Bipolaris (Manamgoda et al. 2012a). It is recommended
to use a combination of ITS and GPDH. Another useful
gene is TEF.
Fungal Diversity (2014) 67:21–125
47
Fig. 8 Phylogram generated from parsimony analysis based on combined ITS, GADPH, CHS-1, ACT, HIS and β- tubulin sequenced data of
Colletotrichum gloeosporioides complex. Parsimony bootstrap support
values and Bayesian posterior probabilities greater than 50 % are indicated above the nodes. The ex-type (ex-epitype) and voucher strains are in
bold. The tree is rooted with C. coccodes ITCC6079
Diaporthe
including economically important crops (Uecker 1988; Farr
and Rossman 2014; Udayanga et al. 2011). The genus belongs
to class Sordariomycetes, order Diaporthales and the family
Diaporthaceae, typified by the species Diaporthe eres
Nitschke (Wehmeyer 1933). With the change to one scientific
name for fungi (McNeill et al. 2012), Diaporthe has priority,
being the older generic name compared to Phomopsis. Many
Background
Diaporthe (=Phomopsis) is a cosmopolitan genus of fungi
comprised of endophytes, plant pathogens, and saprobes occurring on a wide range of annual and perennial hosts,
48
Fungal Diversity (2014) 67:21–125
Table 8 Details of the isolates used in the phylogenetic tree
Species
Code
C. heteropogonis
C. intermedia
DAOM 46365
MFLUCC10703*
MFLUCC10705
CBS 172.57
ICMP 103444
88109-1
CBS 193.62*
ICMP 6160
BRIP 23186
DAOM165085
BRIP 15933
BRIP 10972
CBS 284.91*
8797-1
C. lunata
C. ovariicola
C. perotidis
C. ravenelii
C. spicifera
C. trifolii
C. tripogonis
C. tuberculata
C. verrucosa
Alternaria alternata
CBS 730.96*
CBS 470.90*
CBS 7846-2
BRIP 13165*
CBS 274.52
ICMP 6149
BRIP 12375*
CBS 146.63*
MAFF235540
EGS 34.0160*
Curvularia affinis
C. alcornii
C. australiensis
C. clavata
C. cymbopogonis
C. ellisii
C. gladioli
C. graminicola
C. gudauskasii
C. hawaiiensis
Host
Gene bank accession numbers
Zea mays
Panicum sp.
Oryza sativa
Lawn
Air
Gladiolus sp.
Chloris gayana
Chloris gayana
Heteropogon contortus
Human lung biopsy
Eragrostis interrupta
Perotis rara
Sporobolus fertilis
Soil
Setaria glauca
Dactyloctenii aeygeptii
Zea mays
Triticum aestivum
ITS
GPDH
AF071335
JX256420
JX256421
JN601026
JX256444
AF071351
JN192375
JX256426
JN192376
AF071338
JN601028
JN192377
JN192379
AF071327
AF081390
JX276433
JX276434
JN601036
JX276455
AF081403
JN600963
JX276438
JN600964
AF081393
JN600965
JN600968
JN600969
AF081383
JX256429
JN601031
AF071320
JN192386
JN192387
JX256434
JN192388
JN192374
AB444667
AF017346
JX276441
JN600976
AF081374
JN600978
JN600979
JX276457
JN600980
JN601037
AF081388
AF081400
TEF
JX266589
JX266590
JN601003
JN601007
JX266595
JN601008
JN601009
JN601012
JN601013
JX266596
JN601020
JN601024
JN601023
JX266600
JX266600
JX266599
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
species are able to colonise diverse hosts as opportunists;
some species are host specific and multiple species can even
co-occur on the same host (Mostert et al. 2001; Farr et al.
2002a; Crous and Groenewald 2005). Species of Diaporthe
cause cankers, diebacks, root rots, fruit rots, leaf spots, blights
and wilts on a wide range of plant host including some
economically important hosts and have been the subject of
considerable phytopathological research. Examples of diseases on major crops include Diaporthe/Phomopsis complex
causing soybean seed decay, pod and stem blight and cankers,
sunflower stem canker (D. helianthi), dead arm of grapevines
(D. ampelina) and melanose in Citrus (D. citri) (Van Niekerk
et al. 2005; Santos et al. 2011; Thompson et al. 2011;
Udayanga et al. 2014a, b). In addition, several species of
Diaporthe are known from clinical reports of immunocompromised patients, although these pathogens are only
provisionally identified to species level (Garcia-Reyne et al.
2011; Mattei et al. 2013). Diaporthe comprises a major component of endophytes in tropical and temperate trees, and
several species have been used in secondary metabolite research (Isaka et al. 2001; Li et al. 2010a, b; Kaul et al. 2012).
Species identification and numbers
The Genealogical Concordance Phylogenetic Species
Recognition (GCPSR) has been applied in the genus
Diaporthe to define the species boundaries in recent studies
(Udayanga et al. 2012b; Gomes et al. 2013; Tan et al. 2012).
Therefore species delimitation is currently based on DNA
sequence data and comparison of morphological characters
(Santos and Phillips 2009; Santos et al. 2010; Diogo et al.
2010; Udayanga et al. 2014a, b). Although the genus
Diaporthe has received much attention, few phylogenetic
studies have thus far been conducted; hence the taxonomy of
some of the species in this genus is still uncertain including
many of the common plant pathogens. Index Fungorum lists
892 Diaporthe names and 983 Phomopsis names whereas
MycoBank (2014) lists 919 Diaporthe names and 1,040
Phomopsis names. However, the names available in the literature are mostly applied based on host association and morphology except fewer species described in last two decades
based on DNA sequence data. Ex-type cultures are available
for less than 100 species known despite the large number of
Fungal Diversity (2014) 67:21–125
49
Fig. 9 Phylogram generated
from parsimony analysis based on
combined ITS and GPDH
sequenced data of Curvularia.
Parsimony bootstrap support
values greater than 50 % are
indicated above the nodes. The
ex-type (ex-epitype) and voucher
strains are in bold. The scale bar
indicates ten changes. The tree is
rooted with Alternaria alternata
species listed in databases and literature. The delimitation of
species within the genus Diaporthe improved once DNA
sequence data were incorporated (Castlebury and Mengistu
2006; Van Rensburg et al. 2006; Santos et al. 2010; Udayanga
et al. 2012b, 2014a, b), since this facilitates obtaining detailed
insight into complex evolutionary relationships.
Molecular phylogeny
Since the first molecular phylogenetic study in Diaporthe
(Rehner and Uecker 1994), rDNA ITS, partial sequences
of translation elongation factor 1-α (TEF) and mating
type genes (MAT 1-1-1/1-2-1) have commonly been used
in molecular phylogenetic studies in this genus (Van
Niekerk et al. 2005; Van Rensburg et al. 2006; Santos
et al. 2010; Udayanga et al. 2011; Sun et al. 2012).
Udayanga et al. (2012a) used ITS, TEF, β- tubulin and
CAL genes with a selected set of ex-type cultures and
additional isolates to infer the phylogeny of the genus. In
a parallel study, a multi-marker phylogeny was effectively used to describe novel species in Diaporthe based on
fresh collections from Thailand (Udayanga et al. 2012b).
Gomes et al. (2013) used a Brazilian collection of
isolates and existing ex-type cultures for a combined
phylogenetic analysis of five genetic markers which included ITS, TEF, β- tubulin, CAL and HIS. They
introduced several novel taxa from Brazilian collections
from medicinal plants with one epitype for Diaporthe
anarcardi from Kenya. Udayanga et al. (2014a, b)
revisited the Diaporthe species associated with Citrus
worldwide with comprehensive assessment of the genes
including ITS, TEF, β- tubulin, CAL and ACT. The
study revisited several important phytopathogens
including D. citri, D. cytosporella, D. forniculina and
D. rudis, with the epitypes designated with modern
descriptions. The clarification of D. foeniculaina and
D. rudis revealed the potential extensive host
association of some species.
Udayanga et al. (2014a) further emphasized that ITS alone
can cause much confusion in defining closely related taxa,
which has also been noted by several previous researchers
regarding closely related species in Diaporthe (Farr et al.
2002a, b; Murali et al. 2006; Santos et al. 2010). The
variation of ITS sequences can result in superfluous, multiple terminal branches in combined analyses, even when
other gene regions do not support these distinctions
50
(Udayanga et al. 2014a, b). The TEF gene is informative
when it comes to clarifying species limits in Diaporthe
(Table 9, Fig. 10).
Recommendations
ITS and TEF are recommended for preliminary identification
of the species (Castlebury et al. 2001; Castlebury 2005; Santos
and Phillips 2009; Santos et al. 2010). ITS, TEF, β- tubulin,
CAL, HIS and ACT should be used in combined analysis
(selection of 4–5 genes), with recommended primers in relevant publications (Udayanga et al. 2012b, 2014a, b; Gomes
et al. 2013).
Diplodia
Background
Species of Diplodia (Botryosphaeriaceae) are endophytes,
pathogens, or saprobes associated with cankers, dieback and
fruit rot (Crous et al. 2006; Slippers and Wingfield 2007) in a
wide range of hosts of agricultural and forestry importance
(Farr and Rossman 2014). Cryptic speciation is common in
the genus Diplodia, which makes species identification difficult
if only based on morphological characters (Phillips et al. 2012,
2013). Denman et al. (2000) suggested that Lasiodiplodia could
be a synonym of Diplodia, however recent studies accepted
them as distinct genera (Pavlic et al. 2004; Burgess et al. 2006;
Damm et al. 2007; Alves et al. 2008).
The genus Diplodia was introduced by Montagne (1834)
with concepts altering over the years and has been regarded as
including species with dark brown, 1-septate conidia (Phillips
et al. 2005). Diplodia is defined by having uni or multilocular
conidiomata lined with conidiogenous cells that form hyaline,
aseptate, thick-walled conidia at their tips (Phillips et al.
2005). Diplodia mutila is the type species of Diplodia
(Montagne 1834; Fries 1849), however, there are no living
cultures linked to the holotype. As this has severely hampered
studies on taxonomy and phylogeny of Diplodia, Alves et al.
(2004) provided a detailed description of this species based on
one isolate from grapevines in Portugal (CBS 112553).
Species identification and numbers
Diplodia is a large genus and a search in MycoBank (2014)
revealed 1,317 names. Species in Diplodia were described, often
based on host association, which later resulted in a proliferation
of species names. According to Slippers et al. (2004d), host is
not of primary importance in species differentiation, thus, many
of the names in Diplodia are likely to be synonyms.
Based on DNA sequence data (single or multimarker) and
minor differences in conidial morphology, there are currently
Fungal Diversity (2014) 67:21–125
about 20 Diplodia species (de Wet et al. 2003; Alves et al.
2004, 2006; Gure et al. 2005; Damm et al. 2007; Lazzizera
et al. 2008; Pérez et al. 2010; Jami et al. 2012; Phillips et al.
2012, 2013; Linaldeddu et al. 2013; Lynch et al. 2013). The
phylogenetic analysis was performed based on up to date
holotype or ex-epitype sequence data available in GenBank
(Table 10).
Molecular phylogeny
Studies on the taxonomy and phylogeny of Diplodia were
hampered by a lack of an ex-type culture linked to the generic
type, D. mutila. A collection of D. mutila from Populus with
an ex-type culture was designated as epitype by Alves et al.
(2014). They obtained a large collection of Diplodia strains
from ash and other woody hosts showing V-shaped cankers
and branch dieback. These strains were identified based on
morphological characters and DNA sequence data. Since
2003 several new species have been described in Diplodia
and these species were recognized mainly from DNA sequence data. Diplodia scrobiculata was differentiated from
D. sapinea on the basis of multiple gene genealogies inferred
from six protein coding genes and six microsatellite loci (de
Wet et al. 2003). Diplodia africana (Damm et al. 2007),
D. olivarum (Lazzizera et al. 2008) and D. cupressi (Alves
et al. 2006) have been differentiated from D. mutila on the
basis of formation of distinct clades in phylogenies based on
ITS and TEF sequence data and due to their unique conidial
morphology (Phillips et al. 2012).
Combined morphological and phylogenetic analyses of
DNA sequence data from ITS and TEF (Alves et al. 2014)
showed that the Fraxinus isolates from Italy, Netherlands,
Portugal and Spain belong to three distinct species namely
Diplodia fraxini, D. mutila and D. subglobosa. The phylogenetic tree constructed with holotype or ex-epitype sequences is
presented in Fig. 11.
Recommended genetic markers
&
&
LSU and SSU–generic level
ITS, TEF and β-tubulin–species level
ITS, TEF and β-tubulin are the common genetic markers
used in identification of Diplodia species. Combined ITS and
TEF genes provide satisfactory resolution for resolving species.
Dothiorella
Background
Dothiorella (Botryosphaeriaceae) was proposed by Saccardo
in 1880 (Crous and Palm 1999) with D. pyrenophora as the
Fungal Diversity (2014) 67:21–125
51
Table 9 Diaporthe. Details of the isolates used in the phylogenetic tree
Species
Isolate
Host
GeneBank accession numbers
ITS
β-tubulin
TEF 1-α
CAL
Diaporthe acaciigena
D. alleghaniensis
D. alnea
D. ambigua
D. ampelina
D. amygdali
D. anacardii
D. angelicae
D. aquatica
D. arecae
D. arengae
D. aspalathi
D. australafricana
D. beilharziae
CBS 129521*
CBS 495.72*
CBS 146.46*
CBS 114015*
CBS 114016*
CBS 126679*
CBS 720.97*
CBS 111592*
IFRDCC 3051*
CBS 161.64*
CBS 114979*
CBS 117169*
CBS 111886*
BRIP 54792*
Acacia retinodes
Betula alleghaniensis
Alnus sp.
Pyrus communis
Vitis vinifera
Prunus dulcis
Anacardium ocidentale
Heracleum sphondylium
–
Areca catechu
Arenga engleri
Aspalathus linearis
Vitis vinifera
Indigofera australis
KC343005
KC343007
KC343008
KC343010
AF230751
KC343022
KC343024
KC343027
JQ797437
KC343032
KC343034
KC343036
KC343038
JX862529
KC343973
KC343975
KC343976
KC343978
JX275452
KC343990
KC343992
KC343995
–
KC344000
KC344002
KC344004
KC344006
KF170921
KC343731
KC343733
KC343734
KC343736
AY745056
AY343748
KC343750
KC343753
–
KC343758
KC343760
KC343762
KC343764
JX862535
KC343247
KC343249
KC343250
KC343252
AY230751
KC343264
KC343266
KC343269
–
KC343274
KC343276
KC343278
KC343280
–
D. bicincta
D. brasiliensis
D. caulivora
D. celastrina
D. citri
D. citriasiana
D. citrichinensis
D. crotalariae
D. cuppatea
CBS 121004*
CBS 133183*
CBS 127268*
CBS 139.27*
CBS 135422*
ZJUD 30*
ZJUD 34*
CBS 162.33*
CBS 117499*
Juglans sp.
Aspidosperma tomentosum
Glycine max
Celastrus sp
Citrus sp.
Citrus sp.
Citrus sp.
Crotalaria spectabilis
KC343134
KC343042
KC343045
KC343047
KC843311
JQ954645
JQ954648
KC343056
KC344102
KC344010
KC344013
KC344015
KC843187
KC357459
KC344024
KC343860
KC343768
KC343771
KC343773
KC843071
JQ954663
JQ954666
KC343782
KC343376
KC343284
KC343287
KC343289
KC843157
KC357491
KC357494
KC343298
D. cynaroidis
D. cytosporella
D. endophytica
D. eres
P. cotoneastri
D. fraxini-angustifoliae
D. foeniculina
D. foeniculina
D. foeniculina
CBS 122676*
FAU461*
CBS 133811*
AR5193*
CBS 439.82*
BRIP 54781*
CBS 123208*
CBS 123209*
CBS 187.27 *
Aspalathus linearis
Protea cynaroides
Citrus limon
Schinus terebinthifolius
Ulmus Sp.
Cotoneaster sp.
Fraxinus angustifolia
Foeniculum vulgare
Foeniculum vulgare
Camellia sinensis
KC343057
KC343058
KC843307
KC343065
KJ210529
KC343090
JX862528
KC343104
KC343105
KC343107
KC344025
KC344026
KC843221
KC343065
KJ420799
KC344058
KF170920
KC344072
KC344073
KC344075
KC343783
KC343784
KC843116
KC343791
KJ210550
KC343816
JX862534
KC343830
KC343831
KC343833
KC343299
KC343300
KC843141
KC343307
KJ434999
KC343332
–
KC343346
KC343347
KC343349
D. ganjae
D. gulyae
D. helianthi
D. helicis
D. hickoriae
D. hongkongensis
D. inconspicua
D. infecunda
D. kochmanii
D. kongii
D. longispora
D. lusitanicae
D. mayteni
CBS 180.91*
BRIP 54025*
CBS 592.81*
AR5211*
CBS 145.26*
CBS 115448*
CBS 133813*
CBS 133812*
BRIP 54033*
BRIP 54031*
CBS 194.36*
CBS 123212*
Cannabis sativa
Helianthus annuus
Helianthus annuus
Hedera helix
Carya glabra
Dichroa febrífuga
Maytenus ilicifolia
Schinus terebinthifolius
Helianthus annuus
Helianthus annuus
Ribes sp.
Foeniculum vulgare
KC343112
JF431299
KC343115
KJ210538
KC343118
KC343119
KC343123
KC343126
JF431295
JF431301
KC343135
KC343136
KC344080
–
KC344083
KJ420828
KC344086
KC344087
KC344091
KC344094
–
–
KC344103
KC344104
KC343838
JN645803
KC343841
KJ210559
KC343844
KC343845
KC343849
KC343852
JN645809
JN645797
KC343861
KC343862
KC343354
–
KC343357
KJ435043
KC343360
KC343361
KC343365
KC343852
–
–
KC343377
KC343378
CBS 133185*
CBS 507.78 *
CBS 129519*
Maytenus ilicifolia
Glycine soja
Musa sp.
KC343139
KC343141
KC343143
KC344107
KC344109
KC344111
KC343865
KC343867
KC343869
KC343381
KC343383
KC343385
D. melonis
D. musigena
52
Fungal Diversity (2014) 67:21–125
Table 9 (continued)
Species
Isolate
Host
GeneBank accession numbers
ITS
β-tubulin
TEF 1-α
CAL
D. neoarctii
D. nothofagi
D. novem
D. oxe
D. paranensis
D. pascoei
D. perjuncta
D. pseudomangiferae
D. pseudophoenicicola
D. psoraleae
D. psoraleae-pinnatae
D. pterocarpi
D. pterocarpicola
D. pulla
D. raonikayaporum
D. rudis
D. rudis
D. saccarata
CBS 109490*
BRIP 54801*
CBS 127270*
CBS 133186*
CBS 133184*
BRIP 54847*
CBS 109745*
CBS 101339*
CBS 462.69*
CBS 136412*
CBS 136413
MFLUCC 10-0571*
MFLUCC 10-0580*
CBS 338.89*
CBS 133182*
CBS 109291*
CBS 113201*
CBS 116311*
Ambrosia trifida
Nothofagus cunninghamii
Glycine max
Maytenus ilicifolia
Maytenus ilicifolia
Persea americana
Ulmus glabra
Mangifera indica
Mangifera indica
Psoralea pinnata
Psoralea pinnata
Pterocarpus indicus
Pterocarpus indicus
Hedera helix
Spondias mombin
Laburnum anagyroides
Vitis vinifera
Protea repens
KC343145
JX862530
KC343155
KC343164
KC343171
JX862532
KC343172
KC343181
KC343183
KF777158
KF777159
JQ619899
JQ619887
KC343152
KC343188
KC843331
KC343234
KC343190
KC344113
KF170922
KC344123
KC344132
KC344139
KF170924
KC344140
KC344149
KC344151
KF777251
KF777252
JX275460
JX275441
KC344120
KC344156
KC843177
KC344202
KC344158
KC343871
JX862536
KC343881
KC343890
KC343897
JX862538
KC343898
KC343907
KC343909
KF777245
–
JX275416
JX275403
KC343878
KC343914
KC843090
KC343960
KC343916
KC343387
–
KC343397
KC343406
KC343413
–
KC343414
KC343423
KC343425
–
–
JX197451
JX197433
KC343394
KC343430
KC843146
KC343476
KC343432
D. salicicola
D. schini
D. sclerotioides
D. siamensis
BRIP 54825*
CBS 133181*
CBS 296.67*
MFLUCC 10-0573a*
Salix purpurea
Schinus terebinthifolius
Cucumis sativus
Dasymaschalon sp.
JX862531
KC343191
KC343193
JQ619879
JX862531
KC344159
KC344161
JX275429
JX862537
KC343917
KC343919
JX275393
–
KC343433
KC343435
D. terebinthifolii
D. thunbergii
D. toxica
Diaporthella corylina
P. lithocarpus
P. mahothocarpus
P. ternstroemia
CBS 133180*
MFLUCC 10-0576*
CBS 534.93*
CBS 121124*
CGMCC 3.15175*
CGMCC 3.15181*
CGMCC 3.15183*
Schinus terebinthifolius
Thunbergia grandifolia
Lupinus angustifolius
Corylus sp.
Lithocarpus glabra
Lithocarpus glabra
Ternstroemia gymnanthera
KC343216
JQ619893
KC343220
KC343004
KC153104
KC153096
KC153098
KC344184
JX275449
KC344188
KC343972
–
–
–
KC343942
JX275409
KC343946
KC343730
KC153095
KC153087
KC153089
–
KC343458
JX197440
KC343462
KC343246
–
–
–
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
generic type. The delimitation of the genus has been in a state
of flux since it was introduced, and detailed explanations of its
taxonomy have been given by Sutton (1977), Crous and Palm
(1999) and Phillips et al. (2008, 2013). Crous and Palm (1999)
examined the holotype of D. pyrenophora and synonymised
Dothiorella under Diplodia based on a broad morphological
concept of Diplodia. That treatment was followed by Denman
et al. (2000), Zhou and Stanosz (2001) and Slippers et al.
(2004a). Phillips et al. (2005) re-examined the type of
D. pyrenophora and found that the conidia become brown
and 1-septate when they are still attached to the conidiogenous
cells, while in Diplodia the conidia are hyaline and become
dark and septate only after discharge from the conidiomata.
Crous et al. (2006) confirmed these morphological differences
by re-examining types of both Diplodia and Dothiorella. The
sexual state of the species is rarely found in nature and no
sexual morph was formed in culture for any of the species,
except for D. sarmentorum and D. iberica. Therefore,
differentiation of species is mostly derived based on the
asexual morphs and cultural characteristics.
Species identification and numbers
As members of Botryosphaeriaceae, species of Dothiorella are
known as endophytes, pathogens and saprobes in association
with various woody plants, and species in Dothiorella were
Fig. 10 Phylogram generated from parsimony analysis based on
combined ITS, EF1-α, β- tubulin, and CAL sequenced data of
Diaporthe. Parsimony bootstrap support values and Bayesian posterior
probabilities greater than 50 % are indicated above the nodes. The ex-type
(ex-epitype) and voucher strains are in bold. The tree is rooted with
Diaporthella corylina CBS 121124
Fungal Diversity (2014) 67:21–125
53
54
Fungal Diversity (2014) 67:21–125
Table 10 Diplodia. Details of the isolates used in the phylogenetic tree
Species
Isolate no.
Host
GenBank
ITS
TEF
β-tubulin
Diplodia africana
D. agrifolia
D. alatafructa
D. allocellula
D. bulgarica
D. corticola
D. cupressi
D. fraxini
D. intermedia
D. malorum
D. mutila
D. olivarum
D. sapinea
D. pseudoseriata
CBS 120835*
CBS 132777*
CBS 124931*
CBS 130408*
CBS 124254*
CBS 112549*
CBS 168.87*
CBS 136010*
CBS 124462*
CBS 124130*
CBS 112553*
CBS 121887*
CBS 393.84*
CBS 124906*
Prunus persica
Quercus agrifolia
Pterocarpus angolensis
Acacia karroo
Malus sylvestris
Quercus suber
Cupressus sempervirens
Fraxinus angustifolia
Malus sylvestris
Malus sylvestris
Vitis vinifera
Olea europaea
Pinus nigra
Blepharocalyx salicifolius
EF445343
JN693507
FJ888460
JQ239397
GQ923853
AY259100
DQ458893
KF307700
GQ923858
GQ923865
AY259093
EU392302
DQ458895
EU080927
EF445382
JQ517317
FJ888444
JQ239384
GQ923821
AY573227
DQ458878
KF318747
GQ923826
GQ923833
AY573219
EU392279
DQ458880
EU863181
–
JQ411459
–
JQ239378
–
DQ458853
DQ458861
–
–
–
DQ458850
HQ660079
–
–
D. quercivora
D. rosulata
D. scrobiculata
D. seriata
D. subglobosa
D. tsugae
Lasiodiplodia theobromae
CBS 133852*
CBS 116470*
CBS 109944*
CBS 112555*
CBS 124133*
CBS 418.64*
CBS 164.96*
Quercus canariensis
Prunus africana
Pinus greggii
Vitis vinifera
Lonicera nigra
Tsuga heterophylla
Fruit along coral reef coast
JX894205
EU430265
DQ458899
AY259093
GQ923856
DQ458888
AY640255
JX894229
EU430267
DQ458884
AY573219
GQ923824
DQ458873
AY640258
–
EU673132
AY624258
DQ458856
–
DQ458855
EU673110
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
mostly described based on host association, much as for other
members of Botryosphaeriaceae. This led to the introduction of
many species names, and there are 368 epithets for Dothiorella
in Index Fungorum (2014) and 393 species names in
MycoBank (2014). Slippers et al. (2013) suggested that host
association should not be considered an important factor
in species definition of the Botryosphaeriaceae, therefore
most of these names are likely synonyms. There are 19
described species with available cultures, and with the
exception of D. sarmentorum all have been described
after 2005. The phylogenetic analysis was performed
based on up to date holotype or ex-epitype sequence data
available in GenBank (Table 11).
Do. symphoricarpa (the type species of Dothidotthia) belongs
in a distinct family within the Pleosporales, while
D. sarmentorum, D. iberica and D. viticola fall within
two separate genera in the Botryosphaeriaceae and a new
genus, Spencermartinsia was introduced to accommodate
D. viticola. Phillips et al. (2013) listed all cultures of
available Dothiorella species, and provided a key to
species, as well as a phylogenetic tree. Abdollahzadeh
et al. (2014) introduced five new Dothiorella species which
were associated with woody plants in Iran, New Zealand,
Portugal and Spain. The phylogenetic tree constructed with
holotype or ex-epitype sequences is presented in Fig. 12.
Recommended genetic markers
Molecular phylogeny
&
Phillips et al. (2005) broadened the concept of Botryosphaeria
and included Dothiorella in Botryosphaeria based on ITS
analysis. Crous et al. (2006) recognised ten lineages within
Botryosphaeriaceae corresponding to different genera based
on phylogenetic analysis of 28S rDNA, and the three species
D. iberica, D. sarmentorum and D. viticola formed a clade
within Botryosphaeriaceae. These were assigned to
Dothidotthia. Subsequently, Phillips et al. (2008) showed that
&
&
ITS–placement within the Botryosphaeriaceae (the generic level), and also some specific delineation.
TEF–the generic level and inter-specific delineation.
β-tubulin–inter-specific delineation.
Slippers et al. (2013) suggested that all of the known
species of Dothiorella in culture can be separated based solely
on ITS, but bootstrap support values for some of the internal
nodes are quite low. Due to the studies on the other members
Fungal Diversity (2014) 67:21–125
55
Fig. 11 Phylogram generated
from parsimony analysis based on
combined ITS, TEF and βtubulin sequenced data of
Diplodia. Parsimony bootstrap
support values and Bayesian
posterior probabilities greater
than 50 % are indicated above the
nodes. The ex-type (ex-epitype)
and voucher strains are in bold.
The tree is rooted with
Lasiodiplodia theobromae CBS
164.96
of Botryosphaeriaceae, therefore, we strongly recommend
that it is necessary to combine ITS and TEF (or intended βtubulin gene) when molecular studies are carried out on
Dothiorella.
Fusarium
Background
The genus Fusarium was described by Link (1809) and later
became a sanctioned name (Fries 1821). It is based on the type
species Fusarium sambucinum (Nirenberg 1995). Species in
Fusarium were described largely on the basis of the morphology of the canoe shaped septate conidia produced by most
species as well as the shape and formation of other asexual
spores Leslie and Summerell 2006). The sexual morphs (ascospores produced in perithecia) have played little role in the
differentiation of most species as they are rare, if produced at
all (Seifert 2001). Fusarium includes a number of species that
are very important plant pathogens, some that are potent
producers of an array of mycotoxins and several species or
species complexes that are involved in diseases of humans
(Leslie and Summerell 2006). There are also many species
that are apparently endophytic in plants as well as species that
are saprobes in soil and in organic matter.
Two species, F. graminearum and F. oxysporum, were
included in an assessment of the top 10 fungal plant
pathogens by Dean et al. (2012). Fusarium graminearum
is the cause of head blight of wheat (Windels 2000), and
F. oxysporum causes wilt diseases in a range of crops
including bananas, tomatoes and other vegetables as well
as cotton (Beckman 1987). Other species of Fusarium
cause stalk and cob rots in maize and sorghum, canker
diseases in woody plants and root and crown diseases
across a vast spectrum of plant species (Summerell et al.
56
Table 11 Dothiorella. Details
of the isolates used in the
phylogenetic tree
Ex-type (ex-epitype) strains are
bolded and marked with an * and
voucher stains are bolded
Fungal Diversity (2014) 67:21–125
Species name
Strain no.
Host
ITS
TEF
Dothiorella americana
D. americana
D. brevicollis
D. brevicollis
D. casuarinae
CBS 128309*
CBS 128310
CBS 130411*
CBS 130412
CBS 120688*
Vitis sp.
Vitis sp.
Acacia karroo
Acacia karroo
Casuarina sp.
HQ288218
HQ288219
JQ239403
JQ239404
DQ846773
HQ288262
HQ288263
JQ239390
JQ239391
DQ875331
D. casuarinae
D. dulcispinae
D. dulcispinae
D. dulcispinae
D. iberica
D. iberica
D. iberica
D. iranica
D. longicollis
D. longicollis
D. moneti
D. moneti
D. parva
D. parva
D. pretoriensis
D. pretoriensis
CBS 120690
CBS 130413*
CBS 130414
CBS 130415
CBS 115041*
CBS 113188
CAA 005
IRAN1587C*
CBS 122068*
CBS 122067
MUCC 505*
MUCC 507
IRAN1579C*
IRAN1585C
CBS 130404*
CBS 130403
Casuarina sp.
Acacia karroo
Acacia karroo
Acacia karroo
Quercus ilex
Quercus ilex
Quercus ilex
Olea europaea
Lysiphyllum cunninghamii
Lysiphyllum cunninghamii
Acacia rostellifera
Acacia rostellifera
Corylus avellana
Corylus avellana
Acacia karroo
Acacia karroo
DQ846774
JQ239400
JQ239401
JQ239402
AY573202
AY573198
EU673312
KC898231
EU144054
EU144052
EF591920
EF591922
KC898234
KC898235
JQ239405
JQ239406
DQ875333
JQ239387
JQ239388
JQ239389
AY573222
EU673278
EU673279
KC898214
EU144069
EU144067
EF591971
EF591973
KC898217
KC898218
JQ239392
JQ239393
D. prunicola
D. Santali
IRAN1541*
MUCC 509*
Prunus dulcis
Santalum acuminatum
EU673313
EF591924
EU673280
EF591975
D. santali
D. sarmentorum
D. sarmentorum
D. sempervirentis
D. sempervirentis
D. striata
D. striata*
D. thailandica
D. thripsita
D. uruguayensis
D. vidmadera
D. vidmadera
D. vidmadera
Spencermartinsia viticola
MUCC 508
IMI 63581b*
CBS 115038
IRAN1581C
IRAN1583C*
ICMP16819
ICMP16824*
MFLUCC 11-0438*
BRIP 51876*
CBS 124908*
DAR78992*
DAR78993
DAR78994
CBS 117009*
Santalum acuminatum
Ulmus sp.
Malus pumila
Cupressus sempervirens
Cupressus sempervirens
Citrus sinensis
Citrus sinensis
Unknown
Acacia harpophylla
Hexalamis edulis
Vitis vinifera
Vitis vinifera
Vitis vinifera
Vitis vinifera
EF591923
AY573212
AY573206
KC898237
KC898236
EU673320
EU673321
JX646796
FJ824738
EU080923
EU768874
EU768876
EU768877
AY905554
EF591974
AY573235
AY573223
KC898220
KC898219
EU673287
EU673288
JX646861
2011). Species of Fusarium produce a very large number
of secondary metabolites, but two toxin groups, trichothecenes and fumonisins, are particularly detrimental to livestock and humans (through consumption) and as such are
heavily regulated in many parts of the world (Desjardins
2005). As a result of the importance of these diseases, the
genus is one of the most heavily researched of all genera
of fungi and an enormous body of work on all facets of
its biology exists (Leslie and Summerell 2006).
Several sexual morph genera are associated with
Fusarium, the most important of which is Gibberella
EU863180
EU768881
EU768882
EU768883
AY905559
(Desjardins 2003). Most Fusarium species, particularly
the plant pathogenic species, have a Gibberella sexual
morph. Other sexual morph genera include Albonectria,
Haematonectria and Neocosmospora as well as a number of other generic names (Gräfenhan et al. 2011).
With the changes to the International Code of
Nomenclature for Algae, Fungi and Plants providing
the opportunity to have a single name for fungi of this
nature there has been a strong consensus amongst the
community of researchers working on Fusarium that
this name be used for all the fungi in the so-called
Fungal Diversity (2014) 67:21–125
57
Fig. 12 Phylogram generated
from parsimony analysis based on
combined ITS and TEF
sequenced data of Dothiorella.
Parsimony bootstrap support
values greater than 50 % are
indicated above the nodes, and
branches with Bayesian posterior
probabilities greater than 0.95 are
given in bold. The ex-type (exepitype) and voucher strains are in
bold. The scale bar indicates ten
changes. The tree is rooted with
Spencermartinsia viticola CBS
117009
terminal Fusarium clade (Geiser et al. 2013). The end
result of this is that species of Fusarium such as
F. solani, F. decemcellulare and F. dimerum are included with species with Gibberella sexual morphs in the
current generic definition of Fusarium (Geiser et al.
2013).
Species identification and numbers
It is difficult to accurately quantify the number of extant,
currently recognized species of Fusarium. Over 1,500
names are listed in MycoBank; Leslie and Summerell
(2006) documented 72 species, although this was not
intended as a monograph, and many of species have been
described in the intervening period (e.g. Jacobs et al. 2010;
Laurence et al. 2011; Schroers et al. 2009; Walsh et al.
2010). Recent investigations into a number of important
species (e.g. F. graminearum, F. incarnatum, F. oxysporum,
F. solani) have provided evidence that they are complexes
of phylogenetically distinct lineages that have been, or will
eventually be described as species (Aoki et al. 2005;
O’Donnell et al. 2004, 2008, 2009).
Molecular phylogeny
There has been substantial work on understanding the phylogenetic relationships within Fusarium, and in defining generic
boundaries (e.g. Geiser et al. 2013; O’Donnell et al. 2013).
This has provided refined concepts for several important plant
p a t h o g e n i c s p e c i e s ( e . g . F. g r a m i n e a r u m ,
F. pseudograminearum, F. subglutinans, F. verticillioides) and
it has also shown that several important plant pathogens
(especially F. oxysporum and F. solani) are in fact
species complexes (Laurence et al. 2014; O’Donnell
et al. 2008). A genus-wide phylogeny was inferred
using the RNA polymerase largest subunit (RPB1)
and RNA polymerase second largest subunit (RPB2)
(O’Donnell et al. 2013), as these genes are very informative from a phylogenetic perspective across the whole
genus (Table 12, Fig. 13)
58
Fungal Diversity (2014) 67:21–125
Table 12 Fusarium. Details of the isolates used in the phylogenetic tree
Table 12 (continued)
Species
Species
Isolate
GenBank accession numbers
RPB1
RPB2
Fusarium falciforme
F. solani
Fusarium sp.
F. ambrosium
F. phaseoli
F. virguliforme
Fusarium sp.
Fusarium sp.
Fusarium sp.
Fusarium sp.
F. aywerte
F. longipes
F. longipes
F. longipes
NRRL 43529
NRRL 45880
NRRL 22436
NRRL 20438
NRRL 22276
NRRL 31041
NRRL 22632
NRRL 13444
NRRL 28578
NRRL 13338
NRRL 25410
NRRL 13368
NRRL 13374
NRRL 20723
JX171541
JX171543
JX171497
JX171470
JX171495
JX171530
JX171501
JX171454
JX171526
JX171447
JX171513
JX171448
JX171450
JX171483
JX171653
JX171655
JX171610
JX171584
JX171608
JX171643
JX171614
JX171568
JX171639
JX171561
JX171626
JX171562
JX171564
JX171596
Fusarium cf. compactum
Fusarium sp.
F. sambucinum
F. venenatum
F. poae
F. sporotrichioides
F. langsethiae
F. armeniacum
F. asiaticum
F. graminearum
F. culmorum
F. pseudograminearum
F. equiseti
F. lacertarum
F. equiseti
Fusarium sp.
Fusarium sp.
F. subglutinans
NRRL 13829
NRRL 31008
NRRL 22187
NRRL 22196
NRRL 13714
NRRL 3299
NRRL 54940
NRRL 6227
NRRL 13818
NRRL 31084
NRRL 25475
NRRL 28062
NRRL 13402
NRRL 20423
NRRL 20697
NRRL 26417
NRRL 32175
NRRL 22016
JX171460
JX171529
JX171493
JX171494
JX171458
JX171444
JX171550
JX171446
JX171459
JX171531
JX171515
JX171524
JX171452
JX171567
JX171481
JX171522
JX171532
JX171486
JX171574
JX171642
JX171606
JX171607
JX171572
JX171558
JX171662
JX171560
JX171573
JX171644
JX171628
JX171637
JX171566
JX171581
JX171595
JX171635
JX171645
JX171599
F. circinatum
F. guttiforme
F. fujikuroi
F. proliferatum
F. mangiferae
F. sacchari
F. verticillioides
F. thapsinum
F. xylarioides
Fusarium sp.
F. nisikadoi
F. miscanthi
F. gaditjirrii
F. lyarnte
F. commune
NRRL 25331
NRRL 22945
NRRL 13566
NRRL 22944
NRRL 25226
NRRL 13999
NRRL 20956
NRRL 22045
NRRL 25486
NRRL 52700
NRRL 25179
NRRL 26231
NRRL 45417
NRRL 54252
NRRL 28387
JX171510
JX171505
JX171456
JX171504
JX171509
JX171466
JX171485
JX171487
JX171517
JX171544
JX171507
JX171521
JX171542
JX171549
JX171525
JX171623
JX171618
JX171570
JX171617
JX171622
JX171580
JX171598
JX171600
JX171630
JX171656
JX171620
JX171634
JX171654
JX171661
JX171638
Isolate
GenBank accession numbers
RPB1
RPB2
F. inflexum
F. oxysporum
F. oxysporum
F. foetens
Fusarium sp.
F. redolens
F. hostae
Fusarium sp.
F. burgessii
F. beomiforme
F. concolor
F. anguioides
Fusarium sp.
F. babinda
Fusarium sp.
F. torulosum
F. flocciferum
F. tricinctum
NRRL 20433
NRRL 25387
NRRL 34936
NRRL 38302
NRRL 25184
NRRL 22901
NRRL 29889
RBG 5116
RBG 5319
NRRL 25174
NRRL 13459
NRRL 25385
NRRL 25533
NRRL 25539
NRRL 22566
NRRL 22748
NRRL 25473
NRRL 25481
JX171469
JX171512
JX171533
JX171540
JX171508
JX171503
JX171527
KJ716216
KJ716217
JX171506
JX171455
JX171511
JX171518
JX171519
JX171500
JX171502
JX171514
JX171516
JX171583
JX171625
JX171646
JX171652
JX171621
JX171616
JX171640
HQ646395
HQ646392
JX171619
JX171569
JX171624
JX171631
JX171632
JX171613
JX171615
JX171627
JX171629
F. nurragi
F. heterosporum
F. buharicum
F. sublunatum
F. lateritium
F. sarcochroum
F. stilbioides
Fusarium sp.
F. dimerum
F. lunatum
NRRL 36452
NRRL 20693
NRRL 13371
NRRL 13384
NRRL 13622
NRRL 20472
NRRL 20429
NRRL 54149
NRRL 20691
NRRL 36168
JX171538
JX171480
JX171449
JX171451
JX171457
JX171472
JX171468
JX171548
JX171478
JX171536
JX171650
JX171594
JX171563
JX171565
JX171571
JX171586
JX171582
JX171660
JX171592
JX171648
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher
stains are bolded
Recommended genetic markers
The recommended and most frequently used gene for identification of species of Fusarium is the translation elongation
factor 1α gene (TEF) and this is generally used for routine
identifications, effectively performing a DNA barcoding function, and forms a significant component of the FUSARIUMID database (http://isolate.fusariumdb.org/; Geiser et al.
2004). This database provides a similar facility to GenBank
but is based on sequences from accurately identified and
validated cultures held in reference collections (Geiser et al.
2004). Using a standard approach (Summerell et al. 2003),
sequencing the TEF gene and comparing the sequence with
the FUSARIUM-ID database makes it possible to rapidly and
accurately identify most pathogenic Fusarium species. The
ITS region is less informative in Fusarium from both a
Fungal Diversity (2014) 67:21–125
59
Fig. 13 Fusarium The single most parsimonious tree inferred from a
combined RPB1 and RPB2 dataset indicating the phylogenetic relationships among species complexes in the genus Fusarium. Branches with
bootstrap intervals greater than 70 % and Bayesian posterior probabilities
greater than 0.95 are indicated in bold. The NRRL (Agricultural Research
Service Culture Collection, Peoria, Illinois USA) and RBG (Royal
Botanic Gardens Trust Culture Collection, Sydney, New South Wales,
Australia) numbers are indicated for all reference taxa
barcoding and phylogenetic perspective and as a result it has
not been used extensively. This is primarily because there are
nonorthologous copies of ITS2 that are incongruent with
species phylogenies derived from other unlinked loci in species of economic importance {O’Donnell and Cigelnik (1997)
#1278}. As a consequence it is not recommended that ITS be
used for differentiation or identification of Fusarium species
(Summerell et al. 2003).
Gilbertella
Background
The monotypic genus Gilbertella belongs to the family
Choanephoraceae and subfamily Gilbertelloideae (Mucorales,
former Zygomycota). It was established by Hesseltine (1960) for
species described earlier as Choanephora persicaria by Eddy
60
Fungal Diversity (2014) 67:21–125
(1925), and consequently the type species of the genus is
Gilbertella persicaria. Benny (1991) proposed a new family,
Gilbertellaceae to accommodate this genus. Currently, the genus
belongs to the family Choanephoraceae and subfamily
Gilbertelloideae that can be distinguished from
Choanephoroideae (Voigt and Kirk 2012) by ornamented zygospores and opposed suspensors (Voigt 2012). Although
G. persicaria was originally described as Choanephora
persicaria (Eddy 1925), its separate position within the family
has been confirmed in several studies (Papp et al. 2003;
Hoffmann et al. 2013).
In tropical and subtropical regions Gilbertella is a common
postharvest pathogen, causing rots of pears (Mehrotra 1963a),
peaches (Hesseltine 1960; Mehrotra 1963b; Ginting et al.
1996) and tomatoes (Mehrotra 1966). It was reported by
Butler et al. (1960) and Hesseltine (1960) from mulberry
(Morus sp.) in USA. It was also recently isolated from pitaya
fruits (Hylocereus undatus, Cactaceae) in Japan (Taba et al.
2011) and China (Guo et al. 2012).
enough for correct species identification. Moreover, the morphological identification may be easily confirmed by ITS
sequencing (Table 13, Fig. 14).
Molecular phylogeny
The phylogenetic relationships based on the complete ITS
region of Gilbertella representatives and related Mucorales
taxa was completed by Papp et al. (2003). All Gilbertella
cultures available in the CBS culture collection have been
sequenced for their ITS region and were included in a molecular analysis by Walther et al. (2013). These studies showed
that the universal fungal DNA barcoding marker–the ITS
region (Schoch et al. 2012)–is sufficient for Gilbertella species identification (Fig. 16). The multi-marker phylogenetic
analysis including representatives of this genus performed by
Hoffmann et al. (2013), confirmed a distinct, well-supported
position of Gilbertella within Choanephoraceae family.
Recommended genetic markers
Species identification and numbers
&
Currently, Gilbertella persicaria is the only species within the
genus. Although another species–Gilbertella hainanensis–has
been described (Cheng and Hu 1965), after recent molecular
studies of its ITS sequence, it is not currently recognized as a
separate species (Walther et al. 2013). Two varieties of
G. persicaria have been described: G. persicaria var. persicaria
and G. persicaria var. indica, however only the former was
accepted in the monograph published by Benny (1991).
Gilbertella persicaria produces sporangia with a persistent
wall that ruptures at preformed sutures in two halves.
Ellipsoid, smooth-walled, hyaline sporangiospores with polar
appendages are released in droplet of fluid. Light brown
ornamented zygospores are formed on opposed suspensors
(Hesseltine 1960). Examination of morphology is usually
Table 13 Gilbertella. Details
of the isolates used in the
phylogenetic tree
Ex-type (ex-epitype) strains are
bolded and marked with an * and
voucher stains are bolded
&
The internal transcribed spacer (ITS) region–generic and
species level
The large and small subunits (LSU and SSU) of nrDNA–
placement within the Mucorales order, higher-level
phylogeny
Lasiodiplodia
Background
Lasiodiplodia (Botryosphaeriaceae) was introduced by Ellis
in 1894 with L. tubericola as the type species. Clendenin
(1896) provided a description of the genus and the species,
but did not refer to any type or other specimens of the genus or
Species
Isolate
Host
GenBank no
Gilbertella persicaria
G. persicaria
G. persicaria
G. persicaria
G. persicaria
G. persicaria
G. persicaria
G. persicaria
G. persicaria
G. persicaria
Choanephora cucurbitarum
C. cucurbitarum
CBS 190.32*
CBS 785.97
CBS 442.64
CBS 325.71A
CBS 403.51
CBS 246.59
CBS 421.77
CBS 532.77
CBS 325.71D
CBS 565.91
CBS 120.25
CBS 150.51
Prunus persica
–
–
Saccharum officinarum
–
Trickling filter plant system
Soil
Dung of mouse
Wood
Dung of swine
–
–
HM999958
JN206218
JN206219
JN206220
JN206221
JN206222
JN206223
JN206224
JN206225
JN206226
JN206231
JN206232
Fungal Diversity (2014) 67:21–125
61
was performed based on up to date holotype or ex-epitype
sequence data available in GenBank (Table 14).
Molecular phylogeny
Fig. 14 Phylogram generated from Maximum likelihood analysis based
on ITS sequenced data of Gilbertella. Bootstrap support values greater
than 50 % are indicated above the nodes. The ex-type (ex-epitype) and
voucher strains are in bold
species. Pavlic et al. (2004) could not locate the types, nor find
any specimens from the original hosts or origins, but gave a
clear concept of the genus and the type. A new status for the
type species of Lasiodiplodia has been proposed by Phillips
et al. (2013) and they designated CBS 164.96 as ex-neotype
culture, and deposited a dried specimen as neotype with
convincing reasons, although this specimen was collected
from an unidentified fruit in Papua New Guinea, whereas
the type was collected in Ecuador on cocoa plant. Twenty
new species have been described since 2004; however the
generic application of the name, L. theobromae, has not been
resolved.
Denman et al. (2000) suggested that Lasiodiplodia could be
a possible synonym of Diplodia based on the ITS data
analysis. However, phylogenetic studies by Zhou and
Stanosz (2001), Slippers et al. (2004a) and Phillips et al.
(2008) show that it clusters separately from Diplodia. As
more genes and molecular data have become available,
more complex sections within Botryosphaeriaceae have
been resolved. By combining TEF and β-tubulin genes
with ITS, Phillips et al. (2005, 2008) reinstated the genus
Neodeightonia in the Diplodia/Lasiodiplodia complex and
also showed that the latter asexual genera are morphologically and phylogenetically distinct. Most of the known
species with available cultures have been described based
on at least two genetic markers (ITS, TEF/ β-tubulin). The
phylogenetic tree constructed with holotype or ex-epitype
sequences is presented in Fig. 15.
Recommended genetic markers
&
&
&
ITS–placement within the Botryosphaeriaceae (the generic level), and also some species-level delineation.
TEF–generic level and inter-specific delineation.
β-tubulin–generic level and inter-specific delineation,
mostly for inter-specific delineation.
In most cases, a combination of ITS and TEF will separate
all species and a minimal requirement for Lasiodiplodia species separation. However, for some groups, such as
L. theobromae, β-tubulin is needed.
Species identification and numbers
Mucor
Lasiodiplodia differs from Diplodia species in having striations on the conidia, and differs from Neodeightonia as
Lasiodiplodia has conidiomatal paraphyses. Barriopsis differs
as it has unique striate conidia, with the striations present on
immature, hyaline conidia. A sexual morph has been reported
for L. theobromae, which has been linked to Botryodiplodia
rhodina (Cooke) Arx, but this link has not been unequivocally
proven (Alves et al. 2008; Phillips et al. 2008). Phillips et al.
(2013) transferred Auerswaldia lignicola (Liu et al. 2012) to
Lasiodiplodia, and this is the only species where the asexual
morph and sexual have been definitively linked. There are 30
epithets of Lasiodiplodia recorded in Index Fungorum (2014)
and 32 species names in MycoBank (March 2014), and 24
species are currently kept in culture. Species can be differentiated based on conidial morphology (especially dimensions)
and morphology of the paraphyses. The phylogenetic analysis
Background
The genus Mucor belongs to the Mucoraceae, which is the
largest and the most diverse family within Mucorales (former
Zygomycota; Hoffmann et al. 2013). It was described by
Fresenius (1850). The type species of the genus is Mucor
mucedo, although the name Mucor had been used long before
also by other authors to describe species currently classified as
Rhizopus stolonifer (syn. Mucor mucedo L. 1753 or Mucor
mucedo (Tode) Pers. 1801).
There has been no comprehensive molecular phylogenetic
study in the genus Mucor and consequently its taxonomy is
still widely based on morphological characters. Mucor representatives produce nonapophysate sporangia arising directly
from the substrate and they do not form stolons. Rhizoids
62
Table 14 Lasiodiplodia. Details
of the isolates used in the
phylogenetic tree
Ex-type (ex-epitype) strains are
bolded and marked with an * and
voucher stains are bolded
Fungal Diversity (2014) 67:21–125
Species name
Strain no.
Host
ITS
TEF
Diplodia mutila
Lasiodiplodia brasiliense
L. brasiliense
L. brasiliense
L. brasiliense
L. citricola
L. citricola
L. crassispora
L. crassispora
L. egyptiacae
L. egyptiacae
L. euphorbicola
L. euphorbicola
L. gilanensis
L. gilanensis
L. gonubiensis
L. gonubiensis
L. hormozganensis
L. hormozganensis
L. iraniensis
L. jatrophicola
L. lignicola
L. lignicola
L. macrospora
L. mahajangana
L. mahajangana
L. margaritacea
L. margaritacea
L. marypalme
L. marypalme
L. marypalme
L. marypalme
L. missouriana
L. missouriana
L. parva
L. parva
L. plurivora
L. plurivora
L. pseudotheobromae
L. pseudotheobromae
L. rubropurpurea
L. rubropurpurea
L. subglobose
L. subglobosa
L. theobromae
L. theobromae
L. venezuelensis
L. venezuelensis
L. viticola
L. viticola
CBS 112553*
CMM 4015*
CMM 2320
CMM 2319
CMM 2314
CBS 124707*
CBS 124706
CBS 118741*
WAC 12534
CBS 130992*
BOT 29
CMM3609*
CMM3652
CBS 124704*
CBS 124705
CBS 115812*
CBS 116355
CBS 124709*
CBS 124708
CBS 124710*
CMM3610
MFLUCC 11-0435*
MFLUCC 11-0656
CMM3833*
CBS 124927*
CBS 124925
CBS 122519*
CBS 122065
CMM 2275*
CMM 2274
CMM 2272
CMM 2271
CBS 128311*
CBS 128312
CBS 456.78*
CBS 494.78
CBS 120832*
CBS 121103
CBS 116459*
CBS 447.62
CBS 118740*
WAC 12536
CMM3872*
CMM4046
CBS 164.96*
CBS 111530
CBS 118739*
WAC 12540
CBS 128313*
CBS 128315
Vitis vinifera
Mangifera indica
Mangifera indica
Mangifera indica
Mangifera indica
Citrus sp.
Citrus sp.
Santalum album
Eucalyptus urophylla
Mangifera indica
Mangifera indica
Jatropha curcas
Jatropha curcas
Unknown
Unknown
Syzigium cordatum
Syzigium cordatum
Olea sp.
Mangifera indica
Salvadora persica
Jatropha curcas
Unknown
Unknown
Jatropha curcas
Terminalia catappa
Terminalia catappa
Adansonia gibbosa
Adansonia gibbosa
Carica papaya
Carica papaya
Carica papaya
Carica papaya
Vitis vinifera
Vitis vinifera
Cassava-field soil
Cassava-field soil
Prunus salicina
Prunus salicina
Gmelina arborea
Citrus aurantium
Eucalyptus grandis
Eucalyptus grandis
Jatropha curcas
Jatropha curcas
Fruit on coral reef coast
Unknown
Acacia mangium
Acacia mangium
Vitis vinifera
Vitis vinifera
AY259093
JX464063
KC484814
KC484798
KC484813
GU945354
GU945353
DQ103550
DQ103551
JN814397
JN814401
KF234543
KF234554
GU945351
GU945352
AY639595
AY639594
GU945355
GU945356
GU945346
KF234544
JX646797
JX646798
KF234557
FJ900597
FJ900595
EU144050
EU144051
KC484843
KC484841
KC484842
KC484844
HQ288225
HQ288226
EF622083
EF622084
EF445362
AY343482
EF622077
EF622081
DQ103553
DQ103554
KF234558
KF234560
AY640255
EF622074
DQ103547
DQ103548
HQ288227
HQ288228
AY573219
JX464049
KC481544
KC481529
KC481543
GU945340
GU945339
EU673303
DQ103558
JN814424
JN814428
KF226689
KF226715
GU945342
GU945341
DQ103566
DQ103567
GU945343
GU945344
GU945334
KF226690
JX646862
JX646863
KF226718
FJ900643
FJ900641
EU144065
EU144066
KC481567
KC481565
KC481566
KC481568
HQ288267
HQ288268
EF622063
EF622064
EF445395
EF445396
EF622057
EF622060
EU673304
DQ103572
KF226721
KF226723
AY640258
EF622054
EU673305
DQ103569
HQ288269
HQ288270
Fungal Diversity (2014) 67:21–125
63
Fig. 15 Phylogram generated
from parsimony analysis based on
combined ITS and TEF
sequenced data of Lasiodiplodia.
Parsimony bootstrap support
values greater than 50 % are
indicated above the nodes, and
branches with Bayesian posterior
probabilities greater than 0.95 are
given in bold. The ex-type (exepitype) and voucher strains are in
bold. The scale bar indicates ten
changes. The tree is rooted with
Diplodia mutila CBS 112553
were also considered to be absent in Mucor, but it is now
known that they can be produced under certain conditions
(Walther et al. 2013).
Mucor representatives are saprotrophs that can be found
mainly in soil or on plant debris. They are also known as
postharvest plant pathogens, e.g. M. mucedo (Moline and
Millner 1981) and M. piriformis (Michailides and Spotts
1990a). In case of peach and nectarine rots, Michailides
and Spotts (1990b), Spotts (1990) and Michailides et al.
(1992) regarded flies (especially Drosophila melanogaster)
and nitidulid beetles (Carpophilus hemipterus and
C. freemani) as effective vectors. Mucor rot symptoms
include softening of juicy decayed tissue, often with a
sweet odour, lesions with a sharp margin and eventually
developing of grey mycelium with sporangia. Mucor isolated from several different plant hosts, angiosperms and
gymnosperms, monocots as well as dicotyledons. USDA
Fungus-Host Database reports 375 cases of Mucor infections from plants from approximately 40 countries in
Europe, Central and South-East Asia, Australia, Africa,
and North and South America (Farr and Rossman 2014).
Mucor circinelloides causes rots in tomatoes (Smith et al.
1976), mangoes (Johnson 2008), yam (Amusa et al. 2003)
and peaches (Restuccia et al. 2006). Mucor hiemalis can be
pathogenic on guavas (Kunimoto et al. 1977), carrots and
cassava (Snowdon 1991). Mucor piriformis is a destructive
pathogen of fresh strawberries (Snowdon 1990; Pitt and
Hocking 2009) and a major cause of rotting of coldstored pears, apples, peaches, nectarines and tomatoes
(Smith et al. 1979; Bertrand and Saulie-Carter 1980;
Michailides and Spotts 1986; Michailides 1991; Mari
et al. 2000; Pitt and Hocking 2009; Ukeh and Chiejina
2012), plums (Børve and Vangdal 2007), sweet persimmons (Kwon et al. 2004) and yams (Amusa and Baiyewu
1999; Iwama 2006). Mucor piriformis may infect the stem,
calyx or wounds on the skin of fruits (Michailides and
Spotts 1990a, b). Mucor mucedo was reported as important
postharvest pathogen of strawberries (Dennis and Davis
1977), and from tomatoes (Moline and Kuti 1984). Mucor
racemosus was noted causing soft rot of cherry tomato
fruits in Korea (Kwon and Hong 2005). Some Mucor
species (e.g. M. circinelloides) are also human opportunistic
pathogens, especially dangerous to immunodeficient patients (Walther et al. 2013).
64
Species identification and numbers
The last extensive studies of the genus Mucor (Schipper 1973,
1975) are from the pre-molecular era. Based on morphological
features and mating experiments Schipper (1976, 1978) recognized 39 species, 4 varieties and 11 formae. In the following
years further species were described (e.g. Watanabe 1994;
Zalar et al. 1997). Molecular phylogenetic analyses of the
entire Mucorales revealed the polyphyly of the genus (Voigt
and Wöstemeyer 2001; O’Donnell et al. 2001). The study of
Walther et al. (2013) on the genetic diversity within the
Mucorales based on sequences of the nuclear ribosomal internal transcribed spacer region (ITS) and the large ribosomal
subunit (LSU) strongly supported the polyphyly of Mucor.
The genus was split into several morphological groups differing in the size of the sporangia and the branching mode of the
sporangiophores that are widely in agreement with the
intrageneric classification of Schipper (1973). However, ?in
molecular analyses these groups are intermingled by other
sporangia-forming genera such as Pilaira und Pirella and
sporangiola-forming genera such as Ellisomyces,
Chaetocladium, Helicostylum and Thamnidium (Walther
et al. 2013). The position of the Mycotyphaceae and the
Choanephoraceae in relation to the Mucoraceae is still not
resolved (Hoffmann et al. 2013).
Recently, the introduction of new species or changes of
the taxonomic status were supported by sequence analyses
of the ITS and/or rDNA genes (Jacobs and Botha 2008;
Budziszewska et al. 2010; Álvarez et al. 2011; Madden
et al. 2011). Several studies on certain species or species
complexes (Li et al. 2011; Lu et al. 2013) or a particular
ecological group (Hermet et al. 2012) used multi-marker
approaches for phylogenetic species recognition in the
genus Mucor. However, a comprehensive study on the
entire genus is still lacking. As a consequence, species
and even generic boundaries are still unclear for Mucor.
Currently 58 species are recognised within the genus
(Walther et al. 2013) (Table 15, Fig. 16).
Fungal Diversity (2014) 67:21–125
was successfully used for multi-marker studies at the
species level (Li et al. 2011; Hermet et al. 2012; Lu
et al. 2013). Hermet et al. (2012) also used the fragment
of a mini-chromosome maintenance protein (MCM7)
and of the 20 S rRNA accumulation protein (tsr1).
The multi-marker analysis of the entire Mucorales including representatives of genus Mucor by Hoffmann
et al. (2013) were based on partial genes of actin and
the translation elongation factor 1-alpha in addition to
the rRNA genes.
Recommended genetic markers
&
&
&
&
The internal transcribed spacer (ITS)–genus and species
level
The RNA polymerase II largest subunit gene (RPB1)–
species level
The large and small subunits (LSU and SSU) of nrDNA–
placement within the Mucorales order, higher-level
phylogeny
The mini-chromosome maintenance proteins gene
(MCM7–higher-level phylogeny)
Neofusicoccum
Background
Pennycook and Samuels (1985) listed Fusicoccum parvum as
the asexual morph when they described Botryosphaeria
parvum. Neofusicoccum was introduced by Crous et al.
(2006) for species that have an asexual morph that occurs
with a “Dichomera” like synanamorph (morphologically similar, but phylogenetically distinct from Botryosphaeria). They
suggested the name as it provides more information of the
morphological state.
Species identification and numbers
Molecular phylogeny
The ITS region allows identification to species level for most
mucoralean representatives (Walther et al. 2013). Detailed
molecular species identification is currently not possible for
species complexes such as M. circinelloides or M. flavus
because of unclear species boundaries (Walther et al. 2013).
Along with the ITS region for species identification,
the LSU (e.g. Fig. 16, Álvarez et al. 2011) or the SSU
(e.g. Budziszewska et al. 2010) genes have frequently
been used in molecular phylogenetic analyses of Mucor
because the ITS is too variable to be confidently
aligned across the entire genus (Walther et al. 2013).
In addition, the RNA polymerase subunit gene (rpb1)
On the basis of conidial dimensions and pigmentation, pigment production in media and ITS sequence data, 22 species
are currently recognized in Neofusicoccum, although some of
th ese ch ar ac ters ha ve rec en tly be en que sti one d
(Abdollahzadeh et al. 2013). Four new species,
N. batangarum, N. cordaticola, N. kwambonambiense and
N. umdonicola were identified in this complex based on
congruence between genealogies of multiple genes (Pavlic
et al. 2009a, b; Begoude et al. 2010). Though many species
of Neofusicoccum are morphologically similar and can be
very difficult to distinguish from one another, an attempt has
been made to differentiate all species in a key by Phillips et al.
(2013) (Table 16).
Fungal Diversity (2014) 67:21–125
Table 15 Mucor. Details of the
isolates used in the phylogenetic
tree
65
Species
Isolate
Country of collection
GenBank accession no
Mucor abundans
M. aligarensis
CBS 521.66
Germany
JN206457
CBS 993.70*
UK
JN206461
M. amphibiorum
CBS 763.74*
Germany
HM849688
M. ardhlaengiktus
CBS 210.80*
India
JN206504
M.azygosporus
CBS 292.63*
USA
JN206497
M. bacilliformis
CBS 251.53*
USA
JN206451
M. bainieri
CBS 293.63*
India
JN206424
M. brunneogriseus1
CBS 129.41
Netherlands
M. circinelloides f. circinelloides
CBS 195.68*
Netherlands
M. circinelloides f. griseocyanus
CBS 116.08
Norway
JN206421
M. circinelloides f. janssenii
CBS 205.68*
South Africa
JN206425
M.circinelloides f. lusitanicus
CBS 968.68
–
JN206419
M. ctenidius
CBS 293.66
USA
JN206417
M. durus
CBS 156.51*
Ukraine
JN206456
M. endophyticus
CBS 385.95*
China
JN206448
M. exponens
CBS 141.20*
Germany
JN206441
M. falcatus
CBS 251.35*
Germany
JN206509
M. flavus
CBS 234.35*
Germany
JN206468
M. fuscus
CBS 282.78
France
JN206442
M.fusiformis
CBS 336.68*
Finland
JN206447
M. genevensis
CBS 114.08*
Switzerland
JN206435
M.gigasporus
CBS 566.91*
China
JN206494
M. guiliermondii
CBS 174.27*
Russia
JN206475
M.heterogamus
CBS 405.58*
–
JN206487
M. hiemalis f. corticola
CBS 362.68
Norway
JN206449
M. hiemalis f. hiemalis
CBS 201.65*
USA
HM849683
M. inaequisporus
CBS 255.36*
Ghana
JN206502
M. indicus
CBS 226.29*
Switzerland
HM849690
M.irregularis
CBS 103.93
India
HM849684
M. japonicus
CBS 154.69*
Russia
JN206446
M. lanceolatus
CBS 638.74
France
JN206443
M. laxorrhizus
CBS 143.85*
United Kingdom
JN206444
M. luteus1
CBS 243.35*
Germany
M. megalocarpus
CBS 215.27*
France
M. microsporus1
CBS 204.28
France
M. minutes
CBS 586.67
India
JN206463
M. moelleri
CBS 444.65*
USA
HM849682
M. mousanensis
CBS 999.70*
India
JN206434
M. mucedo
CBS 640.67*
Netherlands
HM849687
M. multiplex
CBS 110662*
China
JN206484
M. nederlandicus
CBS 735.70
–
JN206503
M. odoratus
CBS 130.41*
Denmark
JN206495
M. parviseptatus
CBS 417.77
Australia
JN206453
M. piriformis
CBS 169.25*
–
HM849681
M. plasmaticus
CBS 275.49
Netherlands
JN206483
M. plumbeus
CBS 634.74
Germany
HM849677
M. prayagensis
CBS 652.78
India
JN206498
M. racemosus f. racemosus
CBS 260.68*
Switzerland
HM849676
M. racemosus f. sphaerosporus
CBS 115.08*
Norway
JN206433
M. ramosissimus
CBS 135.65*
Uruguay
HM849678
HM849680
JN206489
66
Fungal Diversity (2014) 67:21–125
Table 15 (continued)
Ex-type (ex-epitype) strains are
bolded and marked with an * and
voucher stains are bolded
Species
Isolate
GenBank accession no
M. saturninus
CBS 974.68*
Netherlands
JN206458
M. silvaticus
CBS 249.35*
Denmark
JN206455
M. strictus
CBS 100.66
Austria
JN206477
M. ucrainicus
CBS 674.88
Ukraine
JN206507
M. variisporus
CBS 837.70*
India
JN206508
M. zonatus
CBS 148.69*
Germany
JN206454
M. zychae
CBS 416.67*
India
JN206505
Backusella lamprospora
CBS 195.28
USA
JN206530
B. grandis
CBS 186.87*
India
JN206527
Molecular phylogeny
Crous et al. (2006) proposed new combinations for 13 species
based on the sequence data from cultures. Based on DNA
sequence data for five nuclear markers, Pavlic et al. (2009a, b)
identified three new species of Neofusicoccum within the
N. parvum/N. ribis species complex in South Africa.
N. batangarum was described from Terminalia catappa by
Begoude et al. (2010). Analysis of TEF, β-tubulin and LSU
gene sequences (Alves et al. 2008; Abdollahzadeh et al. 2010)
and Genealogical Sorting Index (GSI) has been used to resolve the asexual morph of Neofusicoccum (Sakalidis et al.
2011) (Fig. 17).
Recommended genetic markers
&
&
Country of collection
LSU, SSU and ITS–genus level
β-tubulin and TEF–species level
Common genetic markers that are used for the identification of Botryosphaeriaceae species are ITS, TEF, β- tubulin,
LSU and SSU. Recent studies have shown that the combination of TEF, ITS and β- tubulin is sufficient to characterize
species in this lineage. However, even when using only the
TEF gene, it is possible to identify distinct species. The
unavailability of the TEF sequence of several type species
makes species identification using molecular phylogeny problematic. Therefore, in future research, it is recommended to
use the combination of TEF, ITS and β- tubulin for better
species level delimitation.
Pestalotiopsis
Background
Pestalotiopsis is an appendage-bearing conidial asexual
coelomycetous genus in the family Amphisphaeriaceae,
Xylariales, Sordariomycetes (Ascomycota) (Barr 1975;
Kang et al. 1998) that is common in tropical and temperate
ecosystems (Maharachchikumbura et al. 2011, 2012). The
sexual state is Pestalosphaeria and only 13 species are known
as compared to the asexual state (253 species names). Species
of Pestalotiopsis cause a variety of disease in plants, including
canker lesions, shoot dieback, leaf spots, needle blight, tip
blight, grey blight, scabby canker, severe chlorosis, fruit rots
and leaf spots (Espinoza et al. 2008; Maharachchikumbura
et al. 2013a, b; Tagne and Mathur 2001). Species belonging to
the genus Pestalotiopsis are thought to be a rich source for
bioprospecting, and chemical exploration of endophytic
Pestalotiopsis species is on the increase (Aly et al. 2010; Xu
et al. 2010, 2014). Pestalotiopsis species have been recorded
as saprobes where they are recyclers of dead plant material
(Maharachchikumbura et al. 2012) and are also known to
cause human and animal infections (Pestalotiopsis
clavispora) (Monden et al. 2013).
Most Pestalotiopsis names in the literature are described
based on host association. However, molecular data have
shown that the genus needs revision (Maharachchikumbura
et al. 2011, 2012; Zhang et al. 2013c), and many of the
traditional species may be spurious. There are also numerous
cryptic species, very few distinct species, species with wide
host ranges, those with cosmopolitan distribution and some
species being opportunistic pathogens. This calls for critical
re-examination of the genus, using both morphological studies
and a multi-marker phylogeny based on ex-type and exepitype cultures (Maharachchikumbura et al. 2012, 2013c).
Species identification and numbers
According to Index Fungorum (2014) there are 253
Pestalotiopsis names, while in MycoBank (2014) there are
264 names. The reason for the large number of names is
historical and may not reflect the actual number of species
(Jeewon et al. 2004). Kohlmeyer and Kohlmeyer (2001) described P. juncestris, which was isolated from the host Juncus
roemerianus; this species is morphologically similar to
P. versicolor and several other species of Pestalotiopsis, but
Fungal Diversity (2014) 67:21–125
67
Fig. 16 Maximum likelihood tree based on partial LSU sequences for Mucor species and main groups within the genus. Detailed phylogenetic trees for
each group may be found in Walther et al. (2013)
the taxon was described as a new species based on the host
occurrence. However, recent molecular data have shown that
host association and geographical location is less informative
for distinguishing taxa (Jeewon et al. 2004; Hu et al. 2007).
Isolation of endophytic Pestalotiopsis strains for
bioprospecting for new biochemical compounds has shown
that the same species can be found in a range of hosts. It has
been shown that most of the key conidial characters used in
species level separation are not stable and vary with host
range, generation, culture and other environmental conditions
(Hu et al. 2007). Furthermore, the arrangement of species by
Steyaert (1949) and Guba (1961) in various coloured groupings is problematic because this character has been shown to
be variable within a species (Liu et al. 2010). Thus, most
species in the above arrangements may be confused and many
species are probably synonyms. Therefore, most of the species
recorded in checklists and the literature may not reflect what
actually occurs. Thus, many names assigned to Pestalotiopsis
probably lack any accurate taxonomic basis, leaving the taxonomy of the genus markedly confused. Until 1990,
68
Fungal Diversity (2014) 67:21–125
Table 16 Neofusicoccum. Details of the isolates used in the phylogenetic tree
Species
Isolate
GenBank accession numbers
SSU
ITS
LSU
TEF
β-tubulin
Neofusicoccum andinum
N. arbuti
N. australe
N. batangarum
N. cordaticola
N. corticosae
N. eucalypticola
N. grevilleae
N. kwambonambiense
N. luteum
N. macroclavatum
N. mangiferae
N. mediterraneum
N. nonquaesitum
CBS 117453*
CBS 116131*
CMW 6837*
CBS 124924*
CBS 123634*
CBS 120081*
CBS 115679*
CBS 129518*
CBS 123639*
CBS 110299*
CBS 118223*
CBS 118532*
CBS 121718*
CBS 126655*
N/A
KF531814
N/A
N/A
N/A
N/A
N/A
N/A
N/A
EU673148
N/A
EU673154
N/A
N/A
AY693976
AY819720
AY339262
FJ900607
EU821898
DQ923533
AY615141
JF951137
EU821900
AY259091
DQ093196
AY615186
GU251176
GU251163
N/A
DQ377915
N/A
N/A
N/A
N/A
N/A
JF951157
N/A
AY928043
N/A
DQ377921
N/A
N/A
AY693977
KF531792
AY339270
FJ900653
EU821868
N/A
AY615133
N/A
EU821870
AY573217
DQ093217
DQ093220
GU251308
GU251295
N/A
KF531792
AY339254
FJ900634
EU821838
N/A
AY615125
N/A
EU821840
DQ458848
DQ093206
AY615173
GU251836
GU251823
N. occulatum
N. parvum
N. pennatisporum
N. protearum
N. ribis
N. umdonicola
N. viticlavatum
N. vitifusiforme
Spencermartinsia viticola
CBS 128008*
CMW 9081*
WAC 13153*
CBS 114176*
CBS 115475*
CBS 123645*
CBS 112878*
CBS 110887*
CBS 117009*
N/A
EU673151
N/A
N/A
N/A
N/A
N/A
N/A
EU673165
EU301030
AY236943
EF591925
AF452539
AY236935
EU821904
AY343381
AY343383
AY905554
N/A
AY928045
EF591942
N/A
N/A
N/A
N/A
N/A
DQ377873
EU339509
AY236888
EF591976
N/A
AY236877
EU821874
AY343342
AY343343
AY905559
EU339472
AY236917
EF591959
N/A
AY236906
EU821844
N/A
N/A
EU673104
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
phylogenetic understanding of the taxonomy associated with
Pestalotiopsis and allied genera was based mainly on conidial
characters (Steyaert 1949; Guba 1961; Nag Rag 1993),
conidiogenesis (Sutton 1980) and sexual state association
(Barr 1975). More recently, some new species have been
introduced based on host occurrence, plus morphological
and molecular data (Maharachchikumbura et al. 2012,
2013a, b; Strobel et al. 2000). Furthermore, currently only
36 Pestalotiopsis species have either ex-type or ex-epitype
sequences.
Molecular phylogeny
Recently, many Pestalotiopsis species have been defined using
ITS sequence data, however, there are only a few type cultures
available for Pestalotiopsis. For example, Pestalotiopsis
clavispora, P. disseminata, P. microspora, P. neglecta, P.
photiniae, P. theae, P. virgatula and P. vismiae have numerous
ITS sequences in GenBank. However, in phylogenetic studies
all these species scattered throughout the phylogram and there
appears to be no living ex-type strain for any of these species
(Maharachchikumbura et al. 2011). Therefore it is unwise to
use GenBank sequences to represent any of these names. Rapid
development in molecular phylogeny has had a great impact on
Pestalotiopsis taxonomy. For example, random amplification
of polymorphic DNA (RAPD) can be used to detect genetic
diversity in the genus (Tejesvi et al. 2007). Watanabe et al.
(2012) evaluated the use of the ITS2 region and showed that it
is conserved at the level of secondary structure rather than the
level of primary sequence, which can be used for classification
of the Pestalotiopsis. Hu et al. (2007) showed that the ITS
region is less informative than the β-tubulin gene in differentiating endophytic species of Pestalotiopsis in Pinus armandii
and Ribes spp. A combination of β-tubulin and ITS gave
improved phylogenetic resolution, and they suggested that at
least two genetic markers should be used to resolve the
phylogeny of species of Pestalotiopsis. However, Liu et al.
(2010) disagreed with above statement concerning the ITS
region as being less informative when compared to the βtubulin region. They indicated that alignment of the ITS region
can be a useful character in grouping Pestalotiopsis to different
types of pigmentation, which can be used as a key character for
Fungal Diversity (2014) 67:21–125
69
markers, the authors also tested LSU, SSU, ACT and GPDH
(low resolution), GS and RPB1 (cannot be synthesized using
available primers or multiple copies) and CAL (species resolution is high, PCR success rate low).
Recommended genetic markers
&
&
The large subunits of nrDNA (LSU)–placement within the
Amphisphaeriaceae (generic level)
The internal transcribed spacer (ITS), β-tubulin and TEF–
species level (as outlined in Maharachchikumbura et al.
2012)
Phyllosticta
Background
Fig. 17 Phylogram generated from parsimony analysis based on combined ITS, TEF, β- tubulin, LSU and SSU sequenced data of
Neofusicoccum. Parsimony bootstrap support values and Bayesian posterior probabilities greater than 50 % are indicated above the nodes. The
ex-type (ex-epitype) and voucher strains are in bold. The scale bar
indicates ten changes. The tree is rooted with Spencermartinsia viticola
CBS 117009
the phylogeny of the species. In order to select suitable markers
for better species resolution, Maharachchikumbura et al. (2012)
analyzed a combined ACT, β-tubulin, CAL, GPDH, GS, ITS,
LSU, RPB 1, SSU and TEF dataset. They compared the morphological data versus the sequence data from each gene to
establish which characters satisfactorily resolve the species.
They narrowed down the 10 gene regions to three most applicable regions (ITS, β-tubulin and TEF), which were tested
individually and in combination, to evaluate the differences
between species. The species sequenced with ITS had a high
PCR and sequence success rate and β-tubulin and TEF gene
regions proved to be favourable taxonomic markers for
Pestalotiopsis since they resolved the taxonomic relationships
of most species studied. Further, TEF had better PCR amplification success rates and was found to be superior to β-tubulin.
TEF is therefore a powerful tool to resolve lineages within
Pestalotiopsis. Because of the better PCR and sequencing
success rate and fewer difficulties with alignment, editing and
better resolution, the TEF gene appears to be a very good
molecular marker for phylogenetic investigation of
Pestalotiopsis. Furthermore, a combination of ITS, β-tubulin
and TEF gene data gave the best resolution as compared to any
single marker (Table 17, Fig. 18). In addition to the above three
Phyllosticta is an important plant pathogenic genus with
coelomycetes asexual states. It was previously placed in
Botryosphaeriaceae, Botryosphaeriales, Dothideomycetes,
Ascomycota. However following phylogenetic analysis,
Wikee et al. (2013c) placed this genus in Phyllostictaceae
which is sister to the Botryosphaeriaceae. Phyllosticta species
are known to cause leaf spots and various fruit diseases
worldwide on a diverse range of hosts including some economically important crops and ornamentals such as citrus,
banana, apple, grapes, cranberry, orchids, mai dong and maple
(Uchida and Aragaki 1980; Paul and Blackburn 1986; Baayen
et al. 2002; McManus 1998; Olatinwo et al. 2003; Paul et al.
2005; Liu et al. 2009b; Wikee et al. 2011, 2012; Shivas et al.
2013b). Some species such as P. capitalensis are endophytes
and weak pathogens (Baayen et al. 2002; Glienke et al. 2011;
Wikee et al. 2013a), while others such as P. cocoicola are
saprobes (Punithalingam 1974; Taylor and Hyde 2003).
Phyllosticta species have been also used as bio-control agents
and produce novel bioactive metabolites such as phyllostine
and phyllostoxin (Yan et al. 2011; Evidente et al. 2008a, b;
Wikee et al. 2011, 2013b).
The sexual state of Phyllosticta was named Guignardia
which comprises 353 records in MycoBank (Hyde 1995;
Crous et al. 1996; Hyde et al. 2010). Phyllosticta species have
sometimes been named in Leptodothiorella after their spermatial state (Van der Aa 1973). Most species of Phyllosticta
and Guignardia have been described independently, and only
a few Phyllosticta species have been linked to their
Guignardia sexual morphs (Wulandari et al. 2010). On the
other hand, the host ranges of many diseases are poorly
understood (Van der Aa and Vanev 2002; Wikee et al.
2011). It has been recommended that Phyllosticta which is
the older, more commonly used and more species-rich, should
70
Fungal Diversity (2014) 67:21–125
Table 17 Pestalotiopsis. Details of the isolates used in the phylogenetic tree
Species
Isolates
Host
GenBank accession number
ITS
β -tubulin
TEF
Pestalotiopsis adusta
P. adusta
P. anacardiacearum
P. asiatica
P. camelliae
P. camelliae
P. chrysea
P. chrysea
P. clavata
P. clavispora
P. clavispora
P. coffeae–arabicae
P. coffeae–arabicae
P. diversiseta
ICMP6088*
MFLUCC10-146
IFRDCC2397*
MFLUCC12-0286*
MFLUCC12-0277*
MFLUCC12-0278
MFLUCC12-0261*
MFLUCC12-0262
MFLUCC12-0268*
MFLUCC12-0280
MFLUCC12-0281*
HGUP4015*
HGUP4019
MFLUCC12-0287*
On refrigerator door PVC gasket
Syzygium sp.
Mangifera indica
Unidentified tree
Camellia japonica
Camellia japonica
Dead plant
Dead plant
Buxus sp.
Magnolia sp.
Magnolia sp.
Coffeae arabica
Coffeae arabica
Rhododendron sp.
JX399006
JX399007
KC247154
JX398983
JX399010
JX399011
JX398985
JX398986
JX398990
JX398978
JX398979
KF412647
KF412649
JX399009
JX399037
JX399038
KC247155
JX399018
JX399041
JX399042
JX399020
JX399021
JX399025
JX399013
JX399014
KF412641
KF412643
JX399040
JX399070
JX399071
KC247156
JX399049
JX399074
JX399075
JX399051
JX399052
JX399056
JX399044
JX399045
KF412644
KF412646
JX399073
P. ellipsospora
P. ellipsospora
P. ericacearum
P. foedans
P. foedans
P. foedans
P. furcata
P. gaultheria
P. inflexa
P. intermedia
P. licualacola*
P. linearis
MFLUCC12-0283*
MFLUCC12-0284
IFRDCC2439*
CGMCC3.9178
CGMCC3.9123*
CGMCC3.9202
MFLUCC12-0054*
IFRD411-014*
MFLUCC12-0270*
MFLUCC12-0259*
HGUP4057*
Dead plant
Dead plant
Rhododendron delavayi
Neodypsis decaryi
Mangrove leaves
Calliandra haematocephala
Camellia sinensis
Gaultheria forrestii
Unidentified tree
Unidentified tree
Licuala grandis
JX398980
JX398981
KC537807
JX398989
JX398987
JX398988
JQ683724
KC537805
JX399008
JX398993
KC436006
JX399016
JX399015
KC537821
JX399024
JX399022
JX399023
JQ683708
KC537819
JX399039
JX399028
KC481683
JX399047
JX399046
KC537814
JX399055
JX399053
JX399054
JQ683740
KC537812
JX399072
JX399059
KC481684
P. magna
P. rhododendri
P. rhodomyrtus
P. rosea
P. samarangensis
P. saprophyta
MFLUCC12-0271*
MFLUCC12-652*
IFRDCC2399*
HGUP4230*
MFLUCC12-0258*
MFLUCC12-0233*
MFLUCC12-0282*
Trachelospermum sp.
Pteridium sp.
Rhododendron sinogrande
Rhodomyrtus tomentosa
Pinus sp.
Syzygium samarangense
Litsea rotundifolia
JX398992
KF582795
KC537804
KF412648
JX399005
JQ968609
JX398982
JX399027
KF582793
KC537818
KF412642
JX399036
JQ968610
JX399017
JX399058
KF582791
KC537811
KF412645
JX399069
JQ968611
JX399048
P. simitheae
P. simitheae
P. shorea
P. steyaertii
P. theae
P. theae
P. trachicarpicola
P. trachicarpicola
P. trachicarpicola
P. trachicarpicola
P. trachicarpicola
P. trachicarpicola
P. trachicarpicola
P. umberspora
P. unicolor
MFLUCC12-0121*
MFLUCC12-0125
MFLUCC12-0314*
IMI192475*
MFLUCC12-0055*
SC011
MFLUCC12-0263
MFLUCC12-0264
MFLUCC12-0265
MFLUCC12-0266
MFLUCC12-0267
IFRDCC2403
OP068*
MFLUCC12-0285*
MFLUCC12-0275
Pandanus odoratissimus
Pandanus odoratissimus
Shorea obtuse
Eucalyptus viminalis
Camellia sinensis
Camellia sinensis
Unidentified tree
Chrysophyllum sp.
Schima sp.
Sympolocos sp.
Unidentified tree
Podocarpus macrophyllus
Trachycarpus fortunei
Unidentified tree
Unidentified tree
KJ503812
KJ503813
KJ503811
KF582796
JQ683727
JQ683726
JX399000
JX399004
JX399003
JX399002
JX399001
KC537809
JQ845947
JX398984
JX398998
KJ503815
KJ503816
KJ503814
KF582794
JQ683711
JQ683710
JX399031
JX399035
JX399034
JX399033
JX399032
KC537823
JQ845945
JX399019
JX399029
KJ503818
KJ503819
KJ503817
KF582792
JQ683743
JQ683742
JX399064
JX399068
JX399067
JX399066
JX399065
KC537816
JQ845946
JX399050
JX399063
Fungal Diversity (2014) 67:21–125
71
Table 17 (continued)
Species
P. unicolor
P. verruculosa
Seiridium sp.
Isolates
MFLUCC12-0276*
MFLUCC12-0274*
SD096
Host
GenBank accession number
Rhododendron sp.
Rhododendron sp.
–
ITS
β -tubulin
TEF
JX398999
JX398996
JQ683725
JX399030
–
JQ683709
–
JX399061
JQ683741
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
have priority over Guignardia (Zhang et al. 2013a, b, c; Wikee
et al. 2013c).
Phyllosticta species have been historically indentified
based on morphology, culture characters as well as host association, which has resulted in several taxonomic revisions
(Van der Aa 1973; Van der Aa and Vanev 2002). Fresh
collections and future molecular analyses should help resolve
species relationships (Hyde et al. 2010). Phylogenetic analysis
has been routinely used in species identification, in combination with morphological characters (Crous and Groenewald
2005; Hyde et al. 2010; Wikee et al. 2013c). To create a stable
and workable taxonomy, neo- or epitypification are required
for many species of Phyllosticta (Hyde et al. 2010; Wikee
et al. 2013c).
Species identification and numbers
The genus Phyllosticta was first introduced as the generic name for Sphaeria lichenoides by Persoon (1818).
Desmazieres (1847) re-defined Phyllosticta, in which he
did not restrict the genus to species with one-celled
conidia. Consequently, many fungi with one-celled or
septate conidia were named as Phyllosticta (Desmazieres
1847; Van der Aa 1973). Saccardo (1878) however,
restricted Phyllosticta to species with one-celled conidia,
and after that Phyllosticta was further restricted to leaf
inhabiting species (Saccardo 1878, 1884; Van der Aa
1973; Petrak and Sydow (1927) published a compilation
of Phyllosticta names, and gave extensive descriptions
of 28 species. Van der Aa (1973) proposed a morphological identification criterion for the genus and detailed
46 Phyllosticta species based mostly on material
collected in Europe and North America. The genus
was revised by Van der Aa and Vanev (2002) and they
accepted 141 species. The currently used generic circumscription of Phyllosticta is: “pycnidia globose,
subglobose or tympaniform, conidiogenous cells holoblastic, with percurrent proliferation, conidia hyaline,
1-celled, ovoid, overate, ellipsoid, short cylindrical, or
globose to subglobose, usually bearing a slime layer
and an apical appendage” (Van der Aa 1973; Van der
Aa and Vanev 2002). During 2002–2014, about 30 new
species were described (Motohashi et al. 2008;
Wulandari et al. 2009, 2010; Glienke et al. 2011;
Wang et al. 2012; Su and Cai 2012; Wong et al.
2012; Wikee et al. 2012, 2013c; Zhang et al. 2013b;
Shivas et al. 2013b), with the currently accepted species
possibly being more than 171. Unfortunately, molecular
data are currently available for about only 69 species
(Table 18).
Molecular phylogeny
Phylogenetic analysis has become a standard approach
in fungal identification and has been well applied in
several other coelomycetous genera such as
Colletotrichum (Cai et al. 2009; Crouch et al. 2009b,
c; Hyde et al. 2009a, b) and Phoma (Aveskamp et al.
2008, 2010; de Gruyter et al. 2010). Recent reports on
Phyllosticta have shown that molecular phylogenetic
tools have significantly improved species identification
and delimitation; similarly it has improved the resolution in species complexes (Wulandari et al. 2009;
Glienke et al. 2011; Wicht et al. 2012).
Baayen et al. (2002) evaluated the P. citricarpa sensu
lato from Citrus and associated hosts based on ITS
sequence analysis and found that two phylogenetically
distinct groups existed: a slowly growing pathogenic
group and morphologically similar but fast-growing,
non-pathogenic group which latter proved to be
P. capitalensis. Wicht et al. (2012) used a polyphasic
approach including morphological, molecular and proteomic techniques to analyze samples of G. bidwellii collected from grapevine cultivars and ornamental plants of
various geographic origins, and showed that
P. ampelicida isolated from grapevine cultivars should
be split into two species.
Recent studies have provided clear phylogenetic relationships in the group. These efforts primarily used
intron-dominated genes (ITS, ACT, TEF), and highly
conserved gene coding regions (LSU, GPDH) that can
recognize cryptic species in traditionally morphologically circumscribed species complexes, e.g. P. citricarpa
on citrus, P. musarum on banana, P. vaccinii on
72
Fungal Diversity (2014) 67:21–125
Fig. 18 Strict consensus combined (ITS + β-tubulin + TEF) tree from
Bayesian analysis of the analyzed Pestalotiopsis. Thickened lines indicate
Bayesian posterior probabilities (PP) of 100 %. Strain accession numbers
(ex-type are in bold) are followed by the species name. The scale bar
represents the expected changes per site. The tree is rooted to Seiridium
spp. (D96)
Vaccinium, G. philoprina on Rhododendron, Hedera,
Ilex, Magnolia and Taxus (Glienke et al. 2011; Wang
et al. 2012; Wulandari et al. 2009; Wikee et al. 2013c,
a, b, c; Wong et al. 2012; Zhang et al. 2013a) (Fig. 19).
Recommendations
&
The large and small subunits of nrDNA (LSU and SSU)–
placement within the ascomycetes (generic and family level)
Fungal Diversity (2014) 67:21–125
73
Table 18 Phyllosticta. Details of the voucher and extype isolates used in the phylogenetic tree
Species
Strain no.
Host
Locality
GenBank accession number
ITS
ACT
TEF
GPDH
Botryosphaeria
obtusa
Guignardia alliacea
G. bidwellii
CMW8232
Conifers
South Africa
AY972105 AY972111 DQ280419
MUCC0014*
NBRC9757
Japan
Japan
AB454263
AB095510
G. gaultheriae
G. mangiferae
G. philoprina
G. vaccinii
Phyllosticta
abieticola
P. aloeicola
P. ampelicida
CBS447.70*
IMI260.576*
CBS447.68*
CBS126.22*
CBS112067*
Allium fistulosum
Parthenocissus
tricuspidata
Gaultheria humifusa
Manifera indica
Taxus baccata
Oxycoccus macrocarpos
Abies concolor
USA
India
Netherlands
USA
Canada
JN692543 JN692519 JN692531
JF261459 JF343641 JF261501
AF312014
FJ538353
KF170306 KF289238
CPC21020*
ATCC200578*
Aloe ferox
Vitis riparia
South Africa
USA
KF154280 KF289311 KF289193 KF289124
KC193586 KC193581
KC193584
P. ardisiicola
P. aspidistricola
P. beaumarisii
P. bifrenariae
P. brazilianiae
P. capitalensis
NBRC102261*
NBRC102244*
CBS535.87=IMI 298910 *
CBS128855*
CBS126270*
CBS128856*
CPC16592
BRIP554196*
CBS 120486*
CBS100098*
CBS127454*
CPC16603
ZJUCC200956*
Ardisia crenata
Aspidistra elatior
Muehlenbekia adpressa
Bifrenaria harrisoniae
Mangifera indica
Stanhopea sp.
Citrus limon
Musa cv. Formosana
Citrus maxima
Citrus limon
Citrus limon
Citrus limon
Citrus reticulata
Japan
Japan
Australia
Brazil
Brazil
Brazil
Argentina
Taiwan
Thailand
Brazil
Australia
Uruguay
China
AB454274
AB454260
AY042927
JF343565
JF343572
JF261465
KF206187
JQ743562
FJ538360
FJ538352
JF343583
KF170295
JN791620
P. concentrica
P. cordylinophila
P. cornicola
P. cussoniae
CBS136059*
CBS 937.7*
CPC20261*
CBS111639
CBS136060*
Citrus maxima
Hedera helix
Cordyline fruticosa
Cornus florida
Cussonia sp.
Thailand
Italy
Thailand
USA
South Africa
P. ericarum
P. fallopiae
P. foliorum
P. hamamelidis
P. hostae
P. hubeiensis
P. hymenocallidicola
P. hypoglossi
P. ilicis-aquifolii
P. kerriae
P. leucothoicola
P. ligustricola
P. maculate
CBS132534*
NBRC102266*
CBS 447.68
MUCC149
CGMCC3.14355*
CGMCC3.14986*
CBS 131309*
CBS 434.92*
CGMCC3.14358*
NBRC102251*
CBS136073*
MUCC0024*
CPC18347*
P. mangifera-indica
P. minima
P. musarum
P. musicola
CPC20264*
CBS 585.84*
BRIP55434*
CBS123405*
Erica gracilis
Fallopia japonica
Taxus baccata
Hamamelis japonica
Hosta plantaginea
Viburnum odoratissimim
Hymenocallis littoralis
Ruscus aculeatus
Ilex aquifolium
Kerria japonica
Leucothoe catesbaei
Ligustrum obtusifolium
Musa cv. Goly-goly
pot-pot
Mangifera indica
Acer rubrum
Hill banana
Musa acuminata
P. cavendishii
P. citriasiana
P. citribraziliensis
P. citricarpa
P. citrichinaensis
P. citrimaxima
JN692508
JF343748
KF306232
JF343649
JF343656
JF343647
KF289273
KF289170
JF343586
JF343593
JF261507
KF289178
KF289074
JF343744
JF343758
JF343776
KF289092
FJ538476
FJ538468
JF343667
KF289274
JN791533
FJ538418
FJ538410
JF343604
KF289213
JN791459
JF343686
JF343691
JF343771
KF289147
KF170304
FJ538350
KF170287
KF170307
JF343578
KF289300
KF289257
KF289295
KF289234
JF343662
KF289222 KF289157
FJ538408 JF411745
KF289172 KF289076
South Africa
Japan
Netherlands
Japan
China
China
Australia
Italy
China
Japan
Japan
Japan
Australia
KF206170
AB454307
KF170309
KF170289
JN692535
JX025037
JQ044423
FJ538367
JN692538
AB454266
AB454370
AB454269
JQ743570
KF289291 KF289227 KF289162
Thailand
USA
India
Thailand
KF170305 KF289296 KF289190 KF289121
KF206176 KF289249 KF289204 KF289135
JQ743584
FJ538334 FJ538450 FJ538392
KF289247
KF289309
JN692511
JX025032
KF289242
FJ538483
JN692514
JF343599
JF343764
KF289201 KF289132
JN692523 JN692503
JX025042 JX025027
KF289211 KF289142
FJ538425 JF343695
JN692526
KF289310
AB704212
74
Fungal Diversity (2014) 67:21–125
Table 18 (continued)
Species
Strain no.
Host
Locality
P. neopyrolae
P. owaniana
P. pachysandricola
P. parthenocissi
P. paxistimae
P. philoprina
P. podocarpi
P. podocarpicola
P. pseudotsugae
P. rhaphiolepidis
P. schimae
P. speewahensis
CPC21879*
CBS776.97*
MUCC0124*
CBS111645*
CBS112527*
CBS616.72
CBS111647
CBS728.79*
CBS111649
MUCC0432*
CGMCC3.14354*
BRIP58044
Pyrola asarifolia
Brabejum stellatifolium
Pachysandra terminalis
Parthenocissus quinquefolia
Paxistima mysinites
Ilex aquifolium
Podocarpus lanceolata
Podocarpus maki
Pseudotsuga menziesii
Rhaphiolepis indica
Schima superb
Orchids
P. spinarum
P. styracicola
P. telopeae
P. vaccinii
P. vacciniicola
P. yuccae
CBS292.90
CGMCC3.14985*
CBS777.97*
ATCC46255*
CPC18590*
CBS117136
Chamaecyparis pisifera
Styrax grandiflorus
Telopea speciosissima
Vaccinium macrocarpon
Vaccinium macrocarpum
Yucca elephantipes
Japan
South Africa
Japan
USA
USA
Germany
South Africa
USA
USA
Japan
China
northern
Australia
France
China
Tasmania
USA
USA
New Zealand
GenBank accession number
ITS
ACT
AB454318
FJ538368
AB454317
EU683672
KF206172
KF154279
KF154276
KF206173
KF154277
AB454349
JN692534
KF017269
AB704233
KF289254
AB704232
JN692518
KF289239
KF289251
KF289235
KF289252
KF289236
AB704242
JN692510
JF343585
JX025040
KF206205
KC193585
KF170312
JN692541
JF343669
JX025035
KF289255
KC193580
KF289287
JN692517
TEF
GPDH
FJ538426
JF343767
JN692530
KF289209
KF289205
KF289232
KF289203
KF289231
KF289140
KF289136
KF289168
KF289134
KF289167
JN692522 JN692506
KF017268
JF343606
JX025045
KF289210
KC193582
KF289229
JN692529
JF343773
JX025030
KF289141
KC193583
KF289165
JN692507
Ex-type strains are bolded and marked with an * and voucher stains are bolded
&
&
The internal transcribed spacer (ITS)–generic
level
Combined ITS, TEF, GPDH and ACT–inter-specific
delineation
Phytophthora
Background
While resembling Eumycotan fungi with the production of hyphae, the genus is placed in the kingdom Straminipila, class
Oomycetes, order Peronosporales, and family Peronosporacae.
The type species is P. infestans described by de Bary in 1876.
Since this time over 128 species have been described, many of
which are important plant pathogens capable of significantly
impacting agricultural production and natural ecosystems.
Some species have a rather narrow host range (P. infestans, P.
lateralis, P. sojae) while others are capable of infecting a wide
range of plant host species (P. cinnamomi, P. nicotianae, P.
ramorum). From a historical perspective, most investigations
on the genus have focused on the impact of the genus on
agricultural production systems, however, more recently there
has been an increased interest in investigating the role this genus
plays in natural ecosystems as exemplified by the number of
publications concerning species such as P. ramorum and P. alni,
as well as the description of many new species recovered from
environmental sampling (Martin et al. 2012).
Although Phytophthora species resemble Eumycotan fungi with the production of hyphae, evolutionarily they are more
closely related to chromophyte algae and plats than to
Eumycotan fungi (Wainright et al. 1993). They have cell walls
that are primarily cellulose rather than chitin as observed in
fungi and they are incapable of synthesizing β-hydroxysterols
(which are required for synthesis of hormones regulating
sexual reproduction). In addition, Oomycetes are diploid
throughout their life cycle in contrast to most true fungi.
An excellent overview of the ecology, biology and taxonomy of the genus (although missing more recently described
species) can be found in Erwin and Ribeiro (1996), a review of
the recent taxonomic status in Kroon et al. (2012) and an
overview of the genus, including molecular identification
and diagnostics, in Martin et al. (2012). There are several
publically available databases that provide a wealth of up to
date information on the genus, along with sequences useful for
species identification via BLAST analysis, including the
Phytophthora Database (www.phytophthoradb.org),
Phytophthora ID (www.phytophthora-id.org) and Q-Bank
(www.q-bank.eu). Cline et al. (2008) have published an online
list of Phytophthora spp. with a hyperlink for each species to
the USDA SMML database that includes host range, distribution and supporting literature.
Fungal Diversity (2014) 67:21–125
Fig. 19 Phylogram generated
from parsimony analysis based on
combined ITS, TEF, GPDH and
ACT sequenced data of
Phyllosticta. Parsimony bootstrap
support values greater than 50 %
are indicated above the nodes.
The ex-type (ex-epitype) and
voucher strains are in bold
75
76
Species identification and numbers
A complicating factor when trying to identify Phytophthora
species or investigate phylogenetic relationships is hybridization among distinct evolutionary lineages. While this does not
appear to be a common occurrence, several stable hybrid
species have been identified, e.g. P. andina (Goss et al.
2011; Blair et al. 2012); P. alni (Brasier et al. 1999);
P. x pelgrandis (Nirenberg et al. 2009); P. x serindipita
(Man in ’t Veld et al. 2012) as well as hybrid clade 1 species
recovered from the field (Man in ’t Veld et al. 1998, 2007;
Hurtado-Gonzales et al. 2009; Bonants et al. 2000). While
conducting a detailed evaluation of clade 6 Phytophthora spp.
from natural ecosystems in Australia, Burgess et al. (2010)
observed ‘hybrid swarms’ that contained mixtures of parent,
offspring, and intermediate isolates with high tendencies for
back-crossing and out crossing. The authors’ concluded that
the presence of such hybrid swarms was indicative of sexual
and somatic hybridization events; the high proportion of these
variant isolates within the population also suggested that these
hybridization events were not uncommon. Recently four interspecific hybrid clade 6 species have been recovered from
riparian ecosystems in Australia and South Africa that reflect
outcrossing between P. amnicola, P. thermophila and P. taxon
PgChlamydo (Nagel et al. 2013). Additional putative interspecific hybrids from riparian ecosystems in Australia were
reported by Hüberli et al. (2013). Hybridization is a topic that
requires a more detailed investigation as it could have a
profound influence on gene flow among species and the
evolution of new species with an expanded host range that
could impact agricultural and natural ecosystems (as observed
with P. alni).
Traditional classification to species level has been based on
morphological characterization of reproductive structures
(reviewed in Martin et al. 2012). This includes the sporangium
(asexual) and oospore (sexual) as well as the production of
chlamydospores (asexual structure not produced by all species). Important features of the sporangium include their dimensions (length and breadth), shape, thickening at the terminus (papilla), length of stalk (pedicle), whether or not the
sporangium can be easily dislodged from the sporangiophore
(caducity), and proliferation of sporangia (internal, external or
nested).
The sexual reproductive structures consist of the antheridium and oogonium (paternal and maternal gametangia, respectively) and are produced when cultures are grown on the
appropriate sterol-containing medium. Their fusion leads to
the formation of an oogonium that matures into a thick-walled
resting structure referred to as an oospore. While most species
are homothallic and form oospores in single culture, there are
heterothallic species where pairing with opposite mating types
is essential to stimulate production of sexual reproductive
structures. Since Phytophthora is sexually dimorphic (an
Fungal Diversity (2014) 67:21–125
isolate of a heterothallic species can function either as the
maternal or paternal parent depending on the isolate it is
paired with) it is advisable to pair self-sterile isolates with
two tester isolates of opposite mating type. While the use of
tester isolates of the same species is advisable, isolates of other
heterothallic species (such as P. cryptogea or P. cambivora)
may also be used. Characteristics such as the diameter of the
oogonium and oospore, thickness of the oospore wall, whether or not the oospore fills the oogonium (plerotic), ornamentation on the oogonial wall, and mode of attachment of the
antheridium are useful for species classification.
In an effort to simplify isolate identification and establish
groupings of isolates for comparison of morphological features (but not phylogenetic relationships), Waterhouse (1963)
introduced the concept of morphological groups I through VI
based on a number of characteristics, and is still useful today.
Unfortunately a dichotomous key that includes recently described species is not available for identification of isolates but
there are several recent efforts to simplify morphological
identification of species, including a manual for identification
of 60 species of Phytophthora by integration of a dichotomous
key with a DNA fingerprinting technique based on PCRsingle strand conformational polymorphism (SSCP)
(Gallegly and Hong 2008). A LUCID key for identification
of 55 common Phytophthora spp. is available (Ristaino 2011)
and an expanded LUCID key including most described species should be available on a dedicated website in the near
future (G. Abad and Y. Balci, personal communication). A
tabular presentation of morphological features enabling comparison among 117 species may be found in Martin et al.
(2012; a downloadable file of the table alone is available on
the journal website).
In 1999 the number of described species in the genus
Phytophthora was approximately 55 (Brasier 2007) but since
then there has been a significant increase., Brasier (2007)
reported a doubling in number to 105 described species, with
this number recently increasing to 117 (Martin et al. 2012).
Additional species have recently been described; P. lacustris
(Nechwatal et al. 2012) P. pluvialis (Reeser et al. 2013),
P. mississippiae (Yang et al. 2013), P. cichorii, P. dauci and
P. lactucae (Bertier et al. 2013), P. pisi (Heyman et al. 2013),
P. stricta and P. macilentosa (Yang et al. 2014) and the hybrid
species P. x serendipita and P. x pelgrandis (Man in ’t Veld
et al. 2012), bringing the total to at least 128 described species.
With the number of provisional species names used in the
literature, and research efforts to evaluate the distribution of
this genus in natural ecosystem, this number is likely to
continue to increase in the future.
Molecular phylogeny
Historically the genus Phytophthora has been placed in the
Pythialeswith Pythium and related genera but more recent
Fungal Diversity (2014) 67:21–125
phylogenetic analysis with the large (LSU) or small (SSU)
rDNA sequences or cox2 gene has indicated a closer affiliation
with downy mildews and white rusts (Albugo.) in the
Peronosporales (Beakes and Sekimoto 2009; Thines et al.
2009). However, additional multigene analyses with a larger
number of downy mildew species is needed to better characterize this relationship and the placement of Phytophthora
spp. in clade 9 and 10 (Blair et al. 2008). The relationship
between the Peronosporales and Pythium (Pythiales) needs
clarification as well. A new genus, Phytopythium, was erected
to accommodate an inconsistency between taxonomic and
phylogenetic grouping for certain “intermediate” Pythium
species (Bala et al. 2010), and it is likely that additional
taxonomic revisions of the Peronosporomycetidae will be
needed to fully resolve taxonomic conflicts.
Early efforts to understand phylogenetic relationships in
Phytophthora focused on the use of the nuclear encoded
rDNA, primarily the ITS region (Förster et al. 2000; Cooke
and Duncan 1997; Crawford et al. 1996). Cooke et al. (2000)
published the first comprehensive phylogenetic analysis of the
genus using the ITS region to examine the phylogeny of 50
species. Most isolates grouped within eight primary clades
(numbered 1 to 8) with several other species placed in two
additional clades (clades 9 and 10). Kroon et al. (2004) expanded this analysis using two nuclear (translation elongation
factor 1α, β-tubulin) and two mitochondrial (cox1 and nad1)
genes. While in general the results were congruent with those
reported by Cooke et al. (2000), there were some notable
differences in the grouping of some species. Subsequent analysis by Blair et al. (2008) using seven nuclear genes (60S
ribosomal protein L10, ß-tubulin, enolase, heat shock protein
90, large subunit rDNA, TigA gene fusion and translation
elongation factor 1α) representing 8.1 kb of sequence data
for 82 Phytophthora spp. clarified these differences. This
larger, multi-marker analysis supported the observations of
Cooke et al. (2000) with eight main clades plus two additional
closely affiliated clades (clades 9 and 10) as the sister clades to
the rest of the genus. More recently, Martin et al. (2014)
expanded on this analysis by adding four mitochondrial genes
(cox2, nad9, rps10 and secY) and additional species. The
resulting phylogeny from this 11-marker analysis (10,828 bp
per isolate) was similar to the prior observations of Blair et al.
(2008) and subsequent analysis indicated that similar results
could be obtained when using only five markers (LSU, βtubulin, cox2, nad9 and rps10).
While the ITS region may be useful for species identification (see below), length variation among species makes it
impossible to construct an unambiguous alignment across
the entire genus, thus hampering the utility of this marker for
phylogenetic analysis. Likewise, the translation elongation
factor 1α has been used for phylogenetic analysis, but recent
analysis of Phytophthora genomic data indicates that the gene
is duplicated; divergence among duplicates may complicate
77
phylogenetic interpretations of species evolution (J. E. Blair,
unpublished).
While the above noted phylogenetic analyses have provided insight into the broader evolutionary relationships within
the genus, there is still ambiguity when examining some
closely related species and species complexes. Significant
progress has been made with the clarification of the
P. megasperma complex and other clade six species (Brasier
et al. 2003; Durán et al. 2008; Hansen et al. 2009; Jung et al.
2011a, b) but there are still several provisional species
awaiting more comprehensive analysis (for example,
P. taxon PgChlamydo, P. taxon raspberry, P. taxon canalensis,
P. taxon erwinii, P. taxon hungarica, P. taxon oregonsis and
P. taxon paludosa). While there have been advances in understanding the relationships among some clade 2 species, there
is need for additional analysis to clarify species complexes
such as P. citricola and P. citrophthora. One clade 8 species
complex where phylogenetic resolution has been elusive is
P. cryptogea and the closely related species P. drechsleri. The
multigene analysis of Mostowfizadeh-Ghalamfarsa et al.
(2010) confirmed that while P. drechsleri was monophyletic,
the P. cryptogea complex formed three well-defined phylogenetic groups with group I closely affiliated with
P. erythroseptica and group II and III as a separate clade
(group III isolates have been reported as the provisional species, P. sp. kelmania; Martin et al. 2014). Some isolates were
placed intermediate between groups II and III and exhibited a
greater amount of heterozygosity than the other isolates, suggesting possible outcrossing between these groups. Using a
parsimony-based ancestral recombination graph and genealogies inferred from the β-tubulin and translation elongation
factor 1-α genes from greenhouse recovered isolates, Olson
et al. (2011) suggested that divergence between P. cryptogea
and P. drechsleri was recent and that speciation is still in
progress.
In addition to the choice of markers to use for phylogenetic
analysis, another important consideration is the type of analysis
used for estimating phylogenetic relationships or for the description of new species. While traditional methods of phylogenetic analysis (maximum likelihood, neighbour-joining,
Bayesian) have adequately described relationships among
most species, they have been unable to fully resolve the deeper
relationships among the ten Phytophthora clades or among
related genera. A recent study by Martin et al. (2014) used a
novel variation of a multispecies coalescent approach to evaluate the ten clades; in general support was higher than that
observed in the phylogenetic analysis for the recovered relationships, but the position of certain clades (Clade 3 and the
unique grouping of P. sp. ohioensis and P. quercina) remained
ambiguous. Here we present an analysis using a more powerful
and complex Bayesian method (Drummond et al. 2012) with
five genetic markers (Fig. 20), and recover strong support for
basal relationships among the clades that are quite similar to
78
Fungal Diversity (2014) 67:21–125
Fig. 20 Bayesian analysis of phylogenetic relationships within Phytophthora. Asterisks on nodes indicate posterior probabilities greater than 0.95
(95 %) generated from an analysis of five genes (nuclear LSU and β-tubulin; mitochondrial cox2, nad9, rps10). Evolutionary rates were estimated under
a GTR + I + G model for nuclear markers and an HKY + I + G model for mitochondrial gene; each marker was treated as a separate partition. The
analysis was run twice with 50 million generations under a strict clock model in BEAST v1.7.5. A 20 % burn in was removed before the maximum clade
credibility tree was constructed. Ex-type isolates are shown in bold. Separate isolate numbers are shown for those few species that did not have sequence
data available for both nuclear and mitochondrial genes from a single isolate
the 11-marker study of Martin et al. (2014). Newer phylogenetic methods may allow for more complex modelling of the
evolutionary process, however they are still sensitive to the
accuracy of a priori information provided by the user.
Additional studies will be needed to provide more basic information on the tempo of molecular evolution within this group.
The description of new species is also an area were traditional phylogenetic methods may not accurately describe
species relatedness. Aside from morphological characterization, recent species descriptions typically contain molecular
evidence from one or a few genetic markers (primarily ITS
and perhaps cox1 or 2). However, as described above, alignment ambiguity and the presence of intraspecific polymorphisms can seriously impact the recovered phylogeny; recent
hybridization events and incomplete lineage sorting of ancestral polymorphisms also violate the assumptions made by
Fungal Diversity (2014) 67:21–125
79
Fig. 20 (continued)
traditional phylogenetic methods. The use of coalescent-based
approaches to estimate species trees from a collection of gene
trees has been gaining popularity among many other taxonomic groups, but has seen little attention in Phytophthora or
oomycete research in general. The recent description of P. pisi
(Heyman et al. 2013) employed a multispecies coalescent
approach, which confirmed the individual analyses of ITS
and cox2 data. In addition, a recent study of the hybrid species
P. andina (Blair et al. 2012) used several coalescent methods
to determine the likely parental lineages of this species, one of
which was clearly P. infestans. In the future, the use of more
complex phylogenetic methods as well as coalescent-based
approaches will be needed to clarify relationships at both ends
of the spectrum, from deep basal nodes to recently evolved
and potentially interbreeding species complexes.
A common observation among all phylogenetic studies is there is no consistent correlation between phylogenetic grouping and morphological features (Cooke et al.
2000; Kroon et al. 2004, 2012; Blair et al. 2008; Martin
et al. 2014). While there is some correlation with sporangial type (clade 4, 5, and 10 have primarily papillate
sporangia while clade 3 has primarily semipapillate
sporangia and clades 6, 7, and 9 primarily nonpapillate
sporangia), other clades show combinations of these
80
features (clade 1, 2 and 8). Characteristics such as oogonial ornamentation, heterothallism, and mode of antheridial attachment are all polyphyletic.
Because of the large number of species, intraspecific variation of some morphological features, and overlapping morphology among closely related species, traditional methods of
species identification can be challenging and require some
level of expertise to be effective. The use of molecular criteria
has simplified this task and provides a tool for delineating
distinct taxa within morphologically similar species complexes. The most accurate molecular method for species identification is sequence analysis of specific markers. The internal
transcribed spacer (ITS) region of the nuclear ribosomal DNA
(rDNA) has been widely used and a large number of sequences are currently available in public databases.
However, this marker may not be ideal for the identification
of all species, especially those that are closely related. For
example, many clade 1C species (P. infestans, P. mirabilis)
cannot be distinguished using this marker alone, nor can
P. fragariae and P. rubi. More recently a portion of the cox1
gene, along with the ITS region, have been proposed as the
markers to use in the Barcode of Life Database (www.
boldsystems.org) and representative sequences for all
described and some provisional species have been deposited
(Robideau et al. 2011).
Several nuclear (60S ribosomal protein L10, β-tubulin,
enolase, heat shock protein 90, large subunit rRNA, TigA
gene fusion, translation elongation factor 1α; (Blair et al.
2008; Kroon et al. 2004; Villa et al. 2006)) and mitochondrial
(cox1, nad1, cox2, nad9, rps10 and secY; (Kroon et al. 2004;
Martin 2008; Martin and Tooley 2003a, b; Martin et al. 2014)
markers have been sequenced for phylogenetic analysis of
Phytophthora and can also be used for species identification.
Background information for amplification and sequencing of
many of these markers, as well as the capability for BLAST
searches against a curated database for isolate identification,
may be found at the Phytophthora Database (www.
phytophthoradb.org). A dataset for ITS and cox1 and 2
spacer sequences is also available at Phytophthora ID
((Grünwald et al. 2011), www.phytophthora-id.org) and
sequence data for several markers (ITS, β-tubulin,
elongation factor 1 alpha, and cox1), along with pictures
of morphological features, may be found at Q-Bank
(www.q-bank.eu).
There are several caveats to consider when using BLAST
analysis to identify isolates to species level to prevent misidentification (Kang et al. 2010; Nilsson et al. 2012). BLAST
scores are dependent on the length of the aligned sequences as
well as the level of sequence identity; instances where high
levels of sequence identity occur for only a portion of the
target sequence may result in incorrect species identification.
Also, it is common to encounter situations where scores are
similar among multiple species, making it difficult to draw
Fungal Diversity (2014) 67:21–125
conclusions about an isolate’s identity (this can be especially
problematic for isolates within or related to species complexes). In addition, the use of markers known to contain
intraspecific polymorphisms may lead to inaccurate species
identifications due to potentially lower similarities among
closely related sequences. Heterozygosity in nuclear markers
may also complicate identification efforts; while the presence
of distinct alleles may indicate outcrossing (as Phytophthora
is a known diploid), heterozygosity may also result from
hybridization events between distinct lineages (as described above). Phylogenetic analysis of several markers
is therefore suggested to confirm species identification,
especially when working with species complexes.
Additional gel based techniques, such as PCR-RFLP,
SSCP, random amplified polymorphic DNAs (RAPDs),
amplified fragment length polymorphisms (AFLP) and
simple sequence repeat (SSR) analysis, for species identification and population analysis are reviewed in Martin
et al. (2012).
Recommended genetic markers
The following genetic markers have been found to amplify
well across all species and provided a similar level of
phylogenetic resolution as a concatenated dataset of seven
nuclear and four mitochondrial genes (Martin et al. 2014).
Information on amplification and sequencing primers for
these genes may be found at the Phytophthora Database
(www.phytophthoradb.org).
Nuclear genes–LSU, β-tubulin
Mitochondrial–cox2, nad9, rps10
Phytophthora Data
Sequence alignments of the seven nuclear and four
mitochondrial markers used in Martin et al. (2014) and
Fig. 20 may be downloaded at TreeBASE (http://purl.
org/phylo/treebase/phylows/study/TB2:S14595). A table
with additional information on isolates used in the analysis
may be found in Martin et al. (2014) with GenBank accession
numbers listed in the supplementary material of this citation.
These sequences can also be downloaded from the
Phytophthora Database (www.phytophthoradb.org).
Pythium
Background
Pythium is classified as belonging to the family Pythiaceae
sensu lato (s.l.), order Peronosporales s.l., class
Peronosporomycetes, phylum Oomycota, and kingdom
Fungal Diversity (2014) 67:21–125
Straminipila (Beakes et al. 2014). Although many species are
considered to be saprobes, the genus is known primarily for its
parasitic interactions with plants. Several species also parasitize algae (green and red), fungi, other oomycetes, nematodes,
insects, crustaceans, and fish. One species, P. insidiosum, is
the causal agent of pythiosis in mammals, including humans
(Van der Plaats-Niterink 1981; de Cock et al. 1987). Plant
pathogenic Pythium species often target young below-ground
plant parts such as fine roots, germinating seeds and emerging
growth, resulting in damping-off, root rot and poor crop stands
with stunted plants and reduced yield. Some species can also
cause fruit rot, and at least one species, P. vexans, has been
associated with trunk cankers of rubber trees (Van der PlaatsNiterink 1981; Zeng et al. 2005). Although some species have
a limited host range, such as P. arrhenomanes that seems to be
exclusively associated with gramineous crops, species like
P. aphanidermatum, P. irregulare and P. ultimum are known
for being highly virulent on an extensive range of plant hosts
(Van der Plaats-Niterink 1981). However, not all Pythium
species have a negative impact on the plants they are associated with. Besides saprobes, others can benefit plants by
acting as biocontrol agents that parasitize pathogenic fungi
and/or induce host resistance, e.g. Pythium oligandrum
(Benhamou et al. 1997). Other species of Pythium have also
been reported to stimulate plant growth (Mazzola et al. 2002).
Recent genome sequencing of six Pythium species found high
levels of variation in the number of CRN (“Crinkler”) effectors found in the different species, possibly suggesting
species-specific infection strategies (Adhikari et al. 2013) that
may contribute to the range of interactions of Pythium species
with their hosts. Such species-specific host-interactions along
with the ubiquitous nature of the genus in soils all over the
world make accurate species identification necessary to facilitate disease diagnosis and management.
Debates regarding possible genera within Pythium were initially sparked by differences in sporangial morphology. Based on
these characters some of the novel genera that have been proposed are Nematosporangium (for species with filamentous
zoosporangia), Rheosporangium (species with lobulate
zoosporangia), and Sphaerosporangium (species with ovoid,
spherical or citriform sporangia) (Schröter 1897; Sparrow
1931). The legitimacies of these genera have been questioned
for various reasons (Sideris 1931a; Sparrow 1932; Van der
Plaats-Niterink 1981), and aside from some attempts at transferring Pythium species to Nematosporangium (Jaczewski and
Jaczewski 1931; Sideris 1931b) the scientific community has
stuck with the generic classification of Pythium versus these
genera. As molecular taxonomy became a more popular approach to studying systematics, the paraphyletic nature of
Pythium became apparent and the debate on splitting the genus
was rekindled. Early sequence-based phylogenies provided
strong arguments for P. vexans to be part of a separate genus
(Briard et al. 1995; Cooke et al. 2000). The ITS and 28S
81
phylogenies of Lévesque and de Cock (2004) divided Pythium
into 11 clades (A-K) of which clade K (including P. vexans) is
more closely related to Phytophthora than to the rest of the
Pythium clades (Villa et al. 2006). A new genus, Phytopythium,
was subsequently erected to include all clade K species, with
Phytopythium sindhum as type species (Bala et al. 2010), although the official transfer of all clade K Pythium species to
Phytopythium has not yet been published. The remaining ten
clades (A-J) can be divided into two groups: species with filamentous zoosporangia (clades A-D) and species with globose
zoosporangia (clades E-J) (Lévesque and de Cock 2004), calling
to mind early suggestions of splitting the genus based on this
character (Schröter 1893; Sparrow 1931). This division is echoed
to varying degrees by phylogenies of the 28S rRNA, ITS,
cytochrome c oxidase subunits 1 and 2 (cox1 and cox2), and
β-tubulin, although the different gene trees are often incongruent
and support for internal nodes low or absent (Martin 2000;
Riethmüller et al. 2002; Villa et al. 2006; Hulvey et al. 2010;
Robideau et al. 2011). Despite the shortcomings of these gene
regions, Uzuhashi et al. (2010) used 28S and cox2 phylogenies to
divide Pythium into five genera: Pythium (clades A-D),
Globisporangium (clades E-G, I and J), Elongisporangium
(clade H), Ovatisporangium (clade K, syn. Phytopythium), and
Pilasporangium (distinct from any of the aforementioned 11
clades). Although this division is more or less in agreement
with previous phylogenetic studies, it is problematic with
regards to a lack of bootstrap support for the Pythium and
Globisporangium clades, and the relationship and distinction between Elongisporangium and Globisporangium is
not resolved with support (Fig. 21, Uzuhashi et al. 2010).
Additionally, the genera Pythiogeton and Lagena seem to
be phylogenetically situated within, or closely related to
Pythium emend Uzuhashi, Tojo and Kakishima (Fig. 21,
Huang et al. 2013a), so even this revised version of
Pythium is paraphyletic. For these reasons investigators
have generally been slow to adopt the proposed genera.
Following this trend references to “Pythium” in this manuscript refer to Pythium s.l. (i.e. Pythium Pringsheim)
unless stated otherwise.
Species identification and numbers
A combined list of Pythium species in MycoBank
(2014) and Index Fungorum (2014) includes a total of
Fig. 21 Maximum likelihood phylogeny of Pythium s.l. and related
genera based on the concatenated 18S rRNA, ITS, 28S rRNA,
cytochrome c oxidase subunit 2 (cox2), and β-tubulin regions.
Bootstrap support values below 60 % are not indicated. Strains in bold
typeface represent type-derived material, authentic strains or strains used
by Van der Plaats-Niterink (1981) for descriptions. The 11 clades (A–K)
of Lévesque and de Cock (2004) and the genera erected by Bala et al.
(2010) and Uzuhashi et al. (2010) are indicated on the right along with
related taxa such as Phytophthora, Lagenidium, Lagena, and Pythiogeton
82
328 names of which several are either synonyms, orthographic variants or varieties that are rarely referred to
and are possibly synonyms of other species (i.e. all
varieties excluding varieties of P. ultimum). Excluding
such cases along with putative synonyms based on cox1
and ITS sequence homology as identified by Robideau
et al. (2011) leaves more or less 230 species of
Pythium. Undoubtedly this number still includes species
that should be synonymized and/or transferred to genera
other than Pythium (Van der Plaats-Niterink 1981; Dick
1990, 2001), but for now this should serve as a rough
Fungal Diversity (2014) 67:21–125
estimate of the number of actual Pythium species discovered to date. Of these species 152 (66 %) are known
to be represented by sequence(s) in GenBank, including
at least 123 (53 %) species for which type-material, extype strains or strains described by Van der PlaatsNiterink (1981) were used to generate sequence data
(Table 19, Fig. 21).
Identification of Pythium isolates to the species level is
generally straightforward when comparing both ITS and
cox1 sequences to that of ex-type, authentic or other reliable
representative strains. For this purpose the sequences
Fungal Diversity (2014) 67:21–125
Fig. 21 (continued)
83
84
Table 19 Pythium. Strain numbers, host information and GenBank accession numbers for species included in Fig. 21
Species
Isolate
Host
GenBank accession numbers
SSU
ITS
LSU
cox2
β- tubulin
DAOM BR89-12
CBS 580.84
ATCC 6680
DAOM 242348
CBS 127284
CBS 127285
CBS 127283
DAOM 242886
LEV6103
LEV6562
P1319
P8495
DAOM 238986
UZ300
Triticum aestivum
Mosquito larva
Pandalus borealis
Soil nematode
Soil nematode
Soil nematode
Soil nematode
Soil nematode
Soil nematode
Oedogonium sp.
Capsicum annuum
Beaucamea sp.
Soil (Musa sp.)
Soil
KJ716869
KJ716868
AB284577
KJ716871
HQ343198
HQ343197
HQ343199
N/A
KJ716870
KJ716873
JN635215
JN635088
HQ643396
N/A
KJ716869
KJ716868
AB285498
KJ716871
HQ111472
HQ111470
HQ111471
KJ716872
KJ716870
KJ716873
FJ801727
FJ802007
HQ643396
AB458660
KJ716869
KJ716868
AB285220
KJ716871
HQ395652
HQ395651
HQ395653
KJ716872
KJ716870
N/A
EU079741
EU079953
HQ643396
AB458651
KJ595434
KJ595392
AF290311
KJ595438
HQ605945
HQ660435
HQ680580
KJ595442
KJ595441
KJ595443
GU221958
GU221971
KJ595436
AB458820
N/A
KJ595516
N/A
KJ595561
N/A
N/A
N/A
KJ595565
KJ595564
KJ595566
EU079737
EU079949
KJ595559
N/A
Pilasporangium apinafurcum
Pythiogeton zeae
Pythium abappressorium
P. acanthicum
P. acanthophoron
P. acrogynum
P. adhaerens
P. afertile
P. amasculinum
P. anandrum
P. angustatum
P. aphanidermatum
P. apiculatum
P. apleroticum
UZ301
ATCC MYA-862
CBS 110198
CBS 377.34
CBS 337.29 (AUTH)
CBS 549.88 (AUTH)
CBS 520.74
LEV2066
CBS 552.88 (AUTH)
CBS 285.31
CBS 522.74 (VdPN)
CBS 118.80
CBS 120945
CBS 772.81
Soil
Zea mays
Triticum aestivum
Solanum tuberosum
Ananas sativus
Soil (Spinacia oleracea)
Soil
Turf grass
soil (vegetable garden)
Rheum rhaponticum
Soil
Unknown
soil (Vitis sp.)
Nymphyoides peltata
N/A
N/A
HQ643408
AY598617
AY598711
N/A
AY598619
N/A
AY598671
AY598650
AY598623
AY598622
HQ643443
AY598631
AB458657
HQ643405
HQ643408
AY598617
AY598711
AY598638
AY598619
HQ643416
AY598671
AY598650
AY598623
AY598622
HQ643443
AY598631
AB458652
HQ665310
HQ643408
AY598617
AY598711
AY598638
AY598619
HQ643416
AY598671
AY598650
AY598623
AY598622
HQ643443
AY598631
AB458818
N/A
KJ595409
KJ595380
KJ595376
AB362324
KJ595386
KJ595440
KJ595390
AB362328
KJ595387
KJ595344
KJ595422
KJ595400
N/A
N/A
KJ595533
KJ595504
KJ595500
KJ595458
KJ595510
KJ595563
KJ595514
KJ595450
KJ595511
KJ595472
KJ595547
KJ595524
P. aquatile
P. aristosporum
P. arrhenomanes
P. attrantheridium
CBS 215.80
CBS 263.38
CBS 324.62 (VdPN)
DAOM 230386
Soil
Triticum aestivum
Zea mays
Prunus serotina
AY598632
AY598627
AKXY02050628
HQ643476
AY598632
AY598627
AY598628
HQ643476
AY598632
AY598627
AY598628
HQ643476
KJ595355
AB507410
AKXY02053172
AB512889
KJ595481
DQ071297
KJ595451
AB512822
P. boreale
CBS 551.88
Soil
AY598662
AY598662
AY598662
EF408876
EF408882
Fungal Diversity (2014) 67:21–125
Lagena radicicola
Lagenidium giganteum
Lagenidium myophilum
Lagenidium sp. PWL-2010e
Lagenidium sp. PWL-2010f
Lagenidium sp. PWL-2010h
Lagenidium sp. PWL-2010i
Lagenidium sp. SLG-2014a
Lagenidium sp. SLG-2014a
Lagenidium sp. SLG-2014b
Phytophthora capsici
Phytophthora cinnamomi
Phytopythium sindhum
Pilasporangium apinafurcum
Species
Isolate
Host
GenBank accession numbers
SSU
ITS
LSU
cox2
β- tubulin
P. buismaniae
P. camurandrum
P. canariense
P. capillosum
P. carbonicum
P. carolinianum
P. catenulatum
P. caudatum
P. cederbergense
P. chamaehyphon
P. chondricola
P. citrinum
P. coloratum
P. conidiophorum
P. contiguanum
P. cryptoirregulare
P. cucurbitacearum
P. cylindrosporum
CBS 288.31
CBS 124059
CBS 112353
CBS 222.94
CBS 112544
CBS 122659
CBS 842.68 (VdPN)
CBS 584.85
CBS 133716
CBS 259.30 (AUTH)
CBS 203.85
CBS 119171
CBS 154.64
CBS 223.88
CBS 221.94
CBS 118731
CBS 748.96
CBS 218.94
Linum usitatissimum
Hordeum vulgare
Soil
Soil
Soil (spoil heap)
soil
Turf grass
Xiphinema rivesi
Aspalathus linearis
Carica papaya
Chondrus crispus
Soil (Vitis sp.)
Soil (tree nursery)
Soil
Soil (salt marsh)
Euphorbia pulcherrima
Unknown
Soil
AY598659
GQ244426
HQ643482
AY598635
HQ643373
N/A
AY598675
HQ643136
N/A
AY598666
N/A
HQ643375
AY598633
AY598629
HQ643514
HQ643515
AY598667
AY598643
AY598659
GQ244426
HQ643482
AY598635
HQ643373
HQ643484
AY598675
HQ643136
JQ412768
AY598666
AY598620
HQ643375
AY598633
AY598629
HQ643514
HQ643515
AY598667
AY598643
AY598659
GQ244426
HQ665069
AY598635
HQ643373
HQ665111
AY598675
HQ665277
KJ716864
AY598666
AY598620
HQ643375
AY598633
AY598629
HQ665162
HQ643515
AY598667
AY598643
KJ595368
KJ595433
JX397983
KJ595360
AB690678
KJ595427
KJ595404
AF290309
JQ412805
AB257280
KJ595354
AB690679
KJ595346
KJ595361
KJ595358
GU071763
AB690680
GU071762
KJ595493
KJ595558
JX397969
KJ595485
KJ595464
KJ595551
KJ595528
KJ595459
JQ412781
KJ595448
KJ595480
KJ595465
KJ595474
KJ595486
KJ595483
GU071888
KJ595460
GU071877
P. cystogenes
P. debaryanum
P. delawarense
P. deliense
P. diclinum
P. dimorphum
P. dissimile
P. dissotocum
P. echinulatum
CBS 675.85
CBS 752.96
CBS 123040
CBS 314.33
CBS 664.79
CBS 406.72
CBS 155.64
CBS 166.68 (VdPN)
CBS 281.64 (VdPN)
Vicia faba
Tulipa sp.
Glycine max
Nicotiana tabacum
Beta vulgaris
Pinus taeda
Pinus radiata
Triticum aestivum
Soil (forest nursery)
HQ643518
AY598704
KF853241
AY598674
N/A
AY598651
AY598681
AY598634
AY598639
HQ643518
AY598704
EU339312
AY598674
AY598690
AY598651
AY598681
AY598634
AY598639
HQ643518
AY598704
KF853240
AY598674
HQ665282
AY598651
AY598681
AY598634
AY598639
KJ595396
KJ595399
KJ595430
KJ595372
KJ595394
AB362331
KJ595347
KJ595351
AB362327
KJ595520
KJ595523
KJ595555
KJ595497
KJ595518
KJ595454
KJ595475
KJ595479
KJ595449
P. emineosum
P. erinaceum
P. flevoense
P. folliculosum
P. glomeratum
P. graminicola
CBS 124057
CBS 505.80
CBS 234.72
CBS 220.94
CBS 122644
CBS 327.62
Juniperus communis
Soil
Soil
Soil
Soil
Saccharum officinarum
N/A
N/A
AY598691
AY598676
N/A
AY598625
GQ244427
AY598694
AY598691
AY598676
HQ643542
AY598625
GQ244427
HQ665243
AY598691
HQ665160
HQ665097
AY598625
KJ595432
AB362326
KJ595363
N/A
KJ595424
AF196593
KJ595557
KJ595456
KJ595488
N/A
KJ595548
KJ595452
Fungal Diversity (2014) 67:21–125
Table 19 (continued)
85
86
Table 19 (continued)
Species
Isolate
Host
GenBank accession numbers
SSU
ITS
LSU
cox2
β- tubulin
AY598692
AY598653
AY598665
AY598654
AY598692
AY598653
AY598665
AY598654
AY598692
AY598653
AY598665
AY598654
KJ595367
AB362329
DQ071377
AB512919
KJ595492
KJ595453
AB511994
AB512850
AY598672
AY598693
AY598626
AY598637
AY598647
AY598702
AKYA02012602,
AKYA02013659
AY598672
AY598693
AY598626
AY598637
AY598647
AY598702
AKYA02013659,
AKYA02016578,
AKYA02016542
AY598648
HQ643671
HQ665259
HQ643386
HQ665071
HQ665099
HQ643681
HQ665163
HQ665119
KJ595364
AB362325
KJ595352
KJ595391
AB507410
GU071760
AKYA02009930,
AKYA02012077
KJ595489
KJ595447
N/A
KJ595515
AB512836
GU071886
AKYA02004337
JX397979
KJ595429
KJ595389
KJ595418
KJ595413
KJ595426
KJ595415
KJ595359
KJ595343
JX397965
KJ595553
KJ595513
KJ595543
KJ595538
KJ595550
KJ595540
KJ595484
KJ595554
CBS 286.79
CBS 393.54 (AUTH)
CBS 286.31 (AUTH)
CBS 450.67
Decaying leaf (Zostera marina)
Rumex acetosella
Phaseolus vulgaris
Soil (Sambucus)
P. hydnosporum
P. hypogynum
P. inflatum
P. insidiosum
P. intermedium
P. irregulare
P. iwayamai
CBS 253.60 (VdPN)
CBS 234.94
CBS 168.68 (VdPN)
CBS 574.85
CBS 266.38 (VdPN)
CBS 250.28
CBS 132417
Unknown
Soil
Saccharum officinarum
Equus ferus
Agrostis stolonifera
Phaseolus vulgaris
Poa annua
P. iwayamai
P. kashmirense
P. kunmingense
P. litorale
P. longandrum
P. longisporangium
P. lucens
P. lutarium
P. lycopersici
CBS 156.64 (VdPN)
CBS 122908
CBS 550.88
CBS 118360
CBS 112355
CBS 122646
CBS 113342
CBS 222.88
CBS 122909
AY598672
AY598693
AY598626
AF289981
AY598647
AY598702
AKYA02013211,
AKYA02014361,
AKYA02012602
Soil (Pinus sp.)
AY598648
Soil
HQ643671
Soil (Vicia faba)
AY598700
Soil (Phragmites australis)
HQ643386
Soil
HQ643679
Soil (Vitis sp.)
N/A
Triticum
HQ643681
Soil
HQ643682
Soil (Lycopersicum esculentum) N/A
P. macrosporum
CBS 574.80
Flower bulb
AY598646
AY598646
AY598646
AB512916
AB512842
P. mamillatum
P. marinum
P. marsipium
P. mastophorum
P. megacarpum
P. megalacanthum
P. mercuriale
P. middletonii
P. minus
P. monospermum
P. montanum
CBS 251.28 (VdPN)
CBS 750.96
CBS 773.81
CBS 375.72 (VdPN)
CBS 112351
CBS 101356
CBS 122443
CBS 528.74 (VdPN)
CBS 226.88
CBS 158.73 (VdPN)
CBS 111349
Beta vulgaris
Soil
Nymphyoides peltata
Apium graveolens
Soil (Vitis sp.)
Chrysanthemum
Macadamia integrifolia
Soil
Soil
Soil
Soil (Picea abies)
AY598703
N/A
N/A
AY598661
HQ643388
N/A
KF853243
N/A
HQ643696
HQ643697
HQ643389
AY598703
AY598689
AY598699
AY598661
HQ643388
HQ643693
DQ916363
AY598640
HQ643696
HQ643697
HQ643389
HQ665173
AY598689
HQ665297
AY598661
HQ643388
KJ716865
KF853236
AY598640
HQ665168
HQ643697
HQ643389
AB362325
KJ595398
KJ595401
KJ595378
AB690665
KJ595435
AB690666
AB362318
AB362320
KJ595350
KJ595410
AB512844
KJ595522
KJ595525
KJ595502
KJ595536
N/A
KJ595466
KJ595457
KJ595446
KJ595478
KJ595534
AY598648
HQ643671
AY598700
HQ643386
HQ643679
HQ643680
HQ643681
HQ643682
HQ643683
Fungal Diversity (2014) 67:21–125
P. grandisporangium
P. helicandrum
P. helicoides
P. heterothallicum
Species
Isolate
Host
GenBank accession numbers
SSU
ITS
LSU
cox2
β- tubulin
P. multisporum
P. myriotylum
P. nagaii
P. nodosum
P. nunn
CBS 470.50
CBS 254.70
CBS 779.96
CBS 102274
CBS 808.96
Soil
Arachis hypogaea
Soil
Soil
Soil
AY598641
AY598678
AY598705
N/A
AY598709
AY598641
AY598678
AY598705
HQ643709
AY598709
AY598641
AY598678
AY598705
HQ665055
AY598709
AB362319
KJ595365
KJ595402
KJ595407
AF196609
KJ595455
KJ595490
KJ595526
KJ595531
DQ071325
P. oedochilum
P. okanoganense
P. oligandrum
P. oopapillum
P. ornacarpum
P. ornamentatum
P. orthogonon
P. ostracodes
P. pachycaule
P. paddicum
P. paroecandrum
P. parvum
P. pectinolyticum
P. periilum
P. periplocum
P. perplexum
P. phragmitis
P. pleroticum
CBS 292.37 (AUTH)
CBS 315.81
CBS 382.34 (VdPN)
CBS 124053
CBS 112350
CBS 122665
CBS 376.72
CBS 768.73 (VdPN)
CBS 227.88
CBS 698.83
CBS 157.64 (VdPN)
CBS 225.88
CBS 122643
CBS 169.68 (VdPN)
CBS 289.31
CBS 674.85
CBS 117104
CBS 776.81
Unknown
Triticum aestivum
Viola sp.
Cucumis sativus
Soil
Soil
Zea mays
Soil
Soil
Triticum and Hordeum
Soil
Soil
Soil
Soil
Citrullus vulgaris
Vicia faba
Soil (Phragmites australis)
Nymphyoides peltata
AY598664
AY598649
AY598618
N/A
HQ643721
N/A
AY598710
AY598663
AY598687
AY598707
AY598644
AY598697
HQ643739
AY598683
AY598670
AY598658
HQ643746
AY598642
AY598664
AY598649
AY598618
FJ655174
HQ643721
HQ643722
AY598710
AY598663
AY598687
AY598707
AY598644
AY598697
HQ643739
AY598683
AY598670
AY598658
HQ643746
AY598642
AY598664
AY598649
AY598618
FJ655174
HQ643721
HQ665117
HQ665221
AY598663
HQ665169
AY598707
AY598644
AY598697
HQ643739
HQ665141
AY598670
AY598658
HQ665081
AY598642
AB108011
KJ595373
KJ595381
KJ595431
KJ595411
KJ595428
KJ595379
AB690668
KJ595362
JX397982
DQ071391
AB362322
N/A
N/A
KJ595369
KJ595395
AJ890351
AB362321
EF408883
KJ595498
KJ595505
KJ595556
KJ595535
KJ595552
KJ595503
EF408880
KJ595487
JX397968
DQ071332
KJ595445
KJ595469
KJ595444
KJ595494
KJ595519
EU152854
KJ595461
P. plurisporium
P. polare
P. polymastum
P. porphyrae
CBS 100530
CBS 118203
CBS 811.70 (VdPN)
CBS 369.79 (VdPN)
Agrostis
Sanionia uncinata
Lactuca sativa
AY598684
KJ716858
AY598660
AY598684
AB299390
AY598660
AY598684
KJ716859
AY598660
KJ595405
KJ595417
KJ595403
KJ595529
KJ595542
KJ595527
P. prolatum
P. pyrilobum
P. radiosum
P. recalcitrans
P. rhizo-oryzae
P. rhizosaccharum
CBS 845.68
CBS 158.64
CBS 217.94
CBS 122440
CBS 119169
CBS 112356
Porphyra yezoensis
Rhododendron sp.
Pinus radiata
Soil
Soil (Vitis vinifera)
Soil
Soil (Saccharum officinarum)
AY598673
AY598652
AY598636
N/A
N/A
HQ643757
N/A
AY598673
AY598652
AY598636
AY598695
DQ357833
HQ643757
HQ643760
AY598673
AY598652
AY598636
HQ665156
KJ716861
HQ643757
HQ665072
KJ595377
AB362330
KJ595349
KJ595356
KJ595423
KJ595420
AB362323
KJ595501
KJ595462
KJ595477
N/A
EF195143
KJ595545
KJ595463
Fungal Diversity (2014) 67:21–125
Table 19 (continued)
87
88
Table 19 (continued)
Species
Isolate
Host
GenBank accession numbers
SSU
ITS
LSU
cox2
β- tubulin
CBS 115464
CBS 533.74
CBS 471.50 (VdPN)
CBS 129726
CBS 294.37 (AUTH)
CBS 112354
CBS 129728
CBS 122490
CBS 119359
CBS 113341
CBS 101876
STE-U 7549
STE-U 7550
CBS 122645
CBS 275.67 (VdPN)
CBS 462.48 (VdPN)
DAOM 240293
CBS 110030
Soil (Malus sp.)
Soil
Lupinus angustifolius
Glycine max
Ipomoea batatas
Soil
Zea mays
Soil (forest)
Phaseolus vulgaris
Soil
Arabidopsis thaliana
Aspalathus linearis
Aspalathus linearis
Soil (Vitis sp.)
Compost
Unknown
Soil
Soil
HQ643761
AY598696
AY598630
N/A
AY598680
HQ643772
N/A
HQ643773
N/A
KF853244
HQ643778
N/A
N/A
KF853242
AY598701
AY598655
N/A
N/A
HQ643761
AY598696
AY598630
JF836869
AY598680
HQ643772
JF836871
HQ643773
EF688275
KF853244
HQ643778
JQ412770
JQ412777
KF853242
AY598701
AY598655
KJ716866
HQ643836
HQ643761
AY598696
AY598630
KJ716862
AY598680
HQ643772
KJ716863
HQ643773
KJ716860
KF853244
HQ643778
KJ716867
N/A
KF853242
AY598701
AY598655
KJ716866
HQ665059
KJ595416
KJ595388
KJ595384
JF895530
KJ595370
KJ595412
JF895532
AB362317
KJ595421
KJ595414
KJ595406
JQ412783
JQ412813
KJ595425
KJ595366
AB512921
KJ595437
KJ595408
KJ595541
KJ595512
KJ595508
KJ595470
KJ595495
KJ595537
KJ595471
KJ595467
KJ595546
KJ595539
KJ595530
JQ412807
JQ412789
KJ595549
KJ595491
AB512852
KJ595560
KJ595532
P. sulcatum
P. sylvaticum
P. takayamanum
P. tardicrescens
P. torulosum
P. tracheiphilum
P. ultimum var. sporangiiferum
P. ultimum var. ultimum
CBS 603.73
CBS 453.67
CBS 122491
LEV1534
CBS 316.33 (VdPN)
CBS 323.65
CBS 219.65
Daucus carota
Soil
Soil
Turf grass
Grass
Lactuca sativa
Chenopodium album
AY598682
AY598645
HQ643854
N/A
AY598624
N/A
AKYB02045405
AY598682
AY598645
HQ643854
HQ643855
AY598624
AY598677
AY598656
HQ665281
AY598645
HQ643854
HQ643855
AY598624
HQ665207
AY598656
KJ595393
KJ595383
AB362315
KJ595439
KJ595374
KJ595375
KJ595357
KJ595517
KJ595507
KJ595468
KJ595562
KJ595499
N/A
KJ595482
CBS 398.51
CBS 518.77
CBS 157.69 (VdPN)
CBS 295.37
CBS 119.80 (VdPN)
CBS 119168
CBS 132.37
CBS 159.64 (VdPN)
Lepidium sativum
Lactuca sativa
Soil (Pinus sp.)
Triticum aestivum
Soil
Soil (Vitis sp.)
Viola tricolor
Soil
AY598657
AY598712
AY598708
AY598685
HQ643400
HQ643956
AY598717
AY598706
AY598657
AY598712
AY598708
AY598685
HQ643400
HQ643956
AY598717
AY598706
AY598657
AY598712
AY598708
AY598685
HQ643400
HQ643956
AY598717
AY598706
KJ595382
KJ595385
KJ595348
KJ595371
GU133518
KJ595419
KJ595345
JX397980
KJ595506
KJ595509
KJ595476
KJ595496
EF426556
KJ595544
KJ595473
JX397966
P. uncinulatum
P. undulatum
P. vanterpoolii
P. vexans
P. viniferum
P. violae
P. violae
Fungal Diversity (2014) 67:21–125
P. rostratifingens
P. rostratum
P. salpingophorum
P. schmitthenneri
P. scleroteichum
P. segnitium
P. selbyi
P. senticosum
P. solare
P. sp.
P. sp. “jasmonium”
P. sp. rooibos 2
P. sp. rooibos 2
P. spiculum
P. spinosum
P. splendens
P. stipitatum
P. sukuiense
89
Species names of type strains (including ex-type, type, neotype, holotype, isotype, and paratype material), authentic strains (AUTH), and strains used by Van der Plaats-Niterink (1981) for descriptions
(VdPN) are indicated in bold. Details regarding amplification and sequencing are included in GenBank records for sequence data generated de novo for this analysis
N/A
KJ595521
N/A
KJ595353
KJ595397
N/A
HQ665143
AY598686
HQ665155
AY598715
AY598686
AY598679
AY598715
AY598686
N/A
CBS 178.86
CBS 699.83
CBS 216.82
P. violae
P. volutum
P. zingiberis
Daucus carota
Triticum and Hordeum
Zingiber mioga
ITS
SSU
Isolate
Species
Table 19 (continued)
Host
GenBank accession numbers
LSU
cox2
β- tubulin
Fungal Diversity (2014) 67:21–125
generated by Lévesque and de Cock (2004) and Robideau
et al. (2011) are excellent resources. Using only the ITS region
would more often than not allow suitably accurate species
identification, but some species are indistinguishable using
ITS and require cox1 sequences for further identification
(see Text S1A of Robideau et al. 2011). Several other species
are indistinguishable even when both ITS and cox1 sequences
are compared (see Text S1B of Robideau et al. 2011), and
many of these should probably be formally synonymized
pending more thorough investigations with multiple hypervariable genes. This approach should also resolve species
complexes found in the group formed by P. irregulare,
P. paroecandrum, P. cylindrosporum, P. cryptoirregulare
and P. mamillatum (Barr et al. 1997; Matsumoto et al. 2000;
Garzón et al. 2007; Spies et al. 2011a), the varieties of
P. ultimum (Barr et al. 1996), and the P. vexans and
P. cucurbitacearum group (Spies et al. 2011b). Some species
epithets have been applied to multiple phylogenetic species
due to imprecise species descriptions and/or misidentificat i o n s . E x a m p l e s o f t h e s e i n c l u d e P. i w a y a m a i ,
P. okanoganense and P. violae (Lévesque and de Cock 2004;
McLeod et al. 2009; Bahramisharif et al. 2013). Mislabelling
or contamination of reference strains and/or data cause similar
problems, as illustrated by the case of P. terrestre (published as
“terrestris”) of which the holotype strain ITS sequence published with the description suggests phylogenetic placement in
clade E (Paul 2002), while the ITS and cox1 sequences generated for the ex-type strain available from the Centraal
Bureau voor Schimmelcultures (CBS) suggests phylogenetic
placement in clade F (Robideau et al. 2011). Species identification within genetically diverse species complexes (see Text
S1C of Robideau et al. 2011 for a partial list) can also be
tricky, more due to uncertain species boundaries than due to
the ineffectiveness of ITS and/or cox1 as barcoding regions.
The onus is on the investigator to keep such issues in mind
when identifying strains to the species level and to consider
the identification in context of the taxonomic history of the
species and its closest relatives.
Molecular phylogeny
The first molecular phylogenies of Pythium were inferred
from sequences of the 28S, ITS, and cox2 regions respectively, and although each analysis included only a few
species, the observed variation merited speculation regarding the polyphyletic nature of Pythium at least for the ITS
and 28S phylogenies (Briard et al. 1995; Cooke et al. 2000;
Martin 2000). The first study to provide an extensive DNA
sequence based phylogeny of Pythium was that of
Lévesque and de Cock (2004) who sequenced the 28S
region of 51 species and complete ITS region (ITS1-5.8S
rRNA-ITS2) region of 116 species. Although a two-marker
phylogeny of the ITS-28S region was presented by
90
Fungal Diversity (2014) 67:21–125
Lévesque and de Cock (2004), these markers are adjacent
multi-copy markers that might not accurately represent the
evolutionary relationships in Pythium. Villa et al. (2006)
used multiple markers (ITS, cox2, β-tubulin) in individual
phylogenetic analyses with 39 species and confirmed previous suggestions of an intermediate evolutionary position
of clade K species between Pythium and Phytophthora, but
also suggested that clade H species (represented by
Phytophthora undulata ≡ Pythium undulatum) occupy a
similar intermediate position, which contrasted the position
of this clade nestled among clades E, F, G, I, and J as
suggested by Lévesque and de Cock (2004). The multimarker phylogeny (18S-ITS-28S, cox2 and β-tubulin) of
152 Pythium species and some related taxa presented here
confirms the association of clade K with Phytophthora, but
fails to provide support for the evolutionary association of
clade H with any of the other recognized groups within
Pythium (Fig. 21). Furthermore, organisms such as the
obligate root pathogen Lagena radicicola and strains resembling Lagenidium form an unresolved cluster of taxa
related to clade C (Fig. 21). In itself this phylogenetic
placement of the genus Lagena necessitates a further taxonomic revision of the genus Pythium that can only be
achieved once the internal nodes of the Pythium phylogeny
have been resolved with support. Despite the fact that the
phylogeny in Fig. 21 represents the most extensive sampling of taxa and genetic markers in a multi-marker phylogeny of Pythium to date, it still fails to achieve this goal.
Phylogenetic markers additional or alternative to those currently used in Pythium systematics are needed to resolve
these issues and elucidate taxon boundaries.
Recommended genetic markers
&
&
&
The 18S (small subunit, SSU) and 28S (large subunit,
LSU) nuclear rRNA genes–generic level phylogenies
within Pythium s.l.
The internal transcribed spacers (ITS including ITS1, 5.8S
rRNA, and ITS2), cytochrome c oxidase subunit 2 (cox2)–
sub-generic, inter- and intra-specific level phylogenies
ITS and cox1–non-phylogenetic species identification
Mitochondrial regions such as cox1 and cox2 should be
used with consideration of the fact that they mainly reflect
evolution of maternal lineages and can produce incongruent
phylogenies. This is especially true for cox1, which is why this
region was not included in Fig. 21. The β-tubulin region has
also been used to a limited extent in Pythium phylogenies
(Villa et al. 2006; Belbahri et al. 2008; Spies et al. 2011a, b).
Although this region fails to resolve Pythium into the genera
observed when using the dataset from Fig. 21 (data not
shown) and has limited power in resolving species-level phylogenies (Spies et al. 2011a, b), it amplifies and sequences
well for most Pythium species and is an easy resource for use
in concatenated datasets (e.g. Bahramisharif et al. 2013;
Fig. 21).
Pyrenophora
Background
Pyrenophora represents a genus of plant pathogenic fungi
associated with a wide variety of substrates. Fries (1849) list
the genus as Pyrenophora typified with Pyrenophora
phaeocomes. The genus Pyrenophora clusters in the suborder
Pleosporineae of the family Pleosporaceae (Berbee 1996;
Zhang and Berbee 2001; Hyde et al. 2013a, b; Zhang et al.
2012; Ariyawansa et al. 2014). Recent studies using multigene analysis and some coupled with morphology have provided the groundwork for classification of species in
Pyrenophora (Berbee 1996; Zhang and Berbee 2001; Hyde
et al. 2013a, b; Zhang et al. 2012).
Pyrenophora has been linked to asexual morphs in
Drechslera. Pyrenophora species are important plant pathogens as well as saprobes. Many species cause disease on their
graminicolous hosts and are usually present in their asexual
state (Drechslera) (Zhang and Berbee 2001). Species of
Pyrenophora are serious plant pathogens (Zhang and Berbee
2001). Pyrenophora teres (Drechslera teres) is a necrotrophic
pathogen of economically important crops, such as barley
(Gupta and Loughman 2001; Kingsland 1991). Pyrenophora
graminea (Drechslera graminea) causes barley stripe
resulting in significant yield losses (Tekauz 1983, 1990).
Pyrenophora graminea lives within barley kernels as mycelium, and when seeds germinate, hyphae enter the seedling
through the coleorrhiza, causing a systemic infection
(Platenkamp 1976; Porta-Puglia et al. 1986). Pyrenophora
tritici-repentis causes tan spot of wheat (Lamari and Bernier
1989) which occurs in all the major wheat-growing areas of
the world and causes 3 to 50 % yield losses (Ballance et al.
1996). Its prevalence has increased recently.
Some Pyrenophora species have been used as biocontrol
agents. Bromus tectorum is a dominant winter annual weed in
cold deserts of the western United States (Meyer et al. 2007).
Together with other annual brome grasses it has invaded many
ecosystems of the western United States creating nearmonocultures in which the native vegetation cannot compete
(Meyer et al. 2007). Pyrenophora semeniperda has be used as
a biocontrol agent to kill the dormant seeds of Bromus
tectorum (Meyer et al. 2007). Several studies have assessed
chemical production by Pyrenophora species. A new phytotoxic sesquiterpenoid penta-2,4-dienoic acid (pyrenophoric
acid) was isolated from solid wheat seed culture of
P. semeniperda.
Fungal Diversity (2014) 67:21–125
Species identification and numbers
Pyrenophora is characterized by immersed, erumpent to nearly superficial ascomata, indefinite pseudoparaphyses, clavate
to saccate asci usually with a large apical ring, and muriform
terete ascospores. Morphologically, the terete ascospores of
Pyrenophora can be easily distinguished from Clathrospora
and Platyspora. The indefinite pseudoparaphyses and smaller
ascospores of Pyrenophora can be clearly separated from
those of Pleospora (Sivanesan 1984). Pyrenophora species
can easy be distinguished from species in Cochliobolus and
Setosphaeria on the basis of the shape, septation and colour of
the ascospores (Zhang and Berbee 2001). Drechslera species
were initially categorized in Helminthosporium on the basis of
their dark colour, transversely septate conidia and a
graminicolous habitat (Shoemaker 1959). Consequently,
graminicolous Helminthosporium species were segregated
into three genera, Bipolaris, Drechslera, and Exserohilum,
defined based on their association with their sexual states
Cochliobolus, Pyrenophora, or Setosphaeria, respectively
(Zhang and Berbee 2001). Currently 198 species of
Pyrenophora and 135 species of Drechslera are listed in
Index Fungorum (2014).
Molecular phylogeny
Rapid identification of diseases caused by Pyrenophora has
been determined via different DNA markers. Identification of
molecular genetic markers in Pyrenophora teres f. teres associated with low virulence on ‘Harbin’ barley was assessed by
random amplified polymorphic DNA (RAPD) (Weiland et al.
1999) and five RAPD markers were obtained that were associated in coupling with low virulence. The data suggested that
the RAPD technique can be used to tag genetic determinants
for virulence in P. teres f. teres (Weiland et al. 1999). Specific
polymerase chain reaction (PCR) primers were developed
from amplified fragment length polymorphism (AFLP) fragments of P. teres, in order to distinguish the two forms, P. teres
f. teres (which cause net form blotch on barley leaves) and
P. teres f. maculata (which causes spot form); the two forms
are morphologically very similar in culture (Leisova et al.
2005). The PCR assay was certified with 60 samples of
Pyrenophora species. The amplification with four designed
PCR primer pairs provided P. teres form-specific products. No
cross-reaction was observed with DNA of several other species, such as P. tritici-repentis and P. graminea (Leisova et al.
2005). Pyrenophora graminea is the causal agent of barley
leaf stripe disease (Mokrani et al. 2012). Two leaf stripe
isolates PgSy3 (exhibiting high virulence on the barley cultivar ‘Arabi Abiad’) and PgSy1 (exhibiting low virulence on
Arabi Abiad), were mated and 63 progeny were isolated and
phenotyped for the reaction on Arabi Abiad (Mokrani et al.
2012). From 96 AFLP markers, three AFLP markers,
91
E37M50-400, E35M59-100 and E38M47-800 were linked
to the virulence locus VHv1 in isolate PgSy3. Lubna et al.
(2012) suggested that the three markers are closely linked to
VHv1 and are unique to isolates carrying the virulence locus.
Pecchia et al. (1998) developed an efficient PCR protocol for
amplification of the IGS region in P. graminea and to characterize this region by restriction fragment analysis. During the
study based on the length of the IGS-PCR product, ca. 3.8 or
4.4 kb, two groups of isolates were identified from six cultures
i.e. I3/88 (Italy; CBS 100862), I7/88 (Italy; CBS100861), 60/
93 (Austria; CBS 100866), I10/95 (Tunisia; CBS 100863),
I28/95 (Tunisia; CBS 100864), I33/95 (Tunisia; CBS
100865). The RFLP patterns of isolates obtained with the 6base cutting enzymes ApaI, BglII, DraI, EcoRV, HindIII and
SacI were similar within each group and different between the
two groups (Pecchia et al. 1998). Restriction patterns of IGSPCR products digested with the 4-base cutting enzyme AluI
were polymorphic among isolates in spite of their IGS-PCR
product length (Pecchia et al. 1998).
Molecular studies of Pyrenophora/Drechslera species
have detailed the taxonomic placement of the genus. Initially
the 18S rRNA gene was used for the classification of
Pyrenophora/Drechslera and related genera (Berbee 1996).
Phylogenetic analysis based on 18S rRNA showed
Pyrenophora to cluster within the Pleosporaceae (Zhang
and Berbee 2001) rather than in Pyrenophoraceae (Zhang
and Berbee 2001). Later, phylogenetic analysis of the ITS
and gdp data showed that Pyrenophora is monophyletic
(Zhang and Berbee 2001), and the asexual state Drechslera
clustered with their predicted sexual relatives (Table 20,
Fig. 22).
Recommended genetic markers
&
&
Large small subunits of nrDNA (LSU)–generic level
ITS and gdp–inter-specific delineation
Based on our phylogeny, we observed that gdp gives high
resolution compared to ITS and LSU, such that it can be
readily used to determine the placement of Pyrenophora
species.
Puccinia
Background
Puccinia is the type genus of the family Pucciniaceae in the
order of rust fungi, Pucciniales (Basidiomycota). Puccinia has
approximately 4,000 named species (Kirk et al. 2008), and is a
widespread genus of plant pathogens that has shaped history.
For example, Puccinia graminis, the type species of Puccinia,
92
Table 20 Pyrenophora. Details
of the isolates used in the
phylogenetic tree
Ex-type (ex-epitype) strains are
bolded and marked with an * and
voucher stains are bolded
Fungal Diversity (2014) 67:21–125
Species
Isolate
GenBank accession numbers
ITS
LSU
GPDH
Drechslera andersenii
D. andersenii
CBS 258.80
CBS 967.87
AY004804
AY004805
AY004835
D. andersenii
D. avenae
D. avenae
D. biseptata
DAOM 229292
CBS 189.29
CBS 279.31
DAOM 208987
JN943646
AY004795
AY004796
AY004786
JN940084
D. biseptata
D. biseptata
D. biseptata
D. campanulata
CBS 308.69
CBS 599.7
CBS 108940
BRIP15927
JN712464
AY004787
AY004788
AF163058
JN712530
D. catenaria
D. catenaria
D. dactylidis
D. dematioidea
DAOM 63665A
CBS 191.29
DAOM 92161
CBS 108963
AY004802
AY004803
AY004781
AY004789
JN712532
AY004833
AY004834
AY004812
AY004820
D. dematioidea
D. dematioidea
D.dematioidea
Drechslera dictyoides
DAOM 229295
CBS 108962
CBS 108962
DAOM 63666
JN943648
JN712465
AY004790
AY004806
JN940094
JN712531
JN712531
JN940080
AY004821
AY004836
D. erythrospila
D. erythrospila
D. fugax
D.nobleae
CBS 108941
DAOM 55122
CBS 509.77
CBS 259.80
AY004782
AY004783
AY004791
AY004792
D. nobleae
D. nobleae
D. nobleae
D. phlei
DAOM 229296
CBS 966.87
CBS 316.69
CBS 315.69
JN943647
AY004793
AY004794
AY004807
JN940095
D. phlei
D. poae
D. poae
D. siccans
DAOM 225627
DAOM 145373
DAOM 169240
DAOM 115701
JN943656
AY004801
JN943651
AY004797
JN940077
JN940082
D. siccans
Drechslera sp.
Drechslera sp.
Drechslera sp
DAOM 115702
DAOM126766
DAOM126772
CBS313.69
AY004799
AY004800
AY004784
AY004785
D. triseptata
Pleospora herbarum
Pyrenophora bromi
P. chaetomioides
NZ6120
CBS 191.86*
DAOM 127414
DAOM 208989
AF163059
DQ491516
AY004809
AF081445
P. dictyoides
P. japonica
P. lolii
DAOM 75616
DAOM 169286
CBS 318.69
JN943654
AF071347
AY004798
JN940079
P. phaeocomes
P. semeniperda
P. tetrarrhenae
P. tritici-repentis
DAOM 222769
DAOM 213153
DAOM 171966
DAOM 226213
JN943649
AF081446
JN943663
JN943670
DQ499596
JN940089
JN940090
AY544672
P. tritici-repentis
P. tritici-repentis
P. graminea
P. teres
DAOM 208990
DAOM 107224
11
PM2
AF071348
AY004808
Y10748
Y08746
JN940071
DQ384097
AY004827
AY004828
AY004817
AY004819
AY004818
AY004813
AY004814
AY004822
AY004823
AY004824
AY004825
AY004837
AY004832
JN940078
AY004831
AY004815
AY004816
DQ247804
JN940074
JN940091
AY316969
AY004839
AF081371
AF081369
AY004829
AY004826
AF081370
AY004838
AY004830
Fungal Diversity (2014) 67:21–125
93
Fig. 22 Phylogram generated from parsimony analysis based on combined of ITS, gdp and LSU sequenced data of Pyrenophora. Parsimony
bootstrap support values greater than 50 % are indicated above the nodes.
The ex-type (ex-epitype) and voucher strains are in bold. The tree is
rooted with Pleospora herbarum CBS 276.37
was investigated as a biological warfare agent in the cold war
(Line and Griffith 2001). It was the impetus for breeding
wheat cultivars resistant to disease that started the Green
Revolution, lead by 1970 Nobel Laureate, Norman Borlaug
(Zeyen et al. 2014). Epidemics of stem rust of wheat caused
by P. graminis remain a threat with the emergence of races
such as Ug99 (Singh et al. 2011). Other species of Puccinia
are also serious pathogens of grasses (Poaceae), including
P. coronata and P. striiformis (Kirk et al. 2008). Rusts of
Asteraceae, e.g., P. helianthi, and rusts of Fabaceae in the
closely related genus Uromyces, e.g., U. viciae-fabae,
U. appendiculatus and U. ciceris-arietini, are important pathogens of cultivated fodder and food crops.
Among the ca. 120 to 160 genera of rust fungi (Cummins
and Hiratsuka 2003; Kirk et al. 2008), Puccinia is readily
recognized by the two-celled teliospores and the shape of
94
the spermogonia (Cummins and Hiratsuka 2003). Uromyces
with one-celled teliospores is typically differentiated from
Puccinia, although some species of Puccinia have both onecelled (mesospores) and two-celled teliospores, e.g.,
P. lagenophorae. Teliospore morphology is homoplasious,
and Puccinia and Uromyces were polyphyletic in systematic
studies based on the LSU and SSU regions of nuclear ribosomal DNA (Maier et al. 2007; Aime 2006), and the two
nuclear genes: elongation factor and β- tubulin (Van der
Merwe et al. 2007). Some rust fungi have teliospores morphologically similar to Puccinia, but are not closely related or
have an uncertain systematic position. For example, Allodus
podophylli has two-celled teliospores convergent with
Puccinia. A systematic analysis based on the nLSU and
nSSU regions of rDNA determined Allodus and Puccinia
were unrelated (Minnis et al. 2012). Puccinia psidii, which
spread from South America to much of the Pacific region and
South Africa, now infects 30 genera of Myrtaceae out of its
natural host range (Pegg et al. 2013). It has two-celled teliospores, but its placement within the Pucciniales is unknown.
Phylogenetic analyses of the nLSU and nSSU (Pegg et al.
2013) and the protein coding gene beta-tubulin (Van Der
Merwe et al. 2008) indicated that P. psidii was sister to the
Pucciniaceae. Several families and genera of rust fungi are
polyphyletic, namely the Raveneliaceae, Phakopsoraceae and
Pucciniaceae. These polyphyletic families and genera await
resolution by molecular phylogenetic analyses.
Species identification and numbers
Rust fungi are usually considered host specific (Cummins and
Hiratsuka 2003), although some, e.g., Puccinia psidii and
P. lagenophorae, infect multiple host genera (McTaggart
et al. 2014; Pegg et al. 2013). Some species of rust fungi are
heteroecious, requiring two hosts in different families to complete their life cycle, e.g., P. graminis on Triticum (Poaceae)
and Berberis (Berberidaceae).
Rust fungi have a complicated life cycle with up to five
spore states (Cummins and Hiratsuka 2003). Consequently, up
to three names have been proposed for the same taxon based
on different life cycle stages. To add to the confusion, there are
two systems of terminology that describe these spore states,
one based on morphology (Laundon 1967), and the other on
ontogeny (Arthur and Kern 1926; Cummins and Hiratsuka
2003; Hiratsuka 1973). These systems of terminology were
summarised by Hennen and Hennen (2000).
Species of rust fungi are often identified on the basis of their
host specificity, and monographs were organised by plant family
(Sydow and Sydow 1904; McAlpine 1906; Cummins 1971,
1978). Morphological characters of the teliospores and
urediniospores, such as size, apex shape and wall thickness,
ornamentation, and germ pore position and number, are useful
for species identification.
Fungal Diversity (2014) 67:21–125
Molecular diagnostic tools have been developed for some
species of Puccinia based on the ITS region of rDNA, e.g.,
P. coronata (Beirn et al. 2011; Pfunder et al. 2001), P. kuehnii
(Glynn et al. 2010) and P. psidii (Langrell et al. 2008). The ITS
region has successfully distinguished phylogenetic species in
Uromyces (Barilli et al. 2011) and it was used in combination
with TEF to resolve the taxonomy of P. melampodii (Seier
et al. 2009). However, the ITS region was polymorphic in
Puccinia lagenophorae (Littlefield et al. 2005; Scholler et al.
2011), and Morin et al. (2009) discovered a paralagous copy
of the ITS region, which may have resulted from a hybridization event. A paralagous copy of the ITS region was also
reported in P. kuehnii in the study by Virtudazo et al. (2001).
Polymorphisms and paralogous copies are caveats for studies
based on the ITS region in rust fungi.
Molecular phylogeny
Large-scale systematic studies of rust fungi have focused
mainly on the SSU and LSU regions of rDNA (Aime
2006; Beenken et al. 2012; Dixon et al. 2010; Maier
et al. 2003, 2007; Minnis et al. 2012; Wingfield et al.
2004; Yun et al. 2011) (Table 21). Protein coding genes
such as beta-tubulin (Morin et al. 2009; Van der Merwe
et al. 2007, 2008) and elongation factor (TEF) (Seier et al.
2009; Van der Merwe et al. 2007) were successfully used
at the family, genus and species level in rust fungi, although beta-tubulin required cloning rather than direct
sequencing of PCR product. Liu et al. (2013) included
ITS, beta-tubulin, ribosomal polymerase subunit 2 (RPB2)
and cytochrome c oxidase subunit 1 (COI) in a systematic
study to resolve the P. coronata species complex. They
discussed the difficulty of PCR amplification of older
herbarium specimens, and that DNA repair was
successful in some cases. Vialle et al. (2009) compared
mitochondrial genes to rDNA markers in two genera of
rusts, Chrysomyxa and Melampsora. They found rDNA
had better species resolution than mitochondrial genes.
Mitochondrial genes were since used in studies of the
genera Chrysomyxa (Feau et al. 2011) and Dasyspora
(Beenken et al. 2012), but have not yet been used for
Puccinia.
Recommended genetic markers
&
&
The large subunit of nrDNA (LSU)–is useful for genus
and species level identification of all rust fungi
The internal transcribed spacer (ITS)–is useful for species
level identification, but may contain polymorphic sites and
paralagous copies. Rust specific primers are recommended.
Rusts are obligate biotrophs and difficult to maintain in
pure culture, which has posed a challenge for DNA extraction
Fungal Diversity (2014) 67:21–125
Table 21 Puccinia. Details of the
isolates used in the phylogenetic
tree
Ex-type (ex-epitype) strains are
bolded and marked with an * and
voucher stains are bolded
95
Species
Isolate
Host
GenBank accession no.
LSU
SSU
Aecidium kalanchoe
BPI 843633
Kalanchoe blossfeldiana
AY463163
DQ354524
Allodus podophylli
Caeoma torreyae
Cumminsiella mirabilissima
Helicobasidium purpureum
Dietelia portoricensis
Miyagia pseudosphaeria
Pileolaria toxicodendri
Prospodium lippiae
P. tuberculatum
Puccinia caricis
P. convolvuli
P. coronata
P. dampierae
P. gilgiana
P. graminis
BPI 842277
ECS 553
BPI 871101
CBS324.47
BPI 844288
BPI 842230
BPI 871761
BPI 843901
BRIP 57630
BPI 871515
BPI 871465
BRIP 57724
BRIP 57719
NA
Podophyllum peltatum
Torreya californica
Mahonia aquifolium
Not provided
Mikania micrantha
Sonchus oleraceus
Toxicodendron sp.
Aloysia plystachya
Lantana camara
Grossularia sp.
Calystegia sepium
Rhamnus cathartica
Dampiera linearis
Lechenaultia linarioides
Not provided
DQ354543
AF522183
DQ354531
AY885168
DQ354516
DQ354517
DQ323924
DQ354555
KJ396195
DQ354514
DQ354512
DQ354526
KF690688
KF690691
AF5221779
DQ354544
AY123284
DQ354530
D85648
AY125414
AY125411
AY123314
DQ831024
KJ396196
DQ354515
DQ354511
DQ354525
NA
NA
P. haemodori
P. hemerocallidis
P. hordei
P. lagenophorae
BRIP 56965
BPI 843967
BPI 871109
BRIP 57563
Anigozanthus sp.
Hemerocallis sp.
Poaceae
Emilia sonchifolia
KF690692
DQ354519
DQ354527
KF690696
NA
NA
DQ354518
DQ415278
NA
P. menthae
P. psidii
P. poarum
P. polysora
P. saccardoi
P. smilacis
P. stylidii
P. ursiniae
P. violae
P. xanthosiae
Pucciniosira solani
Uromyces appendiculatus
U. ari-triphylli
U. scaevolae
U. viciae-fabae
BPI 871110
BRIP 57991
NA
BPI 863756
BRIP 57725
BPI 871784
BRIP 60107
BRIP 57993
BPI 842321
BRIP 57729
NA
NA
BPI 871111
BRIP 60113
NA
Cunila origanoides
Melaleuca leucadendra
Tussilago sp.
Zea mays
Scaevola spinescens
Smilax rotundifolia
Stylidium armeria
Ursinia anthemoides
Viola cucullata
Xanthosia rotundifolia
Solanum aphyodendron
Phaseolus vulgaris
Arisaena triphyllum
Selliera radicans
Pisum sp.
DQ354513
KF318443
DQ831028
GU058024
KF690701
DQ354533
KJ622214
KF690705
DQ354509
KF690706
EU851137
AY745704
DQ354529
KJ622213
AY745695
AY123315
KF318455
DQ831029
NA
NA
DQ354532
NA
NA
DQ354508
NA
NA
DQ354510
DQ354528
NA
NA
(Aime 2006). This is reflected by the relatively few species of
Puccinia represented in GenBank, for example, there are ~110
species of Puccinia represented by the ITS and LSU regions
of rDNA. This is less than 3 % of the estimated 4,000 species
of Puccinia (Kirk et al. 2008). Reliance on molecular identification for some species of Puccinia is not recommended. For
example, McTaggart et al. (2014) determined that several
species of Puccinia on different plant families in Australia
had near-identical ITS and LSU rDNA sequences (Fig. 23
Puccinia).
Rhizopus
Background
Rhizopus is a genus of cosmopolitan saprotrophic fungi, currently included in the family Rhizopodaceae within the
Mucorales (former Zygomycota; Hoffmann et al. 2013).
Many Rhizopus species are common postharvest pathogens,
causing fruit rots, and spoilage of crops, vegetables and wide
range of stored foods (Pitt and Hocking 2009; Ray and Ravi
96
Fungal Diversity (2014) 67:21–125
Fig. 23 Puccinia. Phylogram obtained from a ML search in RAxML
with the SSU and LSU regions of nrDNA. Bootstrap values (≥70 %) from
a ML search with 1,000 replicates above nodes; posterior probabilities
(≥0.95) from Bayesian inference below nodes. Puccinia and Uromyces
are polyphyletic, and genera such as Cumminsiella, Dieteila, Miyagia and
Pucciniosira are paraphyletic. The LSU region is not sufficient to distinguish closely related taxa in Australia as seen in the P. lagenophorae clade
2005; Shtienberg 1997). Some species of this genus (e.g.
R. arrhizus, R. microsporus and R. stolonifer) may also cause
head rot disease in sunflowers (Yildirim et al. 2010). Among
all Rhizopus species, R. arrhizus (syn. R. oryzae), and
R. stolonifer are of particular importance, taking into account
the frequency of isolation records (Farr and Rossman 2014).
Extremely fast growth rates and abundant production of early
maturing dry sporangiospores by Rhizopus species facilitate
rapid spread of infection (Pitt and Hocking 2009). According
to USDA Fungus-Host Database (Farr and Rossman 2014),
Rhizopus species have been isolated from a wide range of
plant taxa, both angiosperms and gymnosperms. Several
members of the genus, among them R. arrhizus and
R. microsporus are reported to cause human mucormycoses
Fungal Diversity (2014) 67:21–125
(Pitt and Hocking 2009), mostly in immunocompromised
patients (Roden et al. 2005; Pitt and Hocking 2009;
Chakrabarti et al. 2010; Skiada et al. 2011). Nevertheless,
Rhizopus species are used by humans. Fermentation process
of several kinds of Asian food and beverage strongly depends
on Rhizopus strains (Henkel 2005; Nout and Aidoo 2010).
Species identification and numbers
Identification of Rhizopus species was traditionally based on
the complexity of rhizoids, the length of the sporangiophores
and the size of the sporangia along with the ability to grow in
certain temperatures. In their revision, Schipper and Stalpers
(1984) recognized five species in three major complexes.
Later several new species and varieties were described (e.g.
Ellis 1985; Schipper and Samson 1994). Following a comprehensive morphological revision, Zheng et al. (2007) recognized ten species and seven varieties. Molecular analyses
(Abe et al. 2006, 2010; Hoffmann et al. 2013; Walther et al.
2013) supported the three complexes defined by Schipper and
Stalpers (1984), but revealed that Rhizopus is paraphyletic
containing Sporodiniella umbellata and Syzygites
megalocarpus (Hoffmann et al. 2013; Walther et al. 2013).
Based on molecular phylogenetic analyses several species
were recognized to represent synonyms: e.g. Amylomyces
rouxii is now treated as synonymous with R. arrhizus (Abe
et al. 2006), R. reflexus was recognized as a synonym of
R. lyococcus (Liou et al. 2007), and R. azygosporus was
revealed to be conspecific with R. microsporus (Abe et al.
2006). Dolatabadi et al. (2014b) showed that the morphologically defined varieties of R. microsporus are not recognized
in multi-marker phylogenies and consequently they reduced
the varieties to synonyms. Abe et al. (2007) revealed that
strains of R. arrhizus (as R. oryzae) split into producers of
lactic acid and producers of fumaric and malic acid and that
these two groups were molecular phylogenetically distinct. As
a consequence, the authors treated fumaric-malic acid producers as a separate species, R. delemar, formerly regarded as
a variety by Zheng et al. (2007). Gryganskyi et al. (2010)
supported this concept by molecular phylogenetic studies
based on several markers including mating type genes. In
agreement with the previous studies, Dolatabadi et al.
(2014a) recognized two phylogenetic species. However, they
treated them as varieties of a single biological species because
of the formation of zygospores between strains of the
arrhizus- and strains of the delemar-group, the lack of differences in morphology and ecology and the small genetic distance between the two groups compared to the remaining
species in Rhizopus. Variety tonkinensis, a third variety besides var. arrhizus and var. delemar, was recognized morphologically (Zheng et al. 2007) and through the use of short
tandem repeat motives of IGS rDNA sequences (Liu et al.
2008), but it has not come out as a separate lineage in
97
molecular phylogenetic studies (Walther et al. 2013;
Dolatabadi et al. 2014a) and is regarded as doubtful. Abe
et al. (2010) consider R. americanus and R. sexualis as varieties of R. stolonifer, while other authors (e.g. Zheng et al.
2007) recognize them as separate species. However, the large
genetic distances of the ITS region among these taxa (Walther
et al. 2013) rather suggest separate species. In the ITS trees of
Walther et al. (2013), the strains morphologically defined as
R. stolonifer form two distinctly separated groups suggesting
the existence of an undescribed species. Currently seven species are accepted in Rhizopus: R. americanus, R. arrhizus
including var. arrhizus and var. delemar, R. homothallicus,
R. lyococcus, R. microsporus, R. sexualis, and R. stolonifer
(Table 22).
Molecular phylogeny
The marker of choice for species identification in the
genus Rhizopus is the ITS region (Walther et al. 2013)
that can also distinguish the two varieties of R. arrhizus:
var. arrhizus and var. delemar (Fig. 24). For the three
species R. americanus, R. sexualis and R. stolonifer, sequencing of the ITS is often hampered by extended polyA- and poly-T-regions but the large subunit of the ribosomal DNA (LSU) can be sequenced for species identification in these cases because it can also resolve these
species (Walther et al. 2013). In case of R. americanus,
multiple different ITS sequences within one strain were
found, which should be considered in molecular identification (Liu et al. 2007; Abe et al. 2010).
Several molecular markers have been applied for phylogenetic inference in this genus by using general fungal primers: actin
(Abe et al. 2007, 2010; Dolatabadi et al. 2014a, b), ITS (Abe
et al. 2006, 2007, 2010; Gryganskyi et al. 2010; Walther et al.
2013; Dolatabadi et al. 2014a, b), LSU (Abe et al. 2006; Liou
et al. 2007; Walther et al. 2013; Dolatabadi et al. 2014a, b,),
orotidine-5’-monophosphate decarboxylase gene (pyrG gene)
(Liu et al. 2007), rpb1 (RNA polymerase II largest subunit gene)
(Dolatabadi et al. 2014a), SSU (small subunit of the ribosomal
DNA gene) (Abe et al. 2006), and tef (translation elongation
factor gene) (Abe et al. 2007, 2010; Dolatabadi et al. 2014a, b).
For R. arrhizus s.l., specific primers were designed for the rpb2
(RNA polymerase II second largest subunit gene) and the RNA
helicase and the TP transporter gene of the mating locus by
Gryganskyi et al. (2010) as well as for the lactate dehydrogenase
B by Abe et al. (2007).
The tef marker cannot be recommended for phylogenetic
studies because the gene is found in several different copies at
least in R. arrhizus; these copies typically differ in the third
base of numerous codons of this marker (Dolatabadi et al.
2014a). In the multi-marker study of Dolatabadi et al. (2014a),
the rpb1 was the most variable gene.
98
Fungal Diversity (2014) 67:21–125
Table 22 Rhizopus. Details of the isolates used in the phylogenetic tree
Species
Isolate
Host/source
GenBank
accession
no.
Rhizopus arrhizus
R. arrhizus
R. arrhizus
R. arrhizus
R. arrhizus
R. arrhizus
R. arrhizus
R. microsporus
R. microsporus
CBS111231
CBS544.80
CBS120.12
IFO5438
CBS112.07
CBS146.90
NRRL1469*
CBS357.93
CBS631.82
–
Sorghum malt
–
–
–
Homo sapiens
–
Tempeh
Bread
JN206338
JN206337
AB181318
DQ641276
JN206323
JN206324
DQ641279
JN206343
JN206344
R. microsporus
R. microsporus
R. microsporus
R. microsporus
R. homothallicus
R. homothallicus
R. caespitosus
R. caespitosus
R. schipperae
Syzygites
megalocarpus
CBS536.80
AS3.1145
CBS337.62
CBS699.68*
CBS336.62*
CBS111232
CBS427.87*
33515
CBS138.95*
CBS108947
Sorghum malt
–
–
Soil
Soil
–
–
–
Homo sapiens
Amanita
rubescens
HM999971
DQ641305
JN206362
HM999970
HM999968
JN206365
HM999965
AF115730
HM999969
JN206370
JN206371
Sporodiniella
umbellate
R. stolonifer
Rhizopus sp.
‘stolonifer’
R. stolonifer
R. sexualis
R. americanus
CBS195.77
Umbonia
JN206372
CBS389.95*
CBS442.74
–
Coffee-ground
DQ641318
JN206367
AFTOLID632
CBS336.39*
–
AY997085
R. lyococcus
R. lyococcus
CBS340.62*
CBS319.35
CBS117.43
R. lyococcus
Backusella sp.
JCM5589*
CBS538.80
Fragaria
AB113017
Air
–
Hordeum
vulgare
–
Medicago sativa
HM999967
AB100449
JN206375
DQ641319
HM999964
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher
stains are bolded
Recommended genetic markers
&
&
&
&
The internal transcribed spacer (ITS)–generic and species
level
The RNA polymerase II largest subunit gene (RPB1)–
generic and species level
The large and small subunits of nrDNA (LSU and SSU)–
placement within the Mucorales order, higher-level
phylogeny
The partial actin gene (ACT)–higher-level phylogeny
Stagonosporopsis
Background
Stagonosporopsis is a coelomycetous genus in Didymellaceae
(de Gruyter et al. 2009), accommodating several important
phytopathogenic species, some of which have well-described
sexual forms in Didymella (Diedicke 1912; Aveskamp et al.
2010). Many Stagonosporopsis species are considered serious
quarantine organisms in many parts of the world. Some species have a global distribution. Stagonosporopsis andigena,
the cause of black blight of potato (Turkensteen 1978), and
S. crystalliniformis, a destructive pathogen of tomato and
potato (Loerakker et al. 1986; Noordeloos et al. 1993), have
only been reported in the Andes region, and thus listed as A1
quarantine organisms (EPPO 2014). Stagonosporopsis
chrysanthemi and S. inoxydabilis are the cause of ray
(flower) blight of Asteraceae (Stevens 1907; Van der Aa
et al. 1990; Vaghefi et al. 2012), and A2 quarantine organisms
(EPPO 2014) (listed as Didymella ligulicola). In Australia,
S. tanaceti is known as the causal agent of ray blight of
pyrethrum, capable of causing complete yield loss
(Pethybridge et al. 2008). Stagonosporopsis cucurbitacearum
(sexual state Didymella bryoniae) is a destructive seed-borne
pathogen of Cucurbitaceae worldwide, causing gummy stem
blight and black fruit rot (Punithalingam and Holliday 1972;
Lee et al. 1984; Zitter and Kyle 1992). Stagonosporopsis
species have also been reported from other plant families including Amaranthaceae, Campanulaceae, Caryophyllaceae,
Fabaceae, Lamiaceae, Ranunculaceae, and Valerianaceae. The
only species not isolated from a plant substrate is S. oculohominis, which was reported from human corneal ulcer in the
USA (Punithalingam 1976).
Species identification and numbers
Stagonosporopsis was originally separated from Ascochyta on
the basis of occasional formation of multi-septate
(Stagonospora-like) conidia (Diedicke 1912). No type material was specified by Diedicke (1912) such that the first
species combination described, S. actaeae, was interpreted
as the generic type by some authors (Boerema et al. 1997,
2004). However, S. boltshauseri, currently known as
S. hortensis (Boerema and Verhoeven 1979), was designated
as the lectotype by Clements and Shear (1931).
In vitro, S. hortensis predominantly produces non-septate
Phoma-like conidia, resembling those of Boeremia exigua var.
exigua, while a few larger septate conidia can occasionally be
found. In vivo, however, S. hortensis can be distinguished
from B. exigua by predominance of one-septate (Ascochytalike) conidia and occasional occurrence of two- or multiseptate (Stagonospora-like) spores. It is thus not a typical
Ascochyta or Stagonospora, both of which produce septate
Fungal Diversity (2014) 67:21–125
99
Fig. 24 Phylogram generated
from Maximum likelihood
analysis based on ITS sequenced
data of Rhizopus. Bootstrap
support values greater than 50 %
are indicated above the nodes.
The ex-type (ex-epitype) and
voucher strains are in bold
conidia both in vivo and in vitro, and was classified under the
genus Stagonosporopsis (Boerema and Verhoeven 1979).
Boerema et al. (1997, 1999) described multiple
Stagonosporopsis spp. to be synanamorphs for several
Phoma species in section Heterospora. The characteristic of
section Heterospora is the in vivo production of distinctly large
conidia (ascochytoid /stagonosporoid) in addition to relatively
small (phomoid) conidia. The large conidial phenotypes may
be dominant in vivo, hence described as Stagonosporopsis
synanamorphs (Boerema et al. 1997, 1999, 2004).
Recent phylogenetic delineation of Phoma and allied
genera placed the presumed Stagonosporopsis types in the
family Didymellaceae (de Gruyter et al. 2009), and an
emended description of the genus was proposed
(Aveskamp et al. 2010). Some of the heterosporous
P h o m a s p e c i e s w i t h k n o w n S t a g o n o s p o ro p s i s
synanamorphs were retrieved outside the
Stagonosporopsis clade. On the other hand, many species
from sections Heterospora, Phoma and Phyllostictoides,
for which no records of a Stagonosporopsis synanamorph
had been made, clustered with Stagonosporopsis spp. This
indicated that the connection of Stagonosporopsis with
heterosporous Phoma species was not justified. It also
suggested that presence of Stagonospora-like spores is
not a reliable criterion for identification of
Stagonosporopsis spec ies. Stagonos poropsis
dorenboschiae, S. loticola, and S. ajacis lack the
Stagonospora-like spores and any further features than a
plain, globose pycnidium, and aseptate, hyaline conidia
(Aveskamp et al. 2010). Due to unreliability of morphological characters, phylogenetic species recognition is essential for identification of Stagonosporopsis species.
Stagonosporopsis in its original description by Diedicke
(1912) accommodated seven species, and currently more than
40 species are linked to this genus (data from MycoBank
and Index Fungorum). However, only 21
Stagonosporopsis species have thus far been recognised
based on multi-gene phylogenies (Table 23) (Aveskamp
et al. 2010; Vaghefi et al. 2012). The phylogenetic reassessment of Didymellaceae (Aveskamp et al. 2010) included only those Stagonosporopsis species that had been
designated as Phoma synanmorphs by Boerema et al.
(1997, 1999). Molecular data for multiple other
Stagonosporopsis species are still lacking and, therefore,
the taxonomy of the genus Stagonosporopsis remains to
be comprehensively reviewed.
Molecular phylogeny
Few phylogenetic analyses of Stagonosporopsis species are
available (Pethybridge et al. 2004; Aveskamp et al. 2010; de
Gruyter et al. 2012; Vaghefi et al. 2012, 2014), with the most
comprehensive analysis being the three-marker phylogeny
performed by Aveskamp et al. (2010). The phylogeny of
combined sequences of large subunit nrDNA (LSU), the
internal transcribed spacers and the 5.8 S nrRNA (ITS), and
β-tubulin regions resulted in the recognition of 19 species
(Aveskamp et al. 2010). Phylogenies based on the partial actin
(ACT) sequence were later found to be congruent with the
LSU- ITS- β- tubulin phylogeny (de Gruyter et al. 2012;
Vaghefi et al. 2012). A four-marker phylogeny of the
Stagonosporopsis spp. for which these DNA sequence data
are available is shown (Fig. 25).
Recommended genetic markers
&
&
The internal transcribed spacer (ITS)–family/generic level
β- tubulin and ACT–inter-specific delineation
A high level of infra-specific variation has been recorded
for calmodulin (CAL) in Phoma-like species, however, it may
be difficult to amplify in some Stagonosposopsis species, and
100
Table 23 Stagonosporopsis. Details of the isolates used in the phylogenetic tree
Species name
Strain no.
Host
GenBank accession number
LSU
SSU
ITS
β- tubulin
ACT
CAL
CBS 106.96; PD 94/1318
Actaea spicata
GU238166
QBank
GU237734
GU237671
JN251974
–
CBS 177.93; PD 90/115
CBS 101.80; PD 75/909; IMI 386090
CBS 102636; PD 73/1409
CBS 178.25; MUCL 9915
CBS 248.90
CBS 500.63; MUCL 8090
CBS 713.85; ATCC 76027; PD 83/826
CBS 133.96; PD 79/127
CBS 631.68; PD 68/147
CBS 426.90; IMI 386093; PD 86/551
CBS 109182; PD 74/231
CBS 104.42
CBS 425.90; PD 81/520
CBS 562.81; ICMP 6884
CBS 101494; PD 98/5247
CBS 634.92; IMI 193307
CBS 109180; PD 79/175
CBS 131484; TAS 1
Delphinium sp.
Solanum sp.
Artemisia dracunculus
Astragalus sp.
Carica papaya
Chrysanthemum indicum
Lycopersicon esculentum
Cucurbita sp.
Solidago floribunda
Physostegia virginiana
Heliopsis patula
Unknown
Chrysanthemum parthenii
Lotus pedunculatus
Lupinus albus
Homo sapiens
Rudbeckia bicolor
Tanacetum cinerariifolium
GU238168
GU238169
GU238171
GU238172
GU238175
GU238190
GU238178
GU238181
GU238182
GU238185
GU238186
GU238198
GU238188
GU238192
GU238194
GU238196
GU238197
JQ897461
QBank
GU238233
QBank
QBank
QBank
QBank
QBank
GU238234
GU238235
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
–
GU237791
GU237714
GU237728
GU237792
GU237807
GU237871
GU237903
GU237780
GU237899
GU237862
GU237747
GU237730
GU237861
GU237890
GU237724
GU237901
GU237745
JQ897481
GU237673
GU237674
GU237676
GU237677
GU237680
GU237695
GU237683
GU237686
GU237687
GU237690
GU237691
GU237703
GU237693
GU237697
GU237699
GU237701
GU237702
JQ897496
JN251962
JN251958
JN251971
JN251963
JN251969
JN251973
JN251960
JN251968
QBank
JN251980
QBank
QBank
JN251972
JN251978
QBank
JN251976
QBank
JQ897512
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
QBank
–
S. trachelii
S. valerianellae
CBS 379.91; PD 77/675
CBS 329.67; PD 66/302
Campanula isophylla
Valerianella locusta var. oleracea
GU238173
GU238201
QBank
QBank
GU237850
GU237832
GU237678
GU237706
JN251977
JN251965
QBank
QBank
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
Fungal Diversity (2014) 67:21–125
Stagonosporopsis actaeae*
S. ajacis*
S. andigena
S. artemisiicola
S. astragali
S. caricae
S. chrysanthemi
S. crystalliniformis*
S. cucurbitacearum
S. dennisii
S. dorenboschii*
S. heliopsidis
S. hortensis
S. inoxydabilis*
S. loticola*
S. lupini
S. oculo-hominis*
S. rudbeckiae
S. tanaceti*
Fungal Diversity (2014) 67:21–125
101
Fig. 25 Phylogram generated from Maximum likelihood analysis based
on combined LSU, ITS, β- tubulin and ACT sequenced data of
Stagonosporopsis. Bootstrap support values greater than 50 % are
indicated above the nodes. The ex-type (ex-epitype) and voucher strains
are in bold. The tree is rooted with Phoma herbarum CBS 615.75
requires optimization using different degenerate primers
(Aveskamp et al. 2009, 2010; Vaghefi et al. 2012). Thus use
of β- tubulin and ACT is suggested as they will give sufficient
distinction between species, and are easier to amplify.
systematic studies reserved Ustilago s. lat. for species
that infected Poaceae, with Ustilago s. str. restricted to
the tribe Pooideae (McTaggart et al. 2012a; Stoll et al.
2005). Soral morphology and host range were later
found to be synapomorphic character states for the smut
genera Anthracocystis, Langdonia, Sporisorium, Stollia
and Triodiomyces, which were differentiated from
Ustilago (McTaggart et al. 2012c). Melanopsichium is
closely related to Ustilago, and appears to have jumped
hosts from Poaceae to Polygonaceae (Begerow et al.
2004; Stoll et al. 2005).
Ustilago
Background
Ustilago is the largest genus of the Ustilaginaceae in the order
of smut fungi, Ustilaginales, with about 200 currently accepted
species (Vánky 2013). Ustilago and related genera contain
many important plant pathogens that destroy the inflorescence
or culms of grasses (Poaceae) (Vánky 2011). Some agriculturally important pathogens of grain and edible crops are U. tritici
on wheat (Triticum), U. hordei on barley (Hordeum) and
U. maydis on corn (Zea mays). Species of Ustilago have been
used as model organisms for the study of plant disease pathways and mating types (Andrews et al. 2000; Bakkeren et al.
2008; Kellner et al. 2011), as well as for studies in the coevolution of pathogens with their hosts (Begerow et al. 2004).
The genomes of U. maydis and U. hordei were released in 2003
and 2012, respectively (Kamper et al. 2006; Laurie et al. 2012).
Ustilago was until recently a catch-all genus for smut fungi
on a diversity of host families, including the Carophyllaceae,
Cyperaceae, Poaceae, Polygonaceae, Restionaceae, and
Tilliaceae (McTaggart et al. 2012b). Closely related genera
were not easily distinguished from Ustilago by morphology,
and formed a complex (Stoll et al. 2003, 2005). Subsequent
Species identification and numbers
The diversity of smuts in the Ustilaginaceae on Poaceae
encompasses over 530 species (Vánky 2011). Cryptic species are certain to be revealed when species complexes,
e.g., Macalpinomyces eriachnes, are investigated. Vánky
(2011) recognised approximately 170 species of Ustilago,
which were delimited by host and spore morphology. It is
likely the species number of Ustilago will decrease when
generic concepts are resolved in the Ustilaginaceae.
Species currently recognized as Ustilago will be transferred to new or other genera delimited by sorus morphology and host range. For example, U. maydis does not fit the
concept of Ustilago s. str. and warrants transfer to the
earliest valid genus, Mycosarcoma, when these closely
related genera are resolved (McTaggart et al. 2012a; Stoll
et al. 2005; Vánky and Lutz 2011; Piepenbring et al. 2002)
(Table 24).
102
Fungal Diversity (2014) 67:21–125
Table 24 Ustilago. Details of the isolates used in the phylogenetic tree
Species
Isolate
Host
Marker/GenBank accession no.
ITS
LSU
BRIP 46421
Ust. Exs. 472
BRIP 52755
56573 (M)
BRIP 52549
RB 2056 (TUB)
56577 (M)
HUV 13634
BRIP 51858
BRIP 49133
HUV 17548
Ust. Exs. 833
Ust. Exs. 756
MP 2036a (USJ)
Panicum trachyrachis
Panicum miliaceum
Aristida hygrometrica
Eriachne aristidea
Eulalia mackinlayi
Setaria pumila
Loudetia simplex
Eragrostis ferruginea
Sporobolus australasicus
Sporobolus actinocladus
Polygonum glabrum
Paspalum distichum
Schismus arabicus
Sorgum bicolor
DQ459348
AY344976
HQ013096
AY740037
GU014817
AY740056
AY740152
AY740171
NA
HQ013089
AY740040
AY740153
AY344970
AY740021
DQ459347
AY747077
NA
AY740090
HQ013131
AY740109
NA
NA
HQ013130
HQ013125
AY740093
AY740153
AY740129
AF009872
T. triodiae
Tubisorus pachycarpus
Ustilago affinis
U. austro-africana
U. avenae
U. bouriqueti
U. bromivora
HMAS 193085
BRIP 51818
Ust. Exs. 418
BRIP 52543
HUV 17662
HUV 21891
MP 692
56516 (M)
DB 559 (TUB)
56517 (M)
HUV 19322
Capillipedium parviflorum
Sarga timorense
Triodia pungens
Triodia sp.
Triodia microstachya
Mnesithea rottboellioides
Stenotaphrum secundatum
Enneapogon cenchroides
Avena barbata
Stenotaphrum dimidiatum
GU139172
HQ013087
AY740166
NA
AY740074
JN871718
AY344995
AY740061
AY344997
AY740167
GU139171
HQ013127
NA
HQ013136
AY740126
JN871717
AF133581
AY740115
AF453933
NA
U. bullata
U. calamagrostidis
U. crameri
U. curta
U. cynodontis
U. davisii
U. drakensbergiana
MP 2363 (TUB)
56518 (M)
Ust. Exs. 995
Ust. Exs. 1090
MP 1838
HUV 19252
56523 (M)
Bromus catharticus
Bromus diandrus
Calamagrostis epigeios
Setaria italica
Tripogon loliiformis
Cynodon dactylon
Glyceria multiflora
Digitaria tricholaenoides
AY740064
AY344998
AY740065
AY344999
AY740165
AY345000
AY740169
AY740170
AY740118
AF453935
AY740119
AY740143
HQ013123
AF009881
NA
U. echinata
U. esculenta
U. filiformis
U. hordei
U. ixophori
U. maydis
Ust. Exs. 540
Ust. Exs. 590
RB 3011 (TUB)
Ust. Exs. 784
MP 2194
RB 3093
NA
HUV 17782
Ust. Exs. 789
BRIP 51848
Ust. Exs. 887
Ust. Exs. 892
BRIP 39706
HUV 18286
Ust. Exs. 998
Phalaris arundinacea
Zizania latifolia
Glyceria fluitans
Hordeum vulgare
Ixophorus unisetus
Zea mays
Zea mays
Hordeum leporinum
Bromus gracillimus
Enneapogon sp.
Paspalum paniculatum
Dactyloctenium radulans
Sporobolous pyramidalis
Alopecurus pratensis
Digitaria ternata
AY345001
AY345002
AY740066
AY345003
AY740067
AY345004
NA
AY740069
AY345005
HQ013121
AY345006
AY345008
AY772736
AY740172
AY740071
AY740144
AF453937
AY740120
AF453943
AY740121
NA
AF453938
AJ236139
AY740145
HQ013129
AY740146
NA
NA
DQ875375
AY740123
Anomalomyces panici
Anthracocystis destruens
Langdonia aristidae
Macalpinomyces eriachnes
M. mackinlayi
M. neglectus
M. simplex
M. spermophorus
M. viridans
Melanopsichium pennsylvanicum
Moesziomyces bullatus
Sporisorium aegyptiacum
S. sorghi
S. spinulosum
Stollia ewartii
Triodiomyces altilis
U. nuda
U. pamirica
U. schmidtiae
U. schroeteriana
U. sparsa
U. sporoboli-indici
U. striiformis
U. syntherismae
Fungal Diversity (2014) 67:21–125
103
Table 24 (continued)
Species
U. tragana
U. tritici
U. trichophora
U. turcomanica
U. vetiveriae
U. xerochloae
Isolate
56562 (M)
NA
56564 (M)
HUV 23
HUV 17954
Ust. Exs. 1000
Host
Marker/GenBank accession no.
Tragus berteronianus
Triticum aestivum
Echinochloa colona
Eremopyrum distans
Vetiveria zizanioides
Xerochloa imberbis
ITS
LSU
AY7400723
AF13542411
AY3450093
AY3450113
AY3450113
AY3450123
AY7401243
NA
AY7401483
AF4539363
AF4539373
AF4539383
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
Molecular phylogeny
Relationships between Ustilago and closely related genera are
still unresolved, and Ustilago is polyphyletic (Fig. 26
Ustilago). Systematic studies based on the nLSU or ITS
regions of rDNA have assigned taxa within these closely
related genera (Shivas et al. 2013a; Vánky and Lutz 2011;
McTaggart et al. 2012c). Nuclear genes (EF1α, GPDH, RPB1
and RPB2), another ribosomal gene (SSU) and mating loci
were explored as markers for the evolution of smut fungi in
the Ustilaginaceae (Kellner et al. 2011; McTaggart et al.
2012a; Munkacsi et al. 2007). At this stage, these markers
are not as widely used as ITS and LSU, which are recommended for species identification and generic placement,
respectively.
Recommended genetic markers
&
&
The large subunit (LSU) of nrDNA–generic level
The internal transcribed spacer (ITS) of nrDNA–species
level
Verticillium
Background
Verticillium belongs in the family Plectosphaerellaceae of the
Ascomycota. Verticillium species are soilborne, vascular, fungal
plant pathogens that cause Verticillium wilt disease in many
important agricultural crops throughout the world (Pegg and
Brady 2002). Based on susceptibility, 410 plant species that
include nearly 80 plant genera have been recorded as being
infected by Verticillium species (Pegg and Brady 2002).
Correct species identification is important for determining the
ecological roles of Verticillium species and for diagnosing disease. Sexual stages have not been identified for Verticillium
species although mating type idiomorphs MAT1-1 and MAT12 have been identified in separate isolates of V. dahliae, V. albo-
atrum, V. longisporum, V. alfalfa and V. nonalfalfae, indicating
that these species are potentially heterothallic (Inderbitzin et al.
2011a, b; Usami et al. 2009).
Species identification and numbers
The genus Verticillium sensu stricto refers to a monophyletic
group of plant pathogens comprising V. dahliae as the type of
Verticillium (Gams et al. 2005). The genus can be identified
based on its distinct ‘verticillate conidiophores’ with flaskshaped conidiophores arranged in whorls attached along a main
axis that comprise the spore forming cells (Pegg and Brady
2002). The genus Verticillium has a long taxonomic history
and approximately 190 species were originally classified by
Zare et al. (2004). Recently Inderbitzin et al. (2011a) used fourmarker phylogenetic analysis to identify ten Verticillium species.
Earlier studies identified Verticillium species primarily on
the basis of morphology and sub-specific groups by virulence
and aggressiveness on various hosts (Rowe 1995). Variation
in conidial morphology of Verticillium species is minor and
thus cannot be used to separate species (Rowe 1995). Resting
structure morphology has been the major morphological character used to differentiate species of Verticillium.
Verticillium albo-atrum and V. dahliae are the most important plant pathogenic species. Verticillium albo-atrum was
first described in Germany, 1879, by Reinke and Berthold as
the causal agent of potato wilt. The resting structures identified from the diseased plant tissue were brown-pigmented
hyphae which were described as ‘Dauermycelien’. Later this
pigmented hyphae was termed dark ‘resting mycelium’ which
had only transverse walls and no lateral budding (Isaac 1949).
No microsclerotia were produced by V. albo-atrum.
Verticillium dahliae was first isolated by Klebahn in 1913
from wilting Dahlia. The isolate produces smaller and oval to
elongate microsclerotia as a resting structure from budding
hyphae, but not dark resting mycelium (Smith 1965).
Verticillium tricorpus forms large and irregular microsclerotia
with melanised hyphae and chlamydospores (hence the prefix
“tri”). Moreover, V. tricorpus often produces yellow colonies
104
Fungal Diversity (2014) 67:21–125
Fig. 26 Phylogram generated from ML search in RA × ML based on combined ITS and LSU sequenced data of Ustilago. Bootstrap support values
greater than 70 % are indicated above the nodes. The ex-type (ex-epitype) and voucher strains are in bold
on PDA upon first isolation (Goud et al. 2003). Verticillium
nubilum produces only rounded to elongate chlamydospores,
individually or in chains (Inderbitzin et al. 2011a). Verticillium
longisporum refers to the species proposed by Karapapa et al.
(1997) that infected hosts in the family Brassicaceae. Isolates
of this species produce microsclerotia which are rounded to
elongate with relatively long conidia, and nearly double the
nuclear DNA content (Inderbitzin et al. 2011a).
Fungal Diversity (2014) 67:21–125
Molecular techniques have been used in the characterisation and identification of Verticillium species for both species
identification and phylogenetic comparisons (Collins et al.
2003; Collado-Romero et al. 2008). Using restriction fragment length polymorphism (RFLP) analysis, Typas et al.
(1992) reported that mitochondrial DNA of Verticillium species were distinctive and easily differentiated V. albo-atrum
(from alfalfa) from other V. albo-atrum isolates. Carder and
Barbara (1991) used RFLP analysis to differentiate V. dahliae
from all isolates of V. albo-atrum and found intraspecific
variation within V. dahliae isolates. Subsequently, Okoli
et al. (1993) probed Southern blots derived from 17 isolates
of V. dahliae with 71 random genomic clones from V. dahliae
and found that 15 isolates fitted clearly into two RFLP groups
designated A and B. Although these groups correlated with
isozyme patterns they did not show any correlation with host
plant or geographic origin. Random amplified polymorphic
DNA (RAPD) markers clearly differentiated 15 V. albo-atrum
potato isolates from 20 alfalfa V. albo-atrum isolates and
found that these two groups were genetically distinct
(Barasubiye et al. 1995). Komatsu et al. (2001) used repetitive
extragenic palindromic polymerase chain reaction (REPPCR) and RAPD markers to show that V. dahliae isolates
from potato were similar in genetic background, regardless
of geographic origin.
In North America, characterization of vegetative compatibility groups (VCGs have the ability to undergo hyphal anastomosis with other isolates) using molecular markers confirmed that VCG 4A isolates of V. dahliae were more highly
virulent than VCG 4B isolates (Dobinson et al. 2000).
Molecular characterization of VCGs has been determined in
many other crops (Collado-Romero et al. 2006, 2009;
Dobinson et al. 1998).
Molecular phylogeny
Nazar et al. (1991) found only five nucleotide differences
between V. dahliae and V. albo-atrum on the basis of the
non-conserved ITS region (ITS 1 and ITS 2) of rDNA.
Robb et al. (1993) reported 17 nucleotide differences between
V. dahliae and V. tricorpus and 12 between V. albo-atrum and
V. tricorpus (Moukhamedov et al. 1994). Phylogenetic analysis of the complete intergenic spacer (IGS) region of the
nuclear ribosomal RNA (rDNA) and the β-tubulin gene
showed distinct groups comprising isolates of V. albo-atrum,
V. tricorpus, and V. dahliae from cruciferous and
noncruciferous hosts (Qin et al. 2006).
Fahleson et al. (2004) studied three different markers
(mitochondrial cytochrome b gene (cob), the mitochondrial small subunit rRNA gene (rns) and the nuclear
ITS2 region) sequences from five plant pathogenic isolates of Verticillium and found five monophyletic groups
corresponding to the Verticillium species. In addition,
105
V. tricorpus displayed a closer relationship to V. alboatrum, V. dahliae and V. longisporum. But V. nigrescens
was distantly related to the other species. Based on
nuclear large subunit ribosomal DNA (LSU) and ITS
sequences, Zare et al. (2007) proposed Gibellulopsis as
a genus to accommodate V. nigrescens.
Recent molecular phylogenetic studies by Inderbitzin et al.
(2011a) using four gene sequences viz actin, elongation factor
1-alpha, glyceraldehyde-3-phosphate dehydrogenase and
tryptophan synthase, divided Verticillium into two separate
groups, corresponding to the production of yellow pigment
in culture (clade Flavexudans), or the lack of yellow pigment
(clade Flavnonexudans). The species Verticillium albo-atrum,
V. tricorpus, V. zaregamsianum, V. isaacii and V. klebahnii
were placed in the Flavexudans clade of which the latter two
species were morphologically indistinguishable from
V. tricorpus. The species Verticillium dahliae, V. nubilum,
V. longisporum, V. alfalfae and V. nonalfalfae were placed in
the clade Flavnonexudans (Inderbitzin et al. 2011a).
Interestingly, V. longisporum which is a diploid hybrid had
alleles in different clades including the V. dahliae clade
thus reflecting the ancestral origin of the hybrid.
According to Inderbitzin et al. (2011b), each
V. longisporum isolate contained two alleles at each
locus with allele A1 being present in all isolates in
addition to alleles D1, D2 or D3. Therefore, according
to Inderbitzin et al. (2011a), V. longisporum should remain a
polyphyletic species.
The phylogenetic tree of the ten species adopted by
Inderbitzin et al. (2011a) did not include the ribosomal internal
transcribed spacer region ITS, because V. longisporum isolates
only had one ITS allele consistent with all other Verticillium
species and hence this gene sequence could not retrace the
evolution of the species (Inderbitzin et al. 2011b).
Nevertheless, neither the four gene phylogenetic analysis nor
the single ITS phylogenetic tree were able to differentiate
V. longisporum alleles D2 and D3 from V. dahliae
(Inderbitzin et al. 2011b).
In contrast to the above results, a four gene phylogenetic tree composed of only the type isolates (Fig. 27)
failed to differentiate V. isaacii from V. klebahnii; while
V. alfalfa was identical to V. nonalfalfae; and V. dahliae
was identical to V. longisporum allele D2. Nevertheless,
the phylogenetic tree based only on ITS (Fig. 28) provided better discrimination to differentiate V. isaacii
from V. klebahnii, and V. alfalfa from V. nonalfalfae,
albeit with weak bootstrap supports.
Another anomaly with the four gene phylogenetic
tree based on only type isolates was that V. nubilum
claded with the yellow pigment forming Flavexudans
species whereas in the tree by Inderbitzin et al.
(2011a), V. nubilum claded with the Flavnonexudans
species. Nevertheless, the phylogenetic tree based only
106
Fungal Diversity (2014) 67:21–125
&
&
&
Elongation factor 1-alpha (EF)–generic/ species level
Glyceraldehyde-3-phosphate dehydrogenase (GPD)–
generic/ species level
Tryptophan synthase (TS)–generic/ species level
Discussion
Fig. 27 Phylogram generated from parsimony analysis based on combined ACT, TEF, GPD and TS sequenced data of Verticillium. Parsimony
bootstrap support values greater than 50 % are indicated above the nodes.
The ex-type (ex-epitype) and voucher strains are in bold. The tree is
rooted with Gibellulopsis nigrescens
on ITS (Fig. 28) placed V. nubilum in the Flavnonexudans
species group. In fact V. nubilum does not produce yellow
pigment in culture, such that it is better placed in the
Flavnonexudans species group.
Recommended genetic markers
Most of the ten Verticillium species can be identified using the
ITS sequences of the type isolates (Table 25, Fig. 28) however, strong bootstrap support is provided for most clades using
four gene sequences (Table 25, Fig. 27).
&
&
Internal transcribed spacer (ITS)–species level
Actin (ACT)–generic/species level
Fig. 28 Phylogram generated from parsimony analysis based on ITS
sequenced data of Verticillium. Parsimony bootstrap support values greater than 50 % are indicated above the nodes. The ex-type (ex-epitype) and
voucher strains are in bold. The tree is rooted with Gibellulopsis
nigrescens
The present effort is far from exhaustive, and the selection of
fungal lineages reflects the backgrounds of the authors rather
than degree of pathogenicity or economic impact of the underlying fungi. Indeed, several of the groups covered are pathogens
on plants that are used neither in agriculture nor forestry.
Furthermore, the fact that a group is addressed in the present
study should not be taken to mean that no further discoveries or
insights in the group are likely to emerge; the opposite is certain
to be true for all of the groups studied here. Knowledge of
phytopathogenic fungi accumulates at a high pace, and we hope
that the readers will use this study as a starting point in their
pursuit. Towards that end, we aim to maintain rich, updated
backbone trees of as many groups of plant pathogenic fungi as
we can. These will be published as a joint paper on an annual or
biennial basis as new data are produced. Researchers who can
cover any group not presently covered–or improve on any of the
groups that are covered already–are warmly invited to take part
in this effort by contacting the corresponding author.
As one of the pursuits of this effort, we have attempted to
address the question of which genes and genetic markers that
will provide the highest phylogenetic/taxonomic resolution in
various groups of plant pathogenic fungi. These differ markedly
among groups. At the same time, for someone examining a
sample of an unknown phytopathology-related fungus, the
choice of initial genetic markers is easy. The ITS region–the
formal fungal barcode–is the most commonly sequenced marker
in mycology, such that a rich array of reference sequences is
available. Although the ITS region will not always provide
resolution at the species level, it will nearly always provide
enough resolution to support assignment of the species to at least
the level of subgenus/species complex. This information is likely
to be enough for many applications; for others, it makes it much
easier to make an informed choice of what genes to sequence
next. However, researchers sometimes recover fungal ITS sequences that are not easily fitted into the corpus of reference ITS
sequences. The next most sequenced marker in mycology is the
nuclear ribosomal large subunit (nLSU; Begerow et al. 2010),
which is significantly more conserved than the ITS region and
offers resolution at the genus to order level. The nLSU is
something of the mainstay of large-scale phylogenetic inference
in fungi (Blackwell et al. 2006), and nearly all fungal nLSU
sequences can be assigned to at least the ordinal level. For
unknown samples, we thus advice researchers to sequence the
ITS and nLSU regions as a first step.
Fungal Diversity (2014) 67:21–125
107
Table 25 Verticillium. Details of the isolates used in the phylogenetic tree
Species
V. dahliae
V. alfalfae
V. nubilum
V. isaacii
V. nonalfalfae
V. albo-atrum
V. zaregamsianum
V. tricorpus
V. klebahnii
V. longisporum
V. longisporum
Isolate
PD322*
PD489*
PD742*
PD660*
PD592*
PD747*
PD736*
PD690*
PD401*
PD687* Allele D2
PD687* Allele A1
Host
Lettuce
Alfalfae
Soil
Lettuce
Irish Potato
Potato Soil
Lettuce
Garden Tomato
Lettuce
Horseradish
Horseradish
GenBank accession number
ITS
ACT
EF
GPD
TS
HQ206718
JN187971
JN188011
HQ206873
JN187973
JN188016
JN188005
JN187993
JN187967
HQ206718
JN188097
JN188139
HQ206985
JN188099
JN188144
JN188133
JN188121
JN188093
HQ206994
HQ206993
HQ414624
JN188225
JN188267
HQ414688
JN188227
JN188272
JN188261
JN188249
JN188221
HQ414697
HQ414696
HQ414719
JN188161
JN188203
HQ414783
JN188163
JN188208
JN188197
JN188185
JN188157
HQ414792
HQ414791
HQ414909
JN188033
JN188075
HQ414973
JN188035
JN188080
JN188069
JN188057
JN188029
HQ414982
HQ414981
Ex-type (ex-epitype) strains are bolded and marked with an * and voucher stains are bolded
Fungal plant pathogens attract the attention of numerous
scientific and applied fields, including mycology, botany,
agriculture, horticulture, silviculture, and medicine. In
many cases this attention will centre on establishing, or
ruling out, a pathogenic nature of specific fungal samples;
and in many cases, such efforts will be based on molecular
data. Molecular identification of fungi–DNA barcoding–
has a long and rich history but was only recently formalized (Bruns et al. 1990; Schoch et al. 2012). Indeed, many
parts of its realization still loom on the horizon. For instance, central barcoding resources and databases of wide
acceptance in the mycological community are largely lacking. Most researchers, when processing newly generated
fungal sequences, turn to GenBank (Benson et al. 2014) for
sequence identification. Many entries in GenBank suffer
from technical complications or low-resolution annotations, but efforts to standardize and improve on the data
and level of metadata given are under way (Nilsson et al.
2014; Schoch et al. 2014). The largest database focusing
on the formal fungal barcoding region–ITS–is UNITE
(Kõljalg et al. 2013). Sharing data with GenBank, UNITE
serves as the provider of reference fungal ITS datasets for a
long range of applications and downstream uses. The results of the present effort–in particular, the sequences from
type material–are being implemented in UNITE for all its
diverse uses and for subsequent distribution to GenBank.
We hope that this will lead to increased scientific resolution for researchers recovering any of the fungal lineages
treated in this study.
The heterogeneous user base of data pertaining to phytopathogenic fungi suggests that many users of data pertaining
to phytopathogenic fungi will not be–and cannot expected to
be–up to date on recent developments in mycology,
systematics, or the use of molecular data in biology. It is thus
largely up to mycologists to provide the scientific community
with as accurate and easily interpreted information on fungi
and phytopathological fungal species as possible. The mycological community lives up to that expectation with various
degrees of success. Improvement is particularly needed in the
public sequence databases, where many researchers routinely
submit phytopathologically relevant fungal sequences without
any notion of taxonomic affiliation, host association, or country of collection (notably “Uncultured fungus”). Such sequences will be excluded from, or treated only superficially
in, most research efforts and sequence comparisons, leading to
reduced scientific resolution and explanatory power. We urge
mycologists with a phytopathological inclination–indeed,
with any inclination–to set good examples in this regard by
providing rich, reliable annotations for their sequences.
Guidelines on how to establish the integrity and improve the
wide usefulness of fungal sequence data are readily available
for consideration (Nilsson et al. 2012; Hyde et al. 2013a, b;
Schoch et al. 2014). We similarly hope that all mycologists,
when describing new species, will make it a habit to bundle at
least one DNA sequence–starting with the ITS region–with
the description (cf. Seifert and Rossman 2010). This will help
others to interpret the name and will go a long way to make it
available to the general scientific audience. Enclosing molecular data with species descriptions is not required by the
current nomenclatural code governing fungi (McNeill et al.
2012), but we feel that this is a good opportunity for mycology
to show its progressive nature. In a time where mycology
finds it increasingly hard to compete for funding with disciplines deemed more cutting-edge, mycologists should make
every effort to propagate their results and findings to the
widest audience possible.
108
Acknowledgments We would like to thank the CGIAR Research Program 1.2–Humidtropics: Integrated systems for the humid tropics, for
partially funding this work. Kevin D. Hyde thanks the Chinese Academy
of Sciences, project number 2013T2S0030, for the award of Visiting
Professorship for Senior International Scientists at Kunming Institute of
Botany. Thank to Plant Germplasm and Genomics Center in Germplasm
Bank of Wild Species. Sajeewa Maharachchikumbura thanks the National Research Council of Thailand (grant for Pestalotiopsis No:
55201020008) and Mae Fah Luang University (grant for Pestalotiopsis
No: 55101020004) for financial support. S.A. Alias thanks the University
of Malaya for grant number RU006H-2014 entitled “diversity and importance of fungal mangrove disease”. Financial support to Julia
Pawłowska and Marta Wrzosek was partially provided by the Polish
Ministry of Science and Higher Education (MNiSW), grant no.
NN303_548839. Henrik Nilsson acknowledges financial support from
FORMAS (215-2011-498).
Open Access This article is distributed under the terms of the Creative
Commons Attribution License which permits any use, distribution, and
reproduction in any medium, provided the original author(s) and the
source are credited.
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