Fungal Diversity (2020) 103:87–218
https://doi.org/10.1007/s13225-020-00460-8
One stop shop IV: taxonomic update with molecular phylogeny
for important phytopathogenic genera: 76–100 (2020)
Ruvishika S. Jayawardena1,2,7 · Kevin D. Hyde1,2,3,18 · Yi Jyun Chen2,7 · Viktor Papp4 · Balázs Palla4 · Dávid Papp5,6 ·
Chitrabhanu S. Bhunjun2,7 · Vedprakash G. Hurdeal2,7 · Chanokned Senwanna2,8 · Ishara S. Manawasinghe2,9,18 ·
Dulanjalee L. Harischandra2,7,9 · Ajay Kumar Gautam10 · Shubhi Avasthi11 · Boontiya Chuankid2,7 ·
Ishani D. Goonasekara2,7 · Sinang Hongsanan12 · XiangYu Zeng2,7,19 · Kapila K. Liyanage2,17,20 · NingGuo Liu2 ·
Anuruddha Karunarathna2,8 · Kalani K. Hapuarachchi2 · Thatsanee Luangharn2,3 · Olivier Raspé2,7 ·
Rashika Brahmanage2,7,9 · Mingkwan Doilom3,16,17 · Hyang B. Lee13 · Liu Mei9 · Rajesh Jeewon14 ·
Naruemon Huanraluek2 · Napalai Chaiwan2,7 · Marc Stadler15 · Yong Wang1
Received: 20 May 2020 / Accepted: 7 August 2020 / Published online: 24 September 2020
© The Author(s) 2020
Abstract
This is a continuation of a series focused on providing a stable platform for the taxonomy of phytopathogenic fungi and
fungus-like organisms. This paper focuses on one family: Erysiphaceae and 24 phytopathogenic genera: Armillaria, Barriopsis, Cercospora, Cladosporium, Clinoconidium, Colletotrichum, Cylindrocladiella, Dothidotthia,, Fomitopsis, Ganoderma,
Golovinomyces, Heterobasidium, Meliola, Mucor, Neoerysiphe, Nothophoma, Phellinus, Phytophthora, Pseudoseptoria,
Pythium, Rhizopus, Stemphylium, Thyrostroma and Wojnowiciella. Each genus is provided with a taxonomic background,
distribution, hosts, disease symptoms, and updated backbone trees. Species confirmed with pathogenicity studies are denoted
when data are available. Six of the genera are updated from previous entries as many new species have been described.
Keywords Disease · Plant pathology · Phylogeny · Taxonomy · Symptoms
Contents and contributors (main
contributors underlined)
Newly discussed genera and family
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
Armillaria – B Chuankid, M Stadler
Barriopsis – IS Manawasinghe, RS Jayawardena
Cercospora – ID Goonasekara
Clinoconidium – AK Gautam, S Avasthi
Cylindrocladiella – D Harischandra, RS Jayawardena
Dothidotthia – C Senwanna
Erysiphaceae – KK Liyanage, RS Jayawardena, KD Hyde
Fomitopsis – V Papp, B Palla, D Papp
Ganoderma – KK Hapuarachchi, T Luangharn, O Raspe
Golovinomyces – RS Jayawardena
Heterobasidium – V Papp, B Palla, D Papp
Meliola – S Hongsanan, XY Zeng
88.
89.
90.
91.
92.
93.
94.
Neoerysiphe – RS Jayawardena
Nothophoma – IS Manawasinghe, RS Jayawardena
Phellinus – V Papp, B Palla, D Papp
Pseudoseptoria – A Karunarathna, RS Jayawardena
Stemphylium – RS Jayawardena, KD Hyde
Thyrostroma – C Senwanna, KD Hyde
Wojnowiciella – D Harischandra, RS Jayawardena
Updated genera
95.
96.
97.
98.
99.
100.
Cladosporium – NG Liu, RS Jayawardena
Colletotrichum – RS Jayawardena, KD Hyde
Mucor – VG Hurdeal, HB Lee
Phytophthora – CS Bhunjun, RS Jayawardena
Pythium – CS Bhunjun, RS Jayawardena
Rhizopus – VG Hurdeal, HB Lee
* Yong Wang
yongwangbis@aliyun.com
Extended author information available on the last page of the article
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Fungal Diversity (2020) 103:87–218
Introduction
This is the fourth paper in the One Stop Shop series focusing on providing a stable platform for the taxonomy of
plant pathogenic fungi and fungus-like organisms. Genera
included in this series are associated with plant diseases, and
when the data are available we discuss the species that have
been established as pathogens using Koch’s postulates. Some
genera, however, are not well-known plant pathogens and
some may be emerging pathogens, and need further studies
to confirm their pathogenicity. Hyde et al. (2014) launched
this series and stated its specific aims.
Three issues of One Stop Shop (OSS) have been published treating 73 genera and two families of plant pathogenic fungi and fungus-like organisms (Hyde et al. 2014;
Jayawardena et al. 2019a, b, Table 1). In this fourth contribution, a further 24 genera and one family are treated,
providing clarification of their taxonomy and classification.
Six of the entries are updates from previous entries as many
changes have occurred in these genera. For each entry, the
background of the genus, disease symptoms, host distribution, pathogen biology and epidemiology, morphological
based identification, molecular-based identification, updated
phylogeny and recommended genetic markers are provided
and discussed. All contributed entries will be placed in the
database, http://www.onestopshopfungi.org. The main outcome of this series is to enhance the current understanding
of plant pathogens and gain better insights into the current
classification, providing a stable taxonomy and phylogeny
for plant pathogens. This will provide a definitive classification for mycologists and plant pathologists to accurately
identify causal agents of disease and to implement accurate
control strategies.
Materials and methods
Photo plates of the symptoms of the disease and morphological characters are given, when available. Classification
follows Wijayawardene et al. (2020).
For the treated taxa, all species that have been published
until 30 March 2020 are included in the phylogenetic analyses. Sequence data from ex-type, ex-epitype or authentic
or reference/voucher strains for each species were retrieved
from GenBank. Sequence data from single gene regions
Table 1 All entries treated in One stop shop (OSS) series
OSS1 (Hyde et al. 2014)
OSS2 (Jayawardena et al. 2019a)
OSS3 (Jayawardena et al. 2019b)
OSS4 (This paper)
Bipolaris
Botryosphaeriaceae
Botryosphaeria
Botrytis
Choanephora
Colletotrichum
Curvularia
Diaporthe
Diplodia
Dothiorella
Fusarium
Gilbertella
Lasiodiplodia
Mucor
Neofusicoccum
Pestalotiopsis
Phyllosticta
Phytophthora
Puccinia
Pyrenophora
Pythium
Rhizopus
Stagonosporopsis
Ustilago
Verticillium
Alternaria
Bipolaris (update)
Boeremia
Botryosphaeria (update)
Calonectria
Coniella
Corticiaceae
Curvularia (update)
Elsinoë
Entyloma
Erythricium
Fomitiporia
Fulviformes
Laetisaria
Limonomyces
Neofabraea
Neofusicoccum (update)
Phaeoacremonium
Phellinotus
Phyllosticta (update)
Plenodomus
Pseudopyricularia
Tilletia
Venturia
Waitea
Alternaria (update)
Capnodium
Chaetothyrina
Cytospora
Cyphellophora
Cyttaria
Dactylonectria
Diplodia (update)
Dothiorella (update)
Entoleuca
Eutiarosporella
Fusarium (update)
Ilyonectria
Lasiodiplodia (update)
Macrophomina
Medeolaria
Neonectria
Neopestalotiopsis
Pestalotiopsis (update)
Plasmopara
Pseudopestalotiopsis
Rosellinia
Sphaeropsis
Stagonosporopsis (update)
Verticillium (update)
Armillaria
Barriopsis
Cercospora
Cladosporium (update)
Clinoconidium
Colletotrichum (update)
Cylindricladiella
Dothidotthia
Erysiphaceae
Fomitopsis
Ganoderma
Golovinomyces
Heterobasidium
Meliola
Mucor (update)
Neoerysiphe
Nothophoma
Phellinus
Phytophthora (update)
Pseudoseptoria
Pythium (update)
Rhizopus (update)
Stemphylium
Thyrostroma
Wojnowiciella
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Fungal Diversity (2020) 103:87–218
were aligned using Clustal Xv.1.81 (Thompson et al. 1997)
and further alignment of the sequences carried out using
the default settings of MAFFT v.7 (Katoh and Toh 2008;
http://mafft.cbrc.jp/alignment/server/), and manual adjustment was conducted using BioEdit where necessary. Gene
regions were also combined using BioEdit v.7.0.9.0 (Hall
1999). Primers for each gene locus can be found in the bibliography related to the phylogeny presented in each genus.
Phylogenetic analyses consisted of maximum likelihood
(ML), maximum parsimony (MP) and Bayesian posterior
probability (BYPP). Maximum parsimony analysis was
performed using PAUP (Phylogenetic Analysis Using Parsimony) v. 4.0b10 (Swofford 2002) to obtain the most parsimonious trees. Maximum likelihood analyses were also performed in raxmlGUIv.0.9b2 (Silvestro and Michalak 2010)
or RAxML-HPC2 on XSEDE (8.2.8) on the CIPRES science gateway platform (http://www.phylo.org; Miller et al.
2010). Bayesian inference was conducted using MrBayes
v. 3.2.6 on the CIPRES science gateway platform (http://
www.phylo.org; Miller et al. 2010) or stand-alone MrBayes
v.3.1.2 (Ronquist and Huelsenbeck 2003). MrModeltest v.
2.3 (Nylander 2004) or jModeltest v. 2.1.4 (Darriba et al.
2012) was used for the statistical selection of the best-fit
model of nucleotide substitution to parametrize the analyses.
Results
76. Armillaria (Fr.) Staude, Schwämme Mitteldeutschl. 28:
xxviii, 130 (1857)
Background
Armillaria is a plant pathogenic genus in the phylum
Basidiomycota, family Physalacriaceae (He et al. 2019),
collectively referred to as shoestring root-rot fungi or honey
mushrooms. Armillaria can cause root-rot disease in a wide
variety of woody hosts worldwide. Armillaria has undergone significant revision in the past 20 years. The genus
once accommodated any white-spored agaric with broadly
attached gills and an annulus (Volk et al. 1996). Armillaria
mellea is the type species. Most Armillaria species have the
potential to infect healthy and stressed trees, they differ in
their pathogenicity to their hosts and under certain circumstances, they behave as obligate saprobes. Most Armillaria
species are facultative necrotrophs causing root and butt rot
on a broad range of woody plants affecting a variety of forest, shade, ornamental and orchard trees and shrubs. Some
Armillaria species cause significant economic losses to forest trees and in nursery plantations. Armillaria root disease
is found in many temperate and tropical forests throughout
the world. This fungus spreads mainly through the interaction of tree roots. As saprotrophs, Armillaria species are
important wood decomposers that contribute to nutrient
89
cycling in forest ecosystems. As pathogens, they infect and
eventually kill susceptible trees, which impacts forest structure, composition and succession. Trees that are used for
fibre or lumber production, as well as trees located in recreation sites, are affected by these diseases. Such Armillaria
infections may cause yield reduction and tree mortality in
silvicultural and agricultural tree plantations and provoke
economic losses.
Armillaria species are expected to become more aggressive during drought and thus enhance root rot (La Porta et al.
2008; Kolb et al. 2016; Kubiak et al. 2017). The incidence of
Armillaria related root disease is likely to increase as temperatures increase and precipitation decreases due to climate
change (Sturrock et al. 2011). Whilst the ability of the pathogen to sporulate, spread and infect is affected by temperature
and moisture, factors that stress host trees directly may be
just as critical to a successful invasion of host tissues. It
seems likely that the disease will become more severe in
the future, wherever Armillaria susceptible tree species are
subjected to increased levels of climate stress (Klopfenstein
et al. 2009). Currently, Armillaria root disease causes large
growth/volume losses (e.g., 16–55%) in areas of western and
North America (Filip and Goheen 1984; Cruickshank et al.
2011; Lockman and Kearns 2016). Armillaria root disease is
typically more severe in trees that are maladapted to climateinduced stress (Ayres and Lombardero 2000; Kliejunas et al.
2009; Sturrock et al. 2011). Thus, it is likely that climate
change will further exacerbate damage from Armillaria root
disease, which can further predispose trees to beetle attack
(e.g. Hertert et al. 1975; Tkacz and Schmitz 1986; Goheen
and Hansen 1993).
Armillaria mellea is an edible species that has long been
used as a Traditional Chinese Medicine. Some of Armillaria species are is believed to be able to improve health and
prevent various diseases, such as insomnia, pain, and neurasthenia. Extracts of A. mellea exhibit anti-oxidative, antiinflammatory and immune-modulatory activities. Armillaria
mellea can also induce maturation of human dendritic cells.
The chemical constituents isolated from A. mellea include
sesquiterpenoids, steroids, triterpenoids, adenosine and
resin acids. Armillariol C is a furan-based natural product
isolated from Armillaria species. A xylosyl 1,3-galactofucan (AMPS-III) was isolated and identified as a novel antiinflammatory agent from this species.
Classification—Basidiomycota, Agaricomycotina, Agaricomycetes, Agaricomycetidae, Agaricales, Physalacriaceae
(He et al. 2019)
Type species—Armillaria mellea (Vahl) P. Kumm.
Distribution—Worldwide, mostly in temperate areas (northern and southern hemisphere) and some in tropical areas.
Disease symptoms—Armillaria root disease, shoestring root
rot
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Symptoms caused by this fungus can be categorized into
two categories:
Crown symptoms—branch dieback, crown thinning, chlorosis, reddening of foliage or heavier than normal production
of cones.
Basal symptoms—the fungus can grow up from the roots
in the inner bark in some tree species and causes basal
cankers above the infected roots. Resinosis (exudation of
resin) can be observed in resinous conifers. In some plants,
decayed roots or decay in the inner wood of stem bases can
be observed. Species cause a white rot of wood. In white
rot, wood often has a bleached, whitish appearance and are
spongy or stringy, and maybe wet. Black lines called “zone
lines” are usually seen in the decayed wood. These lines
are curved planes in the wood, sometimes called “pseudosclerotial plates”, composed of thickened, dark fungal cells.
They may play a role in the protection of Armillaria from
unfavourable conditions or other fungi that attempt to invade
its territory, including other individuals of the same species.
Actively decaying wood may be luminescent, producing a
faint glow in the dark (Baumgartner and Rizzo 2002; Worrall 2004; Klopfenstein 2009).
There are three major signs of Armillaria root disease in
the field.
Mycelial fans can always be seen in infected and recently
killed trees. These are white mats of fungal mycelium
between the inner bark and wood that are generally substantial and have a mushroom odour.
Rhizomorphs are commonly associated with infection
and are often attached to infected roots, but they may also
be attached to the surface of uninfected roots. Depending
on the species these may be few, small, fragile, hard to find
or abundant and robust. Rhizomorphs can be cylindrical in
soil or flattened under bark, reddish-brown to black branched
and have a cream-coloured tip when actively growing (Guillaumin and Legrand 2013).
Mushrooms that have honey-brown caps can be seen in
clusters near or on the base of trees.
Hosts—Many angiosperms and gymnosperms (especially
conifers) in native, planted forests, orchards and vineyards
(Farr and Rossman 2020).
Pathogen biology, disease cycle and epidemiology
Sexual reproduction results in the diploid mycelium.
Such a mycelium is the dominant phase that is found growing in wood, growing through the soil as rhizomorphs, and
killing trees. Armillaria species can be dispersed through
airborne sexual basidiospores which will establish a new
infection center. These taxa do not reproduce asexually but
disperse by growing mycelium which is the most common
source of infection, through root contacts or root grafts or
by growing through the soil as rhizomorphs. Mycelium in
colonized roots and the rhizomorphs produced serve as the
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Fungal Diversity (2020) 103:87–218
most common mode of infection and may survive for up
to 50 years or more in stumps, depending on the climate,
size of the stump, and other factors (Baumgartner and Rizzo
2002; Worrall 2004; Klopfenstein 2009).
Morphology-based identification and diversity
Armillaria has included only white-spored wood-inhabiting agarics with broadly attached to decurrent gills and macroscopic black to reddish-brown rhizomorphs. Armillaria
basidiomes are easily recognized by their caespitose habit,
annulus and honey colour. It is, however, extremely difficult
to identify some species due to the lack of morphological
apomorphies (Watling et al. 1991; Pegler 2000). Besides,
basidiomata are often not available to differentiate species, which further complicates the taxonomy of Armillaria
(Harrington and Wingfield 1995). In this regard, Armillaria
provides a clear example of where a phylogenetic approach
can contribute significantly to its taxonomy. Until the late
1970s, Armillaria mellea was considered by most researchers to be a polymorphic species with a wide host range and
distribution. Herink (1973), among others, suspected that
this single species might be a species complex. However,
since the morphology of basidiomata is difficult to study
because of overlapping and inconsistent traditionally used
morphological characters, other avenues of research were
pursued. Hintikka (1973) developed a technique that allowed
the determination of mating types in Armillaria. Using a
modification of this method, Korhonen (1978a) was able to
distinguish five European biological species. The cumbersome nature of the mating-type method of species identification prompted a search for other techniques for identifying
collections. They were able to separate all North American species (NABS) of Armillaria except for A. calvescens
and A. gallica, which are apparently very closely related
(Anderson and Stasovski1992). Ten species of Armillaria
in North America have been confirmed from multiple studies utilizing a combination of morphological, biological and
phylogenetic species concepts (Anderson and Ullrich 1979;
Anderson and Stasovski 1992; Burdsall and Volk 1993; Kim
et al. 2006; Ross-Davis et al. 2012). Before, A. mellea shows
great variability in morphology and hosts. These species
were first separated using interfertility tests using cultures
of Armillaria haploid tester strains and morphology. Now,
A. mellea is considered as an independent species, with two
North American biological species (Bérubé and Dessureault
1989; Volk et al. 1996) (Fig. 1).
Molecular-based identification and diversity
Problems surrounding the identification of Armillaria
have led to important advances in developing robust but
rapid DNA techniques. Such techniques have initially
included DNA-base composition (Jahnke et al. 1987) DNADNA hybridization (Miller et al. 1994), sequence analyses of
Fungal Diversity (2020) 103:87–218
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Fig. 1 Disease cycle of Armillaria mellea (redrawn from Agrios 2005)
the IGS-1(Anderson and Stasovski 1992) and ITS (Coetzee
et al. 2001a, b), RFLPs without PCR (Smith and Anderson 1989) and RFLPs of IGS-1 amplicons (Harrington and
Wingfield 1995). Although several of these techniques might
pose some problems (Pérez‐Sierra et al. 2000), by their relative simplicity they have gradually replaced traditional, morphological methods.
The amount of DNA sequence data on Armillaria species has increased substantially since the first publication
on the phylogeny of the genus in the northern hemisphere
(Anderson and Stasovski 1992). As with many other fungal
genera, the focus of such studies initially was set on species
of Europe and North America (Chillali et al. 1998; Coetzee
et al. 2000b). Later, substantial datasets for species in Africa,
Australasia and southeast Asia have become available
(Terashima et al. 1998; Coetzee et al Coetzee et al. 2000a,
2001a). At present, ITS, IGS-1 and tef1 sequences are available in GenBank for the best-known species of Armillaria.
However, there are disjunctions in data sets and relatively
little is known about species from Indo-Malaysia and South
America. Armillaria fruiting bodies are produced seasonally
and not every year; they are, therefore, often not available
during fieldwork (Kile et al. 1991).
Identification using the biological species concept with
species identification based on sexual compatibility tests
(Korhonen 1978a) has been examined for its utility by some
mycologists, but its application was soon abandoned. This
was because of complications due to the absence of known
tester strains, lack of haploid strains, ambiguous mating
interactions and degeneracy of cultures. For these reasons,
DNA-based molecular techniques have finally been preferred in Armillaria taxonomy, either complementing other
methods or on their own. The techniques utilized for the
taxonomy of Armillaria species include comparisons of
RFLPs (Harrington and Wingfield 1995), AFLPs (PérezSierra et al. 2004), and the use of sequences from the ITS,
IGS-1 and tef1 gene in phylogenetic studies (Coetzee et al.
2000b, 2001a; Maphosa et al. 2006; Kim et al. 2006). Phylogenetic methods have made it possible to differentiate the
lineages of the genus in southern Argentina (Pildain et al.
2009). Lineages I and II grouped with A. novae-zelandiae
and A. luteobubalina, respectively, while Lineages III and
IV represented unique taxa that were closely related to A.
hinnulea, Armillaria 4th species from New Zealand (established by Coetzee et al. 2001a, b) and Armillaria Group III
from Kenya (Mwenje et al. 2006). Modern approaches to
identification of Armillaria species are mostly based on the
analyses of DNA sequences. The present study reconstructs
the phylogeny of Armillaria based on a combined ITS, IGS
and tef1 sequence data (Fig. 2, Table 2). However, insufficient data are available for the LSU gene region in GenBank.
Then, it is difficult to have comparative phylogenetic analyses but the single gene analysis of each gene was carried
out to compare the topology of the tree and clade stability.
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Fungal Diversity (2020) 103:87–218
◂ Fig. 2 Phylogenetic tree generated by maximum likelihood analy-
sis of combined ITS-IGS-tef1 sequence data of Armillaria species.
Related sequences were obtained from GenBank. One hundred and
thirty-nine strains are included in the analyses, which comprise 4557
characters including gaps. The tree was rooted with Guyanagaster
lucianii (G31.4) and Guyanagaster necrorhizus (MCA 3950). Single
gene analyses were carried out to compare the topology of the tree
and clade stability. Tree topology of the ML analysis was similar to
the MP and BYPP. ML phylogenetic tree inference was performed
using RAxML version 8.2.12 on the CIPRES web server, using a
mixed-model analysis and the GTRCAT model of substitution. The
four partitions were defined as ITS, IGS, tef1 exons and tef1 introns.
The best scoring RAxML tree with a final likelihood value of −
25308.198187 is presented. The matrix had 1957 distinct alignment
patterns, with 65.74% of undetermined characters or gaps. Estimated
base frequencies of ITS were as follows: A =0.227071, C =0.203923,
G =0.235701, T =0.333305; substitution rates AC =0.628852,
AG=3.751709, AT =1.365607, CG =1.467905, CT =2.788595,
GT = 1.000000. Estimated base frequencies of IGS were as follows:
A =0.244624, C =0.196588, G =0.242370, T =0.316418; substitution
rates AC =0.954911, AG=3.055115, AT =1.041498, CG =1.278095,
CT = 3.421100, GT = 1.000000. Estimated base frequencies of tef1
93
exons were as follows: A =0.228587, C =0.301128, G =0.255865,
T =0.214420; substitution rates AC =0.905728, AG=3.660986,
AT =1.564184, CG =0.648739, CT = 28.048363, GT = 1.000000.
Estimated base frequencies of tef1 introns were as follows:
A =0.215042, C =0.222693, G =0.185633, T =0.376631; substitution
rates AC =1.170263, AG=5.878084, AT =0.847943, CG =1.087990,
CT = 5.095797, GT = 1.000000; gamma distribution shape parameter
α =0.1000000000. The maximum parsimonious dataset consisted
of 2908 constant, 1172 parsimony-informative and 477 parsimonyuninformative characters. The parsimony analysis: CI = 0.610, RI
= 0.861, RC = 0.525, HI = 0.390 in the first tree. Bayesian posterior probability was performed using the Markov chain Monte Carlo
(MCMC) method implemented in MrBayes 3.2.6 with a mixed-model
partition identical to the ones defined in the ML analysis. The best-fit
nucleotide substitution model was separately determined for each partition with jModeltest version 2.1.10 on CIPRES, using the Akaike
Information Criterion. K80+I, K80+I, SYM+G and HKY+G were
selected as best-fit models for ITS, IGS, tef1 exons and tef1 introns,
respectively. At the end of the runs, the average deviation of split frequencies was 0.016675. MP and RAxML bootstrap support value ≥
50% and BYPP ≥ 0.95 are shown, respectively, near the nodes. Holotype or ex-type strains are in bold
Fig. 2 (continued)
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Fungal Diversity (2020) 103:87–218
Table 2 DNA barcodes available for Armillaria
Species
Sources
Country
Armillaria affinis
A. altimontana
JMCR.126
POR100*
A. aotearoa
A. borealis
NZFRI-M 5283*
CMW31075
CMW31072
HKAS 76263,
Gt571
BRNM 699842,
MUAF 501
CMW3172
A1
A5
A618
ST3
Central America? –
USA
AY213579,
AY213580
New Zealand
NR_151846
Belarus
–
China
–
China
KT822294
AF261356 –
–
JN944606,
JF313117
–
KU295542
–
KM205252
–
KM205251
–
KT822426
–
KM205305
KM205304
–
Czech Republic
EU257713
–
EU251402
EU257708
Finland
Finland
Germany
Switzerland
USA
–
JN657467
JN657468
JN657469
AY213559
DQ338540
–
–
–
JF895899
–
JN657440
JN657441
JN657442
AY509163
ST17
USA
TH DJA 91/PUL
F2895
BRNM 706814,
MUAF 516
M110
HKAS 86583,
01108/1
B3
B5
Cameroon
AY213560,
AY213561
KU170952
DQ435623
JN657494
JN657495
JN657496
JF313138,
JF895835
JF895900 JF313130,
JF895836
KU170942 KU289112
–
Czech Republic
EU257715
–
EU251395
EU257709
Canada
China
AY213581
KT822290
–
–
JF313121
KT822417
AY509182
–
Finland
Italy
JN657445
JN657446
–
–
JN657418
JN657419, KJ414318
Japan
UK?
Ukraine
USA
Czech Republic
China
AB510853
–
JN657450
AY213583
EU257716
KT822263
–
–
–
–
–
–
JN657472
JN657473
KJ414321
AB510786
JF746917
JN657477
JF313115
EU251396
KT822416
AB510809
JF288720
JN657423
AY509184
EU257710
–
Korea
Austria
France
France
MG543860
EU257720
–
KT822340
–
–
DQ338547
–
MG544785
EU251403
FJ875698
KT822438
–
EU257712
–
–
Japan
Australia
Ethiopia
AB559000
AF329917
AY882969
–
AB558992
DQ338552 DQ435646
–
–
–
–
AY172032
Kenya
La Reunion
Malawi
South Africa
Tanzania
Zimbabwe
Canada
China
AY882973
AY882974
AY882976
AY882971
AY882978
AY882967
AY213568
–
–
DQ338556
–
–
–
–
–
–
AY882965
AY882963
AY882959
AF204821
AY882961
AF489481
AY509171
KM205313
A. calvescens
A. cepistipes
A. ectypa
A. fumosa
A. fuscipes
A. gallica
13
94-39-04
SY1Ra
C5C-S1
W113
BRNM 695717
HKAS 86586,
97033/1
KFRI1616
BRNM 704974
CMW15693
HKAS 86565,
70011/13
TFM27105, Je-2
CMW4957, 123
CBS 118122,
CMW5844, WG1I
CMW7184
CMW4953
CMW4871
CMW2717
CMW4949
CMW4874
M70
CMW31087
ITS
LSU
tef1
–
DQ435622
–
–
–
–
JF313123
KM205260
IGS1
–
AY509181
AY509164
Fungal Diversity (2020) 103:87–218
95
Table 2 (continued)
Species
A. gemina
A. heimii
A. hinnulea
A. jezoensis
A. limonea
A. lutea
A. luteobubalina
A. mellea
Sources
Country
ITS
LSU
tef1
IGS1
HKAS 86569,
93421/1
BRNM 706835,
MUAF 575
E4
86-016/3
86-008/2
NA4
MEX55
CMW7202
HY2a
Aga235
ST22, EL-1
China
KT822277
–
KT822414
–
Czech Republic
EU257718
–
EU251390
EU636240
France
Germany
Iran
Japan
Mexico
South Africa
Ukraine
USA
USA
–
–
–
–
–
–
–
JF895911
JF895912
Korea
Korea
Korea
Canada
USA
–
–
–
FJ618757
–
JN657479
KJ200952
KJ200954
AB510761
KC111014
–
JN657482
JF895847
JF313126,
JF895848
MG544774
MG544784
MG544777
FJ618670
JF313136
JN657425
KJ200946
KJ200948
AB510834
JX281799
AY190245
JN657428
–
AY509172
Ame10
KA14-1647
Ame7
JB-38A
ST8
JN657452
–
–
AB510881
JX281809
AY190247
JN657455
–
AY213569,
AY213570
MG543850
MG543859
MG543852
FJ664586
AY213555
C4
166
K59
CMW4980
CMW4990
HUA9116
CMW4680
90-4 (Alut)
CMW4977
AFTOL-ID449
B176
HKAS 86590,
00020/6
D1
B1212, CMW4615,
94056/1
B1205, CMW4613,
86009/1
CBS122232,
CMW11265, 426
FFPRI420861,
WD2588, 89-07
HKAS 86598,
PFD84-103
MEX74
CMW3975
B916, CMW4610,
A-5
HY-3
Am115
B927
CMW31161
Congo
–
Kenya
Australia
New Zealand
Japan
New Zealand
USA
Australia
USA
England
China
AY333917
AY333913
AY333916
–
AF329905
–
AF329930
–
AF329912
AY789081
AF163578
KT822251
–
–
–
DQ338555
DQ338555
–
DQ338560
–
DQ338559
AY700194
–
–
–
–
–
DQ435648
DQ435648
–
DQ435655
–
DQ435657
AY881023
–
KT822354
–
–
–
–
AY509158,
AY509159
AY330630
AY330634
AY330627
AF445077
–
D89921
AF445073
AF243066
AF445069
–
AF163602
–
France
Hungary
JN657464
AF163581
–
–
JN657491
–
JN657437
AF163605
Iran
AF163583
–
DQ435637
AF163606
Italy
FJ875692
FJ875694
DQ435636
–
Japan
AB510852
–
AB510796
AB510808
Kenya
KT822248
–
KT822348
–
Mexico
South Africa
South Korea
JX281807
AF310329
AF163592
–
–
–
KC111011
–
DQ435639
JX281797
AF310327
AF163612
Ukraine
USA
USA
China
JN657466
–
AF163595
–
–
JF895920
FJ875695
–
JN657493
JF895856
DQ435634
KM205267
JN657439
–
AF163608
KM205320
13
96
Fungal Diversity (2020) 103:87–218
Table 2 (continued)
Species
A. mexicana
A. montagnei (ex
luteobublina)
A. montagnei (ex
luteobublina)
A. montagnei (Lineage II)
A. montagnei (Lineage II)
A. nabsnona
A. novae-zelandiae
A. novae-zelandiae
(Lineage I)
A. ostoyae
A. puiggarii
A. sinapina
A. singula
13
Sources
Country
ITS
LSU
tef1
IGS1
CMW8082
HUA93110
MEX87*
CMW5446
Bhutan
Japan
Mexico
Argentina
AY554333
–
KR061310
AF448422
–
–
–
DQ338562
–
–
KR061314
DQ435650
AY554335
D89922
KR061306
AF445068
CMW8876
Chile
AF448423
–
DQ435658
AF445065
Arg309
Argentina
FJ660939
FJ711625
–
–
Arg270*
Argentina
FJ711609
–
–
–
ST16
HKAS 85523,
Gt798
M90
USA
China
AY213574
KT822333
–
–
JF313124
KT822411
AY509178
–
Canada
AY213573
–
JF313122
00-3-1
C21
Japan
USA
AB510899
AY213572
–
–
AB510766
JF313119
CMW6905
Juk14411
CMW4967
CMW5448
CMW4143
CMW3951
CMW4722
Arg49
USA
Korea
Australia
Chile
Indonesia
Malaysia
New Zealand
Argentina
–
MG543857
AF329921
AF448417
AF448421
AF448419
AF329926
FJ660935
DQ338542
–
–
DQ338554
DQ338564
DQ338553
DQ338551
FJ711629
DQ435631
MG544782
DQ435651
DQ435653
DQ435654
–
DQ435652
–
AY509176,
AY509177
AB510850
AY509174,
AY509175
–
–
–
–
–
–
–
–
SP308014*
BRNM706815
CMW31102
HKAS 86579,
96043/11
C2
88-01-19
D20
HpAg1
P1404
Ame5
3626
MCA 3111/PUL
F2896/BRG 41295
V48.5
M50
Brazil
Czech Republic
China
China
EF639348
EU257717
–
KT822310
–
–
–
–
–
EU251400
KM205272
KT822428
–
EU257711
KM205325
–
France
Japan
Switzerland
Ukraine
USA
Korea
Australia
Guyana
JN657459
AB510859
JN657463
JN657462
AY213554
MG543851
FJ664607
KU170954
–
–
–
–
–
–
FJ618752
KU254228
JN657486
AB510784
JN657490
JN657489
JF313140
MG544776
FJ618665
KU289104
JN657432
AB510815
JN657436
JN657435
AY509157
–
–
–
Canada
Canada
FJ618763
–
FJ618676
JF313114
–
AY509167
China
China
FJ664609
AY213563,
AY213564
–
KT822323
–
–
KM205277
KT822422
KM205330
–
Japan
USA
USA
Japan
AB510873
–
AY213565
–
–
JF895916
–
–
AB510774
JF895850
JF313132
–
AB510827
–
AY509168
D89926
CMW31112
HKAS 86566,
96015/39
96-7-1
P2-7
ST12
HUA9101*
Fungal Diversity (2020) 103:87–218
97
Table 2 (continued)
Species
Sources
Country
ITS
LSU
tef1
IGS1
A. socialis
A. solidipes
T2
MS2-11
CMW31107
PSpa86.5
Arg12
Arg25
CMW31118
99122/13
CMW3165
CMW31119
HKAS 86604,
CT1097.3
96-1-8
HKAS 86605,
901582
HAt1S5
ATMUS2
France
USA
Finland
Argentina
Argentina
Argentina
China
China
France
Italy
Italy
DQ784801
–
–
FJ664612
FJ660948
FJ660946
–
KT822339
–
–
KT822338
–
JF895918
–
FJ618750
FJ711618
FJ711621
–
–
DQ338546
–
–
–
JF895852
KM205275
–
–
–
KM205280
KT822441
DQ435642
KM205281
KT822440
–
–
KM205328
–
–
–
KM205333
–
–
KM205334
–
Japan
Slovenia
AB510867
KT822337
–
–
AB510804
KT822439
AB510823
–
Ukraine
USA
HQ232292
AY213588
–
–
HQ285906
JF313113
CMW10581
CMW31123
Bhutan
China
AY554329
–
–
–
FJ875699
KM205284
HQ232284
AY509189,
AY509190
AY624365
KM205337
CMW31124
CMW31127
China
China
–
–
–
–
KM205285
KM205286
KM205337
KM205339
CMW31128
CMW31136
China
China
–
–
–
–
KM205287
KM205293
KM205340
KM205346
CMW31138
CMW31140
China
China
–
–
–
–
KM205294
KM205296
KM205347
KM205349
CMW31142
CMW31144
China
China
–
–
–
–
KM205297
KM205298
KM205350
KM205351
CMW31145
CMW31146
China
China
–
–
–
–
KM205299
KM205300
KM205352
KM205353
CMW31148
CMW31150
China
China
–
–
–
–
KM205301
KM205302
KM205354
KM205355
CMW31151
HKAS 86615
HKAS 86621
HKAS 86623
HKAS 86551
HKAS 86613
HKAS 86614
HKAS 86602
HKAS 86606
HKAS 86574
HKAS 86574
HKAS 86570
HKAS 86571
China
China
China
China
China
China
China
China
China
China
China
China
China
–
KT822315
KT822306
KT822318
KT822279
KT822319
KT822305
KT822308
KT822281
KT822324
KT822327
KT822320
KT822288
–
–
–
–
–
–
–
–
–
–
–
–
–
KM205303
KT822384
KT822386
KT822363
KT822367
KT822388
KT822391
KT822378
KT822359
KT822361
KT822364
KT822402
KT822404
KM205356
–
–
–
–
–
–
–
–
–
–
–
–
A. sparrei
A. umbrinobrunnea
A. tabescens
Bhutanese Group 2
Chinese Biological
species C
Chinese Biological
species F
Chinese Biological
species H
Chinese Biological
species J
Chinese Biological
species L
Chinese Biological
species N
Chinese Biological
species O
Chinese Lineage 1
Chinese Lineage 2
Chinese Lineage 3
Chinese Lineage 4
Chinese Lineage 5
Chinese Lineage 6
13
98
Fungal Diversity (2020) 103:87–218
Table 2 (continued)
Species
Sources
Country
ITS
LSU
tef1
IGS1
Chinese Lineage 7
HKAS 83303
HKAS 83361
94-2-1
2000-71-13
China
China
Japan
Japan
KU378047
KU378048
AB510888
AB510879
–
–
–
–
KT822437
KT822436
AB510768
AB510773
–
–
AB510840
AB510832
Japanese Nag. E
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher strains are also in bold
This phylogenetic tree is largely in accordance with earlier
studies from Coetzee et al. (2018) and provides the most
conclusive phylogeny of the genera to date. Genealogical
concordance phylogenetic species recognition (GCPSR)
using the concordance among several gene trees (Taylor
et al. 2000; Dettman et al. 2003) to delineate species has
become standard in fungal taxonomy. However, except for a
few studies (Guo et al. 2016; Tsykun et al. 2013), this taxonomic method has not been widely implemented in Armillaria taxonomy. Sequences of the genomes of key species
are already providing prospects to study the evolution and
systematics of Armillaria. They are certain to lead to important breakthroughs regarding not only the taxonomy but the
biology and ecology of these fungi in the future (Sipos et al.
2017).
Recommended genetic marker (genus level)—ITS
Recommended genetic markers (species level)—ITS, IGS1,
tef1
Additional genetic markers (species level)—LSU, tub2
Accepted number of species—There are 278 epithets in
Index Fungorum (2020) listed for this genus. However,
sequence data are only available for 31 species including 16
groups of unnamed species (Table 2).
References—Watling et al. (1991), Pegler (2000), Harrington and Wingfield (1995) (morphology); Coetzee et al.
(2000a, b, 2001a, b), Maphosa et al. (2006), Mwenje et al.
(2006), Kim et al. (2006), Coetzee et al. (2018) (molecular
phylogeny).
77. Barriopsis A.J.L. Phillips, A. Alves & Crous, in Phillips
et al., Persoonia 21: 39 (2008)
Background
Stevens (1926) originally described the type species of
Barriopsis in Physlospora as Physlospora fusca and Petrak
and Deighton (1952) transferred it to Phaeobotryosphaeria. The fungus that was considered by Stevens (1926),
and Petrak and Deighton (1952) did not have apiculi on its
ascospores and was not similar to Phaeobotryosphaeria
which had small, hyaline apiculi on the ascospores. von
Arx and Müller (1954) considered Phaeobotryosphaeria as
13
a synonym of Botryosphaeria. Based on morphological difference and molecular sequence data, Phillips et al. (2008)
introduced Barriopsis. Species of Barriopsis are mostly saprobic and weak pathogens (Phillips et al. 2013).
Classification—Ascomycota, Dothideomycetes, Incertae
sedis, Botryosphaeriales, Botryosphaeriaceae
Type species—Barriopsis stevensiana A.J.L. Phillips &
Pennycook
Distribution—Species appear to be confined to regions with
tropical or subtropical climates including Australia, Cuba,
Iran and Thailand (Phillips et al. 2008; Abdollahzadeh et al.
2009; Liu et al. 2012; Phillips et al. 2013; Doilom et al.
2014; Konta et al. 2016; Dissanayake et al. 2016; Hyde et al.
2018b; Burgess et al. 2019).
Disease symptoms—Barriopsis species can be weak pathogens and their pathogenicities are uncertain (Phillips et al.
2008; Dissanayake et al. 2016). Barriopsis stevensiana and
B. iraniana were isolated from infected branches, fruits and
leaves with various disease symptoms, including dieback,
canker, rot and necrosis, from Cupressus sempervirens,
Mangifera indica, Citrus sp. and Olea sp. in northern and
southern provinces of Iran (Abdollahzadeh et al. 2009). Species of this genus may be future emerging pathogens.
Hosts—Archontophoenix alexandrae, Cassia sp., Citrus sp.,
Mangifera indica, Olea sp. Tectona grandis (Phillips et al.
2008, 2013; Abdollahzadeh et al. 2009; Liu et al. 2012; Doilom et al. 2014; Konta et al. 2016; Dissanayake et al. 2016;
Hyde et al. 2018b, 2020b).
Pathogen biology, disease cycle and epidemiology
Barriopisis in this article is considered as an emerging pathogen. Further studies to identify the biology, disease cycle
and epidemiology are needed.
Morphological based identification and diversity
The sexual morph is characterized by brown aseptate
ascospores that are widest in the center and lack terminal
apiculi (Phillips et al. 2008, 2013; Doilom et al. 2014; Dissanayake et al. 2016; (Fig. 3)). Barriopsis archontophoenicis forms the sexual morph in culture medium after long
Fungal Diversity (2020) 103:87–218
99
Fig. 3 Barriopsis stevensiana
MFLU 19–1560. a Ascomata on dead twigs of Cassia
sp. b Ascomata cut through
horizontally showing the white
contents with dark spots. c, d
Sections through ascomata. e,
f Ascospores. g Germinated
ascospore. Scale bars: c, d =
200 µm, e, f = 20 µm, g = 100
µm
periods of incubation (up to 6 months, Konta et al. 2016).
The asexual morph is lasiodiplodia-like with hyaline conidia
that become dark-brown and septate with irregular longitudinal striations (Stevens 1926). Abdollahzadeh et al. (2009)
observed the asexual morphs of B. fusca and B. iraniana
and confirmed that the morphology is similar to the description given by Stevens (1926). In their study, they revealed
that this genus can be distinguished from other genera of
Botryosphaeriaceae by the presence of visible striations on
conidia at an early stage of development.
However, using morphology alone in identifying these
species is not wise due to the overlapping of morphological
characters within the genus. Therefore, the use of multi loci
phylogeny along with morphology is recommended for this
genus. Very little is known about the diversity and pathogenicity of this botryosphaeriaceous genus and future studies
are needed to confirm its pathogenic nature.
Molecular based identification and diversity
Phillips et al. (2008) using SSU, ITS, LSU, tef1 and tub2
sequence data established Barriopsis which is sister to Phaeobotryon. Based on ITS and tef1 sequence data, Abdollahzadeh
et al. (2009) introduced B. iraniana. Doilom et al. (2014) introduced B. tectonae based on ITS, tub2 and tef1 sequence data.
In this study, it was mentioned that ITS and tub2 sequence data
have lesser variation, while tef1 sequence data have considerable
variation. Konta et al. (2016) added a new species, B. archontophoenicis with the use of ITS, LSU, SSU and tef1 sequence
data. In this study, we construct the phylogenetic tree for the
accepted species based on ITS and tef1 sequence data (Fig. 4).
Recommended genetic marker (genus level)—ITS
Recommended genetic marker (species level)—tef1
Accepted number of species—There are six species epithets
in Index Fungorum (2020), however only five species have
DNA sequence data (Table 3).
References—Phillips et al. (2008), Abdollahzadeh et al.
(2009) (morphology and phylogeny); Dissanayake et al.
(2016) (accepted number of species, phylogeny); Doilom
et al. (2014), Konta et al. (2016) (new species).
78. Cercospora Fresen. ex Fuckel, Hedwigia 2(15): 133
(1863)
Background
Cercospora includes pathogens, saprobes and endophytes.
Species are widely distributed, occurring on numerous flowering and ornamental plants, ferns, other fungi (as parasites),
gymnosperms, grasses and other monocotyledons such as
lilies, magnoliids and palms, mostly causing leaf spots. The
well-known asexual morph, which is hyphomycetous, are
13
100
Fungal Diversity (2020) 103:87–218
Fig. 4 Phylogram generated
from maximum likelihood
analysis based on combined
ITS, and tef1 sequence data of
Barriopsis species and closely
related taxa. Fifteen strains
are in the combined sequence
analyses, which comprise 865
characters including gaps.
Diplodia mutila (CBS 112553
and CBS 230.30) was used
as the outgroup taxa. Tree
topology of the ML analysis
was similar to the one generated from BI. The best scoring
RAxML tree with a final likelihood value of − 2372.487246
is presented. The matrix had
201 distinct alignment patterns,
with 12.30% of undetermined
characters or gaps. Estimated
base frequencies were as
follows: A = 0.207721, C
= 0.288041, G = 0.271092,
T = 0.233145; substitution
rates AC = 1.068561, AG =
2.489613, AT = 0.682766, CG
= 1.417925, CT = 4.236517,
GT = 1.000000; gamma
distribution shape parameter α
= 1.343820. RAxML bootstrap
support value ≥ 50% and BYPP
≥ 0.95 are shown respectively,
near the nodes. Ex-type strains
are in bold
Table 3 DNA barcodes available for Barriopsis
Species
Isolate
MFLUCC 14-1164*
Barriopsis
archontophoenicis
B.iraniana
IRAN 1448C*
IRAN1449C
B.tectonae
MFLUCC 12-0381*
B. thailandica
MFLUCC 14-1190*
B. stevensiana
CBS 174.26*
ITS
tef1
KX235306
KX235305
FJ919663
FJ919665
KJ556515
KY115675
NR119698
FJ919652
FJ919654
KJ556516
KY115676
–
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and
marked with an asterisk (*). Voucher strains are also in bold
13
among the largest groups of plant pathogenic fungi causing
leaf spots, leading to diseases on many economically important crops (Agrios 2005; To-Anun et al. 2011; Groenewald
et al. 2013; Guatimosim et al 2016; Park et al. 2017). Comparatively only a few sexual morphs have been studied (Hyde
et al. 2013). A photosensitizing toxic compound named ‘cercosporin’ is responsible for Cercospora species inhabiting
such a wide host range (Daub et al. 2005; Thomas et al. 2020).
Classification—Ascomycota, Dothideomycetes, Dothideomycetidae, Capnodiales, Mycosphaerellaceae
Type species—Cercospora apii Fresen., Beitr. Mykol. 3: 91
(1863)
Distribution—Worldwide
Disease symptoms—Leaf blights and spots
Fungal Diversity (2020) 103:87–218
This disease affects the leaves, petioles, stems and peduncles of the tree. Infection and lesion formation initially occur
on older leaves before progressing to newer ones. Small,
brown flecks develop with a reddish border, expanding to
circular spots with an ashy-grey centre. Concentric rings
may be observed as individual lesions expand. This tissue
becomes thin and brittle, and often drops out, leaving a ragged hole. These lesions often resemble frogeyes, giving this
disease its common name. Severely affected leaves wither
and die from coalescing lesions (Shane and Teng 1992; Steddom et al. 2005).
Species of Cercospora cause blights and spots on the
leaves, petioles, stems and peduncles of trees. Often infection and lesion formation occurs on older leaves before progressing to newer ones. Common symptoms include small,
brown lesions that develop with a reddish border, eventually
expanding to larger circular or angular spots. Concentric
rings may be observed as individual lesions expand. The
tissue becomes thin and brittle, and often drops out, leaving
a ragged hole. Severely affected leaves wither and die from
coalescing lesions (Shane and Teng 1992; Steddom et al.
2005).
Hosts—Wide host range including plant genera in Amaranthaceae, Apiaceae, Asteraceae, Arecaceae, Chenopodiaceae, Convolvulaceae, Cryptogammaceae, Cucurbitaceae,
Cyatheaceae, Dennstaedtiaceae, Dioscoreaceae, Euphorbiaceae, Fabaceae, Gunneraceae, Hydrangeaceae, Lamiaceae,
Lygodiaceae, Musaceae, Myrtaceae, Onagraceae, Plumbaginaceae, Poaceae, Pteridaceae, Scrophulariaceae, Solanaceae,
Thelypteridaceae and Urticaceae (Farr and Rossman 2020).
Cercospora apii causes leaf spot disease on celery and C.
beticola on sugar beet (Braun et al. 2013; Guatimosim et al.
2016). The pathogen Cercospora cf. sigesbeckiae infects
various plant families, including economically valuable
crops such as soybean, causing ‘Cercospora leaf blight’, a
disease characterized by leaf bronzing (Albu et al. 2016,
2017). Some other species identified as causative organisms of the leaf blight are C. kikuchii and C. cf. flagellaris
(Soares et al. 2015; Rezende et al. 2020). The yield losses
related to Cercospora disease have been reported from Canada, China, India and other regions in the USA and South
America (Almeida et al. 2005; Cai et al. 2009; Hershman
2009; Wrather et al. 2010; Geisler 2013; Albu et al. 2017;
Bandara et al. 2020). Cercospora is among the leading fungal pathogens that cause a severe threat to soybean, which
is an important grain legume crop, by reducing seed production and quality (Arantes et al. 2020). Two notable pathogens on soybean are C. kikuchii (leaf blight and purple seed
stain) and C. sojina (frogeye leaf spot) (Soares et al. 2015)
Other notable reports include Cercospora leaf spots,
which are the most common and destructive of the Hibiscus
diseases, often resulting in complete crop loss (Park et al.
2017) and more than 200 fungal species in association with
101
various diseases of ‘kenaf’ (Hibiscus cannabinus) worldwide (Park et al. 2017). Key proteins and expression of
genes that could inhibit the pathogen C. kikuchii in soybean
(Arantes et al. 2020) have been investigated. However, based
on previous reports, morphological characters, phylogeny
and pathogenicity of Cercospora cf. nicotianae was identified as one of several cryptic species causing Cercospora leaf
blight (Sautua et al. 2019, 2020). Thomas et al. (2020) proposed the expression of fungal cercosporin auto resistance
genes and silencing of the cercosporin pathway as effective
strategies to combat Cercospora diseases.
Pathogen biology, disease cycle and epidemiology
The taxa survive on undecomposed residues in soil, on weed
hosts and seeds. Leaf spot disease is favoured by warm, wet
weather. Severe outbreaks generally require a period of
showery weather. Infection from germinating fungal spores
occurs via penetration of leaf stomata by fungal hyphae.
Spores spread in wind, rain, irrigation or via mechanical
tools (Vereijssen 2004; Lin and Kelly 2018).
Morphological based identification and diversity
Cercospora has been widely applied to all kinds of dematiaceous hyphomycetous asexual morphs characterized
by holoblastic conidiogenesis and some associated with
“Mycosphaerella”-like sexual morphs (Hyde et al. 2013;
Groenewald et al. 2013). Species resembling the genus type,
C. penicillata, characterized by pigmented conidiophores,
thickened and darkened conidiogenous loci and singly
formed colourless conidia are identified as Cercospora
sensu stricto (Ellis 1971, 1976). Chupp (1954) published
a worldwide monograph of this group which listed 1,419
species. A vast number of studies related to Cercospora
are based on morphology or confined to specific regions
or hosts (Phengsintham et al. 2013a, b). Hence, more than
3000 species of Cercospora have been described (Pollack
1987), often as a result of taxa being considered as hostspecific at a genus or family level (Crous and Braun 2003;
Groenewald et al. 2005). However, based on morphological features of the structure of conidiogenous loci and hila,
absence or presence of pigmentation in conidiophores
and conidia, Crous and Braun (2003) revised the generic
circumscription of Cercospora, resulting in the reduction
of the number of species to 659. A series of publications
related to Cercospora and its allied genera in Mycosphaerellaceae, along with illustrations and descriptions of sexual
morphs was published by Braun et al. (2013, 2014, 2015a,
b, 2016).
Molecular based identification and diversity
Cercospora is monophyletic (Stewart et al. 1999; Hyde et al.
2013). Groenewald et al. (2013) provided a comprehensive
phylogenetic analysis of 360 isolates which included ITS,
13
and protein-coding genes; translation elongation factor
1-alpha (tef1), actin (act), calmodulin (cal) and histone 3
(his). This provided a basis for the identification of Cercospora species, indicating most to be host-specific (Park
et al. 2017). Bakhshi et al. (2018) subjected 170 Cercospora isolates to an eight-gene analysis (tef1, act, cal, his,
tub2, rpb2, gapdh) which resulted in several new clades
within the C. apii, C. armoraciae, C. beticola, C. cf. flagellaris and Cercospora sp. G. complexes. The combination
of tef1, cal, tub2, rpb2 and gapdh provided high phylogenetic resolution for distinguishing Cercospora species with
gapdh being the gene effective in distinguishing the species
complexes (Bakhshi et al. 2018). The genomes for several
species—Cercospora arachidicola, C. aff. canescens, C. cf.
sigesbeckiae, C. kikuchii, C. sojina and C. zeae-maydis have
been published, of which C. cf. sigesbeckiae and C. sojina
are important soybean pathogens (Albu et al. 2017; Sautua
et al. 2019). The mating-type genes of some asexual Cercospora species have been characterised (Groenewald et al.
2013), of which C. beticola, C. zeae-maydis and C. zeina are
heterothallic, while only one mating type was discovered in
populations of C. apii and C. apiicola (Groenewald et al.
2006, 2010).
In soybean cultivation regions such as China, Latin
America or the USA, C. sojina occurs as several pathotypes named as races, and their existence differs from soybean cultivar-to-cultivar (Athow et al. 1962; Yorinori and
Henechin 1978; Mian et al. 2008; Gu et al. 2020). Apart
from being differentiated physiologically, several molecular
genetic tools such as AFLPs (Amplified Fragment Length
Polymorphisms), SSR markers and SNP markers have been
utilized to characterize their population diversity (Gu et al.
2020). The combination of DNA sequence data with ecology, morphological and cultural characteristics named as
the Consolidated Species Concept (Quaedvlieg et al. 2014)
is an effective method for delimiting Cercospora species
(Groenewald et al. 2013; Bakhshi et al. 2015, 2018). Here
we provide an updated phylogenetic tree of combined ITS,
tef1, act, cal, his, tub2, rpb2 and gapdh (Fig. 5).
Recommended genetic markers (genus level)—LSU, ITS
Recommended genetic markers (species level)—ITS, tef1,
act, cal, his, tub2, rpb2, gapdh
Accepted number of species—There are over 3100 epithets
listed in Index Fungorum (2020), however, only 93 have
DNA sequence data (Table 4).
References—Braun et al. (2013, 2014, 2015a, b, 2016) (morphology), Groenewald et al. (2013) (morphology, phylogeny), Albu et al. (2017) (morphology, phylogeny), Guatimosim et al. (2016) (morphology, phylogeny), Bakhshi et al.
(2015, 2018) (morphology, phylogeny).
13
Fungal Diversity (2020) 103:87–218
Fig. 5 The most parsimonious tree generated by MP analysis of combined ITS, tef1, act, cal, his, tub2, rpb2 and gapdh sequence data of
Cercospora species is presented. Related sequences were obtained
from previous publications and GenBank. One hundred and fourteen strains are included in the analysis comprising 4222 characters
including gaps, of which 2942 characters are constant, 514 characters
are parsimony-uninformative and 766 are parsimony-informative. The
parsimony analysis of the data matrix resulted in the maximum of 84
equally most parsimonious trees with a length of 3092 steps (CI =
0.557, RI=0.678, RC = 0.382, HI = 0.443) in the first tree. The tree
was rooted with Septoria provencialis (CBS 118910). Tree topology
of the MP analysis was similar to the ML and BYPP analyses. ML
and MP bootstrap support values ≥70% and BYPP ≥0.95 (ML/ MP/
BYPP) are shown respectively near the nodes. Ex-type strains are in
bold.
79. Clinoconidium Pat., Bulletin de la Société Mycologique
de France 14: 156 (1898)
Background
Clinoconidium is an important genus that causes smut
disease on plants in the family Lauraceae. This genus was
established by Patouillard (1898) and typified with Clinoconidium farinosum. Taxonomically, Clinoconidium is placed in
Cryptobasidiaceae (Exobasidiales, Exobasidiomycetes, Basidiomycota) and characterized by aseptate, colourless, and globose to ovoid basidiospores which are dispersed individually.
The name Clinoconidium was considered illegitimate because
of the designation of an illegitimate type species name; however, it was later validated by Saccardo (1902).
Clinoconidium is a gall producing genus which was once
named as Ustilago by Ito (1935, 1936) due to the presence of
a powdery spore mass on the surface of the galls. This genus
was also transferred to another gall producing genus Melanopsichium by Kakishima (1982). However, it was renamed
as Clinoconidium as its sorus structure and spore features
are quite different from those of Ustilago (Saccardo 1902).
The spores of Ustilago species are formed from sporogenous
hyphae, whereas this fungus produces spores from hymenial
layers in the galls. Spore walls are comparatively thinner
than those of Ustilago. The differentiation from Melanopsichium, a gall producing taxon on plants in Polygonaceae
(Vánky 2013) includes variation in gall structures and sporulation. Melanopsichium produces spores in chambers formed
inside of gall tissues, while this genus produces spores in
peripheral lacunae on the surface of gall tissues. The morphological characters of these taxa showed its close similarity to Clinoconidium.
Classification—Basidiomycota, Ustilaginomycotina,
Exobasidiomycetes, Exobasidiomycetidae, Exobasidiales,
Cryptobasidiaceae
Type species—Clinoconidium farinosum Pat. ex Sacc. &
P. Syd
Distribution—Brazil, China, Costa Rica, India, Japan, Panama, Spain, Taiwan and Venezuela
◂
102
Fungal Diversity (2020) 103:87–218
103
13
104
Fig. 5 (continued)
13
Fungal Diversity (2020) 103:87–218
Fungal Diversity (2020) 103:87–218
Disease symptoms—mainly observed as powdery pappus
gall in fruits. Infection initiates on very young fruits, converted into round, wrinkled galls. The fruit galls are then
covered with a powdery mass of spores during early days
of infection, withering in the rainy season, leaving behind
hard, earthy, brown galls. On Cinnamon, entire young fruits
are molded with buff and spongy smut like taxa in the full
bloom of disease. Interestingly this infection is restricted to
fruits only (Fig. 6).
Hosts—different plants of Lauraceae including, Apollonias barbujana, Cinnamomum burmannii, C. camphora, C.
daphnoides, C. tamala, C. tenuifolium, Nectandra sp., Octea
sp., Oreodaphne sp. and Phoebe neurophylla (Farr and Rossman 2020).
Morphological based identification and diversity
This is an important pathogenic genus; producing galls on
shoot buds of host plants belonging to the family Lauraceae.
Fruits of the host are completely or partially transformed
into reddish-brown to dark brown, irregularly malformed,
enlarged, globose to subglobose galls; larger than normal
fruits. Hymenia formed in peripheral lacunae of the galls are
pale yellow to whitish and covered by the host epidermis.
Inner tissues of galls consist of hyphae and deformed plant
cells. Hyphae are intercellular, hyaline, compact, septate,
smooth-walled and lack clamp connections, while haustoria
are intercellular, slightly lobed to irregular and observed in
deformed host cells. Upon maturation, galls rupture, exposing orange to dark brown or creamish white spore masses
which cover the entire infected young fruits. Sterile hyphae
can be found intermingled between the basidia in some species and are indistinguishable from young basidia or absent
in some species of Clinoconidium. Basidia are clavate, hyaline, depressed, difficult to observe and gastroid, densely
aggregated in masses, formed in irregular fascicles from
basally agglutinated hyphae and the wall is densely foveolate
when mature. Basidiospores are ellipsoid, clavate, pyriform,
fusoid, globose, subglobose to oval, aggregated in a creamish white to brown coloured masses on the surface of the
galls, hyaline or wall pale brown to brown, rugose when
mature; producing long branched hyphae with septa when
germinated on culture media and proliferating sympodially.
Molecular based identification and diversity
There are seven epithets of Clinoconidium recorded on
various plant hosts. Sequence data for Clinoconidium bullatum, C. cinnamomi, C. onumae and C. sawadae are available in GenBank, including sequence data for LSU and ITS.
Clinoconidium farinosum and C. globosum lack sequence
105
data in GenBank. ITS and LSU are the most suitable loci
for f (Fig. 7).
Recommended genetic markers (genus level)—ITS, LSU
Recommended genetic markers (species level)—ITS, LSU
Accepted number of species—There are seven species epithets in Index Fungorum (2020), however, only four species
have DNA molecular data (Table 5).
References—Hendrichs et al. (2003), Jiang and Kirschner
(2016), Kakishima et al. (2017a, b) (morphology, phylogeny)
80. Cylindrocladiella Boesew., Canadian Journal of Botany
60 (11): 2289 (1982)
= Nectricladiella Crous & C.L. Schoch, Studies in Mycology 45: 54 (2000)
Background
Boeswinkel (1982) established Cylindrocladiella to
accommodate five Cylindrocladium-like species producing
small, cylindrical conidia. Even though the generic status of
Cylindrocladiella was initially opposed by Crous and Wingfield (1993), later studies on morphological comparisons by
Crous et al. (1994) and molecular data (Victor et al. 1998;
Schoch et al. 2000) supported the establishment of Cylindrocladiella as a genus. This genus is commonly confused with
the asexual morph of Calonectria but can be distinguished
by clear morphological differences, such as aseptate stipe
extensions, different branching patterns of the conidiophores
and comparatively small, aseptate conidia. Although species
are generally not regarded as important plant pathogens, correct identification is essential for disease control and biosecurity implications.
Classification—Ascomycota, Sordariomycetes, Hypocreomycetidae, Hypocreales, Nectriaceae
Type species—Cylindrocladiella parva (P.J. Anderson)
Boesew.
Distribution—as a soil-borne fungus, the species in Cylindrocladiella have a cosmopolitan distribution in various
geographically and climatically distinct regions around the
world (Farr and Rossman 2020).
Disease symptoms—black-foot disease, damping-off, leaf
spot, root rot and shoot die-back
Many species belonging to Cylindrocladiella are opportunistic plant pathogens but they are not considered as
primary pathogens. They can be isolated associated with
disease symptoms such as leaf spot, damping off and shoot
die-back (Scattolin and Montecchio 2007; Pham 2018).
Chocolate brown lesions around the shoots spread primarily to be followed by wilting of the shoot tip, reddish
13
106
discolouration, dropping of leaves, and finally plant death
(Brielmaier-Liebetanz et al. 2013). Characteristic symptoms
of the black-foot disease include a reduction in root biomass and root hairs with sunken and necrotic root lesions
(Agustí-Brisach and Armengol 2013). Symptoms of Cylindrocladiella root rot are black lesions on the tap and lateral
roots, wilting and foliar necrosis, and the outer bark of the
seedlings will crack and become loose (Sinclair and Lyon
2005).
Hosts—Species are soil-borne, weak pathogens of forestry,
agricultural and horticultural crops. There are 270 records
of Cylindrocladiella associated with different plant species
(Farr and Rossman 2020). Among them, different Vitis species and Eucalyptus species are common hosts associated
with different species of Cylindrocladiella.
Morphological based identification and diversity
Cylindrocladiella can be distinguished from related species by penicillate and/or subverticillate symmetrically
branched conidiophores which produce small, cylindrical,
1-septate conidia and aseptate stipe extensions (Lombard
et al. 2012). The generic status of Cylindrocladiella was
earlier strongly contested (Sharma and Mohanan 1991),
however, based on morphological evaluation and comparisons by Crous and Wingfield (1993) and Crous et al. (2017)
confirmed its generic status. Victor et al. (1998) and Schoch
et al. (2000) provided molecular data to support generic status. Lombard et al. (2012) in his revision of Cylindrocladiella mentioned that only two species have been recognized
with their respective Nectricladiella sexual morph. Rossman
et al. (2013) proposed that the generic name Cylindrocladiella be used rather than Nectricladiella. Lombard et al.
(2015) showed that Cylindrocladiella formed a monophyletic group in Nectriaceae (Wijayawardene et al. 2020).
Molecular based identification and diversity
Using RFLPs and AT-DNA data, Victor et al. (1998)
recognised seven species in the genus. Schoch et al. (2000)
added another species based on ITS and partial tub2. Van
Coller et al. (2005) introduced the use of his3 sequence data
for this group. A combined multilocus phylogeny of his,
tef1, tub2 and ITS was used by Lombard et al. (2012) which
resulted in 18 new Cylindrocladiella species and several
unresolved species complexes. Lombard et al. (2017) introduced six new species based on a combined ITS, tef1 and
tub2 dataset. Pham (2018) introduced five new species based
on his, tef1, tub2 and ITS sequence data and Marin-Felix
et al. (2019) introduced two new species based on ITS, tef1
and tub2 sequence data. Here we reconstruct the phylogenetic analyses of these species based on ITS, tef1 and tub2
sequence data (Fig. 8).
13
Fungal Diversity (2020) 103:87–218
Recommended genetic markers (genus level)—ITS, LSU
Recommended genetic markers (species level)—his, tef1,
tub2
Accepted number of species—There are 47 species epithets
in Index Fungorum (2020). However, only 46 species have
DNA sequence data (Table 6).
References—Crous and Wingfield (1993), Lombard et al.
(2012) (morphology); Victor et al. (1998), Schoch et al.
(2000), Lombard et al. (2015) (morphology, phylogeny).
81. Dothidotthia Höhn., Berichte der Deutschen Botanischen Gesellschaft 36: 312 (1918)
Background
Dothidotthia was assigned to Botryosphaeriaceae, because
of its coelomycetous asexual morph, and characteristic
peridium, pseudoparaphyses and asci (Barr 1989). Ramaley (2005) reported that Thyrostroma is the asexual morph
of Dothidotthia based on the production of hyphomycetes
in culture. Phillips et al. (2008), introduced a new family
Dothidotthiaceae to accommodate Dothidotthia and considered Thyrostroma as the asexual morph of Dothidotthia.
However, the links between the sexual and asexual morphs
are not supported by molecular evidence. Recent molecular
and morphology studies (Marin-Felix et al. 2017; Crous et al.
2019; Senwanna et al. 2019), based on a taxon sampling of
current species indicates that Dothidotthia does not cluster
near Thyrostroma. Thus, Dothidotthia is a distinct genus.
Classification—Ascomycota, Pezizomycotina, Dothideomycetes, Pleosporomycetidae, Pleosporales, Dothidotthiaceae
Type species—Dothidotthia symphoricarpi (Rehm) Höhn.
Distribution—in both temperate and tropical countries
(Italy, Russia, Thailand, Ukraine and the USA)
Disease symptoms—species cause canker, dieback and leaf
spot diseases on twig, branch, bark and leaf
Hosts—Pathogens of Acer negundo, Diapensia lapponica,
Fendlera rupicola, Euonymus alatus, Robinia pseudoacacia,
Verbena asparagoides (Barr 1989; Farr and Rossman 2020;
Index Fungorum 2020).
Morphological based identification and diversity
In previous studies, the asexual morphs of Dothidotthia
have been reported as Thyrostroma (Ramaley 2005), however, phylogenetic analyses indicated that Dothidotthia can be
separated from Thyrostroma (Marin-Felix et al. 2017; Crous
et al. 2016; Senwanna et al. 2019). Dothidotthia is characterized by fusiform to obclavate or obpyriform, 0–3-transversely septate conidia and a sexual morph with clavate,
short pedicellate asci, ellipsoid, 1-septate ascospores (Fig. 9).
The sexual morphs of Dothidotthia and Thyrostroma have
similar morphological characteristics in shape and overlapping
Fungal Diversity (2020) 103:87–218
107
Table 4 DNA barcodes available for Cercospora
Species
Isolate no
ITS
tef1
act
cal
his
tub2
rpb2
gapdh
Cercospora achyranthis
CBS 132613
JX143523
JX143277
JX143031
JX142785
JX142539
–
–
–
CPC 10091
JX143524
JX143278
JX143032
JX142786
JX142540
–
–
–
CBS 117292*
AY647237
AY966897
AY966898
AY966899
AY966900
–
–
–
C. agavicola#
C. alchemillicola#
CPC 5259*
JX143525
JX143279
JX143033
JX142787
JX142541
–
–
–
C. althaeina
CBS 248.67*
JX143530
JX143284
JX143038
JX142792
JX142546
MH496340
–
MH496170
C. apii#
CBS 116455*
AY840519
AY840486
AY840450
AY840417
AY840384
MH496343
–
MH496173
C. apiicola#
CBS 116457*
AY840536
AY840503
AY840467
AY840434
AY840401
–
–
–
C. arecacearum
P 521
KC677879
-
-
-
-
-
-
-
C. ariminensis
CBS 137.56
KF251297
KF253245
KF253606
KF253960
-
KF252779
KF252303
-
C. armoraciae#
CBS 250.67*
JX143545
JX143299
JX143053
JX142807
JX142561
MH496351
–
MH496181
C. artemisiae
LIPIMC 0769
KC776169
–
–
–
–
–
–
–
C. asparagi#
ICMP 21630
KY549097
KY549101
KY549091
KY549093
–
–
–
–
C. aurantia
LSVM12 65
MG956773
–
–
–
–
–
–
–
C. balsaminiana
P608
KC677880
–
–
–
–
–
–
–
C. beticola#
CBS 116456*
AY840527
AY840494
AY840458
AY840425
AY840392
MH496355
KT216555
MH496185
C. bidentis
COAD 1018
JX117826
–
–
–
–
–
–
–
C. bizzozeriana#
CBS 258.67*
JX143546
JX143300
JX143054
JX142808
JX142562
MH496368
–
MH496198
C. brachiata
COAD 2593
–
MK118086
MK118087
–
–
–
–
–
C. brassicicola
Cer 68-18
MN209932
–
–
–
–
–
–
–
C. broussonetiae
P610
KC677882
–
–
–
–
–
–
–
C. cf. brunkii
CBS 132657
JX143559
JX143313
JX143067
JX142821
JX142575
–
–
–
C. campi-silii
CBS 132625
JX143561
JX143315
JX143069
JX142823
JX142577
–
–
–
C. canescens#
CPC 15871
JX143567
JX143321
JX143075
JX142829
JX142583
–
–
–
CBS 111133
AY260065
DQ835084
DQ835103
DQ835130
DQ835157
–
–
–
C. capsici#
CBS 132622
JX143568
JX143323
JX143077
JX142831
JX142585
–
–
–
C. capsicigena
P289
KC677884
–
–
–
–
–
–
–
C. caricis
CG672
AF284390
–
–
–
–
–
–
–
C. carotae
CD1-1
KF941306
–
–
–
KF941303
–
–
–
C. celosiae
CBS 132600
JX143570
JX143326
JX143080
JX142834
–
–
–
–
C. chenopodii#
CBS 132594*
JX143572
JX143328
JX143082
JX142836
JX142590
–
–
–
CCTU 1060
KJ886438
KJ886277
KJ885955
KJ885794
KJ886116
MH496371
MH511862
MH496201
C. chinensis
CBS 132612
JX143578
JX143334
JX143088
JX142842
JX142596
–
–
–
C. christellae
CCR22 isolate
A
FJ460222
–
–
–
–
–
–
–
C. chrysanthemi
LIPIMC 0759
KC776154
–
–
–
–
–
–
–
C. chrysanthemoides
CPC 20529
KC005779
KC005813
KC005764
KC005767
–
–
–
–
C. citrullina#
CBS 119395
EU514222
JX143335
JX143089
JX142843
–
–
–
–
MUCC 576
JX143579
JX143337
JX143091
JX142845
–
–
–
–
C. cocciniae
IPBCC
13.1008
KC776158
–
–
–
–
–
–
–
C. codiaei
LIPIMC 0779
KC776170
–
–
–
–
–
–
–
C. coniogrammes
CBS 132634*
JX143583
JX143341
JX143095
JX142849
JX142603
–
––
–
C. convolvulicola
CCTU 1083*
KJ886441
KJ886280
KJ885958
KJ885797
KJ886119
MH496374
MH511865
MH496204
C. conyzae-canadensis
CCTU 1119*
KJ886445
KJ886284
KJ885962
KJ885801
KJ886123
MH496377
MH511868
MH496207
C. corchori
MUCC 585*
JX143584
JX143342
JX143096
JX142850
JX142604
–
–
–
C. cf. coreopsidis
CBS 132598
JX143585
JX143343
JX143097
JX142851
JX142605
–
–
–
C. cryptomeriicola
TFM:FPH7833 AB277789
–
–
–
–
–
–
–
C. cylindracea
CCTU 1081*
KJ886449
KJ886288
KJ885966
KJ885805
KJ886127
MH496381
MH511872
MH496211
C. delaireae
CBS 13259*
JX143587
JX143345
JX143099
JX142853
JX142607
–
–
–
C. dianellicola
CBS 143453*
MG386075
–
MG674152
MG674153
–
–
–
–
C. dispori
CBS 13260*
JX143591
JX143349
JX143103
JX142857
JX142611
–
–
–
C. cf. erysimi
CBS 115059
JX143592
JX143350
JX143350
JX142858
JX142612
–
–
–
C. euphorbiaesieboldianae
CBS 113306*
JX143593
JX143351
JX143105
JX142859
JX142613
–
–
–
C. fagopyri
CBS 132623*
JX143594
JX143352
JX143106
JX142860
JX142614
–
–
–
13
108
Fungal Diversity (2020) 103:87–218
Table 4 (continued)
Species
Isolate no
ITS
tef1
act
cal
his
tub2
rpb2
gapdh
C. cf. flagellaris#
CCTU 1159
KJ886493
KJ886332
KJ886010
KJ885849
KJ886171
MH496388
MH511879
MH496218
CBS 132653
JX143603
JX143361
JX143115
JX142869
JX142623
MH496390
MH511881
MH496220
CCTU 1204
KJ886505
KJ886344
KJ886022
KJ885861
KJ886183
MH496399
MH511890
MH496229
CBS 132667
JX143604
JX143362
JX143116
JX142870
JX142624
MH496401
MH511892
MH496231
CCTU 1172
KJ886501
KJ886340
KJ886018
KJ885857
KJ886179
MH496409
MH511900
MH496239
MH496240
CCTU 1154
KJ886489
KJ886328
KJ886006
KJ885845
KJ886167
MH496410
MH511901
C. gamsiana
CCTU 1074*
KJ886426
KJ886265
KJ885943
KJ885782
KJ886104
MH496446
MH511937
MH496276
C. cf. gossypii
CCTU 1070
KJ886467
KJ886306
KJ885984
KJ885823
KJ886145
MH496452
MH511943
MH496282
C. helianthicola#
MUCC 716
JX143615
JX143374
JX143128
JX142882
JX142636
–
–
–
C. ipomoeae#
CBS 132639
JX143616
JX143375
JX143129
JX142883
JX142637
–
–
–
C. iranica
CCTU 1137*
KJ886513
KJ886352
KJ886030
KJ885869
KJ886191
MH496455
MH511946
MH496285
C. kikuchii
CBS 128.27*
DQ835070
DQ835088
DQ835107
DQ835134
DQ835161
–
–
–
C. lactucae-sativae
CBS 132604
JX143621
JX143380
JX143134
JX142888
JX142642
–
–
–
C. malayensis
KUS-F27687
KR400012
KY082663
KY082664
KY082665
KY082666
–
–
–
C. cf. malloti
MUCC 575
JX143625
JX143384
JX143138
JX142892
JX142646
–
–
–
C. mercurialis
CBS 550.71*
JX143628
JX143628
JX143141
JX142895
JX142649
–
–
–
C. cf. modiolae
CPC 5115
JX143630
JX143389
JX143143
JXJX142897
JX142651
–
–
–
C. cf. nicotianae
CBS 131.32
DQ835073
DQ835099
DQ835119
DQ835146
DQ835173
–
–
–
CBS 132632
JX143631
JX143390
JX143144
JX142898
JX142652
–
–
–
C. olivascens
CBS 253.67*
JX143632
JX143391
JX143145
JX142899
JX142653
–
–
–
C. cf.physalidicola
SN150520
–
KT275242
KT223391
KT275241
KT275240
–
–
–
C. cf. physalidis#
CBS 765.79
JX143633
JX143392
JX143146
JX142900
–
–
–
–
C. pileicola
CBS 132607*
JX143634
JX143393
JX143147
JX142901
JX142655
–
–
–
C. plantaginis
CBS 252.67*
DQ233318
DQ233342
DQ233368
DQ233394
DQ233420
MH496461
–
MH496291
C. polygonacea
CBS 132614
JX143637
JX143396
JX143150
JX142904
JX142658
–
–
–
C. pseudochenopodii
CBS 136022*
KJ886516
KJ886355
KJ886033
KJ885872
KJ886194
MH496464
MH511954
MH496294
C. punctiformis
CBS 132626
JX143638
JX143397
JX143151
JX142905
JX142659
–
–
–
C. cf. resedae
CBS 118793
JX143639
JX143398
JX143152
JX142906
JX142660
–
–
–
C. cf. richardiicola#
CBS 132627
JX143640
JX143399
JX143153
JX142907
JX142661
MH496465
MH511955
MH496295
C. ricinella#
CBS 132605
JX143646
JX143405
JX143159
JX142913
JX142667
–
–
–
C. rodmanii
CBS 113123
DQ835076
AF146136
DQ835122
DQ835149
DQ835176
–
–
–
C. rumicis
CCTU 1123
KJ886521
KJ886360
KJ886038
KJ885877
KJ886199
MH496466
MH511956
MH496296
C. rumicis
CPC 5439
JX143648
JX143407
JX143161
JX142915
JX142669
–
–
–
C. samambaiae
CPC 24673
KT037514
KT037474
KT037596
KT037463
KT037555
–
–
–
C. senecioniswalkeri
CBS 132636
JX143649
JX143408
JX143162
JX142916
JX142670
–
–
–
C. sesami
Cers52-10
MK027103
–
–
–
–
–
–
–
C. sidicola
P500
KC677888
–
–
–
–
–
–
–
C. cf. sigesbeckiae#
CBS 132675
JX143655
JX143414
JX143168
JX142922
JX142676
–
–
–
C. sojina
CBS 132615
JX143659
JX143419
JX143173
JX142927
JX142681
–
–
–
C. solani#
CCTU 1043
KJ886523
KJ886362
KJ886040
KJ885879
KJ886201
MH496469
MH511959
MH496299
C. sorghicola
CCTU 1173*
KJ886525
KJ886364
KJ886042
KJ885881
KJ886203
MH496471
MH511961
MH496301
Cercospora sp. P
CBS 116365*
AY752141
AY752176
AY752204
AY752235
AY752266
–
–
–
Cercospora sp. P
JZG-2013
JX143714
JX143473
JX143227
JX142981
JX142735
–
–
–
Cercospora sp. G
CCTU 1197
KJ886540
KJ886379
KJ886057
KJ885896
KJ886218
MH496472
MH511962
MH496302
Cercospora sp. G
CCTU 1015
KJ886528
KJ886367
KJ886045
KJ885884
KJ886206
MH496473
MH511963
MH496303
Cercospora sp. G
CCTU 1090
KJ886536
KJ886375
KJ886053
KJ885892
KJ886214
MH496476
MH511965
MH496306
Cercospora sp. G
CBS 115518
JX143681
JX143441
JX143195
JX142949
JX142703
MH496480
–
MH496310
Cercospora sp. T
CCTU 1148
KJ886541
KJ886380
KJ886058
KJ885897
KJ886219
MH496488
MH511976
MH496318
C. tagetea
P609
KC677890
–
–
–
–
–
–
–
C. tetragoniae
HL_Tt-1
MT095118
–
–
–
–
–
–
–
NFCCI3067*
KC351743
KC513746
KC355808
KC513745
KC355807
–
–
–
C. uwebaruniana
CCTU 1200*
KJ886408
KJ886247
KJ885925
KJ885764
KJ886086
MH496489
MH511977
MH496319
C. vignigena
CBS 132611*
JX143734
JX143493
JX143247
JX143001
JX142755
–
–
–
13
Fungal Diversity (2020) 103:87–218
109
Table 4 (continued)
Species
Isolate no
ITS
tef1
act
cal
his
tub2
rpb2
gapdh
C. violae#
CBS 251.67*
JX143737
JX143496
JX143250
JX143004
JX142758
MH496492
–
MH496322
C. zeae-maydis#
CBS 117757*
DQ185074
DQ185086
DQ185098
DQ185110
DQ185122
–
–
–
C. zebrina#
CCTU 1225
KJ886550
KJ886389
KJ886067
KJ885906
KJ886228
MH496495
MH511981
MH496325
CCTU 1239
KJ886551
KJ886390
KJ886068
KJ885907
KJ886229
MH496504
MH511987
MH496334
C. zeina#
CBS 118820*
DQ185081
DQ185093
DQ185105
DQ185117
DQ185129
–
–
–
C. cf. zinniae
CBS 132624
JX143756
JX143518
JX143272
JX143026
–
–
–
–
CCTU 1003
KJ886552
KJ886391
KJ886069
KJ885908
KJ886230
MH496505
MH511988
MH496335
LIPIMC 0771
KC776162
–
–
–
–
–
–
–
C. zinniicola
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher strains are also in bold. Species confirmed with pathogenicity studies are marked with#
Fig. 6 Clinoconidium sp. on
Cinnamomum sp. a host plant
with infected and healthy fruits,
b healthy fruits, c, d infected
fruits at various stages of infection
dimensions of asci and ascospores (Barr 1989; Ramaley 2005;
Phillips et al. 2008; Hyde et al. 2013; Senwanna et al. 2019).
However, Dothidotthia can be differentiated from Thyrostroma
by peridium structure and conidial morphology and molecular
phylogeny (Senwanna et al. 2019). Crous et al. (2019) introduced Neodothidotthia to accommodate N. negundinicola and
Dothidotthia aspera was synonymized under N. negundinis
based on analysis of LSU sequence data. However, Senwanna
et al. (2019) showed that Neodothidotthia negundinicola and N.
negundinis group with D. robiniae and D. symphoricarpi (type
species). Furthermore, the conidial morphology of Neodothidotthia is similar to Dothidotthia symphoricarpi (Pseudotthia
symphoricarpi) and D. robiniae (Phillips et al. 2008; Zhang
et al. 2012; Crous et al. 2019; Senwanna et al. 2019). Therefore,
Neodothidotthia had been treated as a synonym of Dothidotthia.
Molecular based identification and diversity
Dothidotthia species can be separated from Thyrostroma
based on LSU sequence data (Marin-Felix et al. 2017; Crous
et al. 2019). Multigene phylogenetic analyses of a combined
LSU, SSU, ITS and tef1 dataset for Dothidotthia is presented in
this study, which is similar to Senwanna et al. (2019) (Fig. 10).
Recommended genetic markers (genus level)—LSU, SSU
Recommended genetic markers (species level)—ITS, tef1,
rpb2 and tub2
Accepted number of species—There are 14 epithets listed
in Index Fungorum (2020), however only four species have
DNA molecular data (Table 7).
References—Barr (1989), Ramaley (2005) (morphology);
Phillips et al. (2008), Zhang et al. (2012), Hyde et al. (2013),
13
110
Fungal Diversity (2020) 103:87–218
Fig. 7 Phylogram generated from MP analysis based on combined
sequences of LSU and ITS sequences of all the species of Clinoconidium with molecular data. Related sequences were obtained from
GenBank. Five taxa are included in the analyses, which comprise
1100 characters including gaps, of which 910 characters are constant, 182 characters are parsimony-uninformative, eight characters
parsimony-informative. The parsimony analysis of the data matrix
resulted in the maximum of two equally most parsimonious trees with
a length of 202 steps (CI = 0.980, RI 0.500, RC = 0.490, HI = 0.020)
in the first tree Single gene analyses were carried out and compared
with each species, to compare the topology of the tree and clade stability. The tree was rooted with Microbotryum violaceum (AFTOLID1819). Maximum parsimony bootstrap support value ≥ 50% and
BYPP ≥ 0.9 are shown respectively near the nodes
Table 5 DNA barcodes available for Clinoconidium
obtain nutrients without killing host cells and without which
they are unable to survive. As they are obligate plant pathogens,
researchers have not had the advantage of routinely cultivating
these taxa on artificial media. However, many powdery mildews have been grown on detached leaves of their hosts (Hirose
et al. 2005). Powdery mildews seldom kill their host, but are
responsible for water and nutrient loss and impaired growth and
development. They can increase respiration and transpiration
and interfere with photosynthesis and reduce yields.
Changes in host range directly cause the niche separation of powdery mildews and thus may become a trigger
of speciation in their evolution. It is possible that studying the evolutionary history of powdery mildews will not
only reveal facts on fungal evolution but may also lead us
to consider the evolutionary history of angiosperm plants
(Takamatsu 2004; Matsuda and Takamatsu 2003; Hirata
et al. 2000; Mori et al. 2000).
The first systematic trial to identify the conidial states
of powdery mildews at the species level was made by Ferraris (1910), who grouped species of Oidium according to
the size and shape of their conidia and provided a key to
its species. Foex (1913), Jaczewski (1927), and Brundza
(1934) contributed to the classification of the conidiophore
types. Jaczewski (1927) introduced the terms ‘Euoidium
and Pseudoidium’ for Oidium states with catenate and
solitary conidia, respectively. Yarwood (1957) provided a
survey on the Erysiphaceae, including the asexual morphs.
Species name
Strain Name
ITS
LSU
Clinoconidium bullatum
C. cinnamomi
C. onumae
C. sawadae
TUK-MA-01
–
AB178259
R. Kirschner 4213 KX196602 KX196604
TUK-MA-02
–
AB178260
R. Kirschner 4219 KX196600 KX196603
Marin-Felix et al. (2017), Crous et al. (2019), Senwanna
et al. (2019) (morphology and phylogeny)
82. Erysiphaceae Tul. & C. Tul. [as ‘Erysiphei’], Select.
fung. carpol. (Paris) 1: [191] (1861)
Background
Powdery mildews belong to Erysiphales of Ascomycota
(Mori et al. 2000). Powdery mildews are one of the most prevalent and easily recognizable of plant diseases (Glawe 2008).
Mucor erysiphe, published by Linnaeus (1753), was the first
binomial referring to powdery mildew (now known as Phyllactinia guttata) (Braun and Cook 2012). Infections are often
conspicuous owing to the profuse production of conidia that
give them their common name. Powdery mildews are also
models for basic research on host-parasite interactions, developmental morphology, cytology, and molecular biology (Glawe
2008). Erysiphaceae is obligately parasitic and as such, their
life cycle depends completely on living hosts, from which they
13
Fungal Diversity (2020) 103:87–218
111
Fig. 8 Phylogram generated from MP analysis based on combined
sequences of ITS, tef1 and tub2 sequences of all the accepted species of Cylindrocladiella. Related sequences were obtained from
GenBank. Fourty-six taxa are included in the analyses, which comprise 2460 characters including gaps. Single gene analyses were carried out and compared with each species, to compare the topology of
the tree and clade stability. The tree was rooted with Gliocladiopsis
sagariensis (CBS 19955). The best scoring RAxML tree with a final
likelihood value of − 6772.195394 is presented. The matrix had 261
distinct alignment patterns, with 0.96% of undetermined characters
or gaps. Estimated base frequencies were as follows: A = 0.230657,
C = 0.279364, G = 0.252128, T = 0.237852; substitution rates AC
= 1.388608, AG = 2.845402, AT = 2.389715, CG = 0.838197, CT
= 7.220493, GT = 1.000000; gamma distribution shape parameter a
= 0.650385. Maximum likelihood and MP bootstrap support value >
50% are shown respectively near the nodes. Ex-type strains are in bold
Boesewinkel (1980) provided the first comprehensive key
based on a combination of more than 12 morphological
characteristics observed on conidia, conidiophores, appressoria, haustoria, fibrosin bodies, and mycelium. Braun
(1987) issued a second comprehensive monograph of the
Erysiphales encompassing all powdery mildew taxa known
at that time. Shin and La (1993) and Shin and Zheng (1998)
introduced some new morphological features of taxonomic
13
112
Table 6 DNA barcodes
available for Cylindrocladiella
Fungal Diversity (2020) 103:87–218
Species
Isolate No
ITS
tef1
tub2
Cylindrocladiella addiensis
C. arbusta#
C. australiensis
C. brevistipitata
C. camelliae
C. clavata
C. cymbiformis
C. elegans
C. ellipsoidea
C. hahajimaensis
C. hawaiiensis
C. horticola
C. humicola
C. infestans
C. kurandica
C. lageniformis
C. lanceolata
C. lateralis
C. longiphialidica
C. longistipitata
C. malesiana#
C. microcylindrica
C. natalensis
C. nederlandica
C. novazelandica
C. nauliensis
C. obpyriformis#
C. parva
C. parvispora#
C. peruvianum
C. postalofficium
C. pseudocamelliae
C. pseudohawaiiensis
C. pseudoinfestans
C. pseudoparva
C. queenslandica
C. reginae
C. solicola#
C. stellenboschensis
C. terrestris
C. thailandica
C. variabilis
C. viticola#
C. vitis#
C. xishuangbannaensis
CBS 143794*
CMW 47295*
CBS 129567*
CBS 142786*
IMI 346845
CBS 129564*
CBS 129553*
CBS 338.92*
CBS 129573*
MAFF 238172*
CBS 129569*
CBS 142784*
CBS 142779*
CBS 111795*
CBS 129577*
CBS 340.92*
CBS 129566*
CBS 142788*
CBS 129557*
CBS 116075*
CMW 48278*
CBS 111794*
CBS 114943*
CBS 152.91*
CBS 486.77*
CBS 143792*
CMW 47194*
CBS 114524
CMW 47197*
IMUR 1843*
CPC 37513*
CBS 129555*
CBS 210.94*
CBS 114531*
CBS129560*
CBS 129574*
CBS 142782*
CMW47198*
CBS 110668*
CBS 142789*
CBS 129571*
CBS 129561*
CBS 112897*
CBS 142517*
KUMCC 16-0146*
MH111383
MH017015
JN100624
–
AF220952
JN099095
JN099103
AY793444
JN099094
JN687561
JN100621
MF444911
MF444906
AF220955
JN100646
AF220959
JN099099
MF444914
JN100585
AF220958
MH017019
AY793452
JN100588
JN100603
AF220963
MH111387
MH017022
AF220964
MH017025
AF220966
MN562148
JN100577
JN099128
AF220957
JN100620
JN099098
MF444909
MH017021
JN100615
MF444915
JN100582
JN100643
AY793468
KY979751
MH388337
MH111393
MH016977
JN099060
MF444940
JN099087
JN098974
JN098988
JN099039
JN098973
JN687562
JN099057
MF444938
MF444933
JN099037
JN099083
JN099003
JN098978
MF444942
JN098966
JN098993
MH016981
JN099041
JN099016
JN099033
JN099050
MH111397
–
JN099009
MH016987
JN098968
–
JN098958
JN099012
JN099004
JN099056
JN098977
MF444936
MH016983
JN099051
MF444943
JN098963
JN099080
JN099064
KY979891
MH388372
MH111388
MH016958
JN098747
MF444926
AY793471
JN098752
JN098753
AY793474
JN098757
–
JN098761
MF444924
MF444919
AF320190
JN098765
AY793481
JN098789
MF444928
JN098790
AY793506
MH016962
AY793483
JN098794
JN098800
AY793485
MH111392
MH016966
AY793486
MH016968
AY793500
MN556845
JN098814
JN098819
AY793508
JN098824
JN098826
MF444922
MH016964
JN098829
MF444929
JN098834
JN098719
AY793504
KY979918
–
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
relevance. A progressive report was provided by the work
of Cook et al. (1997), who examined the surface of conidia
by scanning electron microscopy and separated Oidium
13
into eight subgenera. Braun (1999) discussed the classification of Erysiphaceae as proposed by Cook et al. (1997) and
introduced some corrections and alterations. Fundamental
Fungal Diversity (2020) 103:87–218
113
Fig. 9 Dothidotthia robiniae (MFLU 16-1704). a, b Sporodochia on the host surface. c Vertical section of sporodochium. d Conidiogenesis. e, g
Conidia attached with the conidiogenous cells. f, h Conidia. i Germinated conidium. Scale bars: b = 1000 µm, c = 200 µm, d–i = 30 µm
innovations in the generic taxonomy of the group based on
molecular and SEM examination and a better insight into the
phylogeny are results of comprehensive investigations over
the last decade (Takamatsu et al. 1998, 1999, 2000, 2005a,
b, 2008; Matsuda and Takamatsu 2003; Hirose et al. 2005;
Liberato et al. 2006; Braun and Cook 2012).
Classification—Ascomycota, Pezizomycotina, Leotiomycetes, Leotiomycetidae, Erysiphales
Type genus—Erysiphe R. Hedw. ex DC.
Distribution—worldwide
Disease symptoms—powdery mildew
The initial signs of infection appear on young leaves in
the form of small, raised blisters, which cause the leaves
to curl and expose the under surfaces. As the disease progresses, round, pinpoint powdery white spots dusting the
upper surfaces of leaves, as well as stems and occasionally
fruiting occurs. As the disease becomes severe, the spots
will become larger, and more interconnected and irregular
in shape. Over time they progress from younger to older
leaves and the undersides of leaves. However, mature leaves
are usually much less severely infected than new or young
leaves. If the white patches (which have a granular, powdery
texture) are wiped away, the growths will return in a matter
of days. Severely infected leaves will turn yellow, dry out
and drop from the plant. Buds and growing tips of shoots
can also become infected, eventually becoming distorted and
stunted (Bushnell and Allen 1962; Davis et al. 2001; Romero
et al. 2003; Oberti et al. 2014; Saharan et al. 2019).
Hosts- The host range of this fungal group is strictly
confined to angiosperms and powdery mildews have never
been reported to infect ferns or gymnosperms (Amano 1986;
Hirata et al. 2000; Takamatsu et al. 2010). They affect a
wide range of angiosperms such as cereals and grasses, vegetables, ornamentals, weeds, shrubs, fruit trees, and broadleaved shade and forest trees. Powdery mildews are considered as host-specific.
Pathogen biology, disease cycle and epidemiology
Powdery mildews tend to grow superficially, or epiphytically, on plant surfaces. During the growing season, hyphae
are produced on both the upper and lower leaf surfaces,
although some species are restricted to one leaf surface.
Infections can also occur on stems, flowers or fruit. Specialized absorption cells, termed haustoria, extend into the
plant epidermal cells to obtain nutrition. While most powdery mildews produce epiphytic mycelium, a few genera
produce hyphae that are within the leaf tissue; this is known
as endophytic growth. Conidia are produced on plant surfaces during the growing season. They develop either singly
or in chains on conidiophores. Conidiophores arise from the
epiphytic hyphae, or in the case of endophytic hyphae, the
conidiophores emerge through leaf stomata. At the end of
the growing season, powdery mildews produce ascospores,
13
114
Fungal Diversity (2020) 103:87–218
Fig. 10 Phylogenetic tree generated by ML analysis of LSU, SSU, ITS
and tef1 sequence data of Dothidotthia species. Related sequences were
obtained from GenBank. The tree was rooted with Thyrostroma compactum (CBS 335.37) and T. lycii (MFLUCC 16-1170). Tree topology
of the ML analysis was similar to the Bayesian analysis. The best scoring RAxML tree with a final likelihood value of − 5116.933762 is presented. The matrix had 115 distinct alignment patterns, with 25.41% of
Table 7 DNA barcodes
available for Dothidotthia
Species
undetermined characters or gaps. Estimated base frequencies were as
follows: A = 0.245094, C = 0.237101, G = 0.269739, T = 0.248067;
substitution rates AC = 3.925871, AG = 7.445430, AT = 2.745308,
CG = 2.728664, CT = 20.049514, GT = 1.000000; gamma distribution
shape parameter α = 0.790240. Maximum likelihood bootstrap support
values greater than 60% and BYPP probabilities ≥ 0.95 are indicated
above the nodes. Ex-type (ex-epitype) and voucher strains are in bold
Isolate no
Dothidotthia negundinicola CBS 145039*
MFLUCC 16-1157
MFLUCC 16-1183
D. negundinis
CPC 12930
CPC 12932
CPC 12933
D. robiniae
MFLUCC 16-1175*
MFLUCC 16-1177
MFLUCC 16-1185
MFLUCC 18-0692
CPC 12929*
D. symphoricarpi
CBS 119687
LSU
SSU
ITS
tef1
MK442537
MK751815
MK751816
EU673274
EU673275
EU673276
MK751817
MK751818
MK751819
MK751821
EU673273
MH874618
_
MK751760
MK751761
EU673226
EU673227
EU673228
MK751762
MK751763
MK751764
MK751766
EU673224
_
MK442597
MK751725
MK751726
MK442599
MK442600
MK442601
MK751727
MK751728
MK751729
MK751731
_
MH863064
_
MK908015
MK908016
_
_
_
MK908017
MK908018
MK908019
MK908021
_
_
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold
in a sac-like ascus enclosed in a fruiting body called a chasmothecium. The chasmothecium is generally spherical with
no natural opening; asci with ascospores are released when
a crack develops in the wall of the fruiting body. A variety of
appendages may occur on the surface of the chasmothecia.
13
These appendages are thought to act as the hooks of a velcro
fastener, attaching the fruiting bodies to the host, particularly
to the bark of woody plants, where they overwinter. They
can survive winter conditions as dormant mycelia within the
buds and other plant tissue of the host. These infected parts
Fungal Diversity (2020) 103:87–218
of the host can be the source of primary inoculum that can
initiate further infection when conditions are right (Misra
2001; Amsalem et al. 2006; Heffer et al. 2006; Te Beest et al.
2008; Saharan et al. 2019; Fig. 11).
Morphological based identification and diversity
Members of Erysiphaceae cause powdery mildew disease
on about 10,000 angiosperm species (Takamatsu et al. 2010).
The Erysiphaceae are divided into five tribes and two basal
genera (Cook et al. 1997). Both tree-parasitic and herb-parasitic species are included in three of the five tribes: Cystotheceae, Erysipheae and Phyllactinieae. Tree-parasitic species
usually take basal positions in these tribes and herb-parasitic
species have derived positions. The tribe, Golovinomycetea
is a group derived from a single ancestor (Mori et al. 2000).
The monophyly of the tribe is also supported by the common
characteristics, i.e., ectophytic parasitism, polyascal ascomata, and Euoidium asexual morphs, with the latter producing conidia in chains without distinct fibrosin bodies. Of these
five lineages, four consists of taxa infectious to dicotyledons.
Blumeria graminis, which is infectious to monocotyledon
plants, formed an independent lineage. Therefore, Blumeria
graminis was accommodated in a monotypic tribe Blumerieae
in the new system (Inuma et al. 2007).
The powdery mildew belonging to the tribe Cystotheceae
have both herbaceous and woody plants as hosts and consist
of three genera, Cystotheca, Podosphaera and Sawadaea, of
which Cystotheca and Sawadaea are restricted to a narrow
range of host families (Meeboon et al. 2013). Podosphaera
consists of two sections, Podosphaera and Sphaerotheca. Section Podosphaera parasitizes woody plants (Takamatsu et al.
2000). The tribe Golovinomyceteae consists of three genera,
Golovinomyces, Neoerysiphe, and Arthrocladiella. Arthrocladiella is a monotypic genus consisting of a single species A.
mougeottii and has only the host genus Lycium. Neoerysiphe
is also a small genus composed of four species and has about
300 herbaceous host species ranging across five plant families
including Lamiaceae. Golovinomyces is a large genus comprising 27 species (Braun 1987), and it is widely distributed
in the world. The tribe Phyllactinieae comprises the genera
Phyllactinia, Leveillula, Pleochaeta and Queirozia which typically have hemi-endophytic (partly external and partly internal mycelia in common (Braun 1987; Liberato 2007; Liberato
et al. 2006; Khodaparast et al. 2001; Ramos et al. 2013).
The tribe Erysipheae forms a separate, monophyletic clade,
which is characterized by asexual morphs belonging to Oidium subgen. Pseudoidium Jacz (Takamatsu et al. 1999; Mori
et al. 2000). This clade comprises Erysiphe and its sections
Erysiphe, Microsphaera and Uncinula. Uncinula forestalis
differs from the species of Erysiphe sect. Uncinula in having terminal, fasciculate, septate, ascoma appendages and
Euoidium-like asexual morph (conidia catenate) and therefore it was placed in Caespitotheca (Takamatsu et al. 2005b).
115
Because of the lack of asexual morphs in Uncinula septata
and U. curvispora and multiseptate chasmothecial appendages
arising from the upper half the fruiting body, the two species
were assigned to Parauncinula (Braun and Takamatsu 2000;
Takamatsu et al. 2005a). A unique taxon, Oidium phyllanthi,
on Phyllanthus acidus, P. amarus and P. reticulatus produces
a germination type designated as Microidium-type and was
placed in a new genus Microidium (To-anun et al. 2005). With
these new classifications, Erysiphales contains 17 accepted
genera, 16 based on the holomorph and one on the asexual
morph (Braun and Cook 2012). With the descriptions of several new species, the number of recognized powdery mildew
species has increased from 515 (including 435 sexual morphs/
holomorphs) in Braun (1987), to about 820 species (including
about 685 sexual morphs/holomorphs) (Braun and Takamatsu
2000; Braun et al. 2002; Takamatsu et al. 2005a, b; Liberato
et al. 2006; Braun and Cook 2012).
Molecular based identification and diversity
Molecular data have proven useful in reassessing species
and clarifying the taxonomic significance of morphology and
host data. Only a few of the described species have been reassessed using molecular data (Braun and Cook 2012). Reports
began appearing in the 1990s, that used ITS and 18S rDNA
sequences to infer phylogenetic relationships of Erysiphales
and other major ascomycete groups (Saenz and Taylor 1999;
Saenz et al. 1994). Analyses of 18S rDNA, ITS1–5.8S-ITS2,
and 28S rDNA sequences led to the opinion that Erysiphales
can be placed in Leotiomycetes along with Cyttariales, Helotiales, and Rhytismatales (Wang et al. 2006). Phylogenetic
analyses demonstrated that Erysiphaceae formed a distinct
monophyletic group (Hirata et al. 2000). Thus, Erysiphaceae is derived from a single ancestral taxon that may have
acquired parasitism just once (Mori et al. 2000a; Takamatsu
2004; Wang et al. 2006). Shirouzu et al. (2020) using nrDNA
and mcm7 sequence data showed that Phyllactinieae is not
monophyletic. However, there is a need to re-assess the tribes
in this family to establish them as subfamilies or genera. In
this paper, we present a phylogenetic tree with combined ITS
and LSU sequences obtained from available type material and
voucher specimens (Table 8, Fig. 12). This can be used as a
backbone in the identification of powdery mildew species.
Recommended genetic markers (genus level)—ITS, LSU
and SSU
Recommended genetic markers (species level)—tub2, chs,
tef1
The ITS region of the precursor molecules of rRNA was
revealed to form a secondary structure including several stemloop structures, and some conserved sequences are found in
the stem regions (Takamatsu et al. 1998). This makes it possible to design PCR primers that work for a wide range of
the powdery mildews. Takamatsu and Kano (2001) designed
13
116
Fungal Diversity (2020) 103:87–218
Fig. 11 The life cycle of a powdery mildew fungus on roses.
Redrawn from Agrios (2005)
and Mulbrhan et al. (2016)
four new PCR primers that are useful to determine the nucleotide sequences of the rDNA of the powdery mildews. These
primers provide stability to work on a wide range of powdery
mildews and specificity to eliminate contaminating DNA by
PCR. Primer sets PM3/P3, ITS1/PM4, PM5/P3, and ITS1/
PM6 were tested with universal primer set ITS1/ITS4 (White
et al. 1990) covering all major clades of Erysiphales. Meeboon and Takamatsu (2013a) used LSU, ITS and IGS (Inter
generic spacer) sequences to identify two different genetic
groups of Erysiphe japonica (= Typhulochaeta japonica),
powdery mildew on Quercus species based on the differences
in host range. Cho et al. (2014) used ITS and 28S rDNA for
the introduction of the powdery mildew species Erysiphe
magnoliicola in Erysiphe sect. Microsphaera. Wang et al.
(2014) also used ITS differences for phylogenetic analysis of
powdery mildew disease on mulberry in Yunnan Province.
Meeboon and Takamatsu (2013b) also used the 28S rDNA
sequences and a combined alignment of the 28S, ITS, and
IGS (Intergeneric spacer) rDNA sequences to construct a
phylogeny of Erysiphe sect. Uncinula on Carpinus species
and showed the cryptic species Erysiphe paracarpinicola. de
Oliveira et al. (2015) used ITS sequences of Erysiphe platani
on Platanus × acerifolia in Brazil as new records of taxa.
Liyanage et al. (2017) used ITS, SSU and LSU sequences
to identify E. quercicola infected rubber trees. Phylogenetic
analyses of B. graminis based on the DNA sequences of four
DNA regions, i.e. ITS, 28S rDNA, chitin synthase 1, and
ß-tubulin were conducted by Inuma et al. (2007) to revealed
distinct groups in the B. graminis isolates from a single host
genus belonged to a single group.
13
83. Fomitopsis P. Karst., Meddn Soc. Fauna Flora fenn. 6:
9 (1881)
Background
Fomitopsis was established by Karsten (1881) based on
four species, with F. pinicola as the generic type (Murrill
1903; Donk 1960). The genus has a cosmopolitan distribution and comprises species causing brown rot on both
living and dead trees (Han et al. 2016). Fomitopsis species also contribute to the decomposition of coarse woody
debris in forest communities (Gilbertson 1980; Haight et al.
2019). There are certain instances of their pathogenic role
in orchards of cultivated species where they cause heart
rot on Citrus (Roccotelli et al. 2014) and Prunus species
(Adaskaveg 1993). A Fomitopsis sp. was also recorded in
oil palm (Elaeis guineensis) as an endophyte (Rungjindamai
et al. 2008; Pinruan et al. 2010).
Classification—Basidiomycota, Agaricomycetes, Incertae
sedis, Polyporales, Fomitopsidaceae
Type species—Fomitopsis pinicola (Sw.) P. Karst.
Distribution—Worldwide
Disease symptoms—Fomitopsis causes brown cubical rot
on both living and dead trees (Mounce 1929). The basidiospores can be dispersed by wind, or by vectors such as
bark beetles (Castello et al. 1976; Pettey and Shaw 1986;
Lim et al. 2005; Persson et al. 2011; Jacobsen et al. 2017;
Vogel et al. 2017). Upon infecting standing trees, stumps, or
logs through wounds, or through the tunnels of penetrating
vectors, the fungus establishes itself in the xylem (Mounce
1929). The growth rate of Fomitopsis species in the substrata
Fungal Diversity (2020) 103:87–218
can differ depending on their ecological requirements (Markovic et al. 2011; Haight et al. 2019). When the decay starts,
the wood turns yellowish-brown, which later splits into cubical fragments. The colour is generally lighter in case of F.
pinicola than other agents of brown rot decay (Markovic
et al. 2011). White mycelial felts can also develop in shrinkage cracks of the decayed wood (Ryvarden and Gilbertson
1993). After establishment, the perennial basidiome appears
relatively rapidly (Mounce 1929, Fig. 13). The infection
results in the breakage of treetops, or further infection of
the base of the trees and weakening of larger roots, which
may lead to eventual windthrow of standing trees.
Hosts—The type species, F. pinicola mostly appears on gymnosperms, such as Abies, Larix, Picea and Pinus, but can also
be found on angiosperms such as Acer, Alnus, Betula, Carpinus, Corylus, Elaeagnus, Fagus, Fraxinus, Malus, Populus,
Prunus, Pyrus, Quercus, Salix, Sorbus, Tilia, Ulmus (Ryvarden
and Gilbertson 1993; Dai 2012). The North American species
in the Fomitopsis pinicola species complex have also been
reported from Pseudotsuga, Sequioa and Tsuga (Haight et al.
2019). Other Fomitopsis species can be found on Ginkgo, Pinus
and various angiosperm genera, such as Betula, Castanopsis,
Cinamomum, Citrus, Delonix, Fagus, Eucalyptus Ligustrum,
Prunus, Quercus and Tilia (Ryvarden and Gilbertson 1993; Dai
2012; Li et al. 2013; Han et al. 2016; Liu et al. 2019).
Morphological based identification and diversity
Based on morphological evidence, over 40 species were
accepted in Fomitopsis (e.g. Ryvarden and Johansen 1980;
Gilbertson and Ryvarden 1986; Ryvarden and Gilbertson
1993; Núñez and Ryvarden 2001; Hattori 2001). However,
phylogenetic studies showed that the morphologically
defined Fomitopsis was polyphyletic and taxa clustered with
other brown-rot genera in the antrodia clade (Ortiz-Santana
et al. 2013; Han et al. 2016). Han et al. (2016) showed that
Pilatoporus and Piptoporus are synonyms of Fomitopsis
sensu stricto, while the segregation of Rhodofomes was
confirmed and five new genera were proposed. Fomitopsis sensu stricto is characterized by annual to perennial,
mostly sessile, occasionally effused-reflexed or substipitate,
soft, corky, tough to woody basidiocarps, a dimitic hyphal
system with clamped generative hyphae and cylindrical
to ellipsoid, hyaline, thin-walled, smooth basidiospores
which are negative in Melzer’s reagent, and cause brown
rot (Fig. 13).
Molecular based identification and diversity
Comprehensive multigene analyses by Han et al. (2016)
accepted ten species in Fomitopsis sensu stricto. Two new
Fomitopsis species were described from Brazil, F. flabellata
and F. roseoalba (Tibpromma et al. 2017). Fomitopsis flabellata was transferred to Rhodofomitopsis and the new combination Fomitopsis bondartsevae was proposed (Soares et al.
117
2017). Mating studies and molecular phylogenetic analyses
resolved four cryptic lineages in the F. pinicola species complex (Haight et al. 2016), that represents three North American
species (F. mounceae, F. ochracea and F. schrenkii), and F.
pinicola sensu stricto, which is restricted to Eurasia (Ryvarden
and Stokland 2008; Haight et al. 2019). Three new species were
proposed by Liu et al. (2019) from Australia (F. eucalypticola),
Puerto Rico (F. caribensis), and China (F. ginkgonis).
The phylogenetic tree of Fomitopsis presented here is based
on analyses of a combined ITS, LSU, tef1 and rpb2 sequence
data (Fig. 14). In our analyses, it appears that the type of F.
bondartsevae is identical to F. iberica and F. hemitephra
sensu stricto (Han et al. 2016), which are grouped close to F.
palustris and other species formerly discussed in Pilatoporus.
Therefore, a thorough revision of the pilatoporus clade is recommended to clarify the status of these species.
Recommended genetic marker (genus level)—LSU
Recommended genetic markers (species level)—ITS, tef1,
rpb2
Accepted number of species—There are 104 epithets listed
in Index Fungorum (2020). However, only 17 species have
DNA sequence data (Table 9).
References—Li et al. (2013) (phylogeny, new species), Han
et al. (2016) (phylogeny), Haight et al. 2019 (phylogeny,
new species), Floudas et al. (2012) (genome, F. pinicola),
Hong et al. (2017) (genome, F. palustris), Liu et al. (2019)
(phylogeny, new species).
84. Ganoderma P. Karst., Revue mycol., Toulouse 3(no. 9):
17 (1881)
Background
Ganoderma was established by Karsten (1881) based
on G. lucidum and characterized by double-walled basidiospores with truncate apices and ornamented endospores,
and a crusty or shiny pileus surface (Moncalvo and Ryvarden
1997). This genus was divided into two subgenera, Ganoderma and Elfvingia by Karsten (1889). Various authors
used different taxonomic characters for the identification of
species (e.g., Murrill 1902, 1903; Atkinson 1908; Coleman
1927; Corner 1947), which resulted in an intricate taxonomy,
with 344 species names in speciesfungorum.org, but an estimated 180 species (He et al. 2019) and Steyaert (1972, 1980)
worked extensively on the genus and introduced many new
species, transferred many to the genus and removed several synonyms. Ryvarden (1985) and Gottlieb and Wright
(1999a,b) studied the macro- and micromorphology. Ganoderma presently comprises sections Amauroderma and Ganoderma, subgenera: Ganoderma and Trachyderma (Index
Fungorum 2020, Wijayawardene et al. 2020).
Relevant characteristics for Ganoderma species delimitation are based on the macro and micromorphological characteristics (see in Fig. 15). The basidiomes are annual or
13
118
Fungal Diversity (2020) 103:87–218
Table 8 Genera in Erysiphaceae
Genera
Strain no
Host
ITS
LSU
Arthrocladiella Arthrocladiella mougeotii
Blumeria
Blumeria graminis
Brasiliomyces Brasiliomyces malvastri
SqGq-1
MUMH1723
NA
JX546296
AB273556
NA
AB022379
AB103065
NA
Caespitotheca forestalis
Cystotheca wrightii
Cystotheca lanestris
Erysiphe
Erysiphe polygoni
Erysiphe heraclei
Erysiphe monascogera
Erysiphe blasti
Erysiphe juglandis
Erysiphe hedwigii
Erysiphe pulchra var.
japonica
Erysiphe symphoricarpi
Erysiphe asiatica
Erysiphe monoperidiata
Erysiphe japonica var.
crispulae
Erysiphe adunca
Erysiphe aphananthes
Erysiphe flexuosa
Erysiphe mori
Erysiphe kenjiana
Erysiphe prunastri var.
prunastri
Erysiphe wadae
Golovinomyces Golovinomyces
cichoracearum
Golovinomyces adenophorae
Golovinomyces cynoglossi
Golovinomyces fischeri
Golovinomyces leuceriae
Golovinomyces Golovinomyces orontii
Golovinomyces sonchicola
Golovinomyces sordidus
Golovinomyces sparsus
Golovinomyces valerianae
Leveilluta
Leveilluta taurica
Leveillula elaeagni
Leveillula lactucae-serriolae
Microidium
Microidium phyllanthi
Neoerysiphe
Neoerysiphe cumminsiana
Neoerysiphe galeopsidis
Neoerysiphe galii
Neoerysiphe geranii
Neoerysiphe joerstadii
Neoerysiphe kerribeeensis
Neoerysiphe nevoi
Parauncinula
Parauncinula septata
MUMH1461
KUS-F27309
NA
UTC206
NA
MUMH4190
MUMH2
MUMH48s
VPRI 22225
MUMH90
MUMH1428
MUMH 4992
MUMH 4987
NA
MUMH40
MUMH 4648
MUMH1429
NA
KW:34760F
MUMH776
MUMH1534
Lycium chinense
Festuca arundinacea
Malvastrum coromandelianum
Schinopsis balansae
Quercus glauca
Quercus agrifolia
Polygonum arenastrum
Daucus carota
Styrax japonica
Lindera umbellata
Microsphaera juglandis
NA
Cornus controversa
Symphoricarpos albus
Castanopsis diversifolia
Castanopsis argyrophylla
Quercus cuspidata
NA
Aphananthe aspera
Aesculus hippocastanum
Morus bombycis
Ulmus minor
Prunus domestica
Fagus crenata
AB193466
KF735066
AB000933
AF011307
AB000942
AB331647
AB015918
AB015928
AF298539
AB000941
AB078970
AB622218
AB622213
AB022416
D84383
AB69396
AB091774
AB000946
AB475118
AB046984
AB091776
AB193467
AB022355
AB022353
NA
AB103371
NA
NA
NA
NA
AB022389
NA
JQ220158
JQ220154
AB022415
AB022374
NA
NA
AB022418
AB475109
AB709961
NA
MUMH623
MUMH144
MUMH3196
MUMH1343
MUMH1406
MUMH683
Mycelis muralis
Adenophora triphylla var.
japonica
Cynoglossum asperrimum
Senecio doronicum
Leuceria thermarum
AB077661
AB077633
AB769454
AB769450
AB246765
NA
AB077632
AB077683
AB769452
NA
MUMH2433
BCRU934
MUMH938
HMNWAFU-CF2011034
Cirsium japonicum
Sonchus arvensis
Plantago sp.
Euphorbia collina
Valeriana officinalis
Triglochin maritime
Elaeagnus angustifolia
Hexinia polydichotoma
AB769413
AB077673
AB769467
AB769461
AB769471
AY912077
AB048350
HQ821500
AB077678
AB077672
AB077657
NA
NA
NA
NA
HQ821501
Phyllanthus acidus
Cacalia delphiniifolia
Chelonopsis moschata
Galium aparine
Geranium sp.
Phagnalon rupestre
Senecio glossanthus
Scolymus hispanicus
Quercus cuspidata var.
horikawae
AB719943
AB329669
AB498949
AB498951
AB498956 AB498976
GU356546
AB498975
AB120758
NA
AB022369
AB103365
AB498952
NA
NA
NA
AB022420
Caespitotheca
Cystotheca
13
Species name
WSP71133
IRAN11138
NA
MUMH(JPN)3361
MUMH 522
MUMH4680
MUMH 4682
MUMH4665 MUMH 4668
DAR 33493
MUMH 4671
MUMH585
AB183533
Fungal Diversity (2020) 103:87–218
119
Table 8 (continued)
Genera
Species name
Strain no
Host
ITS
LSU
Phyllactinia
Phyllactinia guttata
Phyllactinia actinidiae
Phyllactinia alni
Phyllactinia betulae
Phyllactinia- broussonetiaekaempferi
Phyllactinia enkianthi
Phyllactinia eupteleae
Phyllactinia fraxini
Phyllactinia guttata
Phyllactinia juglandis
Phyllactinia magnoliae
Phyllactinia mali
Phyllactinia moricola
MUMH927
MUMH497
MUMH449
MUMH506
MUMH531
MUMH527
MUMH165
MUMH907
MUMH927
TUAMH2072
MUMH531
MUMH619
MUMHn36
AB080565
AB080508
AB080502
AB080507
AB080510
AB080504
AB080498
AB080543
AB080565
AB080531
AB080526
AB080523
AB080518
AB080456
HQ821501
AB080393
AB080398
AB080445
AB080408
AB080402
AB080453
AB080394
AB080422
AB080416
AB080414
AB080373
Pleochaeta
Pleochaeta indica
Pleochaeta shiraiana
Podosphaera myrtillina
Podosphaera leucotricha
Podosphaera spiraeae
Podosphaera cercidiphylli
Podosphaera clandestine
Podosphaera astericola
Podosphaera balsaminae
Podosphaera carpesiicola
Podosphaera elsholtziae
Podosphaera euphorbiaehirtae
Podosphaera fusca
Podosphaera fuliginea
Podosphaera hibiscicola
Podosphaera intermedia
Podosphaera phtheirospermi
Podosphaera pseudofusca
Podosphaera xanthii
Queirozia turbinata
Sawadaea bicornis
Sawadaea nankinensis
Sawadaea polyfida
Sawadaea tulasnei
MUMH3208
MUMH20
NA
HMLAC120001
MUMH 2490
MUMHS67
MUMH 2535
MUMH333
NA
MUMH344
MUMHS131
MUMH319
NA
MUMH809
MUMH605
MUMH331
MUMH774
MUMH346
MUMH74
Corylus sp.
Actinidia arguta
Alnus japonica
Betula platyphylla var.
japonica
Broussonetia kazinoki
Lyonia ovalifolia var.
elliptica
Euptelea polyandra
Syringa vulgaris
Corylus sp.
Juglans mandshurica var.
sachalinensis
Magnolia quinquepeta
Crataegus sp.
Morus cathayana
Celtis australis
NA
Vaccinium myrillus
Photinia serrulata
Spiraea cantoniensis
Cercidiphyllum japonicum
Spiraea japonica
Aster ageratoides subsp.
ovatus
Impatiens balsamina
Carpesium abrotanoides
Ajuga reptans
Acalypha australis
NA
Verbena spicata
Hibiscus mutabilis
Clerodendrum trichotomum
Melampyrum nemorosum
Fatoua villosa
Youngia denticulata
AB243757
D84380
NA
JQ999954
AB525940
AB026140
AB525941
AB040335
FJ625796
AB040350
AB026142
AB040306
AF154324
AB046986
AB040308
AB026145
AB040332
AB040320
AB040351
NA
VIC 26558
MUMH904
MUMH4232
MUMH486
MUMHS112
AB218773
AB193380
AB353762
AB193358
AB193388
NA
AB022403
NA
NA
AB022384
NA
AB103367
AB462779
AB462788
NA
AB462794
AB462770
AB103369
AB462761
NA
AB462777
NA
NA
JX512556
NA
NA
NA
AB103370
NA
AB193393
AB193400
Takamatsuella circinata
NA
NA
NA
Podosphaera
Queirozia
Sawadaea
Takamatsuella
Platycyamus regnellii
Acer pseudoplatanus
Acer buergerianum
Acer amoenum var. matsumurae
Acer mono var. marmoratum
Stachys distans
Type strains are in bold
perennial, dimidiate, sessile or substipitate to stipitate, with
distinctive non-laccate (dull) or weakly to strongly laccate,
glossy, shiny, smooth, spathulate, furrows, which are sulcate on the pileus surface. Some strains have several layers
of thick, dull cuticles or shiny, with thin cuticle or cuticle
of clavate end cells. The context is cream to dark purplish
brown, brown to dark brown, sometimes spongy to firmfibrous. Pores are 4–7 per mm, angular, entire, subcircular
to circular, regular, mostly cream or white when young, light
yellow to brown when mature, which are usually white to
cream when fresh, turning pale yellow on drying, with bruising brown of pore surface. The tube layer is single or stratified, with pale to purplish brown, hard, and becomes woody
when dry. The stipe is central or lateral when present.
The Ganoderma hyphal system is di-trimitic and generative hyphae are thin-walled or occasionally thick-walled,
with clamp connections. Skeletal hyphae are hyaline to
brown, thick-walled, often long, unbranched. Binding
hyphae are almost colourless, thin to thick-walled, branched
and with clamp connections. Basidiospores are 7–30 μm
13
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Fungal Diversity (2020) 103:87–218
Fig. 12 Phylogram generated from parsimony analysis based on combined ITS and LSU sequenced data Erysiphaceae. Maximum parsimony bootstrap support values greater than 60% and BYPP greater
than 0.90 are indicated above the nodes. The type specimens (ex-epitypes) are in bold. The tree is rooted with Parauncinula septata
long, usually broadly to narrowly ellipsoid, truncate, double-walled, and with an apical germ pore. The endosporium
is brown and separated from the hyaline exosporium by
inter-wall pillars, negative in Melzer’s reagent (Núñez and
Ryvarden 2000; Ryvarden 2004). Basidia are broadly ellipsoid, tapering abruptly at the base, and cystidia are lacking.
Ganoderma species are widely distributed in temperate,
subtropical and tropical regions, and appear to thrive in hot
and humid conditions (Pilotti et al. 2004; Hapuarachchi et al.
2019a, b; Luangharn et al. 2019). Basidiomes are commonly
in the form of a bracket (Pilotti et al. 2004). Ganoderma is
cosmopolitan and an important wood-decaying genus. Some
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Fungal Diversity (2020) 103:87–218
121
Fig. 13 Fomitopsis pinicola a
basidiomes on living European
spruce, b causing brown-rot
decay on narrow-leafed ash, c,
d basidiomes on dead standing
conifer tree, e young basidiome
on hardwood log, f hyphal
structure in the trama, g, h
basidiospores. Scale bars: f =
20 µm, g, h = 5 µm
species of Ganoderma are pathogenic, causing root and stem
rot on a variety of monocotyledons, dicotyledons and gymnosperms, including a wide range of economically important
trees and perennial crops which results in the death of affected
trees (Hapuarachchi et al. 2018b). Ganoderma grows as facultative parasites of trees but can also live as saprobes on rotting
stumps and roots (Turner 1981; Pilotti et al. 2004). Hence,
they have ecological importance in the breakdown of woody
plants for nutrient mobilization. Taxa also possess effective
machinery of lignocellulose-decomposing enzymes which
may be useful for bioenergy production and bioremediation
(Hepting 1971; Kües et al. 2015; Hyde et al. 2019).
Several Ganoderma species are prolific sources of highly
active bioactive compounds such as polysaccharides, proteins,
steroids and triterpenoids. These bioactive compounds show a
huge structural and chemical diversity (Shim et al. 2004; Qiao
et al. 2005; Wang and Liu 2008; Teng et al. 2011; De Silva
et al. 2012a, b; 2013; Hapuarachchi et al. 2017; Li et al. 2018;
Hyde et al. 2019). The bioactive constituents have anti-cancer,
anti-inflammatory, anti-tumour, anti-oxidant, immunomodulatory, immunodeficiency, anti-diabetic, anti-viral, anti-bacterial, anti-fungal, anti-hypertensive, anti-atherosclerotic,
anti-ageing, anti-androgenic, hepatoprotective and radical
scavenging properties. They are also promising in neuroprotection, sleep promotion, cholesterol synthesis inhibition, preventing hypoglycemia, inhibition of lipid peroxidation/oxidative DNA damage, maintenance of gut health, prevention of
obesity, and stimulation of probiotics (De Silva et al. 2012a;
Hapuarachchi et al. 2016a, b, Hapuarachchi et al. 2017).
Current studies are identifying secondary metabolites,
developing models for prediction or early detection of diseases,
finding biological control methods as well as understanding
genomes. Using artificial neural network spectral analyses and
foliage of four disease levels, Ahmadi et al. (2017) provided
an early detection method for Ganoderma basal stem rot of oil
palm. Sitompul and Nasution (2020) suggested that to control
Ganoderma diseases non or weakly pathogenic fungi can be
considered as biological control agents. These agents could
break down woody debris faster than the pathogen and occupy
the same resource as the pathogen (compete for nutrients) as
well as producing inhibitory secondary metabolites (Paterson 2007; Sitompul and Nasution 2020). Utomo et al. (2018)
sequenced the nuclear genome of G. boninense, the main
pathogen of basal stem rot, and the draft genome comprised
of 79.24 megabases and 26,226 predicted coding sequences.
Ramzi et al. (2019) conducted a study to understand the plant
cell wall degradation and pathogenesis of G. boninense via
comparative genome analysis. In their study, they found that
similarly to G. lucidium, G. boninense was enriched with carbohydrate-active and cell wall degrading enzymes. Following
plant-host interaction analysis, several candidate genes including polygalacturonase, endo β-1, 3-xylanase, β-glucanase
and laccase were identified as potential cell wall degrading
enzymes that contribute to the plant host interaction and pathogenesis. The study provided fundamental knowledge on the
fungal genetic ability and capacity to secrete carbohydrateactive and cell wall degrading enzymes. Agudelo-Valencia
et al. (2020) pointed out that information regarding the biotechnological importance of Ganoderma species (other than
G. lucidium) is quite limited. Therefore, in their study they
obtained and studied the genome of G. australe, resulting in
gene prediction for the 84-megabase genome, prediction of
22,756 protein-coding genes, prediction of five putative genes
and two enzyme complexes from a ganoderic acid pathway.
Most Ganoderma species are pathogenic or facultatively
pathogenic, causing root and stem rot on a variety of monocotyledons, dicotyledons, and gymnosperms, including
a wide range of economically important trees and perennial crops, which may result in death (Hapuarachchi et al.
2018a). Some species are saprobic and cause white-rot
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Fungal Diversity (2020) 103:87–218
Fig. 14 Phylogram generated from RAxML analysis based on combined ITS, LSU, nSSU, tef1 and rpb2 sequence data of Fomitopsis
species. Related sequences were obtained from GenBank. Thirty-one
strains are included in the analyses, which comprised 4143 characters
including gaps. The tree was rooted with Daedalea quercina (Dai
12152) and D. dickinsii (Yuan 1090). Tree topology of the ML analysis was similar to the Bayesian analysis. ML bootstrap values ˃ 50%
and BYPP ˃ 0.80 are shown respectively near the nodes
decay of wood (Muthelo 2009). Hence, they have ecological importance in the breakdown of woody plants for
nutrient mobilization. They possess effective machinery of
lignocellulose-decomposing enzymes useful for bioenergy
production and bioremediation (Hepting 1971; Adaskaveg
et al. 1991; Kües et al. 2015).
Basal stem rot: Symptoms of basal stem rot disease can
take several years to develop, and the presence of the pathogen is often only visible when the fungus is well-established
and more than half of the tissue has been decayed. Soils
with poor drainage and water stagnation during rainy seasons favour the disease (Kandan et al. 2010).
Butt rot and root rot: The primary symptoms include wilting, mild to severe, of either all leaves or just the lowest
leaves in the canopy, premature death of the oldest leaves
or a general decline of the tree. The advanced decay of the
larger roots is evident after leaves are blown down. Decay
may extend from several cms to over a metre into the lower
(butt) portion of the tree, depending on the species of Ganoderma. It is quite common for basidiomes not to appear
before the severe decline and death of a tree (Glen et al.
2009). Therefore, the only way to determine if Ganoderma
butt rot is the cause is to cut cross-sections through the lower
Classification—Basidiomycota, Agaricomycotina, Agaricomycetes, Incertae sedis, Polyporales, Ganodermataceae
Type species—Ganoderma lucidum (Curtis) P. Karst. 1881
Distribution—worldwide
Disease symptoms—basal stem, butt and root rot in economically important trees and perennial crops, especially in
tropical regions. Ganoderma disease development is affected
by environmental factors and tree death could be either slow
or rapid depending on water availability and temperature
(Coetzee et al. 2015).
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Fungal Diversity (2020) 103:87–218
Table 9 DNA barcodes for
accepted species of Fomitopsis
123
Species
Strain
ITS
LSU
nSSU
tef1
rpb2
Fomitopsis betulina
F. betulina
F. bondartsevae
F. cana
F. cana
F. caribensis
F. durescens
F. durescens
F. eucalypticola
F. eucalypticola
F. ginkgonis
F. ginkgonis
F. hemitephra
F. iberica
F. meliae
F. meliae
F. mounceae
F. mounceae
F. nivosa
F. ochracea
F. ochracea
F. ostreiformis
F. palustris
F. pinicola
F. pinicola
F. roseoalba
F. schrenkii
F. schrenkii
F. subtropica
F. subtropica
Dai 11449
Miettinen 12388
X1166*
Dai 9611*
Cui 6239
Cui 16871*
Overholts 4215*
O 10796
Cui 16598*
Cui 16594
Cui 17170*
Cui 17171
O 10808
O 10810
Ryvarden 16893
JV 1109/40-J
JEH-78*
MJL-112-Sp
JV 0509/52-X
JEH-12E
JEH-79
Miettinen X1393
Cui 7615
Cui 10312
LT-323
URM 86923*
JEH-150*
JW18-240-1
Cui 10154*
Cui 10578
KR605798
JX109856
JQ700276
JX435776
JX435777
MK852559
KF937293
KF937292
MK852562
MK852560
MK852563
MK852564
KR605770
KR605771
KR605776
KY264030
KF169629
KF169636
KR605779
KF169597
KF169604
KC595918
KR605780
KR605781
KF169651
KT189139
KU169365
KF169648
JQ067652
KR605787
KR605737
JX109856
JQ700276
JX435774
JX435775
MK860108
KF937295
KF937294
MK860113
MK860110
MK860114
MK860115
KR605709
KR605710
KR605715
–
–
–
KR605718
–
–
KC595918
KR605719
KR605720
–
KT189141
–
–
JX435772
KR605726
KR605895
–
–
KR605825
KR605826
MK860124
KR605835
KR605834
MK860129
MK860126
MK860130
MK860131
KR605841
KR605842
KR605849
–
–
–
–
–
–
–
–
KR605856
–
–
–
–
–
KR605867
KR610726
JX109913
–
KR610660
KR610661
MK900482
–
KR610669
MK900484
MK900483
MK900485
MK900486
KR610675
KR610676
KR610681
–
KF178354
KF178361
KR610686
KF178322
KF178329
–
KR610688
KR610689
KF178376
–
MK236356
KF178373
–
KR610698
KR610816
JX109884
–
KR610762
KR610761
MK900474
–
KR610766
MK900479
MK900476
MK900480
MK900481
–
KR610771
KR610775
–
KF169698
KF169705
KR610777
KF169666
KF169673
–
KR610779
KR610780
KF169720
–
MK208858
KF169717
–
KR610791
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold
meter or so of the trunk after the tree is felled and examine
the cross-sections for the typical pattern of rot: greatest near
the soil line, decreasing in sections further from the soil line.
Ganoderma root rot may cause yellowing, wilting, or
undersized leaves and dead branches. Tree vigour may
decline as the decay of the sapwood advances. The first visible sign of infection is often the formation of basidiomes
(solitary or in clusters) on the lower trunk and exposed root
areas. There are two types: varnished and unvarnished. The
upper surface of varnished fungus rot is typically red-brown
with a white edge, shiny, and lacquered. Conks of the unvarnished fungus rot are brown with a white edge weathering
to grey (Pilotti et al. 2004). When fresh, both have a white,
porous surface on the underside. The rate of decay can lead
to death in as little as 3 to 5 years from the time of infection
and appears to be determined by tree vigour, which is often
influenced by environmental stresses (Nirwan et al. 2016).
Hosts—Ganoderma has a wide host range, with more than
44 species from 34 potential host genera identified (Venkatarayan 1936). The root and stem rots caused by Ganoderma
species, result in decreased forestry yields of e.g. Areca catechu (Palanna et al. 2020), Camellia sinensis, Cocos nucifera,
(Kinge and Mih 2014), Elaeis guineensis, (Glen et al. 2009)
and Hevea brasiliensis (Monkai et al. 2017) worldwide.
Pathogen biology, disease cycle and epidemiology
The fungus is spread by spores produced in the prominent
basidiomes that form on the outside of the tree (conks). New
spores released from the conks are dispersed throughout the
summer during humid periods and infect open wounds on
root flares and lower trunk areas of susceptible trees. The
spores germinate, and the infection progresses to attack the
sapwood of major roots and the lower tree trunk. Over the
years, the number of decayed wood increases leading to
13
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Fungal Diversity (2020) 103:87–218
Fig. 15 Morphology of Ganoderma species. a An old basidiome of Ganoderma australe, b Mature basidiome of G. casuarinicola, c, d hyphae,
e tube layer hyphae, f–h Basidiospores, i Pore characteristics. Scale bars: a, b = 2 cm; c, d = 3 μm; e = 15 μm; f, g, h. = 5 μm; i = 500 μm
13
Fungal Diversity (2020) 103:87–218
dangerously soft, spongy wood in the part of the tree that
functions as its anchor (Paterson 2007).
Morphology-based identification and diversity
Ganoderma species identification, limitations and their
taxonomic segregation have been unclear and recently being
debated (Moncalvo et al. 1995; Wang et al. 2009; Cao et al.
2012; Yao et al. 2013; Richter et al. 2015; Zhou et al. 2015a,
b). Many Ganoderma collections and species have been misnamed because of the presence of heterogenic forms, taxonomic obstacles and inconsistencies in the way the genus has
been subdivided (Mueller et al. 2007). Ganoderma species
are genetically heterogeneous, hence a wide range of genetic
variation has been reported and caused by outcrossing over
generations and different geographical origins (Pilotti et al.
2004). This has led to variation in their listed morphological
characteristics, even within the same species (Hong et al.
2001). Environmental factors, variability, inter hybridization
and individual morphological bias, mean identification of
Ganoderma species is difficult (Zheng et al. 2007a). Hence,
naming a species is confused and traditional taxonomic
methods based on morphology are inconclusive for establishing a stable classification system for Ganoderma species
(Hseu et al. 1996; Hong et al. 2001) which in turn result
in an uncertain nomenclature. This confusing situation is
mainly the result of various criteria used in identification by
different authors. Some authors strictly only focus on hostspecificity, geographical distribution and macro morphology
of basidiomes, while other authors only focus on spore characteristics as the primarily taxonomic characteristics (Sun
et al. 2006; Ekandjo and Chimwamurombe 2012). Richter
et al. (2015) suggested using a combination of morphological, chemotaxonomic and molecular methods to develop a
more stable taxonomy for this genus.
Molecular identification and diversity
Isoenzyme analysis was the first molecular technique
used to separate Ganoderma species (Park et al. 1994; Gottlieb et al. 1995, 1998; Gottlieb and Wright 1999a, b; Smith
and Sivasithamparam 2000). Then, DNA sequences of the
internal transcribed spacer (ITS), partial large subunit rDNA
(Moncalvo et al. 1995, 2000; Cao et al. 2012; Yao et al. 2013;
Richter et al. 2015) and nearly complete small subunit rDNA
sequences (Hong and Jung 2004; Douanla-Meli and Langer
2009) were used. Later, multigene phylogenetic analyses
with protein-coding genes such as β-tubulin (tub2), the largest subunit of RNA polymerase II gene (rpb1), the secondlargest subunit of RNA polymerase II (rpb2), and translation
elongation factor 1-α (tef1) were performed to resolve the
taxonomic confusions within Ganoderma (Park et al. 2012;
Zhou et al. 2015a, b; Hennicke et al. 2016; Jargalmaa et al.
2017). However, many problems remain in the resolution of
125
phylogenetic relationships within the genus. As a result of the
intricate taxonomy of Ganoderma, 65% of the Ganoderma
sequences available in GenBank were reported to be wrongly
identified or ambiguously labelled, (Jargalmaa et al. 2017). In
this study, we reconstruct the phylogenetic tree based on ITS,
tef1 and rpb2 sequence data (Table 10, Fig. 16).
Recommended genetic marker (genus level)—ITS
Recommended genetic markers (species level)—rpb2, tef1
Accepted number of species—There are 456 species and
infra-species epithets in Index Fungorum (2020), for 224
accepted species. However, only 64 species have DNA
sequence data.
References—Coetzee et al. (2015); Xing et al. (2016, 2018);
Tchoumi et al. (2019), Luangharn et al. (2019), Ye et al.
(2019) (phylogeny, new species), Cabarroi-Hernández et al.
(2019) (phylogeny).
85. Golovinomyces (U. Braun) V.P. Heluta, Biol. Zh. Armenii 41: 357 (1988)
Background
Braun (1978) introduced Golovinomyces as a section of
Erysiphe sensu lato and Heluta (1988a) raised it to genus
rank. Braun (1999) and Braun and Takamatsu (2000)
accepted Golovinomyces as a distinct genus and established
a new tribe, Golovinomyceteae. This is a strictly herb-parasitic genus in the Erysiphaceae. Host-parasite co-speciation was reported between Golovinomyces and Asteraceae
hosts using molecular phylogenetic analyses (Matsuda and
Takamatsu 2003). It was suggested that Golovinomyces first
acquired parasitism on Asteraceae and then diverged to the
host tribes Astereae, Cardueae, Heliantheae and Lactuceae.
Bremer (1994) pointed out that Golovinomyces may have
originated in South America and the geographic distribution
expanded into the Northern Hemisphere. However, Takamatsu et al. (2006) suggest that Golovinomyces originated in
the Northern Hemisphere, and not in South America. Fabro
et al. (2008) profiled genome-wide expression on haustorium
formation of G. cichoracearum in Arabidopsis. Research
to understand pathogenesis towards plants has been undertaken. A draft whole genome of G. magnicellulatus, the
causal agent of phlox powdery mildew was provided by
Farinas et al. (2019). McKernan et al. (2020) identified 82
genes associated with resistance to G. chicoracearum, the
causal agent of powdery mildew in cannabis.
Classification—Ascomycota, Pezizomycotina, Leotiomycetes, Leotiomycetidae, Erysiphales, Erysiphaceae
Type species—Golovinomyces cichoracearum (DC.) V.P.
Heluta
Distribution—Worldwide (Mainly in northern hemisphere)
Disease symptoms—powdery mildew
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126
Hosts—Has a wide range of hosts including Asteraceae,
Boraginaceae, Cucurbitaceae, Malvaceae, Fabaceae, Lamiaceae, Polygonaceae, Scrophulariaceae, Solanaceae and
Verbenaceae.
Pathogen biology, disease cycle and epidemiology
Discussed under Erysiphaceae.
Morphological based identification and diversity
Golovinomyces is characterized by chasmothecia with
mycelioid appendages, several, mostly 2-spored asci, an
asexual morph with catenescent conidia that lack fibrosin
bodies, and mostly nipple-shaped appressoria (Braun 1978;
Qiu et al. 2020a). Heluta (1988a) reallocated Erysiphae
cichoracearum to Golovinomyces and now nearly all species of E. cichoracearum are assigned to Golovinomyces.
Braun (1987) confined E. cichoracearum to powdery mildews on hosts of Asteraceae and assigned specimens on
hosts belonging to other plant families to Erysiphe orontii.
Braun and Cook (2012) split G. cichoracearum into several
species based on molecular analyses of this complex which
suggested a co-evolutionary relationship between Golovinomyces species and tribes of Asteraceae (Matsuda and Takamatsu 2003). Golovinomyces cynoglossi sensu lato, a complex of morphologically similar powdery mildews on the
plant family Boraginaceae, was reassessed by Braun et al.
(2018) and split into G. asperifoliorum, G. asperifolii and
G. cynoglossi based on sequence analyses, biological aspects
and morphological differences. Braun et al. (2019) revisited
G. orontii and Qiu et al. (2020b) epitypfied and confirmed
Erysiphe cucurbitacearum was a synonym of G. tabaci.
Molecular based identification and diversity
A comprehensive phylogenetic analysis by Takamatsu
et al. (2013) resulted in a polyphyletic complex that split into
three genetically distinct clades. Golovinomyces ambrosiae
and G. spadiceus were considered as separate species by
Braun and Cook (2012). However, phylogenetic analyses of
ITS and 28S rDNA sequences by Takamatsu et al. (2013),
including Golovinomyces species on Asteraceae, found that
these two species that occur on Asian species of Eupatorium
and a multitude of other hosts, including those on other plant
families, formed a single large, unresolved clade (lineage III
in Takamatsu et al. (2013)). The taxonomic interpretation
posed a serious problem as G. ambrosiae and G. spadiceus
were treated as two morphologically differentiated species.
Hence, the resolution based only on ITS sequence data was
considered insufficient to distinguish closely allied species.
Most subsequent authors followed the taxonomic treatments
in Braun and Cook (2012) and recognized G. ambrosiae and
G. spadiceus as separate species, within lineage III, based
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Fungal Diversity (2020) 103:87–218
on morphological differences (Qiu et al. 2020a). However,
there is minimal multi loci data for the powdery mildews
currently available. Most of the research involves the
intra-specific genetic diversity in species such as Blumeria
graminis (Walker et al. 2011), Erysiphe necator (de Oliveira
et al. 2015), Golovinomyces orontii (Pirondi et al. 2015a)
and Podosphaera xanthii (Pirondi et al. 2015b). Based on
ITS and D1/D2 domain of 28S sequence data, Braun et al.
(2019) introduced G. bolayi and G. vincae. Nayak and Bandamaravuri (2019) developed species-specific PCR primers
CgF2 and CgR2 for G. orontii (the causal agent of powdery
mildew in cucurbits), based on partial ITS and 5.8S rDNA,
which resulted in a 233bp fragment of G. orontii.
Recommended genetic markers (genus level)—ITS, LSU
Recommended genetic markers (species level)—Comprehensive applications of multi loci approaches to solve complex taxonomic-phylogenetic problems connected with the
species level classification of the powdery mildews are lacking. The phylogenetic analyses of multi loci sequence data,
including ITS and LSU, IGS, tub2, chs, and consideration
of morphological characters resolve species delimitation in
a heterogeneous complex within Golovinomyces.
Accepted number of species—There are 81 epithets listed in
Index Fungorum (2020), however, only 41 have molecular
data (Table 11, Fig. 17).
References—Braun (1978, 1987), Heluta (1988a, b) (morphology); Braun and Cook (2012), Takamatsu et al. (2013),
Braun et al. (2019), Qiu et al. (2020a, b) (morphology and
phylogeny).
86. Heterobasidion Bref., Unters. Gesammtgeb.Mykol.
(Liepzig) 8: 154 (1888)
Background
Heterobasidion was introduced by Brefeld (1888) and
is typified by H. annosum (≡ Polyporus annosus). Certain
Heterobasidion species are important forest pathogens of the
Northern Hemisphere, causing root and butt rot, mainly in
conifers (Woodward et al. 1998). In coniferous plantations,
Heterobasidion is one of the most widespread of wood decay
agents, especially when the host is under intensive management. Heterobasidion greatly reduces site productivity and
the amount of harvestable timber; estimated financial losses
caused by Heterobasidion species in Europe were around
800 million euro per year (Korhonen et al. 1998; Garbelotto
2004; Asiegbu et al. 2005). On the other hand, these taxa
have a relatively moderate pathogenic role in natural forest
ecosystems. They affect stand species composition, density
and structure, and they contribute to forest succession, nutrient recycling and even regeneration (Goheen and Otrosina
1998; Garbelotto 2004; Dai et al. 2006).
Fungal Diversity (2020) 103:87–218
Table 10 DNA barcodes
available for Ganoderma
127
Species
Voucher no
ITS
rpb2
tef1
Ganoderma adspersum
G. angustisporum
G. applanatum
G. aridicola
G. australe
G. australe
G. austroafricanum
G. boninense
G. carocalcareus
G. casuarinicola
G. casuarinicola
G. chocoense
G. curtisii
G. destructans
G. ecuadoriense
G. eickeri
G. ellipsoideum
G. enigmaticum
G. enigmaticum
G. flexipes
G. gibbosum
G. hoehnelianum
G. knysnamense
G. leucocontextum
G. lingzhi
G. lobatum
G. lucidum
G. lucidum
G. martinicense
G. mbrekobenum
G. mizoramense
G. multiplicatum
G. multipileum
G. mutabile
G. nasalanense
G. neojaponicum
G. orbiforme
G. orbiforme
G. oregonense
G. philippii
G. podocarpense
G. resinaceum
G. ryvardenii
G. ryvardenii
G. sandunense
G. sandunense
G. sessile
G. shandongense
G. sichuanense
G. sinense
G. steyaertanum
GACP15061220
Cui 13817*
FIN131R610
Dai 12588*
GACP14081671
MFLU 13-0534
CBS138724
WD 2028
DMC 322*
Dai 16336*
HKAS104639
QCAM3123
CBS 100132
CMW43670*
ASL799
CMW49692*
GACP14080966*
CBS 139792*
Dai 15970
Wei 5494
SFC20150630-23
Dai11995
CMW47755*
GDGM 40200*
Wu 1006-38*
JV1212/10J
Rivoire 4195
Cui 14404
LIP SWMart08-55*
UMN7-3GHA*
UMN-MZ4*
Dai 13122
CWN 04670
Yuan 2289*
GACP17060211*
ASI 7032
Cui 13918
GACP14061420
CBS 265.88
E7098
QCAM6422*
CBS 194.76
HKAS 58053*
HKAS 58054
GACP18012501*
GACP18012502
JV 1209/9
Dai 15785
HMAS 42798*
Wei 5327
MEL:2382783
MK345425
MG279170
EF060004
KU572491
MH106871
KP142173
KM507324
KJ143905
EU089969
MG279173
MK817650
MH890527
JQ781849
KR183856
KU128524
MH571690
MH106867
KR183855
KU572486
JN383979
KY364264
KU219988
MH571690
KF011548
JQ781858
KF605676
KJ143909
MG279181
KF963256
KX000896
KY643750
KU572488
KJ143913
JN383977
MK345441
JQ520193
MG279186
MK345447
JQ781875
AJ536662
MF796661
KJ143916
HM138671
HM138672
MK345450
MK345451
KF605629
MG279190
JQ781877
KF494998
KP012964
MK371437
MG367507
–
–
–
–
–
KJ143964
–
MG367508
MK840868
–
KJ143967
–
–
–
–
–
MG367513
–
–
MG367497
–
–
JX029980
–
KJ143969
MG367519
–
–
–
–
KJ143972
–
–
–
MG367522
–
KJ143974
–
–
–
–
–
–
–
–
MG367526
–
MG367529
–
MK371431
MG367563
–
KU572502
–
MN423152
–
KJ143924
–
MG367565
MK871328
–
KJ143927
–
–
MH567287
–
–
KU572496
–
–
MG367550
MH567287
–
JX029976
KU572501
–
MG367573
–
–
–
KU572498
KJ143931
–
–
–
MG367576
–
KJ143933
–
–
KJ143934
–
–
–
–
KJ143936
MG367580
–
KF494976
–
13
128
Table 10 (continued)
Fungal Diversity (2020) 103:87–218
Species
Voucher no
ITS
rpb2
tef1
G. steyaertanum
G. subresinosum
G. thailandicum
G. tropicum
G. tropicum
G. tsugae
G. valesiacum
G. weberianum
G. wiiroense
G. williamsianum
G. wuzhishanensis
G. zonatum
6 WN 20B
7-SU-3-C-70(M)-B
HKAS104640*
Dai 16434
HKAS 97486
Dai12751b
CBS428.84
CBS219.36
UMN-20-GHA
Dai 16809
GACP14081689
FL-02
KJ654462
KJ654472
MK848681
MG279194
MH823539
KJ143919
JQ520218
JQ520219
KT952361
MG279183
KU994772
KJ143921
–
–
MK875831
MG367532
MH883621
KJ143977
–
–
–
MG367535
–
KJ143979
–
–
MK875829
MG367585
–
KJ143939
–
–
–
MG367588
–
KJ143941
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold
Classification—Basidiomycota, Agaricomycotina, Agaricomycetes, Incertaesedis, Russulales, Bondarzewiaceae
Type species—Heterobasidion annosum (Fr.) Bref., Unters.
Gesammtgeb. Mykol. (Liepzig) 8: 154 (1888)
Distribution—North America, Europe, Asia, Australia and
Oceania
Disease symptoms—There are two Heterobasidion species
complexes –H. insulare sensu lato and H. annosum sensu
lato—they cause the same symptoms. The H. annosum species complex is one of the major root-rot pathogenic genera
of the northern temperate hemisphere (Garbelotto and Gonthier 2013; Kärhä et al. 2018). After the primary infection
through stump tops, or stem and root wounds, the taxa can
vegetatively infect uninjured trees (secondary infection) by
the growth of the mycelium through root contacts (Rishbeth 1950, 1951a, b; Asiegbu et al. 2005; Garbelotto and
Gonthier 2013). Heterobasidion could be considered both
necrotrophs and saprotrophs; though some species in the H.
insulare species complex (e.g. H. austral, H. araucariae) are
mainly saprotrophs (Niemelä and Korhonen 1998; Dai and
Korhonen 2009; Chen et al. 2014). In contrast to Europe,
the pathogenicity of H. annosum sensu lato in China and
Japan is uncertain; the complex seems to occur mostly on
dead trees, and no symptoms of tree decline are usually visible near infected trees. These observations could be due to
different, less intensive forest management strategies in the
East-Asian regions, or lack of data on the butt rot symptoms
(Dai et al. 2006; Tokuda et al. 2007).
The infection causes white pocket rot and heart rot in
the roots and the butt of living trees (Korhonen and Stenlid
1998; Asiegbu et al. 2005). Resin, containing mycelium,
may also exude from the infected roots, or the bark-scales
(Rishbeth 1950). In invaded roots and the basal portions
of the trunk, H. annosum sensu lato taxa colonize different plant tissues depending on the host. Heart rot is mainly
13
caused in trees more susceptible to the colonization of the
heartwood, e.g. Picea abies. In the case of Pinus, cambium
and sapwood are the most severely colonized, while the sapwood of Calocedrus or Sequoiadendron trees is the most
colonized (Garbelotto 2004; Asiegbu et al. 2005; Garbelotto
and Gonthier 2013).
After establishment, the basidiomata of H. annosum
sensu lato appear. The localization of the sporocarps is
governed by the species, environmental conditions and
infection strategy. Some species prefer the root collar for
fruiting (H. annosum, H. irregular). Some also produce
sporocarps in decay pockets in stumps and fallen trees (H.
parviporum, H. abietinum and H. occidentale), or under
the intact surface of stumps (H. irregulare, H. occidentale). The sporocarps are sometimes located on the higher
parts of the trunk. When moisture is limited, the fungi
fruit inside stumps; if the climate is moist and humid, the
basidiomata can be found near the ground in the duff at
the base of diseased trees. If during primary infection the
stump surface is infected, the basidiomata form under an
intact top layer. During active pathogenesis, if the standing trees are infected the sporocarps could be found within
decay columns in the sapwood (Rishbeth 1950; Otrosina
and Garbelotto 2010).
The infection kills the functioning sapwood, cambium
and heart wood in the roots and at the basal portions of the
trunk, resulting in white rot, reduced growth rate, crown
dieback (Omdal et al. 2004), and eventually mortality and
windthrow of infected trees (Rishbeth 1950; Oliva et al.
2008; Garbelotto and Gonthier 2013).
Hosts—The host range of Heterobasidion is extremely
wide. The genus has been reported from approximately
200 host species (Korhonen and Stenlid 1998). Taxa mostly
occur on gymnosperms, such as Abies, Agathis, Araucaria,
Calocedrus, Juniperus, Keteleeria, Larix, Picea, Pinus,
Fungal Diversity (2020) 103:87–218
129
Fig. 16 Phylogram of 64 recognized Ganoderma species, obtained
from ML of combined ITS, rpb2, and tef1 datasets. Bootstrap values
from ML (left) and MP (middle) greater than 70% and BYPP, greater
than 0.95, are indicated above the nodes. The tree is rooted with Coriolopsis trogii. Type specimens are indicated in bold
Podocarpus, Pseudolarix, Pseudotsuga, Sequoia, Sequoiadendron, Thuja and Tsuga (Buchanan 1988; Corner 1989;
Dai and Korhonen 2009; Otrosina and Garbelotto 2010;
Garbelotto and Gonthier 2013; Garbelotto et al. 2017).
Occasionally, certain Heterobasidion species grow on broadleaved trees of various angiosperm genera (Garbelotto and
Gonthier 2013; Ryvarden and Melo 2014).
Morphological based identification and diversity
There are 33 Heterobasidion epithets listed in Index Fungorum (2020). Of these, eight are related to other polypore
genera, based on type studies and morphological observations (Ryvarden 1972, 1985; Buchanan and Ryvarden 1988;
Dai and Niemelä1995; Hattori 2003). Besides, the taxonomic status of three further species described from Asia is
13
130
unclear: viz. H. arbitrarium, H. perplexum and H. insulare
(Corner 1989; Ryvarden 1989; Stalpers 1996; Hattori 2001;
Dai et al. 2002; Tokuda et al. 2009). Given that no sequence
data (H. arbitrarium, H. perplexum) or authentic sequences
(H. insulare sensu stricto) are available for the molecular
resolution, further studies are needed to clarify their status.
Formerly, Heterobasidion was considered as a group
consisting of only the generic type, H. annosum and H.
araucariae and H. insulare (Buchanan 1988; Chase 1989).
However, mating studies on Eurasian and North American Heterobasidion collections revealed several intersterile groups, which later became the basis for designating
separate taxonomic species within the H. annosum and H.
insulare species complexes. Mating experiments revealed
three intersterile groups of H. annosum sensu lato in
Europe (Korhonen 1978b, Capretti et al. 1990) and two
in North America (Otrosina et al. 1993). All intersterile
groups have been recognised in the H. annosum species
complex are now formally described as separate taxonomic
species. European groups were described as H. abietinum,
H. parviporum and H. annosum sensu stricto (Niemelä and
Korhonen 1998), whereas North American groups were
named H. irregulare and H. occidentale (Otrosina and Garbelotto 2010).
The mating study by Dai et al. (2002) on Asian “H. insulare” collections revealed three intersterile groups in China,
which were subsequently described as Heterobasidion linzhiense (Dai et al. 2007), H. orientale and H. ecrustosum
(Tokuda et al. 2009). H. australe related to the H. insulare
species complex was also described from China by Dai and
Korhonen (2009). Chen et al. (2014) described two further
Heterobasidion species (H. amyloideum and H. tibeticum)
from the eastern Himalayas based on phylogenetic evidence. These species are morphologically closely related to
the members of the H. insulare species complex, but differ
in presence of cystidia and amyloid skeletal hyphae in the
context. The recently described H. amyloideopsis was collected in the western Himalayas (Pakistan) and formed a
monophyletic group with the H. insulare species complex,
sister to H. amyloideum (Zhao et al. 2017).
The main morphological characters which are used for
the identification are the resupinate to pileate basidiocarps,
the dimitic hyphal system with mostly simple septate generative hyphae, and the asperulate basidiospores showing
no reaction in Melzer’s reagent. Besides morphology, host
preference, geographical distribution, and DNA sequence
data have also been used for species identification (Otrosina
and Garbelotto 2010; Chen et al. 2015a).
Molecular based identification and diversity
Heterobasidion has been intensely studied by molecular
methods. Sequence data are available for the majority of
13
Fungal Diversity (2020) 103:87–218
taxa, and molecular studies were conducted to understand
the evolution (Dalman et al. 2010), mating behaviour (Gonthier and Garbelotto 2011), and pathogenicity (Liu et al.
2018a) of Heterobasidion species.
Various marker types were used to resolve the phylogeny of the H. annosum species complex, such as isoenzyme
(Karlsson and Stenlid 1991a, b), AFLP (Gonthier and Garbelotto 2011) and SSR (Garbelotto et al. 2013) markers.
Sequence analyses were carried out initially on nrITS and
intergenic spacer regions (Kasuga and Mitchelson 1993a,
b; DeScenzo and Harrington 1994), housekeeping genes
(Johanesson and Stenlid 2003), peroxidase (Maijala et al.
2003) and laccase genes (Asiegbu et al. 2004), with which
it was possible to distinguish four lineages (three European
and one North American) within the complex (Asiegbu et al.
2005). Later, allowing the differentiation of a larger number of taxa, further nuclear genes were applied, such as the
calmodulin (cam), translation elongation factor 1-α (tef1),
glyceraldehydes3-phosphate dehydrogenase (gapdh), heat
shock protein (hsp), glutathione-S-transferase (gst1) and
transcription factor (tf) genes (Johanesson and Stenlid 2003;
Ota et al. 2006; Dalman et al. 2010), as well as two mitochondrial genes, the mitochondrial ATP synthase subunit 6
(ATP6) and mitochondrial rDNA region (Linzer et al. 2008).
Dalman et al. (2010) came to the conclusion, that there are
two monophyletic sister clades within the H. annosum species complex, representing the Eurasian and North American
species.
The protein coding largest subunit of RNA polymerase II
(rpb1) and the second subunit of RNA polymerase II (rpb2)
genes were used by Chen et al. (2014) and were suitable
to differentiate Heterobasidion species in the H. insulare
species complex. The variability of these markers was confirmed by Chen et al. (2015a) and Zhao et al. (2017) who,
among other previously mentioned markers, both used the
nuclear large ribosomal subunit (nrLSU) and the mitochondrial small subunit (mtSSU) sequences to their studies
(Fig. 18).
In this study, we provide a phylogenetic tree
(Fig. 19) based on multi-locus phylogenetic analysis of
ITS–gapdh–rpb1–rpb2–tef1 sequence data. Sequences of H.
arbitrarium and H. perplexum could not be analysed as they
are unavailable in GenBank. Furthermore, no sequences are
available for the type of H. insulare hence this species was
not included in the analysis. The results provide a similar
topology to those obtained by Chen et al. (2015a, b) and
Zhao et al. (2017).
Recommended genetic marker (genus level)—nLSU
Recommended genetic markers (species level)—rpb1, rpb2
Accepted number of species –There are 33 epithets in Index
Fungorum (2020), however only 15 species are accepted
Fungal Diversity (2020) 103:87–218
Table 11 DNA barcodes
for accepted species of
Golovinomyces
131
Species
Strain no
ITS
LSU
Golovinomyces adenophorae
G. ambrosiae#
G. arabidis
G. artemisiae#
G. asperifolii
G. asperifoliorum
G. asterum#
G. biocellatus#
G. bolayi#
G. calceolariae
G. chrysanthemi
G. cichoracearum#
G. circumfusus#
G. cucubitarum
G. cynoglossi#
G. depressus
G. echinopis
G. euphorbiicola
G. fischeri
G. glandulariae
G. hyoscyami
G. inulae
G. leuceriae
G. longipes#
G. macrocarpus
G. magnicellulatus#
G. monardae#
G. montagnei
G. neosalviae#
G. ocimi
G. orontii#
G. riedlianus
G. reginae
G. salviae
G. sonchicola#
G. sordidus#
G. spadiceus#
G. tabaci
G. valerianae
G. verbasci#
G. vincae
MUMH < JPN_144
MUMH345
HMNWAFU-CF2009256
MUMH175
KUS-F24884
MUMH769
MUMH941
MUMH4293
OLM 35939*
MUMH 1934
MUMH853
MUMH623
GLM49501
HMJAU-PM91761
VPRI20429
MUMH696
MUMH1363
MUMH3807
MUMH1345
BRIP 70490*
HMNWAFU-CF2013114
MUMH1334
MUMH2527
MUMH2489
HAL 3153*
MUMH441*
MUMH936
MUMH1082
MUMH4294
MUMH<JPN_:1803
G:00295968
HMNWAFU-CF2012033
BCRU4645
MUMH935
MUMH683
MUMHn41
MUMH<JPN_:3708
BP-1TOB
HMNWAFU-CF2011034
MUMH958
MUMH2480
LC516963
AB077642
KR048081
AB077637
MH189697
AB077684
AB769417
AB307671
LC417106
AB430810
AB077654
AB077660
MK452630
MK937796
AB769455
AB077675
AB769414
AB769460
AB769451
NR_166303
KR048155
AB769428
AB246766
AB769440
NR_154105
AB077647
AB307668
AB769413
AB307673
LC306656
LC417099
KR048088
AB246759
AB769437
AB077673
AB077658
LC306664
AF229013
KR048090
AB769468
AB769444
AB077632
AB077641
KR048149
AB077636
MH189696
AB077684
AB769418
AB307671
–
AB430810
AB077653
AB077660
MK452703
MK937801
–
AB077676
–
–
AB769452
MN539541
KR048155
–
–
–
–
AB077646
AB077691
–
–
–
–
KR048157
–
AB077690
AB077672
AB077657
–
AB022412
KR048159
AB769469
–
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
(Table 12). Amongst these, no sequences are available for
H. arbitrarum and H. insulare. Heterobasidion perplexum is
not accepted in the genus, pending further studies.
References—Dai and Korhonen (2009) (new sp., China,
morphology); Tokuda et al. (2009) (new species, East
Asia); Dalman et al. (2010) (Evolution, H. annosum species
complex, haplotype network); Otrosina and Garbelotto
(2010) (new species, North America, biology); Garbelotto
and Gonthier (2013) (biology, epidemiology, control); Chen
et al. (2014) (new species, China, phylogeny); Chen et al.
(2015a) (biogeography, divergence time estimation, phylogeny); Zhao et al. (2017) (new sp., Pakistan, phylogeny).
13
132
Fungal Diversity (2020) 103:87–218
Fig. 17 Phylogram generated from MP analysis based on combined
sequences of ITS and LSU sequences of all species of Golovinomyces with molecular data. Related sequences were obtained from GenBank. Fourty-two taxa are included in the analyses, which comprise
1401 characters including gaps, of which 848 characters are constant,
392 characters are parsimony-uninformative and 161 characters parsi-
mony-informative. The parsimony analysis of the data matrix resulted
in the maximum of ten equally most parsimonious trees with a length
of 927 steps (CI = 0.740, RI=0.699, RC = 0.517, HI = 0.260) in
the second tree. The tree was rooted with Neoerysiphe galeopsidis
(MUMH 4680). MP bootstrap support value ≥ 50% and BYPP ≥ 0.9
are shown respectively near the nodes. Ex-type strains are in bold
87. Meliola Fr., Syst. orb. veg. (Lundae) 1: 111 (1825)
Background
Meliola commonly known as “black mildews” or “dark
mildews” is the largest genus of Meliolaceae (Hongsanan
et al. 2015; Zeng et al. 2017). Fries (1825) established this
genus, with the type species M. nidulans. Species in Meliola
are mostly biotrophs or pathogens of living leaves and occasionally petioles, twigs, and branches (Hansford 1961; Hosagoudar 1994, 1996, 2008; Mibey and Hawksworth 1997; Old
et al. 2003; Hosagoudar and Riju 2013). The phylogenetic
placement of Meliola was established by using sequence
data from fruiting bodies and placed in Sordariomycetes
(Gregory and John 1999; Pinho et al. 2012, 2014, Hongsanan et al. 2015; Justavino et al. 2015). Meliola has been
shown to be polyphyletic (Hyde et al. 2020b; Marasinghe
et al. 2020; Zeng et al. 2020). There is little sequence data
available in GenBank for clarifying relationships between
species and establishiing host-specificity (Hongsanan et al.
2015; Zeng et al. 2017).
13
Classification—Ascomycota, Pezizomycotina, Sordariomycetes, Sordariomycetidae, Meliolales, Meliolaceae
Type species—Meliola nidulans (Schwein.) Cooke
Distribution—commonly found in tropical and subtropical
regions (see Zeng et al. 2017)
Disease symptoms—Black mildews, forming black, radiate
velvety colonies on the surface of plants.
Hosts—has a wide range of hosts (see Zeng et al. 2017)
Fungal Diversity (2020) 103:87–218
Pathogen biology, disease cycle and epidemiology
For pathogen biology, disease cycle and epidemiology see
Hongsanan et al. (2015).
Morphological based identification and diversity
Species in Meliola are characterized by forming web-like
colonies on the host surface, hyphal setae developed from
superficial hyphae, with hyphopodia, 2–4-spored, unitunicate asci, and 3–4-septate pigmented ascospores (Pinho
et al. 2012, 2014; Hongsanan et al. 2015, 2020; Justavino
et al. 2015; Hyde et al. 2020a, b; Fig. 20). Cannon and Kirk
(2007) reported that the asexual morph of the genus develops from the hypha, form ampuliform hyphopodia or flaskshaped which are called “phialides” (Hongsanan et al. 2015).
Conidiogenous cells formed from vegetative hyphae and
small, hyaline, unicellular conidia (Cannon and Kirk 2007;
Hongsanan et al. 2015). Currently, Meliola comprises over
1700 species (Zeng et al. 2017), which have mostly been
introduced by host association, followed by morphology, and
disease distribution (Mibey and Hawksworth 1997). Thus,
species identification is almost impossible without a host
name. However, the same species can be found in different
hosts, but it is not clear if this is widespread (Hongsanan
et al. 2015). Therefore, testing of host-specificity in Meliola
is needed to establish accurate species determination.
Molecular based identification and diversity
Sequence data of species in Meliola are from direct
sequencing of fruiting bodies and fresh mycelium (Pinho
et al. 2012, 2014; Hongsanan et al. 2015; Justavino et al.
2015; Hyde et al. 2016, 2020b). LSU and ITS sequence data
placed Meliola in Sordariomycetes (Hongsanan et al. 2015,
2020; Maharachchikumbura et al. 2015, 2016; Hyde et al.
2016, 2020a, b). By adding more sequence data, Meliola
was shown to be polyphyletic (Marasinghe et al. 2020; Zeng
et al. 2020). A phylogenetic tree for Meliola species is presented in Fig. 21.
Recommended genetic markers (genus level)—LSU, SSU
of nrDNA
Recommended genetic marker (species level)—ITS
Accepted number of species—There are 3064 epithets listed
in Index Fungorum (2020), however only 25 species have
DNA molecular data (Zeng et al. 2017, Table 13).
References—Cannon and Kirk (2007) (morphology); Pinho
et al. (2012, 2014), Hongsanan et al. (2015, 2020), Justavino
et al. (2015), Zeng et al. (2020) (morphology and phylogeny)
88. Neoerysiphe U. Braun, Schlechtendalia 3: 50 (1999)
Background
133
Neoerysiphe was classified in section Galeopsidis within
Erysiphe. Phylogenetic analysis, however, showed Erysiphe
to be polyphyletic, and Galeopsidis was raised to generic
rank (Takamatsu et al. 1998; Braun 1999; Saenz and Taylor
1999). Therefore, in the current classification Neoerysiphe
belongs to the tribe Golovinomyceteae.
Classification—Erysiphaceae, Erysiphales, Leotiomycetidae, Leotiomycetes, Pezizomycotina
Type species—Neoerysiphe galeopsidis (DC.) U. Braun
Distribution—Argentina, Australia, Belarus, Brazil, Bulgaria, Canada, China, Denmark, Finland, France, Germany,
Hungary, India, Israel, Italy, Japan, Korea, Netherlands,
Norway, Poland, Romania, Russia, Slovakia, Sweden, Switzerland, Turkey, UK, Ukraine and USA (Farr and Rossman
2020).
Disease symptoms-powdery mildew
Hosts—Neoerysiphe species have a wide host distribution
infecting more than 300 species from families including
Asteraceae, Acanthaceae, Bignoniaceae, Elaeocarpaceae,
Lamiaceae, Rubiaceae and Verbenaceae (Amano 1986;
Braun 1999; Bahcecioglu et al. 2006). In general, all species have a specific host range confined to one plant family,
except N. galeopsidis which affects several species in four
families (Takamatsu et al. 2008).
Pathogen biology, disease cycle and epidemiology
Discussed under Erysiphaceae.
Morphological based identification and diversity
Neoerysiphe is in the tribe Golovinomyceteae with
Arthrocladiella and Golovinomyces. These genera share a
common asexual morph characterized by catenate conidia
without distinct fibrosin bodies (Braun 1999). Neoerysiphe
is characterized by lobed appressoria and the striate surface
of the conidia (Braun 1981; Cook et al. 1997; Braun and
Cook 2012). Braun and Cook (2012) mentioned that 15 species of Neoerysiphe are described on different hosts belonging to 11 plant families. Of these 15 species, 11 sexual
morphs and 14 asexual morphs have been identified (except
N. joerstadii) (Heluta et al. 2010; Braun and Cook 2012).
Striatodium is now considered as a synonym of Neoerysiphe
and three species viz. N. aloysiae, N. baccharidis and N.
maquii were transferred to Neoerysiphe, while Striatodium
jaborosae was not transferred as its phylogenetic position
are unclear (Wijayawardene et al. 2017a).
Molecular based identification and diversity
The phylogenetic placement of Neoerysiphe within Erysiphaceae has been reported in a few papers (Saenz and
13
134
Fungal Diversity (2020) 103:87–218
Fig. 18 Members of Heterobasidion annosum species complex. a basidiome on Scots pine, b basidiome on European silver fir, c–e basidiomes
on European spruce, f hyphal structure in the trama, g hyphal structure in the context, h–j basidiospores. Scale bars: f, g = 10 µm, h, j = 5 µm
Taylor 1999; Mori et al. 2000; Cook et al. 2006). However,
these treatments used only limited sequence data for the
genus. Takamatsu et al. (2008) conducted the first comprehensive study on this genus using ITS sequence data and
the divergent domains D1 and D2 of the 28S rDNA for 30
strains. In their study, the 30 taxa, clustered into three monophyletic groups that were represented by N. galeopsidis on
Lamiaceae, N. galii on Rubiaceae and N. cumminsiana from
Asteraceae. Takamatsu et al. (2008) used an LSU dataset to
estimate the timing of divergence of Neoerysiphe. Neoerysiphe split from other genera ca 35–45 Mya and the three
groups of Neoerysiphe diverged between 10 and 15 Mya in
the Miocene. Heluta et al. (2010) used 65 ITS sequences in
their analyses for identifying Neoerysiphe species infecting
Asteraceae and Geranium in Eurasia and introduced three
new species, viz. N. hiratae, N. joerstadii and N. nevoi.
Gregorio-Cipriano et al. (2020) introduced a new species
N. sechii causing powdery mildew on Sechium edule and
S. mexicanum in Mexico. The authors mentioned that they
were unable to recover DNA in pure form from some samples, as fragments of infected leaves were used during the
extraction. Therefore, a specific oligonucleotide for Erysiphales at the 5= region of ITS was designed: ErysiF (5=AGGATCATTACWGAGYGYGAG-3=) was used along
with NLP1 (Limkaisang et al. 2006) to amplify a fragment
of approximately 1200 bp (that included the ITS1-5.8S-ITS2
region and a section of approximately 680 nucleotides from
13
28S). Species used in the phylogenetic analyses done in this
study are listed in Table 14 and given in Fig. 22.
Recommended genetic marker (genus level)—ITS and LSU
Recommended genetic markers (species level)—ITS
Accepted number of species—There are 16 species epithets in Index Fungorum (2020), for 15 accepted species.
However, only 12 species have DNA sequence data (N. chelones, N. gnaphalii and N. rubiae do not have molecular
data) (Table 14).
References—Takamatsu et al. (1998), Braun (1999), Saenz
and Taylor (1999) (morphology); Heluta et al. (2010), Braun
and Cook (2012), Gregorio-Cipriano et al. (2020) (morphology and phylogeny).
89. Nothophoma Qian Chen & L. Cai, Stud. Mycol. 82:
212 (2015)
Background
Nothophoma was introduced by Chen et al. (2015b) by
transferring five Phoma species. Species are saprobes and
pathogens. In addition, to the phytopathogens, N. gossypiicola has been isolated from clinical samples of humans
in the respiratory secretion of a patient with pneumonia
and a human bronchial wash sample (Valenzuela-Lopez
et al. 2018). Chethana et al. (2019) showed that the comparative pathogenicity of Nothophoma species is low when
compared to other opportunistic pathogens. Some species
grow on other fungi or occur in soil (Boerema et al. 2004;
Fungal Diversity (2020) 103:87–218
135
Fig. 19 Phylogram generated from ML analysis based on combined
ITS, rpb1, rpb2, gapdh and tef1 sequence data of Heterobasidion species. Related sequences were obtained from GenBank. Fourty-four
strains are included in the analyses, which comprised 4314 characters
including gaps. The tree was rooted with Bondarzewia occidentalis
(HHB 14803) and B. tibetica (Cui 12078). Tree topology of the ML
analysis was similar to the Bayesian analysis. ML bootstrap values ˃
50% and BYPP ˃ 0.80 are shown respectively near the nodes
Aveskamp et al. 2009; 2010; Chen et al. 2015b). Some
Nothophoma species might be host-specific to a single plant
genus or family (Aveskamp et al. 2010; Chen et al. 2015b).
However, there is no study of host-specificity in Didymellaceae. Abdel-Wahab et al. (2017) identified 55 bioactive
compounds from an endophyte, N. multilocularis. Of these,
ten compounds showed strong antimicrobial activity in
combination.
Distribution—Argentina, China, Italy, India, Korea, Netherlands, Spain, Tunisia, Ukraine, United States
Disease symptoms—brown spot of fruits, leaf spots, shoot
canker, stem cankers
Leaf spot produced by Nothophoma anigozanthi is elliptical to circular and black. Nothophoma pruni and N. quercina
develop small, dark red or purple pinpoint lesions (Chethana et al. 2019). Liu et al. (2018b) identified N. quercina
infection on ornamental crab-apple. Symptoms on the trunk
appear as warts, the periderm around warts can become
cracked, and the bark is roughened with a scaly periderm.
During dry weather, these cankers expand and coalesce (Liu
et al. 2018b; Fig. 23). Nothophoma quercina develops shoot
Classification—Ascomycota, Pezizomycotina, Dothideomycetes, Pleosporomycetidae, Pleosporales, Didymellaceae
Type species—Nothophoma infossa (Ellis & Everh.) Qian
Chen & L. Cai
13
136
Table 12 DNA barcodes
for accepted species of
Heterobasidion
Fungal Diversity (2020) 103:87–218
Species
Strain
Heterobasidion abietinum 00057/2
00051/1
PFC 5247
PFC 5373
H. amyloideopsis
MS 8848*
M 118
H. amyloideum
Li 1878*
Li 1675
Li 1883
H. annosum
K 06125/2
K 06071/1
PFC 5252
PFC 5260
H. araucariae
65008
CBS 743.94*
PFC 5434
H. australe
K 05175/2
K 04167/4
K 04164/3
H. ecrustosum
K 05168/1
K 07103/2
PFC 5438
H. irregulare
57001/VE
05025/VE
PFC 5398
PFC 5288
H. linzhiense
Dai 5408*
Cui 7216
MSM 0097
H. occidentale
79034/VE
98005/VE
PFC 5362
PFC 5388
H. orientale
K 97011/7
K 03293/2
K 00085/2
H. parviporum
K 04121/3
08123/VE
PFC 5262
Dai 5537*
H. tibeticum
Dai 5468
Dai 5534
ITS
rpb1
rpb2
gapdh
tef1
KJ651453
KJ651450
KC492895
KC492956
KT598384
KT598385
KJ651455
KJ651454
KJ651456
KJ651459
KJ651458
KC492906
KC492911
KJ651462
MH862503
KX130098
KJ651467
KJ651465
KJ651464
KJ651468
KJ651471
KX130099
KJ651473
KJ651478
KP863586
KP863575
KJ651484
KJ651480
MH233930
KJ651485
KJ651489
KP863584
KP863585
KJ651490
KJ651493
KJ651492
KJ583212
KJ651500
KC492957
KJ651507
KJ651505
KJ651506
KJ651632
KJ651629
–
–
–
–
KF033157
KF033155
KF033156
KF453492
KF453491
–
–
KJ651636
–
–
KF033137
KF033135
KF033134
KF033142
KF033145
–
KJ651638
KJ651643
–
–
KF033154
KF033148
–
KJ651645
KJ651649
–
–
KF033141
KF033140
KF033139
KF453493
KF453495
–
KF033153
KF033151
KF033152
KJ651725
KJ651722
–
–
KT598388
KT598389
KF006538
KF006534
KF006537
KF453498
KF453497
–
–
KJ651729
–
–
KF006506
KF006502
KF006500
KF006513
KF006517
–
KJ651731
KJ651736
–
–
KF006533
KF006524
–
KJ651738
KJ651742
–
–
KF006512
KF006510
KF006508
KF453499
KF453501
–
KF006531
KF006527
KF006529
KJ651756
KJ651753
KP863657
KP863664
–
–
KJ651758
KJ651757
KJ651759
KJ651762
KJ651761
KP863659
KP863661
KJ651766
–
KX130104
KJ651771
KJ651769
KJ651768
KJ651772
KJ651775
KX130105
KJ651777
KJ651782
KP863652
KP863641
KJ651788
KJ651784
–
KJ651789
KJ651793
KP863650
KP863651
KJ651794
KJ651797
KJ651796
KJ651800
KJ651805
KP863662
KJ651812
KJ651810
KJ651811
–
–
KC571636
KC571687
–
–
–
–
–
–
–
KC571646
KC571651
–
–
KX130101
–
–
–
–
–
KX130102
–
–
KP863616
KP863606
–
–
–
–
–
KP863614
KP863615
–
–
–
–
–
KC571688
–
–
–
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold
necrosis, stem browning, and wilted leaves on Chaenomeles sinensis (Yun and Oh 2016). In Tunisia, shoot blights
caused by N. quercina were observed with diffuse cankers
with gummosis on buds (Triki et al. 2019).
13
Hosts— Has a wide range of hosts including Anigozanthos flavidus, Anigozanthus maugleisii, Arachis hypogaea,
Chaenomeles sinensis, Gossypium sp., Fraxinu spennsylvanica, Malus micromalus, Microsphaera alphitoides, Olea
europaea, Phellodendrona murense, Pistacia vera, Prunu
Fungal Diversity (2020) 103:87–218
137
Fig. 20 Morphology of Meliola
species a Meliola thailandicum on Dimocarpus longan. b
Meliola sp. on Citrus reticulata.
c Meliola sp. on Citrus maxima.
d Colony on the host surface.
e Hyphopodia on mycelium.
f Section through ascoma. g
Peridium. h Setae. i Young
ascus. j Mature ascus. k, l
Ascospores. Scale bars: f=50
μm, g, i–l=30 μm, h=10 μm
and e=5 μm
savium, Prunus dulcis, Spiraea salicifolia, Quercus sp. and
Ziziphus jujube (Babaahmadi et al. 2018; Chen et al 2015b,
2017; Chethana et al. 2019; Jianyu et al. 2016; Liu et al.
2018b; Moral et al. 2017, 2018; Soleimani et al. 2018; Triki
et al. 2019; Valenzuela-Lopez et al. 2018; Yun and Oh 2016;
Zhang et al. 2020).
Morphological based identification and diversity
This genus was introduced by Chen et al. (2015b) based
on molecular data to delineate a more natural classification for the Ascochyta-Didymella-Phoma species complex
(Chen et al. 2015b; Fig. 23). Species produce elongate,
barrel-shaped, olivaceous brown chlamydospores in chains
(Chen et al. 2015b). However, there is little morphological
variation among species (Valenzuela-Lopez et al. 2018).
Molecular based identification and diversity
Species identification is based on multi-locus sequence
phylogeny. Phylogenetic analyses of combined LSU, ITS,
tub2 and rpb2 sequence data resulted in several new species
being added to this genus by Chen et al. (2015b), AbdelWahab et al. (2017), Valenzuela-Lopez et al. (2018), Chethana et al. (2019), Marin-Felix et al. (2019) and Zhang et al.
13
138
Fungal Diversity (2020) 103:87–218
Fig. 21 Phylogram generated from RAxML analysis based on combined ITS and LSU sequence data of Meliola species. Related
sequences were obtained from GenBank. Thirty-five strains are
included in the analyses, which comprised 1655 characters includ-
ing gaps. The tree was rooted with Chaetosphaeria innumera (SMH
2748). Tree topology of the ML analysis was similar to the Bayesian
analysis. ML bootstrap values ≥ 50% and BYPP ≥ 0.90 are shown
respectively near the nodes
(2020). Here we provide an updated phylogenetic tree for
this genus (Fig. 24).
90. Phellinus Quél., Enchir. fung. (Paris): 172 (1886)
Background
Phellinus was introduced by Quélet (1886) with P. igniarius (≡ Boletus igniarius) as its type species (Murrill 1903)
and is placed in Hymenochaetaceae (He et al. 2019). Traditionally, most poroid Hymenochaetaceae were placed in
Phellinus, which has been characterized by a dimitic hyphal
system and perennial habit of the basidiomata (Gilbertson
1979; Larsen and Cobb-Poulle 1990; Ryvarden and Gilbertson 1994; Núñez and Ryvarden 2000). However, phylogenetic studies revealed that the morphologically defined
Phellinus sensu lato had polyphyletic origins within the
Hymenochaetoid clade, and most species previously classified as Phellinus are now members of various segregate
genera (e.g. Wagner and Fischer 2001, 2002; Jeong et al.
2005; Dai 2010; Rajchenberg et al. 2015; Drechsler-Santos
et al. 2016). According to the most narrowly defined generic
concept, Phellinus sensu stricto is limited to the P. igniarius
species complex (Fischer and Binder 2004), which includes
species causing a delignifying trunk rot mostly on various
Recommended genetic markers (genus level)—LSU, ITS
Recommended genetic markers (species level)—tub2, rpb2
Since the colony morphology and other morphological features in Didymellaceae often overlap, initial species identification is recommended with LSU and ITS
sequence data using all type species in Didymellaceae.
Once the genus is identified as Nothophoma, the phylogenetic analysis could be done with LSU, ITS, tub2, and
rpb2 sequence data.
Accepted number of species—There are 12 species in Index
Fungorum (2020) with DNA sequence data (Table 15).
References—Chen et al. (2015b), Abdel-Wahab et al. (2017),
Valenzuela-Lopez et al. (2018), Chethana et al. (2019),
Marin-Felix et al. (2019), Zhang et al. (2020) (morphology
and phylogeny)
13
Fungal Diversity (2020) 103:87–218
Table 13 DNA barcodes
available for Meliola
139
Species
Culture/specimen number
LSU
ITS
Meliola aristolochiae-tagalae
M. brachyodonta
M. caesalpiniicola
M. centellae
M. citri-maximae
M. clerodendricola
M. crescentiae
M. danielliae
M. jasmini-sambac
M. lithocarpigena
M. monnieriae
M. mucunicola
M. niessleana
M. panici
M. peruiferae
M. pistaciicola
M. pottsiae
M. puerariae
M. pseudosasae
M. schimigena
M. tamarindi
M. trichostroma
M. variaseta
M. vernaliae
MFLU 16-0088*
VIC32066
VIC32061
VIC31244*
MFLU 14-0288*
MFLU 13-0620*
VIC32056
VIC32057
MFLU 17-1044*
MFLU 13-0628*
VIC32062
MFLU 15-0386
UBC F23799
VIC32063
VIC 31249*
MFLU 16-0070*
MFLU 13-0631*
MFLU 16-0087*
MFLU 16-2136
MFLU 17-1048*
MFLU 14-C0282
VIC32068
DRJ 54 (PMA)
VIC 31240
MN747479
MN747473
KC618644
KC618641
NG042650
KX458474
KT021647
KC618649
KC618648
MN747482
MN747474
KC618647
KT157533
KC833049
KC618651
NG 060294
MN747478
MN747475
MN747472
KX845434
MN747484
KP744489
KC618643
EF094840
JX096808
MN747479
–
–
–
NR137799
–
–
–
–
MN747482
MN747474
–
KT157534
–
–
–
MN747478
MN747475
–
–
MN747484
–
–
–
–
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*)
deciduous trees in temperate areas (Brazee 2015; Zhou et al.
2016). Based on a wider generic concept, several morphologically similar species described from East Asia, Africa
or America are considered as part of Phellinus sensu stricto
(Decock et al. 2006; Yombiyeni et al. 2011; Cui and Decock
2013; Bian et al. 2016; Campos-Santana et al. 2016; Vlasák
and Vlasák 2017; Salvador-Montoya et al. 2018; Zhu et al.
2018). In this study, we follow the broader concept of classification of Phellinus sensu stricto, pending further studies.
Classification—Agaricomycotina, Basidiomycota,
Agaricomycetes, Incertae sedis, Hymenochaetales,
Hymenochaetaceae
Type species—Phellinus igniarius (L.) Quél., Enchir. fung.
(Paris): 177 (1886)
Distribution—If the wider generic concept of Phellinus were
accepted it would be a globally distributed genus, with certain species found in East Asia, Europe, North America (Dai
2010; Cui and Decock 2013; Brazee 2015; Zhou et al. 2016;
Vlasák and Vlasák 2017; Zhu et al. 2018), Central- and
South America (Decock et al. 2006; Campos-Santana et al.
Table 14 DNA barcodes available for Neoerysiphe
Species
Strain no
ITS
LSU
Neoerysiphe aloysiae
N. baccharidis
N. cumminsiana
N. galeopsidis
N. galii
N. geranii
BCRU 04878
BCRU 01609
VPRI 20387
MUMH 4680
MUMH 4682
HMNWAFUCF2013083
MUMH 3442
MUMH 4668
DAR 33493
MUMH 2460
MUMH 4671
AB329683
AB329685
GU356539
AB498949
AB498951
KR048092
–
AB329684
–
AB022369
AB103365
KR048161
AB498962
AB498976
GU356546
AB329686
AB498975
–
–
–
–
–
N. hiratae
N. joerstadii
N. kerribeeensis
N. maquii
N. nevoi
Ex-type/ex-epitype/ex-neotype/ex-lectotype
strains are in bold
strains
and
voucher
13
140
Fungal Diversity (2020) 103:87–218
Fig. 22 Phylogram generated from MP analysis based on combined
sequences of ITS and LSU sequences of all species of Neoerysiphe
with molecular data. Related sequences were obtained from GenBank. 12 taxa are included in the analyses, which comprise 2023
characters including gaps, of which 1790 characters are constant, 167
characters are parsimony-uninformative and 66 characters parsimonyinformative. The parsimony analysis of the data matrix resulted in the
maximum of four equally most parsimonious trees with a length of
316 steps (CI = 0.848, RI=0.678, RC = 0.575, HI = 0.152) in the
first tree. Single gene analyses were carried out and compared with
each species, to compare the topology of the tree and clade stability.
The tree was rooted with Golovinomyces adenophorae (MUMH144).
MP bootstrap support value ≥ 50% and BYPP ≥ 0.9 are shown
respectively near the nodes. Ex-type strains are in bold
2016; Salvador-Montoya et al. 2018) and Africa (Yombiyeni
et al. 2011; Cloete et al. 2016). However, the members of
the P. igniarius species complex are known only from the
Northern Hemisphere (Brazee 2015; Zhou et al. 2016).
Disease symptoms—Members of Phellinus produce
white rot, decaying polysaccharides and delignifying the
substrata (Niemelä 1974, 1977; Ryvarden and Gilbertson
1994; Wagner and Fischer 2002; Decock et al. 2006; Cui and
Decock 2013; Brazee 2015; Cloete et al. 2016, de CamposSantana et al. 2016). The rot could be localized in the trunk
as a column of decay (Brazee 2015), in both fallen and in
standing dead trunks (Niemelä 1977; Campos-Santana et al.
2016). Branches of living trees (Niemelä 1974; Decock et al.
2006), dead, fallen, corticated branches and logs (Niemelä
1972) and dead stumps (Niemelä 1972; Decock et al. 2006;
Campos-Santana et al. 2016) are colonized and decayed.
The fungus penetrates the heartwood, causing heartrot (Niemelä 1974; Larsson et al. 2006), sometimes extending into
the sapwood (Niemelä 1977; Larsson et al. 2006). Decay
characteristics (i.e. colour, fragility and fragmentation) vary
between species (Niemelä 1972, 1974, 1977; Yombiyeni
et al. 2011; Luna et al. 2012; Campos-Santana et al. 2016).
Pathogenic species, such as P. tremulae or P. resupinatus are
usually associated with other basidiomycete species, pathogenic bacteria and basal fungi (Kallio 1972; Cloete et al.
2016). Phellinus tremulae is a common and harmful pathogen of aspen (Populus species), penetrating the heartwood
along dead branches (Niemelä 1974), but is also capable of
spreading through the sapwood (Larsson et al. 2006), forming conks around the decayed tissues (Jones 1998; Fig. 25).
Phellinus resupinatus is also a factor of Esca disease, causing white rot and decline of the cordons in vineyards (Cloete
et al. 2016), besides other symptoms caused by this disease
(Jayawardena et al. 2019a).
Hosts—Most species in the P. igniarius species complex are specialized to a single or few angiosperm genera
(Fischer and Binder 1995; Zhou et al. 2016), and only P.
piceicola has been reported from gymnosperms (Cui and
Dai 2012). Species of the P. igniarius species complex
have been recorded from various host genera, such as Acer,
Alnus, Arctostaphylos, Betula, Carpinus, Fagus, Fraxinus,
Laburnum, Picea, Populus, Prunus, Salix, Sorbus and Tilia
(Tomšovský et al. 2010; Brazee 2015; Zhou et al. 2016).
The members of other Phellinus sensu stricto lineages are
known from several additional angiosperm genera, such as
Artemisia, Astronium, Caesalpinia, Carya, Castanopsis,
Dimorphandra, Minquartia, Morus, Sacaglottis, Schinopsis, Quercus and Vitis (Lombard and Larsen 1985; Decock
et al. 2006; Yombiyeni et al. 2011; Cui and Decock 2013;
13
Fungal Diversity (2020) 103:87–218
Fig. 23 Nothophoma quercina on Malus micromalus a Malus micromalus (Crab-Apple tree). b Canker on the trunk. c, d appearance of
conidiomata on trunk. e longitudinal section through conidiomata. f
141
cross-section of conidiomata g, h conidiogenous cells. i, j conidia. k
upper view on PDA. l reverse view on PDA. Scale bars: d=1000 μm
e, f = 50μm g–j 10 μm
13
142
Fungal Diversity (2020) 103:87–218
Fig. 24 Phylogram generated
from maximum likelihood
analysis based on combined
LSU, ITS, tub2 and rpb2
sequence data of Nothophoma
species. Related sequences were
obtained from GenBank. Seventeen strains are included in the
combined sequence analyses.
Phoma herbarum (CBS 615.75)
and Vacuiphoma bulgarica
(CBS 357.84) was used as the
outgroup taxa. The best scoring
RAxML tree with a final likelihood value of − 5537.646741 is
presented. The matrix had 284
distinct alignment patterns, with
12.23% of undetermined characters or gaps. Estimated base
frequencies were as follows: A
= 0.238395, C = 0.241637, G =
0.276596, T = 0.243371; substitution rates AC = 0.975188,
AG = 4.004775, AT =
1.500008, CG = 0.519461, CT
= 10.843965, GT = 1.000000;
gamma distribution shape
parameter a = 1.764918. ML
bootstrap support value ≥ 50%
and BYPP ≥ 0.95 are shown
respectively near the nodes. Extype strains are in bold
de Campos-Santana et al. 2016; Vlasák and Vlasák 2017;
Salvador-Montoya et al. 2018).
Morphological based identification and diversity
Phellinus in a wider sense is morphologically heterogenous. The main features of the P. igniarius species complex
are the crusted pileal surface (except resupinate species), the
hymenial setae arising from the subhymenium (except specimens of “P. pseudoigniarius”, see Dai and Yang 2008; Zhou
et al. 2016), and the colourless, inamyloid, indextrinoid and
weakly cyanophilous basidiospores (Wagner and Fischer
2001; Dai 2010; Zhou et al. 2016). In many cases, the species separation in the complex is difficult when solely based
on morphological characters (Sell 2008). Host preference is
13
also widely used for delimiting species (Tomšovský et al.
2010).
Similar to members of the P. igniarius species complex,
other Phellinus species also have perennial basidiomata, but
differ in having distinctive macroscopical features (e.g. size
and shape of pores, rimose surface, cracked basidiocarps,
absence of pileus crust, see Dai et al. 2008; Bian et al. 2016;
Cloete et al. 2016; Vlasák and Vlasák 2017) or microscopic
characteristics (e.g. hyphal structure, the shape of setae,
basidiospore reaction in chemical solutions). For example,
P. bicuspidatus is unique in having a monomitic hyphal system with short bicuspid setae (Lombard and Larsen 1985;
Cloete et al. 2016). Members of the P. ellipsoideus group are
Fungal Diversity (2020) 103:87–218
Table 15 DNA barcodes
available for Nothophoma
143
Species
Isolate
LSU
ITS
tub2
RPB2
Nothophoma anigozanthi
N. arachidis-hypogaeae
N. brennandiae
CBS 381.91*
CBS 125.93
CBS 145912*
JW 1066
CBS 377.67
UTHSC:DI16-294
CBS 123395 *
CBS 140674 *
AUMC-12003*
MFLUCC 18–1600 *
MFLUCC18–1601
CBS 633.92
UTHSC:DI16-270
MCC 1082 *
CFCC 53928*
CFCC 53929
UTHSC: DI16-285*
GU238039
GU238043
MN823430
MN823429
GU238079
LN907437
GU238089
LN880537
KY996744
MH827028
MH827026
EU754127
LN907413
–
MN737828
MN737829
LN907428
GU237852
GU237771
MN823579
MN823578
GU237845
LT592943
FJ427025
LN880536
–
MH827007
MH827005
GU237900
LT592929
MF664467
MN737833
MN737834
LT592939
GU237580
GU237583
MN824753
MN824752
GU237611
LT593012
FJ427135
LN880539
–
MH853671
MH853669
GU237609
LT592998
MF664468
MN879295
MN879296
LT593008
KT389655
KT389656
MN824604
MN824603
KT389658
LT593082
KT389659
LT593073
–
MH853664
MH853662
KT389657
LT593067
–
MN879292
MN879293
LT593078
N. gossypiicola
N. infossa
N. macrospora
N. multilocularis
N. pruni#
N. quercina#
N. raii
N. spiraeae
N. variabilis
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
well-characterised by their weakly dextrinoid basidiospores
and hooked hymenial setae (Zhu et al. 2018).
There are several “Phellinus” species which have been
described solely on morphological features. The status of
these species should be critically re-evaluated based on
molecular evidence. Amongst these, certain species (e.g. P.
deuteroprunicola, P. eugeniae, P. formosanus, P. livescens,
P. prunicola, P. setulosus, P. tenuiculus, P. wahlbergii) may
belong to Phellinus sensu stricto (Gilbertson 1979; Chang
1995; Chang and Chou 1999, 2000; Robledo et al. 2003;
Wang et al. 2011; Rajchenberg et al. 2015; Campos-Santana
et al. 2016), but further studies are required to confirm their
placements.
Molecular based identification and diversity
In early molecular studies, the restriction fragment length
polymorphism (RFLP) data of enzymatically amplified
rDNA was used by Fischer (1995) to study the taxonomy of
P. igniarius and its closest relatives in Europe. Later, single
nuclear genes (ITS, Fischer and Binder 2004), or combined
datasets (ITS-tef1, Tomšovský et al. 2010; Zhou et al. 2016)
were used to investigate the species boundaries and phylogenetic relationships within the P. igniarius species complex.
Phylogenetic analyses by Brazee (2015) used ITS, LSU,
tef1 and rpb2, with isolates representing 13 species-level
lineages in the complex. Zhou et al. (2016) distinguished
15 species, five of which are described as new from China
and the USA. Based on our multigene analysis (Fig. 26), 16
species can be found in the P. igniarius species complex,
distributed throughout the Northern Hemisphere. Amongst
these, ten species are known from eastern Asia, eight from
Europe and seven from North America.
Phellinus caribaeo-quercicola was the first species
described from the “P. ellipsoideus group” based on molecular evidence (Decock et al. 2006). The nLSU-based phylogenetic analysis of Decock et al. (2006), have shown that
P. caribaeo-quercicola grouped close to the P. igniarius
species complex and some other Phellinus species (viz. P.
bicuspidatus, P. chaquensis and P. spiculosus). Later molecular taxonomic studies used combined datasets of various
nuclear markers. The combined analyses of nITS, nLSU, tef1
and rpb2 have confirmed the phylogenetic position of P. caribaeo-quercicola and five morphologically similar species
have been accepted in Phellinus sensu stricto (Yombiyeni
et al. 2011; Cui and Decock 2013; Campos-Santana et al.
2016; Zhu et al. 2018). Currently, this later group consists
of six species and mostly has tropical or subtropical distributions (Zhu et al. 2018).
Recommended genetic marker (genus level)—LSU
Recommended genetic markers (species level)—ITS, tef1,
rpb2
Accepted number of species—There are 479 epithets listed
in Index Fungorum (2020. However, most of the species
belong to other poroid Hymenochaetaceae genera, such
as Fomitiporia, Fomitiporella, Fulvifomes, Fuscoporia,
13
144
Fungal Diversity (2020) 103:87–218
Fig. 25 Phellinus igniarius. a causing white-rot decay on willow b–d basidiomes on living willow e, f hymenial setae g tramal skeletal hyphae
h basidiospores, Scale bars: e–h = 10 µm
Nothophellinus, Phellinidium, Phellinopsis, Phellinotus,
Phellopilus, Phylloporia, Porodaedalea, Sanghuangporus
and Tropicoporus (Wagner and Fischer 2001, 2002; Niemalä et al. 2001; Dai 2010; Drechsler-Santos et al. 2016;
Rajchenberg et al. 2015; Zhou et al. 2016). Based on molecular data, 30 species are accepted in Phellinus sensu stricto,
from among 16 species in the P. igniarius species complex
(Table 16; Fig. 26).
References—Tomšovský et al. (2010) (phylogeny, P. igniarius species complex, Europe), Brazee (2015) (phylogeny,
P. igniarius species complex, North America), Zhou et al.
(2016) (phylogeny, P. igniarius species complex), Zhu et al.
(2018) (phylogeny, P. ellipsoideus group)
91. Pseudoseptoria Speg., Anal. Mus. nac. B. Aires, Ser. 3
13: 388 (1910) [1911]
Background
Spegazzini (1910) introduced Pseudoseptoria as an
asexual genus typified with Pseudoseptoria donacicola.
Wijayawardene et al. (2012) placed the genus under Ascomycota, genera incertae sedis. Quaedvlieg et al. (2013)
placed the genus in Dothioraceae and this was accepted
by Thambugala et al. (2014). With LSU sequence data,
Crous et al. (2017) placed Pseudoseptoria to Saccotheciaceae. Wijayawardene et al. (2017a, b, 2018, 2020)
accepted this placement. Species of Pseudoseptoria are
recorded as pathogens on Poaceae (Quaedvlieg et al.
2013), impairing the photosynthetic process resulting in
yield loss.
13
Classification—Ascomycota, Pezizomycotina, Dothideomycetes, Dothideomycetidae, Dothideales, Saccotheciaceae
Type species—Pseudoseptoria donacicola Speg.
Distribution—Australia, Canada, India, Italy, New Zealand,
Poland, Russia, UK and USA (Dennis1986; Ginns 1986;
French 1989; Pennycook 1989; Merezhko 1991; Cunnington
2003; Mulenko et al. 2008; Kamal 2010; Farr and Rossman
2020).
Disease symptoms—halo spot, leaf blotch and stem speckle
Halo spot: Elliptical, tan to brownish-grey spots (<10mm
long) with a dark border surrounded by a prominent yellow
halo that can be observed on the leaf blade, sometimes covering the entire leaf blade. In older lesions, small pycnidia
may be visible (Slopek and Labun 1992; Carmona et al.
1996; Murray et al. 2013).
Leaf blotch: Brown flecks and frog-eye spots on leaf
blades can be observed in early spring, which enlarges to
straw-coloured blotches scattered with minute pycnidia.
These spots may drop out, leaving holes (Horst 2013).
Stem speckle: The disease occurs in the leaves, sheaths,
culms, and head spikes. The lesions are rectangular, ash
white, (1-2 mm long) with a brown, thin border. The lesion
is delimited by leaf veins and becomes distinct with a clear
boundary. The conidia formed on the lesions disperse by
wind and rain.
Pathogen biology, disease cycle and epidemiology
The pathogen is dispersed through spores in rain splash.
Infection requires an extended period of wetness. Spore
Fungal Diversity (2020) 103:87–218
germination and infection occur optimally at temperatures
between 15 and 25 °C. Spores produced in overwintering
crop debris serve as sources of primary inocula (Sinclair
and Dhingra1995). Further studies are needed regarding the
disease mechanisms and disease cycle.
Hosts—members of Poaceae are susceptible: Alopecurus
pratensis, Arrhenatheru melatius, Arundo donax, Bromus
species, Dactylis glomerata, Danthonia spicata, Elymus
alaskanus, Festu carubra, Hordeum vulgare, Panicum virgatum, Phleum species, Phragmites australis and Poa species
(Ginns 1986; Pennycook 1989; Shivas1989; Greuter et al.
1991; Merezhko 1991; Roane and Roane 1996; Gravert and
Munkvold 2002; Mulenko et al. 2008; Farr and Rossman
2020)
Morphological based identification and diversity
The genus is characterized by immersed, branched, septate, pale brown mycelium, pycnidial, solitary or linearly
aggregated, immersed, brown, globose, unilocular, thinwalled conidiomata of walls of pale brown cells of textura
angularis with distinct, central, circular ostioles. Conidiogenous cells are discrete, determinate or indeterminate,
hyaline, smooth, ampulliform with a prominent cylindrical
papilla and falcate. Conidia are fusoid, hyaline, aseptate,
guttulate, smooth and thin-walled, and acutely rounded at
each end (Sutton 1980; Quaedvlieg et al. 2013).
Molecular based identification and diversity
Quaedvlieg et al. (2013) revised the Septoria and septoria-like genera based on morphology and multi loci analyses and introduced two new species. Phylogenetic analysis
conducted by Crous et al. (2017) was based only on LSU
sequence data. In our analysis, we used LSU, ITS and rpb2
and obtained the same topology (Fig. 27).
Recommended genetic marker (genus level)—LSU
Recommended genetic markers (species level)—LSU, ITS
and rpb2
Accepted number of species—There are eight epithets listed
in Index Fungorum (2020). However, only three species
have DNA sequence data (P. collariana, P. donacis and P.
obscura) (Table 17).
References—Sutton (1980) (morphology); Quaedvlieg et al.
(2013), Crous et al. (2017) (morphology and phylogeny)
92. Stemphylium Wallr., Flora Cryptogamica Germaniae 2:
300 (1833)
Background
Stemphylium mainly comprises saprobes or weak plant
pathogens (Woudenberg et al. 2017). However, some species are primary pathogens causing leaf blight on various
crops, resulting in yield and economic losses (Hanse et al.
2015; Brahmanage et al. 2018). The asexual morph is a
145
dematiaceous hyphomycete while the sexual morph was
previously defined as Pleospora sensu stricto (Inderbitzin
et al. 2009; Woudenberg et al. 2017). Rossman et al. (2015)
recommended the use of Stemphylium over Pleospora which
has been followed by various authors (Hongsanan et al.
2017, 2020; Wijayawardene et al. 2018, 2020). Stemphylium
is one of the most important moulds human allergens in the
USA (Gutiérrez-Rodríguez et al. 2011). Brahmanage et al.
(2018) discussed the pathogenicity, disease severity, distribution and molecular phylogenetic affinities of pathogenic
isolates of Stemphylium.
Stemphylium leaf blight caused by S. versicarum was
identified as an emerging disease in New York, USA.
Sharma et al. (2020b) provided two genome resources
for two S. versicarum isolates from leaf blight of onion.
Genomic data allows for an understanding of the population biology, fungicide resistance, as well as development of
control strategies against the disease. Pathogenesis related
511 secreted proteins were predicted from S. lycopersici by
Zeng et al. (2018) which helps in understanding the roles of
proteins in host penetration and tissue necrosis. Stemphylium
loti secretes Tenuazonic acid, inhibiting the plant plasma
membrane H+-ATPase, which results in membrane potential
depolarization and eventually necrosis (Bjørk et al. 2019).
Su et al. (2019) fine-mapped the tomato grey spot resistance
gene Sm, in a 185kb region through a map-based cloning
strategy. Leach et al. (2020) identified a relationship between
thrips (Thrips tabaci) and S. vesicarium in the development
of Stemphylium leaf blight in onion.
Classification—Ascomycota, Pezizomycotina, Dothideomycetes, Pleosporomycetidae, Pleosporales, Pleosporaceae
Type species—Stemphylium botryosum Wallr.
Distribution—worldwide
Disease symptoms—Gray spot, Stemphylium leaf blight
(Leaf spot, defoliation, curling and bending of the leaf margins and stems)
Initial symptoms of the leaves are small, irregular, brown
spots. Generally, the spots gradually lighten and eventually
become greyish as they become necrotic and dry. When
severe, yellow spots can be seen throughout all leaves of the
plant and the heavily infected leaves die (Basallote-Ureba
et al. 1999, Crous et al. 2016; Brahmanage et al. 2018).
Hosts—Species are pathogenic on a wide range of hosts
including Amaryllidaceae, Asparagaceae, Fabaceae, Malvaceae, Poaceae, Rosaceae and Solanaceae
Pathogen biology, disease cycle and epidemiology
Species can survive as saprobes on crop residues, soil,
plant debris and on many alternative hosts and ascospores
become the primary inocula in the following season. Once
the disease is established during favourable conditions,
conidial production in primary lesions may occur, dispersing
13
146
13
Fungal Diversity (2020) 103:87–218
Fungal Diversity (2020) 103:87–218
◂Fig. 26 Phylogram generatedfrom RAxML analysis based on com-
bined ITS, LSU, Tef1-α and rpb2 sequence data of Phellinus species.
Related sequences were obtained from GenBank. Fifty-five strains are
included in the analyses, which comprised 3170 characters including
gaps. The tree was rooted with Phellinopsis conchata (DLL2009-149
and L-7601). Tree topology of the ML analysis was similar to the
Bayesian analysis.ML bootstrap values >50% and BYPP >0.80% are
shown respectively near the nodes
spores to healthy plants by wind and rain splashing. Environmental factors such as temperature and moisture are
key factors in disease development. Seedlings of plants can
transmit the diseases if they become infected in the nursery
(Basallote-Ureba et al. 1998, 1999; Boshuizen et al. 2004;
Zheng et al. 2010; Blancard 2012). However, to date, diseases and epidemiology such as factors affecting the disease
development, interactions with different hosts and genetics
of host resistance are poorly studied (Das et al. 2019).
Morphological based identification and diversity
Species can be distinguished from other hyphomycetes
in Pleosporaceae forming phaeodictyospores, based on
percurrent proliferation of its conidiophores and apically
swollen conidiogenous cells (Köhl et al. 2009). Simmons
(1967) established criteria for morphological identification
of various Stemphylium species and introduced Pleospora
herbarum as the sexual morph of the type species Stemphylium botryosum. However, Simmons (1985) subsequently
reclassified and reported Pleospora tarda as the sexual
morph of Stemphylium botryosum and Pleospora herbarum
as the sexual morph of Stemphylium herbarum (Moslemi
et al. 2017). Morphological features, such as size and time
of pseudothecial maturation, conidiophores and conidia and
ascospore shape and size can be considered as important
characteristics in species identification (Câmara et al. 2002;
Fig. 28).
Köhl et al. (2009) and Woudenberg et al. (2017) pointed
out that the lack of (ex-) type material of species and morphology-based species identifications without molecular
evidence make it difficult in determining correct species
nomenclature. Therefore, relying on morphological characters alone in identifying species is not recommended.
Molecular based identification and diversity
ITS (rDNA) and glyceraldehyde-3-phosphate dehydrogenase (gapdh) sequences were used by Câmara et al. (2002)
to confirm the monophyly of Stemphylium. In the extensive study of 110 Stemphylium strains from various hosts
and DNA sequence data of ITS, gapdh and tef1 loci and
the intergenic spacer between vmaA and vpsA, Inderbitzin
et al. (2009) identified 23 representatives derived from type
strains, while 40 strains remained unnamed. Woudenberg
147
et al. (2017) revised the genus and accepted 28 species,
synonymizing 22 names and proposing two new combinations based on combined analyses of the ITS, gapdh and
cmdA gene regions. Marin-Felix et al. (2019) introduced
three new species (S. rombundicum, S. truncatulae and S.
waikerieanum), while Brahmanage et al. (2018) introduced
S. dianthi based on multi loci phylogeny. In this study, we
reconstruct the phylogeny based on combined ITS, gapdh
and cmdA sequence data (Fig. 29).
Recommended genetic marker (genus level)—ITS
Recommended genetic markers (species level)—cmdA,
gapdh
Accepted number of species—There are 207 epithets listed
in Index Fungorum, however only 32 species have DNA
sequence data (Table 18).
References—Simmons (1967), Köhl et al. (2009) (morphology); Câmara et al. (2002), Inderbitzin et al. (2009), Moslemi et al. (2017), Woudenberg et al. (2017), Brahmanage
et al. (2019), Marin-Felix et al. (2019) (morphology and
phylogeny)
93. Thyrostroma Höhn., Sitzungsberichte der Kaiserlichen
Akademie der Wissenschaften Math.-naturw. Klasse Abt. I
120: 472 (1911)
Background
Thyrostroma belongs to Dothidotthiaceae of Pleosporales
in Dothideomycetes, Ascomycota (Hongsanan et al. 2020).
Thyrostroma was established by Höhnel (Höhnel 1911) and
is typified by T. compactum. Thyrostroma had been treated
as a synonym of Coryneum, Stegonsporium, Stigmina, and
Thyrococcum, Thyrostromella and Wilsonomyces (Höhnel
Höhnel 1911; Morgan-Jones 1971; Sutton and Pascoe 1989;
Sutton 1997; Index Fungorum 2020). Thyrostroma has been
reported as the asexual morph of Dothidotthia based on the
production of a hyphomycete state in culture (Ramaley
2005), however, there is no phylogenetic evidence to support
this link. With new morphological information and phylogenetic analyses, Thyrostroma and Dothidotthia species were
retained in separate genera (Crous et al. 2016; Marin-Felix
et al. 2017; Senwanna et al. 2019). Thyrostroma species are
pathogens, saprobes or endophytes associated with canker,
dieback and leaf spots in terrestrial habitats (Yuan and Old
1990; Marin-Felix et al. 2017; Senwanna et al. 2019). Species of Thyrostroma have been recorded from various plants,
however, host-specificity and pathogenic capacity of Thyrostroma has not yet been clarified.
Classification—Ascomycota, Pezizomycota, Dothideomycetes, Pleosporomycetidae, Pleosporales, Dothidotthiaceae
13
148
Table 16 DNA barcodes
available for Phellinus
Fungal Diversity (2020) 103:87–218
Species
Strain
ITS
LSU
tef1
rpb2
Phellinus alni
FP-134638-Sp
KU139167
KU139213
KU139330
KU139280
P. alni
BRNM 714865
GQ383730
–
GQ383840
–
P. amazonicus
MUCL 53036*
KU499940
KU376305
KU936772
–
P. amazonicus
MUCL 51478
KU499929
KU376294
KU936769
–
P. arctostaphyli
FP-94186-R
KU139145
KU139252
KU139350
KU139266
P. arctostaphyli
FP-94140-R
KU139143
KU139250
KU139348
KU139264
P. artemisiae
JV 1603/1-J*
KY230518
KY230518
–
–
P. austrosinensis
Dai 13680a*
–
KP027474
–
–
P. betulinus
NJB2009-FpG
KU139153
KU139248
KU139368
KU139311
P. betulinus
FP-105325-Sp
KU139154
KU139239
KU139369
KU139312
P. bicuspidatus
CBS 427.86*
MH861982
MH873674
–
–
P. caribaeo-quercicola
MUCL 46004*
HM635698
DQ127280
HM635726
–
P. caribaeo-quercicola
MUCL 46003
HM635697
DQ127279
HM635725
–
P. castanopsidis
CUI 10153*
JQ837944
JQ837956
KU936783
–
P. castanopsidis
CUI 10157
JQ837945
JQ837957
KU936784
–
P.chaquensis
MUCL 46742
–
DQ122396
–
–
P.chaquensis
CTES568170
MG242440
MG242445
–
–
P. ellipsoideus
MUCL 47867
KU954545
KU954540
KU936786
–
P. ellipsoideus
MUCL 45929
KU954544
DQ127283
KU936785
–
P. gabonensis
MUCL 52025*
HM635708
HM635690
HM635731
–
P. gabonensis
MUCL 52007
HM635718
HM635685
HM635729
–
P. igniarius
BRNM 714889
GQ383709
–
GQ383791
–
P. igniariusa
*Yang 67
JQ828880
–
KR013111
–
P. igniarius
CCBAS575
LN714586
–
–
LN714693
P. laevigatus
NJB2011-PLa1-F
KU139148
KU139241
KU139372
KU139305
P. laevigatus
BRNM 714867
GQ383778
–
GQ383856
–
P. lundellii
NJB2011-PLu-F
KU139185
KU139234
KU139337
KU139300
P. lundellii
NJB2011-GR1
KU139182
KU139232
KU139336
KU139301
P. monticola
Dai 5413*
JQ828889
–
KR013087
–
P. monticola
Cui 10482
JQ828888
–
KR013086
–
P. mori
Dai 8309/Dai 8310
FJ627259
HQ328535
–
–
P. nigricans
NJB2011-PA1-F
KU139169
KU139222
KU139340
KU139297
P. nigricans
FP-62186-T
KU139176
KU139227
KU139343
KU139290
P. orientoasiaticus
Cui 9753*
JQ828926
–
KR013079
–
P. orientoasiaticus
Cui 9727
JQ828921
–
KR013076
–
P. padicola
Cui 2257*
JQ828905
–
KR013073
–
P. padicola
Cui 2414
JQ828906
–
–
–
P. parmastoi
Dai 12558*
JQ828900
–
KR013089
–
P. parmastoi
TN-6432
KU139158
KU139245
KU139376
–
P. piceicola
Cui 10440*
JQ828908
–
–
–
P. piceicola
Cui 10455
JQ828910
–
KR013085
–
P. pomaceoides
JV 1403/4-J*
KR013069
–
KR013107
–
P. pomaceoidesb
SRM-158-Sp
KU139140
KU139210
KU139353
KU139267
P. pomaceus
TN-449
KU139142
KU139254
KU139352
KU139263
P. pomaceus
MJ 44/07
GQ383783
–
GQ383858
–
P. populicola
TN-526*
KU139179
KU139231
KU139333
KU139303
P. populicola
JV 0110/21
KR013062
–
KR013093
–
P. resupinatus
STE-U 7769*
KM523246
KM523251
–
–
P. spiculosus
CBS 345.63*
MH858307
MH869918
–
–
P. tremulae
NJB2011-PT1-F
KU139132
KU139201
KU139357
KU139276
P. tremulae
FP-135202-T
KU139134
KU139207
KU139359
KU139271
P. turbinatus
JV 1407/73-J
KT156687
–
–
–
P. vietnamensis
Cui 16434*
–
MG867716
MG867722
MG867719
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher strains are also
in bold
13
a
as P. pseudoigniarius
b
as PhellinusNA2
Fungal Diversity (2020) 103:87–218
149
Fig. 27 Phylogenetic tree generated by maximum likelihood analysis
of combined LSU, ITS and rpb2 sequence data. Fourteen strains are
included in the analyses, which comprised 2207 characters including gaps. The tree was rooted with Elsinoe veneta (CBS 164.29)
and Elsinoe phaseoli (CBS165.31). Tree topology of the ML analysis was similar to the BYPP analysis. The best scoring RAxML tree
with a final likelihood value of − 7330.368152 is presented. The
Table 17 DNA barcodes available for Pseudoseptoria
Species
Isolate
Pseudoseptoria collariana
P. donacis#
P. obscura
CBS 135104* KF251721
CBS 313.68
CBS 135103
LSU
ITS
rpb2
KF251218
KF252223
MH870852 MH859141
KF251722 KF251219 KF252224
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and
marked with an asterisk (*). Voucher strains are also in bold. Species
confirmed with pathogenicity studies are marked with #
matrix had 500 distinct alignment patterns, with 29.98% of undetermined characters or gaps. Estimated base frequencies were as follows: A = 0.250948, C = 0.235140, G = 0.278289, T = 0.235623;
substitution rates AC = 2.242594, AG = 3.171649, AT = 1.699638,
CG = 1.459509, CT = 8.754890, GT = 1.000000; gamma distribution shape parameter α = 0.601361 ML bootstrap values ≥ 65% and
BYPP ≥ 0.90 are shown respectively near the nodes
Type species—Thyrostroma compactum (Sacc.) Höhn
Distribution—Australia, Iran, Korea, Russia, USA,
Uzbekistan
Disease Symptoms—Thyrostroma canker, dieback and leaf
spots (Fig. 30a, b)
Hosts—Pathogens of Acanthophyllum sp., Astragalus sp.,
Capparis parvifiora, Celtis occidentalis, Cornus officinalis,
Echinops sp., Elaeagnus angustifolia, Ephedra equisetina,
Eucalyptus mannifera subsp. maculosa, Franseria sp., Halimodendron halodendron, Lycium barbarum, Morus alba,
Robinia pseudoacacia, Sambucus caerulea, Styphnolobium
13
150
japonicum, Tilia cordata, Ulmus pumila (Farr and Rossman
2020).
Morphological based identification and diversity
Thyrostroma species can be differentiated using conidial
dimensions and septation in aged conidia and molecular
phylogeny (Crous et al. 2016; Marin-Felix et al. 2017; Senwanna et al. 2019; Fig. 30). Senwanna et al. (2019) reported
the sexual morph of Thyrostroma in T. ulmicola for the first
time. The sexual morph is characterized by pseudothecial,
immersed, erumpent or superficial, uniloculate or multiloculate ascostromata, globose to subglobose ascomata, a
two-layered peridium, bitunicate, clavate asci, fusiform to
ellipsoidal, 1-septate, ascospores.
Molecular based identification and diversity
In the past, there has been no comprehensive phylogenetic
study in Thyrostroma and consequently, its taxonomy was
and still is mostly based on morphological characters. Based
on LSU sequence data, Thyrostroma clustered in a wellsupported clade within the Dothidotthiaceae (Marin-Felix
et al. 2017; Crous et al. 2019). The asexual morph and sexual
morph relationship were resolved by Senwanna et al. (2019)
by molecular evidence. To achieve correct generic and species identification and taxonomic placement, phylogenetic
studies using LSU, SSU, ITS, and tef1 were performed (Senwanna et al. 2019). This study reconstructs the phylogeny
using a combined LSU, SSU, ITS, and tef1 sequence dataset
(Fig. 31). The topology is in accordance with Marin-Felix
et al. (2017), Senwanna et al. (2019) and Hyde et al. (2020b).
Recommended genetic marker (genus level)—LSU
Recommended genetic markers (species level)—ITS, tef1,
rpb2 and tub2
LSU, ITS and tef1 are the common genetic markers used
in the identification of Thyrostroma species. Combined LSU,
SSU, ITS and tef1 genes provide a satisfactory resolution
for resolving species. Based on the comparison of ITS and
tef1gene regions, most species in Thyrostroma are not significantly different from one another, therefore, Senwanna
et al. (2019) suggested that rpb2, tub2 are reliable genes for
distinguishing species within Thyrostroma.
Accepted number of species—There are 27 epithets in Index
Fungorum (2020), however only 13 species have DNA
sequence data (Table 19).
References—Höhnel (1911), Yuan and Old (1990), Ramaley (2005) (morphology); Marin-Felix et al. (2017), Crous
et al. (2016, 2019), Senwanna et al. (2019) (morphology
and phylogeny).
13
Fungal Diversity (2020) 103:87–218
94. Wojnowiciella Crous, Hern.-Restr.& M.J. Wingf., Persoonia 34, 201 (2015)
Background
Wojnowiciella was introduced by Crous et al. (2015) to
include Wojnowiciella eucalypti which exhibited somewhat
similar morphological characteristics to Wojnowicia, such
as setose pycnidia, with ampulliform, enteroblastic, phialidic conidiogenous cells, but differed with apapillate conidiomata lacking setae and having dark brown conidia.
Classification—Ascomycota, Pezizomycota, Dothideomycetes, Pleosporales, Phaeosphaeriaceae
Type species—Wojnowiciella eucalypti Crous, Hern.-Restr.
& M.J. Wingf
Distribution—Australia (Hernandez-Restrepo et al. 2016),
China (Crous et al. 2015, Giraldo et al. 2017), Colombia
(Crous et al. 2015, Giraldo et al. 2017), New Zealand (Crous
et al. 2019), South Africa and Western Cape (Crous et al.
2016)
Disease symptoms—Leaf spots
Most species are reported as saprobes with the exception
of Wojnowiciella cissampeli, W. eucalypti and W. vibruni
which were isolated from leaves and twigs of Cissampelos capensis, Eucalyptus and Viburnum utile respectively
(Hernandez-Restrepo et al. 2016). Their pathogenicity or
disease symptoms are not indicated clearly and there is a
need to establish pathogenicity of these species.
Hosts—Cissampelos capensis, Dactylis sp., Eucalyptus
grandis, Rosa sp., Leptocarpus sp., Lonicera sp., Spartium
sp. and Viburnum utile (Farr and Rossman 2020).
Morphological based identification and diversity
Wojnowiciella was introduced to include species that
were phylogenetically distinct but morphologically similar to
Wojnowicia (Crous et al. 2015). Wojnowiciella is characterized by apapillate conidiomata without setae and dark brown
conidia. Some species of Wojnowiciella also produce hyaline
microconidia. Karunarathna et al. (2017) first reported the
sexual morph of W. dactylidis. Phookamsak et al. (2019)
transferred Wojnowicia rosicola to Wojnowiciella rosicola
based on morphology and phylogenetic analyses.
Molecular based identification and diversity
Wojnowiciella is a well-supported genus in the family
Phaeosphaeriaceae (Phookamsak et al. 2019). A combined
multiloci phylogeny of LSU, SSU, tef1 and ITS is used in
placing species of Wojnowiciella within Phaeosphaeriaceae.
To identify species within the genus ITS, LSU, rpb2 and
tef1 are used (Marin-Felix et al. 2019; Phookamsak et al.
2019). Here we provide an updated phylogenetic tree for
this genus (Fig. 32).
Fungal Diversity (2020) 103:87–218
151
Fig. 28 Stemphylium sp. a
Ascomata on host b Vertical
section through an ascoma c
immature and mature asci d
Pseudoparaphyses e Ascospores
f Ascospores in Indian ink.
Scale bars: b = 50 μm, c–f =
10 μm
Recommended genetic markers (genus level)—LSU
Recommended genetic markers (species level)—ITS, rpb2,
tef1
Accepted number of species—Nine species are accepted
with molecular data (Table 20).
References—Crous et al. (2015), Karunarathna et al. (2017),
Marin-Felix et al. (2019), Phookamsak et al. (2019) (morphology and phylogeny)
Updated genera
The following genera are updated due to the addition of
many new species during recent years.
95. Cladosporium Link, Mag. Gesell. naturf. Freunde, Berlin 7: 37 (1816) [1815]
Cladosporium Link, Mag. Gesell. naturf. Freunde, Berlin
7: 37 (1816) [1815]
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152
Fungal Diversity (2020) 103:87–218
Fig. 29 Phylogram generated from MP analysis based on combined
sequences of ITS, gapdh and cmdA sequences of all species of Stemphylium. Related sequences were obtained from GenBank. Thirty
three taxa are included in the analyses, which comprise 1936 characters including gaps, of which 1355 characters are constant, 271 characters are parsimony-uninformative and 310 characters parsimonyinformative. The parsimony analysis of the data matrix resulted in the
maximum of four equally most parsimonious trees with a length of
1112 steps (CI = 0.660, RI=0.721, RC = 0.476, HI = 0.340) in the
first tree. Single gene analyses were carried out and compared with
each species, to compare the topology of the tree and clade stability.
The tree was rooted with Alternaria abundance (CBS 534.83). MP
bootstrap support value ≥ 50% and BYPP ≥ 0.9 are shown respectively near the nodes. Ex-type strains are in bold
Background
Cladosporium belongs to Cladosporiaceae in the order
Capnodiales (Hyde et al. 2013). Established in 1816 with
C. herbarum as type species, Cladosporium is one of the
largest genera of dematiaceous hyphomycetes. Davidiella
was erected by Braun et al. (2003) to accommodate the
sexual morph of Cladosporium sensu stricto. Davidiella
was therefore recognized as a synonym of Cladosporium
as Cladosporium has priority over Davidiella at generic
rank, and is also the more commonly used name in literature (Bensch et al. 2012). Therefore, Cladosporiaceae took
preference over Davidiellaceae (Bensch et al. 2012). Cladosporium species have a worldwide distribution and can
be easily spread in the environment, because of their small
conidia. Cladosporium includes many important pathogens
causing leaf spots and stem rots of many plant hosts. For
example, Cladosporium fulvum is the causal agent of tomato
leaf mold (van Kan et al. 1991). Cladosporium species have
been recorded as endophytes and may have a positive effect,
for example, C. sphaerospermum was isolated from the roots
of Glycine max which can promote its growth (Hamayun
et al. 2009). Some species, such as C. herbarum, are also
known as common contaminants in clinical laboratories and
cause allergic lung disease (de Hoog et al. 2000). Several
species were also isolated from human respiratory samples
(Sandoval-Denis et al. 2016). Thirteen species are fungicolous (Heuchert et al. 2005; Sun et al. 2019) and have the
potential for biological control in agriculture and forestry
(Torres et al. 2017).
There have been studies towards understanding the
genetic components of Cladosporium. Cladosporium fulvum
is an important model species in the plant pathology study.
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Fungal Diversity (2020) 103:87–218
Table 18 DNA barcodes
available for Stemphylium
153
Species name
Isolate/specimen no
ITS
gapdh
cmdA
Stemphylium amaranthi
S. armeriae
S. astragali #
S. beticola#
S. botryosum#
S. callistephi
S. canadense
S. chrysanthemicola#
S. dianthi
S. drummondii
S. eturmiunum#
S. gracilariae
S. halophilum
S. ixeridis
S. lancipes
S. loti
S. lucomagnoense
S. lycii
S. lycopersici
S. majusculum
S. novae-zelandiae
S. paludiscirpi
S. rombundicum
S. sarciniforme
S. simmonsii#
S. solani#
S. symphyti
S. trifolii
S. triglochinicola
S. truncatulae
S. vesicarium#
S. waikerieanum
CBS 124746*
CBS 338.73
CBS 116583*
CBS 141024*
CBS 714.68*
CBS 527.50*
CBS 116602*
CBS 117255*
MFLU 19-0556*
CBS 346.83*
CBS 109845*
CBS 482.90*
CBS 337.73*
CBS 124748*
CBS 133314*
CBS 407.54*
CBS 116601*
CBS 125241*
CBS 122639*
CBS 717.68*
CBS 138295*
CBS 109842*
BRIP 27486*
CBS 110049*
CBS 133518*
CBS 116586*
CBS 115268*
CBS 116580*
CBS 718.68*
BRIP 14850*
CBS 715.68*
VPRI 21969*
KU850505
KU850511
KU850512
KU850520
KC584238
KU850539
KU850641
KU850640
MK500718
GQ395365
KU850541
KU850549
KU850553
KU850590
KU850596
KU850597
KU850629
KU850602
KU850611
KU850618
KU850631
KU850620
MK336819
KU850591
KU850637
KU850627
KU850643
KU850647
KU850648
MK336815
KU850565
MK336832
KU850652
KU850658
KU850659
KU850667
AF443881
KU850686
KU850782
KU850781
–
KU850687
KU850689
AF443883
KU850700
KU850737
KU850742
KU850743
KU850770
KU850748
KU850756
AF443891
KU850772
KU850762
MK336865
KU850738
KU850778
KU850768
KU850784
KU850788
KU850789
MK336861
KU850712
MK336878
KU850793
KU850799
KU850800
KU850808
KU850826
KU850828
KU850932
KU850931
MK500734
KU850829
KU850831
KU850839
KU850843
KU850881
KU850887
KU850888
KU850920
KU850893
KU850902
KU850909
KU850922
KU850911
MK336842
KU850882
KU850928
KU850918
KU850934
KU850938
KU850939
MK336838
KU850855
MK336855
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
Iakovidis et al. (2020) reported classical mapping strategies
for loci of tomato that response to sequence-monomorphic
effector Ecp5. Convergent evolution could be used for choosing different functional genes according to individual plant
breeding needs. Ge et al. (2019) showed that Cladosporium
species have the potential to be used in industrial processes.
They identified a new glucose oxidase gene CtgoxB from
C. tianshanense and suggested this could be a candidate for
the aquatic feed and detergent industries. Transcriptome
and proteome analyses of C. fulvuim showed that 14 out of
59 predicted proteases are expressed during in vitro and in
planta, of which nine belong to serine proteases and the rest
belong to metallo and aspartic proteases (Jashni et al. 2019).
This study also confirmed the presence of six proteases at
proteome level during the infection.
Grinn-Gofroń et al. (2019) developed and evaluated the
models of forecasting possibilities of airborne spore concentrations in 18 sites in six countries across Europe. The study
revealed the possibility of reliable prediction of fungal spore
levels using gridded meteorological data. They concluded
that these forecasting models can be used in the more timely
and efficient management of phytopathogenic and of human
allergic diseases. An environmentally isolated strain of C.
sphaerospoermum substantially enhanced plant growth,
early flowering and increase in crop yield after exposure in
vitro (Li et al. 2019). Pan et al. (2020) identified four new
hybrid polyketides (Cladosin L-O) from C. shaerospermum
which showed strong cytotoxicity, antifungal activity and
moderate antibacterial activity.
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Fig. 30 a, b Symptoms on Ulmus pumila caused by Thyrostroma
ulmicola (MFLU 16-1622); c, d Sporodochia on the host surface. e
Section of sporodochium. f Conidiogenesis and conidiogenous cells.
g–l Conidia. m Germinated conidium. Scale bars: d = 1000 µm, e =
200 µm, f–m = 30 µm
Classification: Ascomycota, Pezizomycotina, Dothideomycetes, Pleosporomycetidae, Capnodiales, Cladosporiaceae
Type species–Cladosporium herbarum (Pers.) Link
Distribution– Worldwide
Disease symptoms–Leaf spots, leaf blight, discolourations,
necrosis, or shot-hole symptoms, on stems and fruits, rots
Hosts– Cladosporium species occur on a wide range of
host plants including Asparagaceae, Asteraceae, Fabaceae,
Myrtaceae, Orchidaceae, Poaceae, Solanaceae and Vitaceae
(Farr and Rossman 2020). Some species can be hyperparasites of insects and fungi (Heuchert et al. 2005; Islam et al.
2019; Sun et al. 2019; Abdel-Baky 2000). These species can
cause allergies in humans such as sneezing, hives and also
can cause eye, ear and sinus infections (de Hoog et al. 2000).
13
Pathogen biology, disease cycle and epidemiology
Cladosporium survives in the soil or on plant debris and
produce spores during humid weather. Fungal spores germinate under high humidity and cool to warm temperatures.
Wind, rain and irrigation splash, workers, tools, and insects
readily disseminate spores (Jordan et al. 1990; Lan and Scherm 2003; Liu et al. 2019).
Fungal Diversity (2020) 103:87–218
155
Fig. 31 Phylogenetic tree generated by maximum likelihood analysis of LSU, SSU, ITS and tef1 sequence data of Thyrostroma species. Related sequences were obtained from GenBank. The tree was
rooted with Dothidotthia robiniae (MFLUCC 16-1175), D. symphoricarpi (CPC 12929) and Wilsonomyces carpophilus CBS 147.36).
Tree topology of the ML analysis was similar to the Bayesian analysis. The best scoring RAxML tree with a final likelihood value of
− 5556.187049 is presented. The matrix had 170 distinct alignment
patterns, with 18.30% of undetermined characters or gaps. Estimated
base frequencies were as follows: A = 0.243922, C = 0.240705, G
= 0.270231, T = 0.245142; substitution rates AC = 3.570314, AG
= 6.771467, AT 4.177691, CG = 1.603201, CT = 31.935571, GT
= 1.000000; gamma distribution shape parameter α = 0.602378.
Maximum likelihood bootstrap support values greater than 60% and
Bayesian posterior probabilities ≥ 0.95 (BYPP) are indicated above
the nodes. Ex-type (ex-epitype) and voucher strains are in bold
Morphological based identification and diversity
The asexual morph of Cladosporium species is characterized by a unique coronate structure of the conidiogenous
loci and conidia, consisting of the central convex dome
surrounded by a raised periclinal rim (Bensch et al. 2012;
Fig. 33), while ascomata of sexual morphs are identical
to those of Mycosphaerella (sect. Tassiana) (Braun et al.
2003). Historically, all types of dematiaceous hyphomycetes with amero- to phragmosporous conidia formed in
acropetal chains had been assigned to Cladosporium sensu
lato, resulting in the complication to resolve a natural classification of Cladosporium. Various mycologists proposed
natural genetic circumscriptions of Cladosporium (David
1997; Braun et al. 2003; Aptroot 2006). David (1997) found
the unique structure of conidiogenous loci and conidial hila
using scanning electron microscopy. Based on the genetic
circumscriptions, some cladosporioid groups, such as Fusicladium being non-coronate (Schubert et al. 2003), have
been excluded from Cladosporium s. str. Various Cladosporium species have been re-examined based on the new
generic concepts (Schubert and Braun 2004, 2005a, b, 2007;
Schubert 2005; Schubert et al. 2006; Braun and Schubert
2007; Braun et al. 2008). A polyphasic approach revealed
three major species complexes within Cladosporium, viz.
C. cladosporioides, C. herbarum and C. sphaerospermum
(Schubert et al. 2007; Dugan et al. 2008; Bensch et al. 2010;
Bensch et al. 2015). A modern monograph of the genus
treated 993 names of Cladosporium sensu lato, of which
169 were recognized in Cladosporium sensu stricto and others remain doubtful (Bensch et al. (2012).
Molecular based identification and diversity
The first molecular examination of Cladosporium-like
hyphomycetes based on ITS and SSU was carried out by
Braun et al. (2003), who confirmed the strong heterogeneity.
A new genus Davidiella was established to accommodate
the sexual morphs of Cladosporium sensu stricto species
which were previously assigned in Mycosphaerella. Aptroot
(2006) made a better circumscription of Davidiella after he
found species of Davidiella have ascospores with irregular
cellular inclusions, which are absent in Mycosphaerella.
Schoch et al. (2006) studied the phylogenetic relationships
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Table 19 DNA barcodes
available for Thyrostroma
Fungal Diversity (2020) 103:87–218
Species
Isolate/Voucher no
LSU
SSU
ITS
tef1
Thyrostroma compactum
T. cornicola
T. ephedricola
T. franseriae
CBS 335.37
CBS 141280*
MFLUCC 18-1125*
CBS 487.71*
CBS 700.70
MFLUCC 18-0787
MFLUCC 16-1186*
MFLU 16-1795*
MFLUCC 16-1170*
MFLUCC 18-1191*
MFLUCC 16-1160*
MFLUCC 16-1176
MFLUCC 16-1178*
MFLUCC 16-1180
MFLUCC 16-1188
MFLUCC 16-1172*
MFLUCC 16-1173
MFLUCC 16-1163
MFLUCC 16-1711
MFLUCC 16-1166*
MFLUCC 16-1164
KY905664
KX228300
MK765854
KX228301
KX228302
MK765857
MK751822
MK751823
MK751824
MK751825
MK751826
MK751827
MK751828
MK751829
MK751830
MK751840
MK751841
MK751834
MK751839
MK751846
MK751845
_
_
MK765853
_
_
MK765858
MK751767
MK751768
MK751769
MK751770
MK751771
MK751772
MK751773
MK751774
MK751775
MK751785
MK751786
MK751779
MK751784
MK751791
MK751790
KY905670
KX228248
MK765855
KX228249
KX228250
MK765856
MK751732
MK751733
MK751734
MK751735
MK751736
MK751737
MK751738
MK751739
MK751740
MK751750
MK751751
MK751744
MK751749
MK751756
MK751755
KY905681
KX228372
_
KY905680
KY905682
_
MK908022
MK908023
MK908024
MK908025
MK908026
MK908027
MK908028
MK908029
MK908030
MK908040
MK908041
MK908034
MK908039
MK908046
MK908045
T. jaczewskii
T. celtidis
T. moricola
T. lycii
T. robiniae
T. styphnolobii
T. tiliae
T. ulmicola
T. ulmigenum
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold
of 96 taxa of the Dothideomycetes using LSU, SSU, tef1 and
rpb2 gene data. Davidiella and its Cladosporium asexual
morphs were assigned to the family Cladosporiaceae in the
order Capnodiales, together with Mycosphaerellaceae. Crous
et al. (2007) delimited Cladosporium from morphologically
similar genera using their morphology and DNA phylogeny based on LSU. Several species were transferred to new
genera such as Hyalodendriella, Ochrocladosporium, Rachicladosporium, Rhizocladosporium, Toxicocladosporium and
Verrucocladosporium. Furthermore, C. castellanii was confirmed as a synonym of Stenella araguata, while the type
species of Stenella resided in Teratosphaeriaceae instead
of Mycosphaerellaceae. Schubert et al. (2007) performed a
comprehensive study of the C. herbarum species complex
based on both morphology and phylogenetic analysis with
five combined genes. Bensch et al. (2010) carried out species and ecological diversity within the C. cladosporioides
species complex. More than 200 isolates belonging to the
C. cladosporioides species complex were examined and
analyzed on the basis of ITS, actand tef1 gene regions. A
comprehensive monograph of Cladosporium sensu lato was
provided by Bensch et al. (2012) based on morphology and
combined ITS, act and tef1 sequence data. In their study, 993
names assigned to Cladosporium sensu lato are treated and
169 names were recognized in Cladosporium sensu stricto.
Bensch et al. (2015) introduced the three major species
13
complexes in Cladosporium, i.e. C. cladosporioides, C. herbarum and C. sphaerospermum, and 19 new species were
described. Razafinarivo et al. (2016) introduced a new species C. lebrasiae from milk bread rolls in France, Ma et al.
(2017) introduced six new soil-inhabiting Cladosporium
species from plateaus in China. Bensch et al. (2018) studied
Cladosporium species from indoor environments and introduced 16 new species. Several new Cladosporium species
including Cladosporium omanense (Halo et al. 2019), C.
passiflorae and C. passifloricola (Rosado et al. 2019) have
been introduced more recently. In this study, we reconstruct
the phylogeny of Cladosporium based on ITS, tef1 and act
sequenced data (Table 21; Fig. 34).
Recommended genetic marker (genus level)—ITS and LSU
Recommended genetic markers (species level)—act and tef1
(in a few cases tub2)
Accepted number of species–There are 844 epithets listed
in Index Fungorum (2020), however, 138 species have DNA
sequence data.
References–David (1997), Aptroot (2006), Schubert and
Braun (2004, 2005a, b, 2007), Schubert (2005), Schubert
et al. (2006), Braun and Schubert (2007), Braun et al. (2008)
(morphology), Braun et al. (2003), Schoch et al. (2006),
Bensch et al. (2010, 2012, 2015), Ma et al. (2017) (morphology and phylogeny)
Fungal Diversity (2020) 103:87–218
Fig. 32 Phylogram generated from MP analysis based on combined
sequences of ITS, LSU and tef1 sequences of all the accepted species of Wojnowiciella. Related sequences were obtained from GenBank. Ten taxa are included in the analyses, which comprise 2460
characters including gaps. Single gene analyses were carried out
and compared with each species, to compare the topology of the tree
and clade stability. The tree was rooted with Galiicola baoshanensis
(HKAS102234). The best scoring RAxML tree with a final likeli-
157
hood value of − 6772.195394 is presented. The matrix had 261 distinct alignment patterns, with 0.96% of undetermined characters or
gaps. Estimated base frequencies were as follows: A = 0.230657, C
= 0.279364, G = 0.252128, T = 0.237852; substitution rates AC =
1.388608, AG = 2.845402, AT = 2.389715, CG = 0.838197, CT =
7.220493, GT = 1.000000; gamma distribution shape parameter a
= 0.650385. ML and MP bootstrap support value ≥ 50% are shown
respectively near the nodes. Ex-type strains are in bold
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Fungal Diversity (2020) 103:87–218
Table 20 Details of Wojnowiciella, isolates used in the phylogenetic analyses
Species
Isolates
ITS
LSU
tef1
References
Wojnowiciella cissampeli
W. dactylidis
W. eucalypti
W. kunmingensis
W. leptocarpi
W. lonicerae
W. rosicola
W. spartii
W. viburni
CBS 141297*
MFLUCC 13-0735*
CBS 139904*
KUMCC18-0159*
CBS 115684*
MFLUCC 13-0737*
MFLUCC 15-0128*
MFLUCC 13-0402*
MFLUCC 12-0733*
KX228272
KP744470
KR476741
MK356380
KX306775
KP744471
MG828979
KU058719
KC594286
KX228323
KP684149
KR476774
MK356354
KX306800
KP684151
MG829091
KU058729
KC594287
LT990616
–
LT990617
MK359071
LT990615
–
–
–
–
Crous et al. (2016)
Liu et al. (2015)
Crous et al. (2015)
Phookamsak et al. (2019)
Hernandez-Restrepo et al. (2016)
Liu et al. (2015)
Phookamsak et al. (2019)
Li et al. (2015)
Wijayawardene et al. (2013)
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
Fig. 33 Cladosporium cladosporioides. a Conidiomata. b,
c, e Macro- and micronematous
conidiophores and conidia
chains. d. Secondary ramoconidia. f. Conidia. Scale bars: b,
c, e, f = 50 µm, d–g=10 µm
96. Colletotrichum Corda, in Sturm, Deutschl. Fl., 3 Abt.
(Pilze Deutschl.) 3(12): 41 (1831)
Background
Colletotrichum was introduced by Corda (1831), belonging to Glomerellaceae (Glomerellales, Sordariomycetes), and
is the sole member of this family (Maharachchikumbura et al.
2015, 2016; Hyde et al. 2020b). Species may occupy different
lifestyles, ranging from necrotrophy to hemibiotrophy as well
13
as endophytism (Crouch et al. 2014). Colletotrichum species
are important plant pathogens in both tropical and temperate
regions on many economically important crops (Hyde et al.
2009a, b, 2014; Cannon et al. 2012; Jayawardena et al. 2016b,
c). Based on recognized scientific and economic importance
this genus was voted the eighth most important plant pathogenic group in the world (Dean et al. 2012). Colletotrichum
species have been identified as endophytes (Manamgoda
Fungal Diversity (2020) 103:87–218
et al. 2013; Tao et al. 2013; Hyde et al. 2014; Jayawardena
et al. 2016c) and some are saprobes on dead plant material
(Photita et al. 2005; Jayawardena et al. 2016b). A few species have been identified to be pathogenic to humans (C.
coccodes, C. dematium, C. gloeosporioides (Natarajan et al.
2013)) and on insects (C. fioriniae (Damm et al. 2012b)).
Colletotrichum species are cosmopolitan in distribution and
show a diverse hosts association (Sharma et al. 2015). A host
plant genus can be infected by many Colletotrichum species
(Silva et al. 2012; Jayawardena et al. 2016c), and on the contrary, a single species of Colletotrichum can infect many host
plants (Damm et al. 2012a, b; Weir et al. 2012).
Correct species identification is important to understand the species diversity, plant pathology and quarantine, concerning human infections, agriculture, bio-control,
plant breeding, whole-genome sequencing, developing
and maintaining knowledge databases, bioprospecting and
understanding the evolutionary history (Jayawardena et al.
2016a). Due to a small number of distinctive morphological characters available for identification, misidentification
of these species is frequent. Misapplication and misidentification of species are also due to the misunderstanding of
their host-specific nature, ambiguous species boundaries and
incorrect sequences (Cannon et al. 2012; Hyde et al. 2014;
Jayawardena et al. 2016a). Therefore, having a stable taxonomy for the identification of these species is a significant
practical concern (Shenoy et al. 2007). To establish a natural
classification system, researchers strongly recommend the
use of geographical, ecological, morphological and genetic
data (Cai et al. 2009; Sharma and Shenoy 2016).
Species of Colletotrichum are extensively studied as model
organisms (Cannon et al. 2012; Hyde et al. 2014). This enables the researchers to understand the pathogen variation,
infection mechanism, evolution and population dynamics.
Pathogenicity genes of C. graminicola, C. higginsianum and
C. orbiculare have been studied (Huser et al. 2009; O’Connell
et al. 2012). Asakura et al. (2009) discovered the importance
of the pexophagy factor ATG26 for appressorium formation.
A total of 28 genome projects that include 25 different Colletotrichum species can be found; 15 of these strains are still at
the annotation stage and 13 are now at the ‘Fungal Standard
Draft’ stage (Carbú et al. 2019). These genomes will allow
further analysis of species diversity and evolutionary mechanisms and may serve as a foundation for genetic analysis
that leads to a greater understanding of interactions between
plants and fungal pathogens (Meng et al. 2020). Baroncelli
et al. (2016) studied four strains of C. acutatum and illustrated the plasticity of Colletotrichum genomes and showed
that major changes in host range are associated with relatively
recent changes in gene content. A genome of C. fructicola
from apple in China was compared with its reference genome,
which identified a number of strong duplication/loss events at
key phylogenetic nodes (Liang et al. 2018). Gan et al. (2019)
159
provided the updated genome for C. orbiculare and also
provided three draft genomes for C. trifolli, C. sidae and C.
spinosum. Colletotrichum higginsianum has a compartmentalized genome consisting of gene-sparse, transposable elements
dense regions with more effector candidate genes and genedense, TE-sparse regions harbouring conserved genes which
help the pathogen to generate genomic diversity (Tsushima
et al. 2019). Comparative genome analysis indicated that there
is a rapid evolution of pathogenicity genes in C. tanaceti (Lelwala et al. 2019).
Species of Colletotrichum can be used as biocontrol
agents and as biocatalysts (C. dematium, C. gloeosporioides, C. graminicola, C. lindemuthianum, C. orbiculare,
C.theobromicola, C. trifoli (Jayawardena et al. 2016b)).
Jayawardena et al. (2016b) discussed the importance of
secondary metabolites produced by species with relation to
pathogenesis, medicines, disease control and toxins.
Classification—Ascomycota, Pezizomycotina Sordariomycetes, Hypocreomycetidae, Glomerellales, Glomerellaceae
Type species—Colletotrichum lineola Corda, in Sturm,
Deutschl. Fl., 3 Abt. (Pilze Deutschl.) 3(12): 41 (1831)
Distribution—Worldwide
Disease symptoms—Anthracnose disease, red rot, crown and
stem rots, ripe rot, seedling blights and brown blotch.
Anthracnose disease symptoms include defined, often
sunken necrotic spots on leaves, stems, flowers or fruits and
may show a lot of variation depending on the host (35a−e).
Hosts—Pathogens on many host families including, Amaryllidaceae, Amaranthaceae, Anacardiaceae, Annonaceae,
Apiaceae, Apocynaceae, Araceae, Araliaceae, Arecaceae,
Asparagaceae, Asteraceae, Bignoniaceae, Campanulaceae,
Caricaceae, Crassulaceae, Cucurbitaceae, Euphorbiaceae,
Fabaceae, Iridaceae, Lamiaceae, Lauraceae, Malvaceae,
Melastomataceae, Menispermaceae, Moraceae, Myrtaceae,
Oleaceae, Olivaceae, Orchidaceae, Passifloraceae, Pinaceae,
Piperaceae, Plumbaginaceae, Poaceae, Podocarpaceae,
Polemoniaceae, Proteaceae, Ranunculaceae, Rosaceae,
Rubiaceae, Rutaceae, Solanaceae, Theaceae and Vitaceae.
Pathogen biology, disease cycle and epidemiology
For Colletotrichum biology, disease cycle and epidemiology see Cannon et al. (2012) and De Silva et al. (2017).
Morphological based identification and diversity
Due to the overlapping morphological characters, species delimitation based on morphology alone is hardly possible (Jayawardena et al. 2016b; Marin-Felix et al. 2017;
Fig. 35f–l).
Molecular based identification and diversity
Cai et al. (2009) proposed the use of a polyphasic
approach with multi-loci sequence analyses combined with
13
160
Table 21 DNA barcodes
available for Cladosporium
13
Fungal Diversity (2020) 103:87–218
Species
Isolate
ITS
tef1
act
Cladosporium acalyphae
C. aciculare
C. aerium
C. aggregatocicatricatum#
C. alboflavescens
C. allicinum
C. allii
C. angulosum
C. angustiherbarum
C. angustisporum
C. angustiterminale
C. antarcticum
C. anthropophilum
C. aphidis
C. arthropodii
C. asperulatum#
C. australiense
C. austroafricanum
C. austrohemisphaericum
C. basiinflatum#
C. chalastosporoides
C. chasmanthicola
C. chubutense
C. cladosporioides#
C. colocasiae#
C. colombiae
C. coloradense
C. crousii
C. cucumerinum#
C. cycadicola
C. delicatulum
C. domesticum
C. dominicanum
C. echinulatum#
C. endophyticum
C. entadae
C. europaeum
C. exasperatum
C. exile
C. fildesense
C. flabelliforme
C. flavovirens
C. floccosum#
C. funiculosum
C. fusiforme
C. gamsianum
C. globisporum#
C. grevilleae
C. halotolerans
C. hebeiense#
C. herbaroides#
CBS 125982*
CBS 140488*
CBS 143356*
CBS 140493*
CBS 140690*
CBS 121624*
CBS 101.81
CBS 140692*
CBS 140479*
CBS 125983*
CBS 140480*
CBS 690.92*
CBS 140685*
CBS 132182*
CBS 124043*
CBS 126340*
CBS 125984*
CBS 140481*
CBS 140482*
CBS 822.84*
CBS 125985*
CBS 142612*
CBS 124457*
CBS 112388*
CBS 386.64*
CBS 274.80B*
CBS 143357*
CBS 140686*
CBS 171.52*
CBS 137970*
CBS 126344*
CBS 143358*
CBS 119415*
CBS 123191
MFLUCC 17-0599*
MFLUCC 17-0919*
CBS 134914*
CBS 125986*
CBS 125987*
ChFC-554*
CBS 126345*
CBS 140462*
CBS 140463*
CBS 122129*
CBS 119414*
CBS 125989*
CBS 812.96*
CBS 114271*
CBS 119416*
JZB390001*
CBS 121626*
HM147994
KT600411
MF472897
KT600448
LN834420
EF679350
JN906977
LN834425
KT600378
HM147995
KT600379
EF679334
LN834437
JN906978
JN906979
HM147998
HM147999
KT600381
KT600382
HM148000
HM148001
KY646221
FJ936158
HM148003
HM148067
FJ936159
MF472945
LN834431
HM148072
KJ869122
HM148081
MF472955
DQ780353
JN906980
MG646956
MK347728
HM148056
HM148090
HM148091
JX845290
HM148092
LN834440
LN834416
HM148094
DQ780388
HM148095
HM148096
JF770450
DQ780364
MG516597
EF679357
HM148235
KT600509
MF473324
KT600547
LN834516
EF679425
JN906983
LN834521
KT600475
HM148236
KT600476
EF679405
LN834533
JN906984
JN906985
HM148239
HM148240
KT600478
KT600479
HM148241
HM148242
KY646227
FJ936161
HM148244
HM148310
FJ936163
MF473372
LN834527
HM148316
KJ869236
HM148325
MF473382
JN906986
JN906987
MG646988
HM148481
KT600607
MF473747
KT600645
LN834604
EF679502
JN906996
LN834609
KT600574
HM148482
KT600575
EF679484
LN834621
JN906997
JN906998
HM148485
HM148486
KT600577
KT600578
HM148487
HM148488
KY646224
FJ936165
HM148490
HM148555
FJ936166
MF473795
LN834615
HM148561
KJ869227
HM148570
MF473805
EF101368
JN906999
HM148298
HM148334
HM148335
MN233633
HM148336
LN834536
LN834512
HM148338
JN906988
HM148339
HM148340
JF770472
JN906989
MG516595
EF679432
HM148543
HM148579
HM148580
MN233632
HM148581
LN834624
LN834600
HM148583
EF101372
HM148584
HM148585
JF770473
EF101397
MG516593
EF679509
Fungal Diversity (2020) 103:87–218
Table 21 (continued)
161
Species
#
C. herbarum
C. hillianum
C. inversicolor
C. ipereniae
C. iranicum#
C. iridis#
C. kenpeggii#
C. langeronii
C. lebrasiae
C. licheniphilum
C. limoniforme#
C. longicatenatum
C. longissimum
C. lycoperdinum
C. macrocarpum#
C. magnoliigena
C. michoacanense
C. montecillanum
C. myrtacearum
C. needhamense
C. neerlandicum
C. neolangeronii
C. neopsychrotolerans
C. omanense
C. ossifragi
C. oxysporum#
C. paracladosporioides
C. parahalotolerans
C. paralimoniforme
C. parapenidielloides
C. parasubtilissimum
C. passiflorae#
C. passifloricola
C. penidielloides
C. perangustum#
C. phaenocomae
C. phlei#
C. phyllactiniicola
C. phyllophilum
C. pini-ponderosae
C. prolongatum
C. pseudiridis
C. pseudochalastosporoides
C. pseudocladosporioides#
C. psychrotolerans
C. pulvericola
C. puyae
C. ramotenellum#
C. rectoides
C. rhusicola
C. ruguloflabelliforme
Isolate
ITS
tef1
act
CBS 121621*
CBS 125988*
CBS 401.80*
CBS 140483*
CBS 126346*
CBS 138.40*
CBS 142613*
CBS 189.54*
CBS 138283*
CBS 125990*
CBS 140484*
CBS 140485*
CBS 300.96*
CBS 126347
CBS 121623*
MFLUCC 18-1559*
CBS 143588*
CBS 140486*
CBS 126350*
CBS 143359*
CBS 143360*
CBS 797.97*
CGMCC 3.18031*
SQUCC 13165*
CBS 842.91*
CBS 125991
CBS 171.54*
CBS 139585*
CGMCC 3.18103*
CBS 140487*
CBS 143361*
COAD 2135*
COAD 2140*
CBS 140489*
CBS 125996*
CBS 128769*
CBS 358.69*
CBS 126352*
CBS 125992*
CBS 124456*
CGMCC 3.18036*
CBS 116463*
CBS 140490*
CBS 125993*
CBS 119412*
CBS 143362*
CBS 274.80A*
CBS 121628*
CBS 125994*
CBS 140492*
CBS 140494*
EF679363
HM148097
HM148101
KT600394
HM148110
EF679370
KY646222
DQ780379
KJ596568
HM148111
KT600397
KT600403
DQ780352
HM148112
EF679375
MK347813
LT907958
KT600406
HM148117
MF473142
KP701887
MF473143
KX938383
MH725789
EF679381
HM148118
HM148120
KP701955
KX938392
KT600410
MF473170
MH682175
EF679440
HM148341
HM148345
KT600491
HM148354
EF679447
KY646228
JN906990
KJ596583
HM148355
KT600494
KT600500
EU570259
HM148356
EF679453
MK340864
LT907945
KT600504
HM148361
MF473570
KP701764
EF679516
HM148586
HM148590
KT600589
HM148599
EF679523
KY646225
EF101357
KJ596631
HM148600
KT600592
KT600598
EF101385
HM148601
EF679529
KT600412
HM148121
JF499837
JN906981
HM148150
HM148154
FJ936160
KX938394
EF679383
KT600415
HM148158
DQ780386
MF473226
KT600418
EF679384
HM148193
KT600440
KT600458
KX938400
MH716047
EF679459
HM148362
HM148364
KP701832
KX938409
KT600508
MF473593
MH724943
MH724948
KT600510
HM148365
JF499875
JN906991
HM148394
HM148398
FJ936164
KX938411
EF679461
KT600513
HM148402
JN906992
MF473648
KT600516
EF679462
HM148438
KT600539
KT600557
LT907961
KT600602
HM148606
MF473991
KP702010
MF473992
KX938366
MH716046
EF679535
HM148607
HM148609
KP702077
KX938375
KT600606
MF474018
MH729795
MH729800
KT600608
HM148610
JF499881
JN907000
HM148639
HM148643
FJ936167
KX938377
EF679537
KT600611
HM148647
EF101365
MF474075
KT600614
EF679538
HM148683
KT600637
KT600655
13
162
Table 21 (continued)
Fungal Diversity (2020) 103:87–218
Species
Isolate
ITS
tef1
act
C. rugulovarians
C. salinae
C. scabrellum
C. silenes
C. sinense
C. sinuatum
C. sinuosum
C. sloanii
C. soldanellae
C. sphaerospermum#
C. spinulosum
C. subcinereum
C. subinflatum
C. subtilissimum#
C. subuliforme#
C. succulentum
C. tenellum#
C. tenuissimum#
C. tianshanense
C. tuberosum
C. uredinicola
C. uwebraunianum
C. variabile#
C. varians
C. velox
C. verrucocladosporioides
C. verruculosum
C. versiforme
C. vicinum
C. vignae#
C. welwitschiicola
C. westerdijkiae
C. wyomingense
C. xanthochromaticum
C. xylophilum
Toxicocladosporium banksiae
CBS 140495*
CBS 119413*
CBS 126358*
CBS 109082*
CBS 143363*
CGMCC 3.18096*
CBS 121629*
CBS 143364*
CBS 132186*
CBS 193.54*
CBS 119907*
CBS 140465*
CBS 121630*
CBS 113754*
CBS 126500*
CBS 140466*
CBS 121634*
CBS 125995*
CGMCC 3.18033*
CBS 140693*
ATCC 46649
CBS 143365*
CBS 121635*
CBS 126362*
CBS 119417*
CBS 126363*
CGMCC 3.18099*
CBS 140491*
CBS 143366*
CBS 121.25
CBS 142614*
CBS 113746*
CBS 143367*
CBS 140691*
CBS 125997*
CBS 128215*
KT600459
DQ780374
HM148195
EF679354
MF473252
KX938385
EF679386
MF473253
JN906982
DQ780343
EF679388
LN834433
EF679389
EF679397
HM148196
LN834434
EF679401
HM148197
KX938381
LN834417
AY251071
MF473306
EF679402
HM148224
DQ780361
HM148226
KX938388
KT600417
MF473311
HM148227
KY646223
HM148061
MF473315
LN834415
HM148230
HQ599598
KT600558
JN906993
HM148440
EF679429
MF473675
KX938402
EF679464
MF473676
JN906994
EU570261
EF679466
LN834529
EF679467
EF679475
HM148441
LN834530
EF679479
HM148442
KT600656
EF101390
HM148685
EF679506
MF474102
KX938368
EF679540
MF474103
JN907001
EF101380
EF679542
LN834617
EF679543
EF679551
HM148686
LN834618
EF679555
HM148687
KX938364
LN834601
HM148712
MF474156
EF679556
HM148715
EF101388
HM148717
KX938371
KT600613
MF474161
HM148718
KY646226
HM148548
MF474165
LN834599
HM148721
LT821371
LN834513
HM148467
MF473729
EF679480
HM148470
JN906995
HM148472
KX938405
KT600515
MF473734
HM148473
KY646229
HM148303
MF473738
LN834511
HM148476
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
geographical, ecological and morphological data for reliable species delimitation. Application of this polyphasic
approach resulted in the delimitation of almost 200 species,
most of them belonging to species complexes such as acutatum, boninense and gloeosporioides. There is no universal
set of loci to use when identifying Colletotrichum species.
Cannon et al. (2012), Damm et al. (2012a, b, 2013, 2014,
2019, Liu et al. 2016) used ITS, gapdh, chs, act, his and tub2
(with some also gs or cal) for studying species within the
acutatum, boninense, dematium, destructivum, gigasporum,
orbiculare, spaethianum and truncatum species complexes,
while Weir et al. (2012) additionally applied gs, cal and sod2
13
within the gloeosporioides species complex. Hyde et al.
(2014), Jayawardena et al. (2016b), Marin-Felix et al. (2017)
used ITS, gapdh, chs, act and tub2 to differentiate the species. Using five loci for the whole genus gave similar results
to 6-7 loci used for the whole genus. In contrast, Crouch
et al. (2009b) applied ITS, sod2, apn2 and mat1/apn2, to
study the graminicola and caudatum species complexes. Use
of ApMat locus to delimit the species within gloeosporioides
species complex was emphasized by Silva et al. (2012) and
Sharma et al. (2015) as it provides a higher resolution when
compared to previously used loci. However, studies by Liu
et al. (2015, 2016) revealed that using this locus with other
Fungal Diversity (2020) 103:87–218
Fig. 34 Phylogram generated from Maximum Likelihood analysis
based on ITS, tef1 and act sequenced data. Bootstrap support values
≥ 75% and Bayesian posterior probabilities ≥ 0.95 are given near the
163
nodes. The ex-type (ex-epitype) and voucher strains are in bold. The
tree is rooted with Toxicocladosporium banksiae CBS 128215
13
164
Fig. 34 (continued)
13
Fungal Diversity (2020) 103:87–218
Fungal Diversity (2020) 103:87–218
loci would provide a satisfactory species delimitation within
the gloeosporioides species complex. For species delimitation, application of the Genealogical Concordance Phylogenetic Species Recognition (GCPSR) has proven to be a
powerful tool (Cai et al. 2009). Coalescent-based species
delimitation methods can also be used to infer the dynamic
of divergence, evolutionary process and the relationships
among species (McCormack et al. 2009, Liu et al. 2016).
Jayawardena et al. (2016b) provided the accepted species for
the genus with backbone trees for each species complex and with
notes for each accepted species. De Silva et al. (2017) reviewed
the lifestyles and how this can be applied to plant biosecurity.
Ariyawansa et al. (2015), Yan et al. (2015), Li et al. (2016), De
Silva et al. (2017), Hyde et al. (2020a, b), Marin-Felix et al.
(2017), Tibpromma et al. (2017, 2018), Samarakoon et al. (2018),
Bhunjun et al. (2019) have introduced new species based on morphology, phylogeny and GCPSR evidence. Damm et al. (2019)
introduced three new species complexes namely, dracaenophilum, magnum and orchidearum based on morphology and phylogeny. Cabral et al. (2020) based on pathological, morphological, cytogenomic, biochemical and molecular data, assigned the
previously known C. kahawae subsp. ciggario as a new species,
C. ciggario. At present, based on multi-loci phylogeny there are
14 species complexes. With 59 new species having been added
since the last treatment (Marin-Felix et al. 2017), here we present
an analysis using five loci (Table 21) for all Colletotrichum species (Fig. 36). From the studies conducted on this genus, it is clear
that the resolution of species differs depending on both locus
and species. Therefore, to select a better genetic marker and the
best secondary barcoding gene/genes is still an ongoing process.
Recommended genetic marker (genus level)—ITS
Recommended genetic markers (species level)—act, apmat,
apn2, cal, chs-1, gapdh, gs, his, mat1/apn2, sod2, and tub2.
Accepted number of species—There are 903 epithets listed
in Index Fungorum (2020), however, 247 species with
molecular data are treated as accepted (Table 22).
References—Cai et al. (2009) (polyphasic approach); Hyde
et al. (2009a, b) (morphology and accepted species); Cannon
et al. (2012) (A review and an updated account of the genus);
Crouch et al. (2009a, b, c, 2014), Damm et al. (2009, 2012a,
b, 2013, 2014, 2019), Weir et al. (2012) (morphology and
phylogeny); Hyde et al. (2014), Jayawardena et al. (2016b),
Marin-Felix et al. (2017) (accepted number of species).
97. Mucor Fresen., Beitr. Mykol. 1: 7 (1850)
Background
Mucor belongs to the order Mucorales, which is among
one of the most studied groups of early diverging lineages
of fungi. The genus has the largest number of species within
the order and half of the sequences submitted to GenBank
for Mucorales are of Mucor (Hoffmann et al. 2013; Spatafora et al. 2016; Hyde et al. 2014; Nguyen and Lee 2018).
165
Mucor belongs to the phylum Mucoromycota, subphylum
Mucoromycotina, class Mucoromycetes, order Mucorales
and family Mucoraceae (Wijayawardene et al. 2018, 2020).
It was described by Fresenius in 1850 and the type species
is Mucor mucedo. Recent molecular studies of mucoralean
species have indicated that Mucor is polyphyletic (Nguyen
et al. 2017). However, even with definite results showing the
polyphyly of Mucor, few clear lineages within Mucor are recognized. Some of these lineages share innate characteristics,
such as sporangium size and branching of tall sporangiophores and the morphology is still widely used in current taxonomy (Walther et al. 2013). Analysis of internal transcribed
spacer (ITS) and large subunit (LSU) rDNA sequence data of
several mucoralean species, showed that some Mucor species
with curved sporangiophores grouped with species of Backusella and hence was transferred to Backusella (Walther et al.
2013; Nguyen et al. 2017). Mucor species are commonly isolated from soil, dung, insect, and fruits (Benny 2008). Some
species are of biotechnological importance such as biofuel,
enzyme, terpernoid production and biotransformation while
other species cause mucoromycosis in immunosuppressed
humans (Nguyen et al. 2017; Steve et al. 2018; Morin-Sardin et al. 2017). Comparative analyses of five Mucor species
based on their lifestyles (M. fuscus and M. lanceolatus (used
for cheese production), M. circinelloides and M. racemosus
(opportunistic pathogens) and M. endophyticus (an endophyte)) revealed the core transcriptome comprising 5566
orthogroups included genes potentially involved in secondary
metabolism. Due to the wide taxonomic range investigated,
the five transcriptomes also displayed specificities that can
be linked to the different lifestyles, such as differences in
the composition of transcripts identified as virulence factors
or carbohydrate transporters. Research on this genus has
changed its course to identify the link between genetic and
biological data, especially in terms of lifestyle and adaptations to a given habitat (Lebreton et al. 2019) (Figs. 37, 38).
Classification—Zygomycota, Mucoromycotina, Mucoromycetes, Mucorales, Mucorineae, Mucoraceae
Type species—Mucor mucedo Fresen.
Distribution—Worldwide
Disease symptoms—Mucor rot and soft rot
Mucor species especially M. fragilis, M. irregularis,
M. piriformis and M. racemosus often cause postharvest
diseases such as Mucor rot and soft rot. The initial symptoms of Mucor rot are similar to plant diseases caused by
green mold, blue mold, and sour mold. The infected tissue becomes soft and watery. The lesions turn light to dark
brown and as the infection progresses, white or shiny grey
sporangiophores form at the lesions. Fungal growth spreads
across the whole host and masses of sporangiophores bearing black to pale brown sporangia are observed. Decaying
fruits become “juicy” within which are abundant spores of
13
166
Fungal Diversity (2020) 103:87–218
the fungus (Li et al. 2014; Saito et al. 2016). Ito et al. (1979)
found that three species of fruit flies namely Certitis capitata, Dacus cucurbitae and D. dorsalis, can transmit Mucor
rot in guava.
Soft rot caused by Mucor racemosus results in watersoaked appearance followed by a softening of the infected
part. When the disease progresses growth of white mycelium
and brownish to grey sporangia can be observed. Finally, the
infected tissue is broken down and disintegrates in a watery
rot (Kwon and Hong 2005; López et al. 2016).
Fig. 36 Phylogram generated from MP analysis based on combined ▸
sequences of ITS, gapdh, chs, act and tub2 sequences of all species of
Colletotrichum with molecular data. Related sequences were obtained from
GenBank. Two hundred and fourty nine taxa are included in the analyses,
which comprise 2296 characters including gaps, of which 868 characters
are constant, 295 characters are parsimony-uninformative and 1133 characters parsimony-informative. The parsimony analysis of the data matrix
resulted in the maximum of ten equally most parsimonious trees with a
length of 10088 steps (CI = 0.283, RI=0.840, RC = 0.237, HI = 0.717)
in the third tree. Single gene analyses were carried out and compared with
each species, to compare the topology of the tree and clade stability. The
tree was rooted with Monilochaetes infuscans (CBS 869.96) and M. populi
(CBS 139623). MP bootstrap support value ≥ 50% and BYPP ≥ 0.9 are
shown respectively near the nodes. Ex-type strains are in bold
Fig. 35 Colletotrichum sp. a Chilli anthracnose symptoms b Crown rot of
strawberry c Leaf blight of Cannas sp. d, e strawberry anthracnose symptoms f, g Conidiomata and spore mass h Conidiophore i Setae j Conidiogenous cells and curved conidia k Conidia of C. gloeosporioides l Appressoria.
Phylogram generated from RAxML analysis based on combined sequences
of ITS and LSU of Mucorand Backusella species. Eighty-one taxa were used
for the analysis, which consisted 1256 characters includinggaps. The tree is
rooted using Backusella lamprospora (CBS 195.28), and B. grandis (CBS
186.87). Likelihoodof the best scoring ML tree was -16174.718247. The
concatenated matrix contained 657 distinct alignmentpatterns with 22.27%
of undetermined characters or gaps. Estimated base frequencies were as follows; A =0.302146, C = 0.168433, G = 0.219872, T = 0.309549; substitution rates AC = 0.776817, AG = 3.154911, AT =1.674079, CG = 0.632500,
CT = 4.808262, GT = 1.000000; gamma distribution shape parameter α =
0.291909.Type species in the dataset are indicated using T. Maximum likelihood RAxML bootstrap support value ≥ 70%and Bayesian posterior probabilities ≥ 0.70 are shown near the nodes (ML/BYPP). – indicates bootstrap
supportvalues lower than 70% and * shows unrecovered branching
13
Fungal Diversity (2020) 103:87–218
167
13
168
Fungal Diversity (2020) 103:87–218
Fig. 36 (continued)
Hosts—Wide host range including, Actinidia deliciosa,
Citrus reticulata, Dioscorea species, Fragaria × ananassa,
Mangifera indica, Manihot esculenta, Prunus species, Psidium guajava, Solanum melongena, Solanum lycopersicum
and Vitis species (Farr and Rossman 2020).
13
Pathogen biology, disease cycle and epidemiology
The pathogen reproduces asexually. Mucor rot often
develops by infecting punctured wounds and cracks on the
surface of the fruit, stem end or calyx of the host. In the
early stages of the infection, the fruit becomes soft and
Fungal Diversity (2020) 103:87–218
169
Table 22 DNA barcodes available for Colletotrichum, isolates used in the phylogenetic analyses
Species name
Isolate no
ITS
gapdh
chs-1
act
tub2
Complex
Colletotrichum abscissum#
C. acerbum
C. acidae
C. acutatum#
C. aenigma#
C. aericola#
C. aeschynomenes#
C. agaves
C. alcornii
C. alatae#
C. alienum#
C. americae-borealis#
C. annellatum
C. anthrisci
C. antirrhinicola
C. aotearoa
C. araceaerum
C. arboricola#
C. artocarpicola#
C. arxii
C. asianum#
C. atractylodicola
C. australe
C. axonopodi
C. beeveri
C. baltimorense
C.bidentis
C. bletillum
C. boninense#
C. brasiliense
C. brassicicola
C. brevisporum#
C. brisbaniense
C. bryoniicola
C. cacao#
C. cairnsense#
C. camelliae#
C. camelliae-japonicae
C. carthami#
C. catinaense#
C. cattleyicola
C. cariniferi
C. caudatum
C. caudasporum
C. cereale#
C. changpingense#
C. chlorophyti#
C. chiangraiense
C. chrysanthemi#
C. chrysophillum
COAD 1877*
CBS 128530*
MFLUCC 17-2659*
CBS 112996*
ICMP 18608*
CGMCC 3.19667*
ICMP 17673
CBS 118190*
IMI176619*
CBS 304.67*
ICMP 12071*
CBS 136232*
CBS 129826*
CBS 125334*
CBS 102189*
ICMP 18537*
CGMCC 3.14982*
CBS 144795*
MFLUCC 18-1167*
CBS 132511*
ICMP 18580*
CGMCC 3.18761*
CBS 116478*
IMI 279189/279189AA
CBS 128527*
BPI892771*
COAD 1020*
CGMCC 3.15117*
CBS 123755*
CBS 128501*
CBS 101059*
BCC 38876*
CBS 292.67*
CBS 109849*
CBS 119297*
BRIP 63642*
CGMCC3.14925*
CGMCC3.18118*
SAPA100011*
CBS 142417*
CBS 170.49*
MFLUCC 14-0100*
CBS 131602*
CGMCC 3.15106*
CBS 129663*
MFLUCC 15-0022*
IMI 103806*
MFLUCC 14-0119*
IMI 364540*
URM7368*
KP843126
JQ948459
MG996505
JQ005776
JX010244
MK914635
JX010176
DQ286221
JX076858
JX010190
JX010251
KM105224
JQ005222
GU227845
KM105180
JX010205
KX853166
MH817944
MN415991
KF687716
JX010196
KR149280
JQ948455
EU554086
JQ005171
JX076866
KF178481
JX625178
JQ005153
JQ005235
JQ005172
JN050238
JQ948291
KM105181
MG600772
KU923672
KJ955081
KX853165
AB696998
KY856400
MG600758
MF448521
JX076860
JX625162
JQ005774
KP683152
GU227894
MF448522
JQ948273
KX094252
KP843129
JQ948790
MH003691
JQ948677
JX010044
MK935455
JX009930
KP843132
JQ949120
MH003694
JQ005797
JX009774
MK935541
JX009799
KP843141
JQ949780
MH003697
JQ005839
JX009443
MK935374
JX009483
KP843135
JQ950110
MH003700
JQ005860
JX010389
MK935498
JX010392
JX009990
JX010028
KM105579
JQ005309
GU228237
KM105531
JX010005
KX893585
MH817950
MN435568
KF687843
JX010053
KR259334
JQ948786
JX009837
JX009882
KM105294
JQ005396
GU228335
KM105250
JX009853
JX009471
JX009572
KM105434
JQ005570
GU227943
KM105390
JX009854
KX893577
MH817956
MN435569 MN435570
KF687780 KF687802
JX009867 JX009584
KR259333 KR132243
JQ949116 JQ949776
JX010383
JX010411
KM105504
JQ005656
GU228139
KM105460
JX010420
KX893581
MH817962
MN435567
KF687881
JX010406
KU058178
JQ950106
JQ005258
JQ005345
JQ005605
KF178506
KC843506
JQ005240
JQ005322
JQ005259
JN050227
JQ948621
KM105532
MG600832
KU923704
KJ954782
KX893584
KF178530
acutatum
acutatum
truncatum
acutatum
gloeosporioides
gloeosporioides
gloeosporioides
singleton
caudatum
gloeosporioides
gloeosporioides
destructivum
boninense
dematium
destructivum
gloeosporioides
singleton
acutatum
gloeosporioides
gigasporum
gloeosporioides
destructivum
acutatum
singleton
boninense
caudatum
orbiculare
spaethianum
boninense
boninense
boninense
magnum
acutatum
destructivum
magnum
acutatum
gloeosporioides
boninense
acutatum
boninense
orchidearum
singleton
caudatum
caudatum
graminicola
gloeosporioides
singleton
gigapsorum
acutatum
gloeosporioides
JQ005519
KF178602
JX625207
JQ005588
JQ005669
JQ005606
JN050244
JQ949942
KM105461
MG601039
KU923688
KJ955230
KX893580
AB696992
KY856224 KY856136 KY855971 KY856482
MG600819 MG600866 MG600963 MG601025
MH351274
KC843512
KF178578
KC843542
JQ005327 JQ005501
JQ005409 JQ005583
JQ005346 JQ005520
JN050216
JQ948952 JQ949612
KM105251 KM105391
MG600878 MG600976
KU923710 KU923716
KJ954363
KX893576
KC843526
JQ005795 JQ005837
KP852469 KP852449 KP683093
GU228286 GU228384 GU227992
MH376383
JQ948603 JQ948934 JQ949594
KX094183 KX094083 KX093982
JX625190
JQ005858
KP852490
GU228188
MH351275
JQ949924
KX094285
13
170
Fungal Diversity (2020) 103:87–218
Table 22 (continued)
Species name
#
C. ciggaro
C. circinans
C. citri
C. citricola#
C. clidemiae
C. cliviicola#
C. cobbittiense
C. coccodes#
C. coelogynes
C. colombiense
C. condaoense
C. conoides#
C. constrictum
C. cordylinicola#
C. cosmi
C. costaricense
C. curcumae#
C. cuscutae
C. cymbidiicola#
C. dacrycarpi
C. dematium#
C. destructivum#
C. doitungense
C. dracaenophilum#
C. duyunensis
C. echinochloae
C. eleusines
C. endophytica#
C. endophytum
C. eremochloae#
C. eriobotryae#
C. eryngiicola
C. excelsum-altitudinum
C. euphorbiae
C. falcatum#
C. feijoicola
C. fioriniae#
C. fructi
C. fructicola#
C. fructivorum#
C. fuscum#
C. fusiforme
C. gigasporum#
C. gloeosporioides#
C. godetiae#
C. graminicola#
C. grevilleae
C. grossum#
C. guajavae
C. guizhouensis
13
Isolate no
ITS
gapdh
chs-1
act
tub2
Complex
ICMP 18539*
CBS 221.81
CBS 134233*
CBS 134228*
ICMP 18658*
CBS 125375*
BRIP 66219a*
CBS 369.75*
CBS 132504*
CBS 129818*
CBS 134299*
CAUG17*
CBS 128504*
MFU 09-0551*
CBS 853.73*
CBS 330.75*
IMI 288937*
IMI 304802*
IMI 347923*
CBS 130241*
CBS 125.25*
CBS 136228*
MFLUCC 14-0128*
CBS 118199*
CGMCC 3.15105*
MAFF 511473*
MAFF 511155*
MFLUCC 13–0418*
CGMCC 3.15108 *
CBS 129661*
GLMC 1935*
MFLUCC 17-0318*
CGMCC 3.15130*
CBS 134725*
CBS 147945*
CBS 144633 *
CBS 128517*
CBS 346.37*
ICMP 18581*
CBS 133125*
CBS 133701*
MFLU 13-0291*
CBS 133266*
CBS 112999*
CBS 133.44*
M 1.001*
CBS 132879*
CAUG7*
IMI 350839*
CGMCC 3.15112*
JX010230
GU227855
KC293581
KC293576
JX010265
MG600733
MH087016
HM171679
MG600713
JQ005174
MH229914
KP890168
JQ005238
JX010226
JQ948274
JQ948180
GU227893
JQ948195
JQ005166
JQ005236
GU227819
KM105207
MF448524
JX519222
JX625160
AB439811
JX519218
KC633854
JX625177
JX519220
MF772487
KY792726
HM751815
KF777146
JQ005772
MK876413
JQ948292
GU227844
JX010165
JX145145
KM105174
KT290266
KF687715
JQ005152
JQ948402
JQ005767
KC297078
KP890165
JQ948270
JX625158
JX009966
GU228247
KC293741
KC293736
JX009989
MG600795
MH094133
HM171673
MG600776
JQ005261
MH229920
KP890162
JQ005325
JX009975
JQ948604
JQ948510
GU228285
JQ948525
JQ005253
JQ005323
GU228211
KM105561
MH049480
JX546707
KC843515
JX009800
GU228345
KY856138
KC293792
JX009877
MG600850
MH094135
JQ005796
MG600836
JQ005348
MH229926
KP890156
JQ005412
JX009864
JQ948935
JQ948841
GU228383
JQ948856
JQ005340
JQ005410
GU228309
KM105277
JX009523
GU227953
KY855973
KC293616
JX009537
MG600939
MH094134
HM171667
MG600920
JQ005522
JX010434
GU228149
KC293661
KC293656
JX010438
MG601000
MH094137
JQ005859
MG600980
JQ005608
MH229923
KP890174
JQ005672
JX010440
JQ949925
JQ949831
GU228187
JQ949846
JQ005600
JQ005670
GU228113
KM105487
MH351277
JX519247
JX625187
gloeosporioides
dematium
acutatum
boninense
gloeosporioides
orchidearum
gloeosporioides
singleton
dracaenophilum
boninense
boninense
gloeosporioides
boninense
gloeosporioides
acutatum
acutatum
truncatum
acutatum
boninense
boninense
dematium
destructivum
boninense
dracaenophilum
caudatum
graminicola
graminicola
gloeosporioides
graminicola
graminicola
acutatum
dematium
dracaenophilum
singleton
graminicola
boninense
acutatum
dematium
gloeosporioides
gloeosporioides
destructivum
truncatum
gigasporum
gloeosporioides
acutatum
graminicola
gloeosporioides
gloeosporioides
acutatum
spaethianum
JX519230
JX519226
KP890144
JQ005586
HM470234
JQ949595
JQ949501
GU227991
JQ949516
JQ005514
JQ005584
GU227917
KM105417
MH376385
JX519238
KC843530
JX519234
KF306258
KC843533
JX519228 JX519236
MF795423 MN191653 MN191648
KY792723 KY792720 KY792717
KC843502
KC843548
KF777131 KF777128 KF777125
JQ005793 JQ005835
MK876475
MK876466
JQ948622 JQ948953 JQ949613
GU228236 GU228334 GU227942
JX010033 JX009866 FJ907426
KC832854
KC843521
JX519243
JX625206
JX519245
MF795428
KY792729
JX625211
KF777247
JQ005856
MK876507
JQ949943
GU228138
JX010405
JX145196
KM105524 KM105244 KM105384 KM105454
KT290255 KT290253 KT290251 KT290256
KF687822 KF687761
KF687866
JQ005239 JQ005326 JQ005500 JQ005587
JQ948733 JQ949063 JQ949723 JQ950053
JQ005788 JQ005830 JQ005851
KC297010 KC296987 KC296941 KC297102
KP890159 KP890153 KP890141 KP890171
JQ948600 JQ948931 JQ949591 JQ949921
KC843507
KC843536 JX625185
Fungal Diversity (2020) 103:87–218
171
Table 22 (continued)
Species name
Isolate no
ITS
C. hanaui
C. hebeiense#
C. hedericola
C. helleniense#
C. henanense#
C. hemerocallidis
C. higginsianum#
C. hippeastri
C. horii#
C. hystricis#
C. hsienjenchang
C. incanum
C. indonesiense
C. insertae
C. jacksonii
C. jasminigenum
C. javanense#
C. jiangxiense
C. jinshuiense#
C. jishouense
C. johnstonii
C. kahawae#
C. kakivorum#
C. karstii#
C. kinghornii
C. laticiphilum#
C. lauri
C. ledebouriae
C. lentis#
C. liaoningense#
C. lilii
C. lini
C. limetticola
C. limonicola#
C. lindemuthianum#
C. lineola#
C. liriopes#
C. lobatum
C. lupini#
C. magnisporum
C. makassarense#
C. magnum
C. malvarum
C. melonis#
C. menispermi
C. metake
C. merremiae
C. miscanthi
C. musae#
C. musicola#
MAFF 305404*
MFLUCC13–0726*
MFLU 15-0689*
CBS 142418*
CGMCC 3.17354*
CDLG5
IMI 349061*
CBS 125376*
NBRC 7478*
CBS 142411*
MAFF 243051
ATCC 64682*
CBS 127551*
MFLU 15-1895*
MAFF 305460*
CGMCC LLTX-01*
CBS 144963a*
CGMCC 3.17363*
CGMCC 3.18903*
GMBC0209*
CBS 128532*
IMI 319418*
KCTC 46679*
CORCG6*
CBS 198.35*
CBS 112989*
MFLUCC 17-0205*
CBS 141284*
CBS 127604*
CGMCC 3.17616*
CBS 109214/BBA 62147*
CBS 172.51*
CBS 114.14*
CBS 142410*
CBS 144.31*
CBS 125337*
CBS 119444*
IMI 79736*
CBS 109225*
CBS 398.84*
CBS 143664a*
CBS 519.97*
CBS 521.97*
CBS 159.84*
MFLU 14-0625*
MAFF 244029
CBS 124955*
MAFF 510857*
CBS 116870*
CBS 132885*
JX519217
KF156863
MN631384
KY856446
KJ955109
JQ400005
KM105184
JQ005231
GQ329690
KY856450
AB738855
KC110789
JQ948288
KX618686
JX519216
HM131513
MH846576
KJ955201
MG748077
MH482929
JQ948444
JX010231
LC324781
HM585409
JQ948454
JQ948289
KY514347
KX228254
JQ005766
KP890104
GU227810
JQ005765
JQ948193
KY856472
JQ005779
GU227829
GU227804
MG600768
JQ948155
KF687718
MH728812
MG600769
KF178480
JQ948194
KU242357
AB738859
MG600765
JX519221
HQ596292
MG600736
tub2
Complex
JX519225
KF289008 KF377532
MN635794 MN635795
KY856270 KY856186 KY856019
KJ954810
KM023257
JQ400012 Q399998
JQ399991
KM105535 KM105254 KM105394
JQ005318 JQ005405 JQ005579
GQ329681 JX009752 JX009438
KY856274 KY856190 KY856023
AB738846 AB738845
KC110807
KC110825
JQ948618 JQ948949 JQ949609
KX618684 KX618683 KX618682
JX519224 JX519233
HM131499
HM131508
MH846572 MH846573 MH846575
KJ954902
KJ954471
MG747995 MG747913 MG747767
MH681658
MH708135
JQ948775 JQ949105 JQ949765
JX010012 JX009813 JX009452
LC324787 LC324783 LC324785
HM585391 HM582023 HM581995
JQ948785 JQ949115 JQ949775
JQ948619 JQ948950 JQ949610
KY514344 KY514341 KY514338
KX228357
KM105597 JQ005787 JQ005829
KP890135 KP890127 KP890097
GU228202 GU228300 GU227908
KM105581 JQ005786 JQ005828
JQ948523 JQ948854 JQ949514
KY856296 KY856213 KY856045
JX546712 JQ005800 JQ005842
GU228221 GU228319 GU227927
GU228196 GU228294 GU227902
MG600828 MG600874 MG600972
JQ948485 JQ948816 JQ949476
KF687842 KF687782 KF687803
MH728820 MH805850 MH781480
MG600829 MG600875 MG600973
KF178504 KF178529 KF178577
JQ948524 JQ948855 JQ949515
KU242356 KU242355 KU242353
JX519242
KF288975
MG600825 MG600872
JX519229
HQ596299 JX009896
MG600798 MG600853
MG601032
JX519246
HQ596280
MG601003
graminicola
gloeosporioides
gloeosporioides
gloeosporioides
gloeosporioides
dematium
destructivum
boninense
gloeosporioides
gloeosporioides
singleton
spaethianum
acutatum
dematium
graminicola
truncatum
acutatum
gloeosporioides
dematium
gigasporum
acutatum
gloeosporioides
dematium
boninense
acutatum
acutatum
acutatum
singleton
destructivum
magnum
spaethianum
destructivum
acutatum
boninense
orbiculare
dematium
spaethianum
magnum
acutatum
gigasporum
gloeosporioides
magnum
orbiculare
acutatum
dematium
singleton
magnum
graminicola
gloeosporioides
orchidearum
gapdh
chs-1
act
KF377495
MG600969
JX519237
HQ596284
MG600942
KY856528
KJ955257
JQ400019
KM105464
JQ005665
JX010450
KY856532
KC110816
JQ949939
KX618685
JX519241
HM153770
MH846574
KJ955348
MG748157
MH727473
JQ950095
JX010444
LC324791
HM585428
JQ950105
JQ949940
KY514350
JQ005850
KP890111
GU228104
JQ005849
JQ949844
KY856554
JQ005863
GU228123
GU228098
MG601035
JQ949806
KF687882
MH846563
MG601036
KF178601
JQ949845
KU242354
13
172
Fungal Diversity (2020) 103:87–218
Table 22 (continued)
Species name
Isolate no
ITS
C. navitas
C. neosansevieriae
C. nicholsonii
C. nigrum#
C. novae-zelandiae#
C. nupharicola#
C. nymphaeae#
C. ocimi
C. ochracea
C. okinawense#
C. oncidii
C. orbiculare#
C. orchidearum#
C. orchidophilum#
C. orchidis
C. panacicola
C. pandanicola
C. panamense
C. paranaense#
C. parallelophorum
C. parsonsiae
C. parthenocissicola
C. paspali
C. paxtonii
C. petchii
C. perseae#
C. phaseolorum#
C. phormii
C. phyllanthi#
C. piperis#
C. pisicola
C. plurivorum#
C. pseudoacutatum#
C. pseudomajus
C. pseudotheobromicola#
C. psidii
C. proteae
C. pyricola
C. pyrifoliae#
C. queenslandicum#
C. radicis
C. rhexiae
C. rhombiforme#
C. riograndense
C. roseum
C. rusci
C. salicis#
C. salsolae#
C. sambucicola
C. sansevieriae#
CBS 125086*
CPC 25127*
MAFF 511115*
CBS 169.49*
CBS 128505*
CBS 470.96*
CBS 515.78*
CBS 298.94*
CGMCC 3.15104*
MAFF 240517*
CBS 129828*
CBS 570.97*
CBS 135131*
CBS 632.80*
MFLUCC 17-1302*
C08087*
MFLUCC 17-0571*
CBS 125386*
CBS 134729*
MFLUCC 14-0083*
CBS 128525*
MFLUCC 17-1098*
MAFF 305403*
IMI 165753*
CBS 378.94*
CBS 141365*
CBS 157.36
CBS 118194*
CBS 175.67*
IMI 71397*
CBS 724.97*
CBS 125474*
CBS 436.77*
CBS 571.88*
MFLUCC 18–1602*
CBS 145.29*
CBS 132882*
CBS 128531*
CGMCC 3.18902*
ICMP 1778*
CBS 529.93*
CBS 133134*
CBS 129953*
ICMP 20083*
CBS 145754 *
CBS 119206*
CBS 607.94*
ICMP 19051*
MFLUCC 16–1388*
MAFF 239721/Sa-1-2
JQ005769
KR476747
JQ005770
JX546838
JQ005228
JX010187
JQ948197
KM105222
JX625156
MG600767
JQ005169
KF178466
MG600738
JQ948151
MK502144
GU935869
MG646967
MG600766
KC204992
MF448525
JQ005233
MK629452
JX519219
JQ948285
JQ005223
KX620308
GU227896
JQ948446
JQ005221
MG600760
KM105172
MG600718
JQ948480
KF687722
MH817395
JX010219
KC297079
JQ948445
MG748078
JX010276
KF687719
JX145128
JQ948457
KM655299
MK903611
GU227818
JQ948460
JX010242
KY098781
LC179806
13
gapdh
chs-1
act
tub2
Complex
JQ005790
JQ005832
KR476790
JQ005833
JX546646
JQ005576
JX009437
JQ949518
KM105432
KC843527
MG600971
JQ005517
KF178563
MG600944
JQ949472
MK496853
GU944758
MG646938
MG600970
KC205077
JQ005853
KR476797
JQ005854
JX546885
JQ005662
JX010398
JQ949848
KM105502
JX625183
MG601034
JQ005603
KF178587
MG601005
JQ949802
MK496859
GU935889
MG646926
MG601033
KC205060
MH351280
JQ005667
MK639360
JX519244
JQ949936
JQ005657
KX620341
GU228190
JQ950097
JQ005655
MG601027
KM105452
MG600985
JQ950131
KF687883
MH853684
JX010443
KC297101
JQ950096
MG748158
JX010414
KF687869
JX145179
JQ950108
KM655300
MK903607
GU228112
JQ950111
JX010403
KY098782
LC180128
graminicola
singleton
graminicola
singleton
boninense
gloeosporioides
acutatum
destructivum
caudatum
magnum
boninense
orbiculare
orchidearum
singleton
dematium
destructivum
gloeosporioides
magnum
acutatum
singleton
boninense
dematium
graminicola
acutatum
boninense
gloeosporioides
dematium
acutatum
boninense
orchidearum
destructivum
orchidearum
singleton
gigasporum
gloeosporioides
gloeosporioides
gloeosporioides
acutatum
singleton
gloeosporioides
gigasporum
gloeosporioides
acutatum
spaethianum
acutatum
singleton
acutatum
gloeosporioides
dematium
singleton
KR476791
JQ005791
JX546742 JX546693
JQ005315 JQ005402
JX009972 JX009835
JQ948527 JQ948858
KM105577 KM105292
KC843513
MG600827
JQ005256 JQ005343
KF178490 KF178515
MG600800 MG600855
JQ948481 JQ948812
MK496857 MK496855
GU935849
MG646934 MG646931
MG600826 MG600873
KC205026 KC205043
MK165695
JQ005320 JQ005407
MK639362 MK639356
JX519227
JQ948615 JQ948946
JQ005310 JQ005397
KX620242
GU228288 GU228386
JQ948777 JQ949107
JQ005308 JQ005395
MG600820 MG600867
KM105522 KM105242
MG600781 MG600841
JQ948811 JQ949141
KF687826 KF687779
MH853675 MH853678
JX009967 JX009901
KC297009 KC296986
JQ948776 JQ949106
MG747996 MG747914
JX009934 JX009899
KF687825 KF687762
JQ948788
KM655298
MK903603
GU228210
JQ948791
JX009916
KY098780
LC180130
JQ005581
MK639358
JX519235
JQ949606
JQ005571
KX620145
GU227994
JQ949767
JQ005569
MG600964
KM105382
MG600925
JQ949801
KF687801
MH853681
JX009515
KC296940
JQ949766
MG747768
JX009447
KF687785
JQ949118 JQ949778
KM655297 KM655295
MK903604
GU228308 GU227916
JQ949121 JQ949781
JX009863 JX009562
KY098779 KY098778
LC180129 LC180127
Fungal Diversity (2020) 103:87–218
173
Table 22 (continued)
Species name
#
C. scovillei
C. sedi
C. serranegrense
C. shisoi#
C. siamense#
C. sidae
C. simmondsii#
C. sloanei
C. somersetense
C. sonchicola
C. sojae
C. spaethianum#
C. spinaciae#
C. spinosum
C. sublineola#
C. sydowii
C. syzygiicola
C. tabacum
C. tainanense
C. tanaceti#
C. tamarilloi#
C. tebeesti
C. theobromicola#
C. temperatum
C. ti#
C. tofieldiae
C. tongrenense
C. torulosum
C. trichellum
C. trifolii#
C. tropicale#
C. tropicicola
C. truncatum#
C. utrechtense
C. verruculosum
C. vietnamense
C. vignae
C. viniferum#
C. vittalense
C. walleri
C. wanningense#
C. watphraense
C. wuxiense#
C. xanthorrhoeae
C. yulongense
C. yunnanense
C. zoysiae
Isolate no
ITS
gapdh
act
tub2
Complex
CBS 126529*
MFLUCC14-1002*
COAD 2100a*
JCM 31818*
MFU 090230*
CBS 504.97*
CBS 122122*
IMI 364297*
CBS 131599*
MFLUCC 17-1299*
ATCC 62257*
CBS 167.49*
CBS 128.57
CBS 515.97*
CBS 131301*
CBS135819*
MFLUCC 10-0624*
CPC 18945*
CBS 143666a*
CBS 132693*
CBS 129814*
CBS 522.97*
ICMP 18649*
CBS 133122*
ICMP 4832*
CBS 495.85*
GZU_TRJ1-37/
GMBC0209*
CBS 128544*
CBS 217.64*
CBS 158.83*
CBS 124949*
BCC 38877*
CBS 151.35*
CBS 130243*
IMI 45525*
LD16(L2)*
CBS 501.97*
GZAAS5.08601*
CBS 181.82*
CBS 125472*
CGMCC 3.18936*
MFLUCC 14-0123*
CGMCC 3.17894*
BRIP 45094*
CFCC 50818*
CBS 132135*
MAFF238573*
JQ948267
KM974758
KY400111
MH660930
FJ972613
KF178472
JQ948276
JQ948287
JX076862
KY962757
MG600749
GU227807
GU227847
KF178474
JQ005771
KY263783
KF242094
KM105204
MH728818
JX218228
JQ948184
KF178473
JX010294
JX145159
JX010269
GU227801
MH482933
JQ948597 JQ948928
KM974755 KM974754
KY407894
MH660931 MH660929
FJ972575 JX009865
KF178497 KF178521
JQ948606 JQ948937
JQ948617 JQ948948
JQ949588
KM974756
KY407892
MH660928
FJ907423
KF178569
JQ949597
JQ949608
JQ949918
KM974757
KY407896
MH660932
FJ907438
KF178593
JQ949927
JQ949938
KY962754
MG600810
GU228199
GU228239
KF178498
KY962751
MG600860
GU228297
GU228337
KF178523
JQ005792
KY263785 KY263787
KF242156
KM105557 KM105274
MH728823 MH805845
JX218243 JX259268
JQ948514 JQ948845
KF178505 KF178522
JX010006 JX009869
KY962748
MG600954
GU227905
GU227945
KF178571
JQ005834
KY263791
KF157801
KM105414
MH781475
JX218238
JQ949505
KF178570
JX009444
acutatum
dematium
gigasporum
destructivum
gloeosporioides
orbiculare
acutatum
acutatum
caudatum
dematium
orchidearum
spaethianum
dematium
orbiculare
graminicola
singleton
gloeosporioides
destructivum
gloeosporioides
destructivum
acutatum
orbiculare
gloeosporioides
gloeosporioides
gloeosporioides
spaethianum
dracaenophilum
JQ005164
GU227812
KF178478
JX010264
JN050240
GU227862
KM105201
GU227806
KF687721
KM105183
JN412804
MG600734
JQ948275
MG830462
MF448523
KU251591
JX010261
MH751507
JX546804
JX076871
JQ005251
GU228204
KF178502
JX010007
JN050229
GU228254
KM105554
GU228198
KF687832
KM105534
JN412798
MG600796
JQ948605
MG830318
MH049479
KU252045
JX009927
MK108986
JX546706
JQ005512
GU227910
KF178575
JX009489
JN050218
GU227960
KM105411
GU227904
KF687792
KM105393
JN412795
MG600940
JQ949596
MG830270
MH376384
KU251672
JX009478
MH777394
JX519239
chs-1
MG601016
GU228101
GU228141
KF178595
JQ005855
KY263793
KF254880
KM105484
MH846558
JX218233
JQ949835
KF178594
JX010447
JX145211
JX009952 JX009898 JX009520 JX010442
GU228193 GU228291 GU227899 GU228095
MH705332
MH717074 MH729805
JQ005338
GU228302
KF178527
JX009870
GU228352
KM105271
GU228296
KF687769
KM105253
MG600851
JQ948936
MG830302
KU251939
JX009823
MH793605
JX519231
JQ005598
GU228106
KF178599
JX010407
JN050246
GU228156
KM105481
GU228100
KF687877
KM105463
JN412813
MG601001
JQ949926
MG830286
MH351276
KU252200
JX010448
MK108987
JX519248
boninense
singleton
orbiculare
gloeosporioides
dracaenophilum
truncatum
destructivum
spaethianum
gigasporum
destructivum
gloeosporioides
orchidearum
acutatum
acutatum
boninense
gloeosporioides
gloeosporioides
gloeosporioides
dracaenophilum
caudatum
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains in bold and marked with an asterisk (*).Voucher strains are also in bold. Species confirmed
with pathogenicity studies are marked with #
13
174
13
Fungal Diversity (2020) 103:87–218
Fungal Diversity (2020) 103:87–218
◂Fig. 37 Phylogram generated from RAxML analysis based on com-
bined sequences of ITS and LSU of Mucor and Backusella species.
Eighty-seven taxa were used for the analysis, which consisted of 1264
characters including gaps. The tree is rooted using Backusella lamprospora (CBS 195.28), and B. grandis (CBS 186.87). Likelihood
of the best-scoring ML tree was − 17553.567209. The concatenated
matrix contained 716 distinct alignment patterns with 21.98% of
undetermined characters or gaps. Estimated base frequencies were as
follows: A = 0.302082, C = 0.168706, G = 0.219403, T = 0.309809;
substitution rates AC = 0.749467, AG = 2.977575, AT = 1.651634,
CG = 0.631954, CT = 4.647089, GT = 1.000000; gamma distribution shape parameter α = 0.302610. The type species are in bold.
Scale bar indicates the number of substitutions per site. ML bootstrap
support values greater than 70% are shown near the nodes
appears water-soaked. The lesions formed are quasicircular
or irregular, light to dark brown and the sporangiophores
protrude through the wounds (Kwon and Hong 2005; Saito
et al. 2016; Michailides and Spotts 1990). As the infection
advances, the infected part disintegrates into a watery rot
and the infection spreads and extends to all extremities of the
fruit or even the surface of the container. The infected part
is covered with a large mass of mycelium with erect sporangiophores and sporangia (Saito et al. 2016; Michailides and
Spotts 1990). When tested, rotten apple and pear by some
Mucor species release an alcoholic odour while Mucor rot
in peaches and nectarines caused by M. piriformis emits a
pleasant aromatic odour. At an advanced stage, Mucor rot
can be distinguished from other rots caused by Rhizopus or
Gilbertella. Differences are observed in the mycelial character, growth, sporangiophores and sporangia. For Mucor rot,
erect, white or yellowish sporangiophore with grey to black
sporangia is observed which covers the decay lesion densely.
However, for Rhizopus rot, the mycelia are interwoven with
stolons with dark sporangiophores and black sporangia.
The sporangial wall eventually dries and falls apart while in
Mucor rot, the sporangia absorb water from the sporangial
wall which dissolves (Michailides and Spotts 1990).
Morphology- based identification and diversity
Mucor is characterized by fast-growing colonies. The sporangiophores are simple or branched without basal rhizoids.
However, under some conditions, they form rhizoids. These
species normally form globose sporangia, containing the
columella and spores. The sporangium is non-apophysate
with pigmented and ornamented zygosporangial walls.
Arthrospores, chlamydospores, and zygospores may be produced by some species. The zygospores lack appendaged
suspenders and broad aseptate or sparsely septate hyphae
are commonly found in Mucor species (Nguyen et al. 2016).
When spores from sporangia are released, a remaining collarette is observed. The sporangiospores are round or slightly
elongated (Larone 1995; Sutton et al. 1998; de Hoog et al.
2000). With 76 accepted species, the genus is the largest
and most studied group in Mucorales (Walther et al. 2019).
175
Molecular identification and diversity
The present taxonomy of Mucor is mostly based on morphological characters and interfertility tests. The genus was
previously diagnosed using biological species recognition
and morphological species recognition (Schipper 1973;
Hermet et al. 2012). However, identification often fails with
only morphology hence phylogenetic species recognition has
been used to resolve species (Taylor et al. 2000). The use of
multi-gene (ITS, tef1 and act) phylogenetic analysis showed
that Mucor is not monophyletic (Nguyen et al. 2017). An
extensive study by Walther et al. (2013), using about 400
Mucor strains, led to a refinement in the classification of
Mucor species. Phylogeny-based on 28S rDNA led to the
transfer of some species to different groups and it was shown
that some of these groups intermingled with other genera,
such as Chaetocladium and Helicostylum, which do not
belong to Mucoraceae. The use of five markers (ITS, rpb1,
tsr1, mcm7 and cfs) phylogeny by Wagner et al. (2019), combined with phenotypic studies, mating tests and the determination of the maximum growth temperatures revealed 16
phylogenetic species of which 14 showed distinct phenotypical traits and were recognized as discrete species.
Recommended genetic markers (genus level)—LSU and
SSU
Recommended genetic markers (species level)—ITS and
rpb 1
Accepted number of species—There are 735 species epithets
in Index Fungorum (2020), however only 76 species have
DNA sequence data (Table 23) (Walther et al. 2019).
References—Larone (1995), Sutton et al. (1998), de Hoog
et al. (2000) (morphology), Nguyen et al. (2016, 2017),
Walther et al. (2013, 2019), Wagner et al. (2019) (morphology and phylogeny).
98. Phytophthora de Bary, J. Roy. Agric. Soc. England, ser.
2 12: 240 (1876)
Background
Phytophthora is classified in the kingdom Straminipila
within the diploid, alga-like Oomycetes in the Stramenopile clade of the Kingdom Chromista (Cavalier-Smith 1986;
Dick 1995; Yoon et al. 2002; Wijayawardene et al. 2020).
Phytophthora consists of about 130 described species with
many important plant pathogens. The Oomycota are biologically different from main fungal groups within the Kingdom
Fungi (Corliss 1994; Cavalier-Smith 1998). For example, their
cell walls are made primarily of cellulose instead of chitin as
in most fungi and they cannot synthesize β-hydroxysterols,
which is vital for synthesizing hormones that regulate sexual
reproduction (Hyde et al. 2014). Another important difference is that oomycetes are diploid throughout their life cycle.
One similarity between Phytophthora species and Eumycotan
fungi is that they both produce hyphae.
13
176
Classification—Oomycota, Peronosporales, Peronosporacae
Type species—Phytophthora infestans (Mont.) de Bary
Distribution—worldwide
Disease symptoms—blight, canker, dieback, root rots and wilt
Species can have a large impact on agriculture (e.g. Phytophthora infestans, potato late blight), arbiculture (e.g. Phytophthora ramorum, sudden oak death) and whole ecosystems
(e.g. Phytophthora cinnamomi in Australia). Phytophthora
species damage plants by killing the tissues and resulting
necrosis can be seen in leaves, stems or roots. Some species
can cause multiple symptoms on a single host, or cause different symptoms on different hosts (Jung and Blaschke 1996).
Blight: Initial symptom is the development of a “watersoaked” appearance, which progresses into brown or black
irregular-shaped spots or wedge-shaped lesions. These
lesions are usually not surrounded by a yellow halo (Babadoost 2004; Pande et al. 2011; Ali et al. 2017).
Canker: A dark discoloured necrotic lesion in the inner bark
of a tree can be seen often on the stem or branches. However,
generally, cankers are visible once the outer bark is removed.
Cankers are often seen with a reddish-brown liquid that oozes
through the bark (Davidson et al. 2002; Jung et al. 2018).
Dieback: Death of shoot tips, twigs and branch tips can
be observed. The infection progresses towards the main stem
accompanied by a loss of foliage (Kuske and Benson 1983;
Akilli et al. 2013).
Decline and Death: This is a gradual process that will
take place over several years. Plants fail to grow and the
canopy becomes thin due to loss of foliage. Then the whole
canopy or sections of the canopy may die (Marais 1980;
Belisario et al. 2004; González et al. 2020).
Rot: Dark discoloured rotten tissues that are common on
roots, but sometimes extend above the soil surface. However,
collar rot occurs at the base of the trunk and extends just
below the soil line (Jung and Blaschke 1996; Graham et al.
2011; Summerell and Liew 2020).
Wilting: This is the first above-ground symptom of root
rot. Foliage becomes flaccid due to lack of water intake
(Vettraino et al. 2009; Xiong et al. 2019).
Phytophthora causes disease in important agricultural and
ecological plants. Phytophthora infestans was responsible for
the Irish potato famine from 1845 to 1852, causing the death
of over 1 million people. Phytophthora ramorum has resulted
in the death of millions of coast live oak, tanoak and Japanese
larch trees, thus altering the forest ecosystems in California and
Oregon, USA (Goheen et al. 2002; Rizzo et al. 2002, 2005).
Hosts—Phytophthora agathidicida (commonly known as
kauri dieback), which causes kauri death, is considered as
one of the world’s most feared fungi (Hyde et al. 2018a). An
extensive survey in previously unexplored ecosystems such
as natural forests (Rea et al. 2010; Vettraino et al. 2011; Jung
et al. 2011, 2017; Reeser et al. 2013), streams (Reeser et al.
2007; Bezuidenhout et al. 2010; Yang et al. 2016; Brazee
13
Fungal Diversity (2020) 103:87–218
et al. 2017), riparian ecosystems (Brasier et al. 2003, 2004;
Hansen et al. 2012), and irrigation systems (Hong et al.
2010, 2012; Yang et al. 2014a, b) has led an exponential
increase in the number of species.
Pathogen biology, disease cycle and epidemiology
Morphological based identification and diversity
Species-level classification is based on the morphological
characterization of reproductive structures including the sporangium (asexual) and oospore (sexual) as well as the production of chlamydospores (Martin et al. 2012). Characteristics
that are important for species classification include the diameter
of the oogonium and oospore, thickness of the oospore wall,
whether or not the oospore fills the oogonium, ornamentation
on the oogonial wall, and mode of attachment of the antheridium
(Hyde et al. 2014). Identification and classification of Phytophthora species into morphological groups based on several characteristics was initially based on the key provided by Waterhouse
(1963), which was later updated by Stamps et al. (1990).
Molecular based identification and diversity
Phytophthora has been historically placed in the Pythiales
with Pythium and related genera, however recent phylogenetic
analysis with the large (LSU) or small (SSU) rDNA sequences
or cox2 gene has indicated a closer relationship with downy mildew and white rusts (Albugo.) in the Peronosporales (Beakes
and Sekimoto 2009; Thines et al. 2009). Additional multigene
analyses are vital to clarify the relationship between the Peronosporales and Pythium. Early efforts focusing on the phylogenetic relationships in Phytophthora used nuclear-encoded
rDNA, primarily the ITS region (Crawford et al. 1996; Cooke
and Duncan 1997; Förster et al. 2000). The first comprehensive
study was based on the phylogenetic study of the ITS region
(Cooke et al. 2000). The study by Kroon et al. (2004) was based
on analysis using two nuclear (tef1, tub2) and two mitochondrial (cox1 and nad1) genes. Subsequent phylogenetic analysis
was based on sequences of seven nuclear genetic markers (60S
ribosomal protein L10, tub2, enolase, heat shock protein90,
large subunit rDNA, TigA gene fusion and tef1) which divided
the species into 10 well-supported clades (Blair et al. 2008).
The phylogenetic study by Martin et al. (2014) was based on
seven nuclear and four mitochondrial genes (cox2, nad9, rps10
and secY). More recently, an extensive study of the genus by
Yang et al. (2017) was based on sequences of seven nuclear
genetic markers as in Blair et al. (2008).
The number of described species in Phytophthora was
approximately 55 in 1999, but since then there has been a
significant increase in the number of species nearly doubling the number of described species to 105 (Brasier 2007),
and over 128 species (Hyde et al. 2014). Additional species
have since been described, for example, P. cocois (Weir et al.
2015), P. crassamura (Scanu et al. 2015), P. attenuata, P.
Fungal Diversity (2020) 103:87–218
177
Fig. 38 Disease cycle of Phytophthora infestans (redrawn
from Bengtsson 2013)
xheterohybrida, P. xincrassata (Jung et al. 2017) bringing
the total to over 150 species (Jung et al. 2019). The phylogenetic tree constructed is presented in Fig. 39 and the
accepted species are given in Table 24.
Recommended genetic markers (genus level)—LSU, SSU
and cox2
Recommended genetic markers (species level)—LSU, tub2
and cox2
Accepted number of species– There are 317 epithets listed
in Index Fungorum (2020), however only 162 species have
DNA sequence data (Table 24).
References—Waterhouse (1963), Stamps et al. (1990) (morphology); Crawford et al. (1996), Cooke and Duncan (1997),
Cooke et al. (2000), Förster et al. (2000), Brasier (2007),
Blair et al. (2008) (morphology and phylogeny); Hyde et al.
(2014) (phylogeny and accepted species) (Fig. 40).
99. Pythium Pringsh., Jb. wiss. Bot. 1: 304 (1858)
Background
Pythium is the largest and most comprehensively studied genus in Pythiaceae sensu lato, order Peronosporales
sensu lato, class Peronosporomycetes, phylum Oomycota,
and kingdom Straminipila (Beakes et al. 2014). Pringsheim
(1858) described the genus. However, the initial classification
of Pythium has changed many times based on several studies
using morphological characteristics (Uzuhashi et al. 2010).
Pythium comprises of more than 230 extant species (Hyde
et al. 2014), however, identification of species has always
been problematic due to limited morphological characters,
difficulty in isolating some taxa and lack of molecular data
for certain species (Lévesque and de Cock 2004).
Classification—Oomycota, Pythiales, Pythiaceae
Type species—Pythium monospermum Pr ingsh.
(Pringsheim 1858)
Distribution—worldwide
Disease symptoms—generally cause rot of fruit, roots and
stem including pre- or post-emergence damping-off of seeds
and seedlings.
Pythium causes crown and root rot in mature plants, where
plants suddenly wilt during warm and sunny weather and
when plants have their first heavy fruit load. Often, upper
leaves of infected plants wilt in the day and recover overnight. However, plants eventually die (Craft and Nelson 1996;
Postma et al. 2000). The first symptoms of Pythium root infections include stunting. In the root system, initial symptoms
are brown to dark-brown lesions on root tips and feeder roots.
As the disease progresses, symptoms are soft, brown, stubby
roots and lack of feeder roots. In larger roots, the outer root
tissue or cortex peels away, leaving the string-like vascular
bundles underneath (Postma et al. 2000; Moorman et al.
2002; Al-Mahmooli et al. 2015). Pythium rot also occurs in
the crown at the stem base. In cucumber, diseased crowns
turn orange-brown, often with a soft rot at the base, while in
strawberry seedling roots have dark brown, water-soaked rot
and rotten crowns (Columbia and English 1988; Ishiguro et al.
2014). Several species of Pythium cause blight of turfgrass,
which initially appears as “greasy” water-soaked areas, but
later turn brown and grey (Vencelli and Powell 2008).
13
178
Fig. 39 Maximum likelihood of
Phytophthora based on the concatenated seven nuclear genetic
markers (60S Ribosomal
protein L10 (60S), beta-tubulin
(tub), elongation factor 1 alpha
(tef1), enolase (Enl), heat
shock protein 90 (hsp90), 28S
ribosomal DNA (28S), and tigA
gene fusion protein (TigA)). ML
bootstrap support values over
60% are indicated and BYPP
≥ 0.90 are shown respectively
near the nodes. The type species
are in bold. Scale bar indicates
number of substitutions per site.
The tree was rooted with Phytopythiumvexansand Pythium
undulatumas as the our group.
Likelihood of the best scoring
ML tree was − 114471.902046.
Estimated base frequencies
were as follows: A = 0.216570,
C = 0.275568, G = 0.312230,
T = 0.195632; substitution
rates AC = 0.414835, AG =
1.176570, AT = 0.600142, CG
= 0.970565, CT = 5.227735,
GT = 1.000000
13
Fungal Diversity (2020) 103:87–218
Fungal Diversity (2020) 103:87–218
179
Fig. 39 (continued)
13
180
Table 23 DNA barcodes
available for Mucor
Fungal Diversity (2020) 103:87–218
Species
Isolate
ITS
LSU
Mucor abundans
CBS 388.35
CBS 521.66
CBS 993.70*
CBS 126943
CBS 763.74
CBS 210.80*
CBS 202.28*
CBS 846.73*
CBS 526.68
CBS 292.63*
CBS 251.53*
CBS 293.63*
URM 7322
B5-2
CBS 108.16
CBS 293.66
CBS 156.51*
ATCC MYA-4767*
CBS 385.95*
CBS 141.20
CBS 251.35*
CBS 230.35*
CBS 893.73
EML-PUKI06-1
CBS 132.22
CBS 230.29
CBS 336.68*
CBS 566.91*
CBS 114.08*
CBS 404.71
CBS 174.27*
CBS 338.74
CBS 405.58
CBS 242.35
CBS 115.18
CBS 255.36
CBS 226.29*
CBS 977.68
EML-PUKI12-1
CBS 154.69
EML-QT1*
EML-QT2
CBS 638.74
CBS 143.85*
CBS 243.35
CBS 215.27*
URM-7908
CBS 586.67*
CBS 444.65*
CBS 999.70*
JN206111
JN206110
NG_063979
JN206457
JN206461
MH875788
NG_057877
JN206504
JN206418
M. aligarensis
M. ambiguus
M. amphibiorum
M. ardhlaengiktus
M. atramentarius
M. amethystinus
M. azygosporus
M. bacilliformis
M. bainieri
M. caatinguensis
M. circinelloides
M. ctenidius
M. durus
M. ellipsoideus
M. endophyticus
M. exponens
M. falcatus
M. flavus
M. fragilis
M. fuscus
M. fusiformis
M. gigasporus
M. genevensis
M. guiliermondii
M. heterogamus
M. hiemalis
M. inaequisporus
M. indicus
M. irregularis
M. japonicus
M. koreanus
M. lanceolatus
M. laxorrhizus
M. luteus
M. megalocarpus
M. merdophylus
M. minutus
M. moelleri
M. mousanensis
13
MH864344
NR_103615
NR_152960
MH854979
JN206014
JN206015
NR_103639
NR_145285
NR_103628
KT876701
JN205954
MH858796
NR_145295
NR_111683
NR_111661
MH854686
NR_103647
JN206061
KY047147
JF723619
JN206204
NR_111660
NR_103646
HM623318
JN206042
NR_103636
JN206169
JN206167
JN206134
JN206127
JN206177
NR_077173
JX976259
KY047151
JN206158
KT936259
KT936260
JN206205
NR_103642
JX976254
NR_145286
MK775467
JN206048
MH858663
NR_103629
JN206426
NG_057928
NG_057916
JN206424
NG_060334
JN206417
NG_057918
NG_042602
NG_057970
JN206441
NG_057931
JN206464
JN206465
NG_057915
NG_057926
NG_057923
JN206488
NG_057929
NG_057878
JN206446
JN206443
NG_057914
NG_057925
MK775466
JN206463
NG_057875
NG_057912
Fungal Diversity (2020) 103:87–218
Table 23 (continued)
181
Species
#
M. mucedo
M. multiplex
M. nidicola
M. odoratus
M. parviseptatus
M. piriformis#
M. plasmaticus
M. plumbeus
M. prayagensis
M. pseudolusitanicus
M. pseudocircinelloides
M. saturninus
M. stercorarius#
M. strictus
M. racemosus
M. ramosissimus
M. silvaticus
M. ucrainicus
M. variisporus
M. variicolumellatus
M. velutinosus
M. zonatus
M. zychae
Ellisomyces anomalus
Isolate
ITS
LSU
CBS 542.66*
JN206086
JN206480
CBS 987.68
CBS 110662*
EML-SBD1
EML-SBD2
CBS 130.41*
CBS 417.77
CBS 169.25*
CBS 275.49
CBS 634.74
CBS 652.78
CBS 540.78*
CBS 543.80
CBS 541.78
CBS 974.68*
CNUFC-UK2-1*
CNUFC-UK2-2
CBS 100.66*
CBS 260.68*
CBS 135.65*
CBS 249.35
CBS 674.88
CBS 837.70*
CBS 236.35*
SF012536
UTHSC-04-1961
CBS 148.69*
CBS 416.67*
CBS 243.57*
CBS 697.76
JN206089
NR_111662
KY047148
KY047149
NR_145287
JN206108
NR_103630
JN206480
NG_057924
HM999955
JN206189
MF495059
MF495060
JN206013
NR_103635
KX839689
KX839680
JN206035
NR_126135
NR_103627
JN206122
JN206192
NR_152951
JN205979
MF495054.1
JF299208
NR_103638
NR_103641
NR_145284
JN205993
NG_057927
JN206453
NG_057874
JN206483
HM849677
JN206498
JN206431
JN206458
JN206477
NG_055727
NG_056280
JN206455
JN206507
NG_057972
JN206422.1
NG_057917
NG_057930
NG_067365
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
Several Pythium species are capable of causing fruit rot
in numerous crops (Martin and Loper 1999). Pythium fruit
rot is commonly known as a cottony leak or watery rot and
occurs during wet weather or in poorly drained areas of
fields (Ho and Abd-Elsalam 2020; Sharma et al. 2020a).
Initial symptoms of the fruit rot are brownish, water-soaked
lesions that quickly become large, watery, soft and rotten.
The rot generally begins on the parts of fruit in contact with
the soil. In cucumber, a brown to dark green blister can be
seen on fruit before they become watery and rot. Later, white
cottony mycelium can be seen on rotten tissues, especially
during humid weather. Pythium fruit rot is most severe in
poorly-drained fields during wet weather. The disease can
render fruit unmarketable (Ho 2009; Sharma et al. 2020a).
Pre-emergence damping-off causes seeds and young seedlings to rot before they emerge from the growing medium in
greenhouses, while post-emergence damping-off kills newly
emerged seedlings. In the latter, the pathogen causes a watersoaked, soft brown lesion at the stem base, near the soil line,
that pinches off the stem causing the seedling to topple over
and die (Weiland et al. 2012).
Hosts—Pythium has a wide range of hosts including species of Cucurbitaceae and Poaceae, Ananas comosus, Arachis hypogaea, Brassica sp., Carica papaya, Beta vulgaris,
Daucus carota subsp. sativus, Dendrobium sp, Solanum sp.
and Zingiber officinale. Some species are pathogens of algae,
fungi, other oomycetes, nematodes, insects, animals and
humans (Van der Plaäts-Niterink1981; Czeczuga et al. 2005;
Kawamura et al. 2005; Hwang et al. 2009; Li et al. 2010;
Weiland et al. 2012; Ho 2013; Hyde et al 2014). Several
species inhabit different soils in cultivated and uncultivated
fields including forest (Uzuhashi et al 2010). Pythium arrhenomanes, P. dissotocum, P. elongatum, P. myriotylum, and P.
spinosum are important pathogens of rice seedlings (Hendrix
13
182
Fungal Diversity (2020) 103:87–218
Table 24 DNA barcodes available for Phytophthora
Species
Strain
60S
tub2
tef1
Enl
HSP90
28S
TigA
Phytophthora ×alni
P. ×heterohybrida
P. ×incrassata
P. ×stagnum#
P. acerina#
P. aff. brassicae#
P. aff. citrophthora#
P. aff. erythroseptica
P. aff. hedraiandra#
P. aff. himalsilva
P. aff. parsiana#
P. agathidicida#
P. alticola
P. amnicola
P. andina#
P. aquimorbida
P. arenaria
P. asiatica
P. asparagi#
P. attenuata
P. austrocedrae
P. bilorbang#
P. bisheria
P. boehmeriae#
P. borealis
P. botryosa#
P. brassicae#
P. cactorum#
P. cajani#
P. cambivora#
P. capensis
P. capsici#
P. captiosa#
P. castaneae
P. chrysanthemi#
P. cichorii
P. cinnamomi#
P. citricola#
P. citrophthora#
P. clandestina
P. cocois
P. colocasiae#
P. constricta
P. crassamura
P. cryptogea#
P. dauci
P. drechsleri#
P. elongata
P. erythroseptica
P. europaea#
47A8
67C1
67C2
36J7
61H1=CBS 133931
CBS 112968
IMI 342898
33A1=P207
33F4=P226
61G4=CBS 128754
47C8
67D5=ICMP 17027
47G5=CBS 121939
61G6=CBS 131652
P13365
40A6=MYA-4578
55C2=CBS 127950
45G1=ATCC 90455
33D7= IMI384046
67C5
41B5=MYA-4073
61G8=CBS 131653
29D2
45F9=CBS 291.29
60B2=CBS 132023
IMI130422=P6945
29D8=CBS 686.95
22E6=P10194
45F6=ATCC 44389
22F6=ATCC 46719
62C1=CBS 128319
22F4=ATCC 15399
46H8=NZFS 430
22H6=MYA-4060
61F1=CBS 123163
62A8=CBS 115029
23B2=ATCC 15401
33H8=ATCC 60440
26H3
32G1=CBS 347.86
67D6=ICMP 16948
22F8=MYA-4159
55C3=CBS 125801
66C9=PH094
61H9=CBS 113.19
32E6=P10728
P10331
33J3=SG1-1 952
61J2=CBS 129.23
62A2=CBS 109049
KX251595
KX251637
KX251644
KX251368
KX250712
EU079880
EU080384
KX251979
KX250411
KX250621
KX252397
KX251076
KX251006
KX251167
EU080182
KX252238
KX251013
KX251651
KX251466
KX251609
KX252161
KX251181
KX250873
EU080161
KX251187
EU079934
KX251993
KX250369
KX251679
KX251494
KX250726
KX250635
KX252554
KX251083
KX252266
KX252007
KX251804
KX250747
KX250551
EU079866
KX251104
KX250558
KX252561
KX251194
KX251867
KX252028
EU079506
KX250880
KX251895
KX251522
KX251596
KX251638
KX251645
KX251369
KX250713
EU079881
EU080385
KX251980
KX250412
KX250622
KX252398
KX251077
KX251007
KX251168
EU080183
KX252239
KX251014
KX251652
KX251467
KX251610
KX252162
KX251182
KX250874
EU080162
KX251188
EU079935
KX251994
KX250370
KX251680
KX251495
KX250727
KX250636
KX252555
KX251084
KX252267
KX252008
KX251805
KX250748
KX250552
EU079867
KX251105
KX250559
KX252562
KX251195
KX251868
KX252029
EU079507
KX250881
KX251896
KX251523
KX251597
KX251639
KX251646
KX251370
KX250714
EU079882
EU080386
KX251981
KX250413
KX250623
KX252399
KX251078
KX251008
KX251169
EU080184
KX252240
KX251015
KX251653
KX251468
KX251611
KX252163
N/A
KX250875
EU080163
KX251189
EU079936
KX251995
KX250371
KX251681
KX251496
KX250728
KX250637
KX252556
KX251085
KX252268
KX252009
KX251806
KX250749
KX250553
EU079868
KX251106
KX250560
KX252563
KX251196
KX251869
KX252030
EU079508
KX250882
KX251897
KX251524
KX251598
KX251640
KX251647
KX251371
KX250715
EU079883
EU080387
KX251982
KX250414
KX250624
KX252400
KX251079
KX251009
KX251170
EU080185
KX252241
KX251016
KX251654
KX251469
KX251612
KX252164
KX251183
KX250876
EU080164
KX251190
EU079937
KX251996
KX250372
KX251682
KX251497
KX250729
KX250638
KX252557
KX251086
KX252269
KX252010
KX251807
KX250750
KX250554
EU079869
KX251107
KX250561
KX252564
KX251197
KX251870
KX252031
EU079509
KX250883
KX251898
KX251525
KX251599
KX251641
KX251648
KX251372
KX250716
EU079884
EU080388
KX251983
KX250415
KX250625
KX252401
KX251080
KX251010
KX251171
EU080186
KX252242
KX251017
KX251655
KX251470
KX251613
KX252165
KX251184
KX250877
EU080165
KX251191
EU079938
KX251997
KX250373
KX251683
KX251498
KX250730
KX250639
KX252558
KX251087
KX252270
KX252011
KX251808
KX250751
KX250555
EU079870
KX251108
KX250562
KX252565
KX251198
KX251871
KX252032
EU079510
KX250884
KX251899
KX251526
KX251600
KX251642
KX251649
KX251373
KX250717
EU079885
EU080389
KX251984
KX250416
KX250626
KX252402
KX251081
KX251011
KX251172
EU080187
KX252243
KX251018
KX251656
KX251471
KX251614
KX252166
KX251185
KX250878
EU080166
KX251192
EU079939
KX251998
KX250374
KX251684
KX251499
KX250731
KX250640
KX252559
KX251088
KX252271
KX252012
KX251809
KX250752
KX250556
EU079871
KX251109
KX250563
KX252566
KX251199
KX251872
KX252033
EU079511
KX250885
KX251900
KX251527
KX251601
KX251643
KX251650
KX251374
KX250718
EU079886
EU080390
KX251985
KX250417
KX250627
N/A
KX251082
KX251012
KX251173
EU080188
KX252244
KX251019
KX251657
KX251472
KX251615
KX252167
KX251186
KX250879
EU080167
KX251193
EU079940
KX251999
KX250375
KX251685
KX251500
KX250732
KX250641
KX252560
KX251089
KX252272
KX252013
KX251810
KX250753
KX250557
EU079872
KX251110
KX250564
KX252567
KX251200
KX251873
KX252034
EU079512
KX250886
KX251901
KX251528
13
Fungal Diversity (2020) 103:87–218
183
Table 24 (continued)
Species
#
P. fallax
P. flexuosa
P. fluvialis
P. foliorum#
P. formosa
P. fragariae#
P. fragariaefolia
P. frigida#
P. gallica
P. gemini
P. gibbosa
P. glovera
P. gonapodyides#
P. gondwanensis
P. gregata#
P. hedraiandra#
P. heveae#
P. hibernalis#
P. himalsilva
P. hydrogena
P. hydropathica#
P. idaei
P. ilicis#
P. infestans#
P. inflata#
P. insolita#
P. intercalaris
P. intricata
P. inundata#
P. ipomoeae#
P. iranica#
P. irrigata
P. kernoviae
P. lactucae
P. lacustris#
P. lateralis#
P. lilii
P. litoralis
P. macilentosa
P. macrochlamydospora#
P. meadii#
P. medicaginis#
P. megakarya#
P. megasperma#
P. melonis#
P. mengei
P. mexicana
P. mirabilis
P. mississippiae
P. morindae
Strain
60S
tub2
tef1
Enl
HSP90
28S
TigA
46J2=P10722
67C3
55B6=CBS 129424
49J8=CBS 121655
67C4
22G6=ATCC 11374
61H4=CBS 135747
47G7
50A1=CBS 111474
46H1=CBS 123382
55B7
31E5
21J5=ATCC 46726
22G7
55B8
38C2
22J1=IMI 180616
32F7=CBS 114104
61G3=CBS 128753
46A3
05D1
34D4=CBS 971.95
23A7=ATCC 56615
27A8
28D1
38E1=CBS 691.79
48A1
67B9
P8619
31B6=P10227
61J4=CBS 374.72
04E4
46C8=P10956
61F4
IMI389725=P10337
22H9
CBS 135746
55B9=CBS 127953
58A5
G231E9=IMI 351473
22G5
23A4
61J5=CBS 238.83
62C7=CBS 402.72
41B4
42B2
45G4=CBS 554.88
30C2=ATCC 64070
57J1
62B5=CBS 121982
KX252568
KX251616
KX251208
KX252112
KX251623
KX251529
KX251853
KX250908
KX252589
KX251125
KX251215
KX250642
KX251229
KX252603
KX251243
KX250390
KX251111
KX252126
KX250579
KX252280
KX252294
EU080129
KX250936
KX250474
KX250761
EU080175
KX252617
KX251630
EU080202
EU080844
KX250439
KX252308
EU080041
KX252042
EU080530
KX252133
AB856779
KX251278
KX252329
EU080658
KX250586
KX251902
KX251034
KX251285
KX251700
KX250656
KX250670
KX250488
KX251291
KX252633
KX252569
KX251617
KX251209
KX252113
KX251624
KX251530
KX251854
KX250909
KX252590
KX251126
KX251216
KX250643
KX251230
KX252604
KX251244
KX250391
KX251112
KX252127
KX250580
KX252281
KX252295
EU080130
KX250937
KX250475
KX250762
EU080176
KX252618
KX251631
EU080203
EU080845
KX250440
KX252309
EU080042
KX252043
EU080531
KX252134
AB856782
KX251279
KX252330
EU080659
KX250587
KX251903
KX251035
KX251286
KX251701
KX250657
KX250671
KX250489
KX251292
KX252634
KX252570
KX251618
KX251210
KX252114
KX251625
KX251531
KX251855
KX250910
KX252591
KX251127
KX251217
KX250644
KX251231
KX252605
KX251245
KX250392
KX251113
KX252128
KX250581
KX252282
KX252296
EU080131
KX250938
KX250476
KX250763
EU080177
KX252619
KX251632
EU080204
EU080846
KX250441
KX252310
EU080043
KX252044
EU080532
KX252135
AB856788
KX251280
KX252331
EU080660
KX250588
KX251904
KX251036
KX251287
KX251702
KX250658
KX250672
KX250490
KX251293
KX252635
KX252571
KX251619
KX251211
KX252115
KX251626
KX251532
KX251856
KX250911
KX252592
KX251128
KX251218
KX250645
KX251232
KX252606
KX251246
KX250393
KX251114
KX252129
KX250582
KX252283
KX252297
EU080132
KX250939
KX250477
KX250764
EU080178
KX252620
KX251633
EU080205
EU080847
KX250442
KX252311
EU080044
KX252045
EU080533
KX252136
AB856791
KX251281
KX252332
N/A
KX250589
KX251905
KX251037
KX251288
KX251703
KX250659
KX250673
KX250491
KX251294
KX252636
KX252572
KX251620
KX251212
KX252116
KX251627
KX251533
KX251857
KX250912
KX252593
KX251129
KX251219
KX250646
KX251233
KX252607
KX251247
KX250394
KX251115
KX252130
KX250583
KX252284
KX252298
EU080133
KX250940
KX250478
KX250765
EU080179
KX252621
KX251634
EU080206
EU080848
KX250443
KX252312
EU080045
KX252046
EU080534
KX252137
AB856794
KX251282
KX252333
EU080661
KX250590
KX251906
KX251038
KX251289
KX251704
KX250660
KX250674
KX250492
KX251295
KX252637
KX252573
KX251621
KX251213
KX252117
KX251628
KX251534
KX251858
KX250913
KX252594
KX251130
KX251220
KX250647
KX251234
KX252608
KX251248
KX250395
KX251116
KX252131
KX250584
KX252285
KX252299
EU080134
KX250941
KX250479
KX250766
EU080180
KX252622
KX251635
EU080207
EU080849
KX250444
KX252313
EU080046
KX252047
EU080535
KX252138
AB856797
KX251283
KX252334
EU080662
KX250591
KX251907
KX251039
KX251290
KX251705
KX250661
KX250675
KX250493
KX251296
KX252638
KX252574
KX251622
KX251214
KX252118
KX251629
KX251535
KX251859
KX250914
KX252595
KX251131
KX251221
KX250648
KX251235
KX252609
KX251249
KX250396
KX251117
KX252132
KX250585
KX252286
KX252300
EU080135
KX250942
KX250480
KX250767
EU080181
KX252623
KX251636
EU080208
EU080850
KX250445
KX252314
KX252631
KX252048
EU080536
KX252139
AB856800
KX251284
KX252335
EU080663
KX250592
KX251908
KX251040
N/A
KX251706
KX250662
KX250676
KX250494
KX251297
KX252639
13
184
Fungal Diversity (2020) 103:87–218
Table 24 (continued)
Species
#
P. multivesiculata
P. multivora#
P. nagaii
P. nemorosa
P. nicotianae#
P. niederhauserii#
P. obscura
P. occultans#
P. ornamentata
P. pachypleura#
P. palmivora#
P. parsiana#
P. parvispora#
P. phaseoli
P. pini#
P. pinifolia
P. pisi
P. pistaciae#
P. plurivora#
P. pluvialis#
P. polonica
P. primulae#
P. pseudocryptogea#
P. pseudosyringae#
P. pseudotsugae
P. psychrophila
P. quercetorum
P. quercina#
P. quininea
P. ramorum#
P. richardiae
P. riparia
P. rosacearum
P. rubi
P. sansomeana#
P. siskiyouensis#
P. sojae#
P. sp. brasiliensis
P. sp. canalensis
P. sp. citricola VIII
P. sp. cuyabensis
P. sp. delaware
P. sp. kelmania
P. sp. lagoariana
P. sp. personii
P. sp. sulawesiensis
P. stricta
P. syringae#
P. taxon parsley
P. taxon walnut
13
Strain
60S
tub2
tef1
Enl
HSP90
28S
TigA
30D4
55C5=CBS 124094
61H5=CBS 133248
28J3
22F9=ATCC 15410
01D5
60E9=CBS 129273
65B9=CBS 101557
66D2=CBS 140647
61H8
22G9
47C3=IMI 395329
30G9
35B6
22F1
47H1=CBS 122924
60A4
33D6=IMI 386658
22E9
60B3
40G9
29E9=CBS 620.97
ATCC52402
30A8=CBS 111772
ATCC52938
29J5=CBS 803.95
15C8
30A4=CBS 783.95
45F2=CBS 406.48
32G2
45F5=CBS 240.3
60B1=CBS 132024
22J9
30D7
47H5
41B7=CBS 122779
22D8=CBS 312.62
ATCC46705=P0630
P10456
27D9
P8213
63H4
24A7
60B4=P8220
P11555
P6306
58A2
23A6
61G1=BPIC 2584
40A7
KX250922
KX250775
KX251860
KX250957
KX250509
KX251714
KX252175
KX250600
KX251319
KX250796
KX251055
KX252357
KX251818
KX250502
KX250803
KX251333
KX251735
KX251748
KX250817
KX250971
KX252532
KX252063
EU080626
KX250978
EU080426
KX250992
KX251069
KX252647
EU080107
KX252147
KX251923
KX251347
KX251431
KX251550
KX251944
KX250677
KX251762
EU080419
EU079569
KX250838
EU080664
KX251396
KX251986
EU080358
EU080312
EU080345
KX252217
KX252203
KX252105
KX251452
KX250923
KX250776
KX251861
KX250958
KX250510
KX251715
KX252176
KX250601
KX251320
KX250797
KX251056
KX252358
KX251819
KX250503
KX250804
KX251334
KX251736
KX251749
KX250818
KX250972
KX252533
KX252064
EU080627
KX250979
EU080427
KX250993
KX251070
KX252648
EU080108
KX252148
KX251924
KX251348
KX251432
KX251551
KX251945
KX250678
KX251763
EU080420
EU079570
KX250839
EU080665
KX251397
KX251987
KX252502
EU080313
N/A
KX252218
KX252204
KX252106
KX251453
KX250924
KX250777
KX251862
KX250959
KX250511
KX251716
KX252177
KX250602
KX251321
KX250798
KX251057
KX252359
KX251820
KX250504
KX250805
KX251335
KX251737
KX251750
KX250819
KX250973
KX252534
KX252065
EU080628
KX250980
EU080428
KX250994
KX251071
KX252649
EU080109
KX252149
KX251925
KX251349
KX251433
KX251552
KX251946
KX250679
KX251764
EU080421
EU079571
KX250840
EU080666
KX251398
KX251988
EU080359
EU080314
EU080346
KX252219
KX252205
KX252107
KX251454
KX250925
KX250778
KX251863
KX250960
KX250512
KX251717
KX252178
KX250603
KX251322
KX250799
KX251058
KX252360
KX251821
KX250505
KX250806
KX251336
KX251738
KX251751
KX250820
KX250974
KX252535
KX252066
EU080629
KX250981
EU080429
KX250995
KX251072
KX252650
N/A
KX252150
KX251926
KX251350
KX251434
KX251553
KX251947
KX250680
KX251765
EU080422
EU079572
KX250841
EU080667
KX251399
KX251989
EU080360
EU080315
EU080347
KX252220
KX252206
KX252108
KX251455
KX250926
KX250779
KX251864
KX250961
KX250513
KX251718
KX252179
KX250604
KX251323
KX250800
KX251059
KX252361
KX251822
KX250506
KX250807
KX251337
KX251739
KX251752
KX250821
KX250975
KX252536
KX252067
EU080630
KX250982
EU080430
KX250996
KX251073
KX252651
KX252522
KX252151
KX251927
KX251351
KX251435
KX251554
KX251948
KX250681
KX251766
EU080423
EU079573
KX250842
EU080668
KX251400
KX251990
EU080361
EU080316
EU080348
KX252221
KX252207
KX252109
KX251456
KX250927
KX250780
KX251865
KX250962
KX250514
KX251719
KX252180
KX250605
KX251324
KX250801
KX251060
KX252362
KX251823
KX250507
KX250808
KX251338
KX251740
KX251753
KX250822
KX250976
KX252537
KX252068
EU080631
KX250983
EU080431
KX250997
KX251074
KX252652
EU080110
KX252152
KX251928
KX251352
KX251436
KX251555
KX251949
KX250682
KX251767
EU080424
EU079574
KX250843
EU080669
KX251401
KX251991
EU080362
EU080317
EU080349
KX252222
KX252208
KX252110
KX251457
KX250928
KX250781
KX251866
KX250963
KX250515
KX251720
KX252181
KX250606
KX251325
KX250802
KX251061
KX252363
KX251824
KX250508
KX250809
KX251339
KX251741
KX251754
KX250823
KX250977
KX252538
KX252069
N/A
KX250984
EU080432
KX250998
KX251075
KX252653
KX252523
KX252153
KX251929
KX251353
KX251437
KX251556
KX251950
KX250683
KX251768
EU080425
N/A
KX250844
EU080331
KX251402
KX251992
EU080363
EU080318
EU080350
KX252223
KX252209
KX252111
KX251458
Fungal Diversity (2020) 103:87–218
185
Table 24 (continued)
Species
Strain
60S
tub2
tef1
Enl
HSP90
28S
TigA
P. taxon-aquatilis
P. taxon-castitis
P. taxon-emzansi
P. tentaculata#
P. terminalis
P. thermophila
P. trifolii
P. tropicalis#
P. uliginosa
P. vignae#
P. virginiana
38J5
61E7=CBS 131246
61F2
29F2=CBS 552.96
65B8=CBS 133865
55C1=CBS 127954
29B2
35C8=CBS 434.91
62A3=CBS 109054
45G9=ATCC 64832
44G6
KX250929
KX252098
KX250859
EU079955
KX250607
KX251354
KX251951
KX250698
EU080011
KX251783
KX252371
KX250930
KX252099
KX250860
EU079956
KX250608
KX251355
KX251952
KX250699
EU080012
KX251784
KX252372
KX250931
KX252100
KX250861
EU079957
KX250609
KX251356
KX251953
KX250700
EU080013
KX251785
KX252373
KX250932
KX252101
KX250862
EU079958
KX250610
KX251357
KX251954
KX250701
KX251571
KX251786
KX252374
KX250933
KX252102
KX250863
EU079959
KX250611
KX251358
KX251955
KX250702
KX251572
KX251787
KX252375
KX250934
KX252103
KX250864
EU079960
KX250612
KX251359
KX251956
KX250703
EU080015
KX251788
KX252376
KX250935
KX252104
KX250865
EU079961
KX250613
KX251360
KX251957
KX250704
KX251573
KX251789
KX252377
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains and voucher strains are in bold. Species confirmed with pathogenicity studies are marked
with #. (VdPN) are strains used by Van der Plaäts-Niterink (1981) for descriptions
Fig. 40 Disease cycle of a
Pythium species (redrawn from
van West et al. 2003)
and Campbell 1973; Hsieh 1978; Ventura et al. 1981; Chun
and Schneider 1998; Eberle et al. 2007; Kreye et al. 2009;
Oliva et al. 2010; Banaay et al. 2012; Van Buyten and Höfte
2013). Pythium insidiosum causes pythiosis in mammals
including humans (van der Plaäts-Niterink 1981; de Cock
et al. 1987). Some species target below-ground plant parts
and some species can cause fruit rot, however, some Pythium
species can also benefit plants as endophytes by acting as
biocontrol agents (Benhamou et al. 1997) and by stimulating
plant growth (Martin and Loper 1999; Mazzola et al. 2002).
Pathogen biology, disease cycle and epidemiology
Pythium species grow and colonize a plant by producing hyphae which extract nutrients from the host. Once
the hyphae from opposite mating types meet, they produce
thick-walled oospores which serve as overwintering structures. Upon germination, an oospore may produce more
hyphae, or develop a zoosporangium, which produces motile
zoospores that swim to and infect plants. Zoosporangia can
also germinate and directly infect plants (Ho 2009; van West
et al. 2003).
13
186
Morphological based identification and diversity
Pythium has hyaline hyphae which are coenocytic without cross septa (van der Plaäts-Niterink 1981). Filamentous
and globose sporangia are present, and zoospores develop
in a vesicle, which is formed at the tip of a discharge tube
from a sporangium. After fertilization with paragynous or
hypogynous antheridia, oospores are formed in smooth or
ornamented oogonia. The oospore can fill the whole organism or can have space between the walls of the oogonia and
oospore. The process of zoospore formation within a vesicle
is a characteristic feature of the genus, which distinguishes it
from morphologically similar genera such as Phytophthora
and Halophytophthora. However, the formation of zoospores
is similar to Lagenidium, which features endobiotic and holocarpic features not observed in Pythium (Dick 2001). Species
delimitation based on morphological characteristics such as
shape and size of sporangia and oogonia is difficult as these
characteristics are often shared among different species.
Molecular based identification and diversity
Lévesque and de Cock (2004) separated the genus into
11 clades (A-K) using phylogenies of ITS and 28S. Clade
K, which includes P. vexans was transferred to a new genus
Phytopythium with Phytopythium sindhum as type species
(Bala et al. 2010), while the remaining clades can be divided
into two groups: species with filamentous sporangia (clades
A-D) and species with globose sporangia (clades E–J).
Identification of Pythium isolates to species level is recommended based on cox1 and ITS gene regions. The use of
ITS region alone cannot accurately identify all Pythium species. Several species are indistinguishable based on both ITS
and cox1 sequences. Lévesque and de Cock (2004) provided
the first extensive study of Pythium, accepting 116 species.
Additional species have recently been described for example
P. alternatum (Rahman et al. 2015), P. biforme, P. brachiatum, P. junctum, P. utonaiense (Uzuhashi et al. 2015), P.
cedri (Chen et al. 2017), P. heteroogonium, P. longipapillum,
P. oryzicollum (Salmaninezhad and Mostowfizadeh-Ghalamfarsa 2019). Currently, there are more than 130 accepted
species in the genus (Arafa et al. 2020). The phylogenetic
tree constructed is presented in Fig. 41 and the information
of species are given in Table 25.
Recommended genetic markers (generic level within
Pythium sensu lato)—18S (small subunit, SSU) and 28S
(large subunit, LSU) nuclear rRNA genes
Recommended genetic markers (sub-generic, inter- and
intra-specific level)—The internal transcribed spacers (ITS
including ITS1, 5.8S rRNA, and ITS2), cytochrome c oxidase subunit 2 (cox2)
Accepted number of species—There are 330 epithets listed
in Index Fungorum (2020), however only 157 species have
DNA sequence data (Table 25).
13
Fungal Diversity (2020) 103:87–218
References—van der Plaäts-Niterink (1981), Dick (2001) (morphology), Lévesque and de Cock (2004), Hyde et al. (2014),
Arafa et al. (2020) (phylogeny and accepted species numbers)
100. Rhizopus Ehrenb., Nova Acta Phys.-Med. Acad. Caes.
Leop.-Carol. Nat. Cur. 10: 198 (1821)
Background
Rhizopus is classified in the subphylum Mucoromycotina,
class Mucoromycetes, order Mucorales and family Rhizopodaceae (Wijayawardene et al, 2018, 2020). The genus is
one of the most diverse and constitutes an important genus
within the order Mucorales. Rhizopus species are common
post-harvest pathogens of fruits, vegetables, crops and stored
foods, while some Rhizopus species are human pathogens.
Rhizopus arrhizus and Rhizopus microsporus can cause mucoromycosis in immunocompromised humans (Yildirim et al.
2010; Benedict and Brandt 2016). Morphology-based (size
of sporangia and sporangiophores, and rhizoids) and physiology-based (growth temperature) identification and classification grouped the genus in three groups: R. microsporus, R.
stolonifer, and R. arrhizus (syn: R. oryzae) (Schipper 1984).
Schipper (1984) and Schipper and Stalpers (1984), provided
the first significant monographs of Rhizopus. Fundamental
morphological-based identification was provided which
is still widely used in current taxonomic classification for
Rhizopus (Schipper 1984; Schipper and Stalpers 1984; Hartanti et al. 2015). The inclusion of DNA-based phylogenetic
tools has resulted in significant changes in the taxonomic
classification (Vebliza et al. 2018). With the implementation
of molecular-based identification, Abe et al. (2006, 2010),
Zheng et al. (2007b), and Liu et al. (2007) provided significant contributions in the classification of Rhizopus. Briefly,
in current taxonomy Rhizopus arrhizus is a synonym of R.
oryzae, R. reflexus to R. lyococcus and Amylomyces rouxii is
a synonym of Rhizopus arrhizus (Liu et al. 2007; Hyde et al.
2014; Vebliza et al. 2018) (Fig. 42).
Phylogenomic approaches have the potential to provide a
clear understanding of the inter-relationships of species (Gryganskyi et al. 2018). In recent revisions, data from wholegenome sequencing have been used (Gryganskyi et al. 2018).
Phylogenetic analysis based on a dataset of 192 orthologous
protein-coding genes extracted from whole-genome sequencing of representative species provided a robust phylogeny
and tree topology for Rhizopus. The phylogenetic analysis
resulted in similar tree topology obtained from studies which
utilize ITS and pyrG genes or 76 orthologous proteins from
the genomes (Liu et al. 2007; Chibucos et al. 2016). In brief,
R. microsporus is suggested to be a monophyletic sister clade
to other Rhizopus clades, R. stolonifer was found to be sister to R. arrhizus and R. delemar and these four species are
monophyletic (Gryganskyi et al. 2010, 2018).
A comparative analysis of the mating-type locus across
Rhizopus revealed that its structure is flexible even between
Fungal Diversity (2020) 103:87–218
187
Fig. 41 Maximum likelihood of
Pythium species based on the
concatenated SSU, ITS, LSU,
cox2 and tub2 regions. The
maximum parsimonious dataset
consisted of 528 constant, 71
parsimony-informative and 556
parsimony-uninformative characters. The parsimony analysis
of the data matrix resulted in
the maximum of ten equally
most parsimonious trees with
a length of 1637 steps (CI =
0.200, RI = 0.737, RC = 0.147,
HI = 0.800). ML and MP bootstrap support values over 60%
and BYPP ≥ 0.90 are indicated.
Type strains are in bold and the
11 clades (A–K) are indicated.
Scale bar indicates number of
substitutions per site. The tree
was rooted with Lagenidium
giganteum (CBS 580.84) and
Lagenidium sp. (DAOM 242348
and CBS 127283). Likelihood
of the best scoring ML tree
was − 28453.969593. Estimated base frequencies were
as follows: A = 0.264872, C
= 0.163069, G = 0.213432,
T = 0.358627; substitution
rates AC = 1.219282, AG =
3.062456, AT = 3.113530, CG
= 0.855790, CT = 4.379562,
GT = 1.000000
13
188
Fig. 41 (continued)
13
Fungal Diversity (2020) 103:87–218
Fungal Diversity (2020) 103:87–218
189
Table 25 DNA barcodes available for Pythium
Species
Isolate
Host
SSU
ITS
Pythium abappressorium#
P. acanthicum#
P. acanthophoron#
P. acrogynum
CBS 110198
Triticum aestivum
HQ643408
HQ643408 HQ643408 KJ595409
KJ595533
CBS 377.34
CBS 337.29
CBS 549.88
AY598617
AY598711
N/A
AY598617 AY598617 KJ595380
AY598711 AY598711 KJ595376
AY598638 AY598638 AB362324
KJ595504
KJ595500
KJ595458
P. adhaerens
P. afertile
P. alternatum
P. amasculinum
CBS 520.74
LEV2066
GUCC0015
CBS 552.88
AY598619
N/A
N/A
AY598671
AY598619
HQ643416
AB998876
AY598671
KJ595386
KJ595440
KJ595390
KJ595510
KJ595563
N/A
KJ595514
P. anandrum#
P. angustatum#
AY598650
AY598623
AY598650 AY598650 AB362328
AY598623 AY598623 KJ595387
KJ595450
KJ595511
Unknown
Soil (Vitis sp.)
Nymphyoidespeltata
Soil
Triticum aestivum
Zea mays
AY598622
HQ643443
AY598631
AY598632
AY598627
AKXY02050628
AY598622
HQ643443
AY598631
AY598632
AY598627
AY598628
AY598622
HQ643443
AY598631
AY598632
AY598627
AY598628
KJ595344
KJ595422
KJ595400
KJ595355
AB507410
AKXY02053172
KJ595472
KJ595547
KJ595524
KJ595481
DQ071297
KJ595451
Prunus serotina
Aquatic
Soil
Aquatic
Linumusitatissimum
Hordeum vulgare
Soil
Soil
Soil (spoil heap)
Soil
Turf grass
HQ643476
N/A
AY598662
N/A
AY598659
GQ244426
HQ643482
AY598635
HQ643373
N/A
AY598675
HQ643476
KJ995584
AY598662
KJ995581
AY598659
GQ244426
HQ643482
AY598635
HQ643373
HQ643484
AY598675
HQ643476
KJ995601
AY598662
KJ995603
AY598659
GQ244426
HQ665069
AY598635
HQ643373
HQ665111
AY598675
AB512889
N/A
EF408876
N/A
KJ595368
KJ595433
JX397983
KJ595360
AB690678
KJ595427
KJ595404
AB512822
N/A
EF408882
N/A
KJ595493
KJ595558
JX397969
KJ595485
KJ595464
KJ595551
KJ595528
P. caudatum#
P. cederbergense#
P. cedri#
P. chamaehyphon#
P. chondricola#
P. citrinum
P. coloratum#
P. conidiophorum#
P. contiguanum
P. cryptoirregulare#
CBS 285.31
CBS 522.74
(VdPN)
CBS 118.80
CBS 120945
CBS 772.81
CBS 215.80
CBS 263.38
CBS 324.62
(VdPN)
DAOM 230386
UZ00796
CBS 551.88
UZ00736
CBS 288.31
CBS 124059
CBS 112353
CBS 222.94
CBS 112544
CBS 122659
CBS 842.68
(VdPN)
CBS 584.85
CBS 133716
Chen 30
CBS 259.30
CBS 203.85
CBS 119171
CBS 154.64
CBS 223.88
CBS 221.94
CBS 118731
Solanum tuberosum
Ananas sativus
Soil (Spinacia
oleracea)
Soil
Turf grass
Soil
Soil (vegetable
garden)
Rheum rhaponticum
Soil
HQ643136
N/A
N/A
AY598666
N/A
HQ643375
AY598633
AY598629
HQ643514
HQ643515
HQ643136
JQ412768
KX423751
AY598666
AY598620
HQ643375
AY598633
AY598629
HQ643514
HQ643515
HQ665277
KJ716864
N/A
AY598666
AY598620
HQ643375
AY598633
AY598629
HQ665162
HQ643515
AF290309
JQ412805
N/A
AB257280
KJ595354
AB690679
KJ595346
KJ595361
KJ595358
GU071763
KJ595459
JQ412781
N/A
KJ595448
KJ595480
KJ595465
KJ595474
KJ595486
KJ595483
GU071888
P. cucurbitacearum#
P. cylindrosporum#
P. cystogenes#
P. debaryanum#
P. delawarense
P. deliense#
P. diclinum#
CBS 748.96
CBS 218.94
CBS 675.85
CBS 752.96
CBS 123040
CBS 314.33
CBS 664.79
Xiphinemarivesi
Aspalathuslinearis
roots of Cedrus
Carica papaya
Chondruscrispus
Soil (Vitis sp.)
Soil (tree nursery)
Soil
Soil (salt marsh)
Euphorbia pulcherrima
Unknown
Soil
Viciafaba
Tulipa sp.
Glycine max
Nicotiana tabacum
Beta vulgaris
AY598667
AY598643
HQ643518
AY598704
KF853241
AY598674
N/A
AY598667
AY598643
HQ643518
AY598704
EU339312
AY598674
AY598690
AY598667
AY598643
HQ643518
AY598704
KF853240
AY598674
HQ665282
AB690680
GU071762
KJ595396
KJ595399
KJ595430
KJ595372
KJ595394
KJ595460
GU071877
KJ595520
KJ595523
KJ595555
KJ595497
KJ595518
P. aphanidermatum#
P. apiculatum
P. apleroticum
P. aquatile#
P. aristosporum
P. arrhenomanes#
P. attrantheridium#
P. biforme
P. boreale
P. brachiatum
P. buismaniae
P. camurandrum
P. canariense
P. capillosum
P. carbonicum#
P. carolinianum#
P. catenulatum#
LSU
AY598619
HQ643416
N/A
AY598671
cox2
tub2
13
190
Fungal Diversity (2020) 103:87–218
Table 25 (continued)
Species
#
P. dimorphum
P. dissimile
P. dissotocum#
P. echinulatum#
P. emineosum
P. erinaceum
P. ershadii
P. flevoense
P. folliculosum#
P. glomeratum#
P. graminicola#
P. grandisporangium#
P. helicandrum
P. helicoides#
P. heteroogonium
P. heterothallicum#
P. hydnosporum#
P. hypogynum#
P. inflatum#
P. insidiosum#
P. intermedium#
P. irregular#
P. iwayamai#
P. jasmonium
P. junctum
P. kashmirense#
P. kunmingense#
P. litorale#
P. longandrum#
P. longipapillum#
P. longisporangium#
P. lucens#
P. lutarium#
P. lycopersici#
P. macrosporum#
P. mamillatum#
P. marinum#
P. marsipium#
P. mastophorum#
P. megacarpum
13
Isolate
Host
SSU
ITS
CBS 406.72
CBS 155.64
CBS 166.68
(VdPN)
CBS 281.64
(VdPN)
CBS 124057
CBS 505.80
IRAN2379C
CBS 234.72
CBS 220.94
CBS 122644
CBS 327.62
Pinus taeda
Pinus radiata
Triticum aestivum
AY598651
AY598681
AY598634
AY598651 AY598651 AB362331
AY598681 AY598681 KJ595347
AY598634 AY598634 KJ595351
KJ595454
KJ595475
KJ595479
Soil (forest nursery)
AY598639
AY598639 AY598639 AB362327
KJ595449
N/A
N/A
N/A
AY598691
AY598676
N/A
AY598625
GQ244427
AY598694
KT894054
AY598691
AY598676
HQ643542
AY598625
KJ595432
AB362326
KJ595363
N/A
KJ595424
AF196593
KJ595557
KJ595456
N/A
KJ595488
N/A
KJ595548
KJ595452
AY598692
AY598692 AY598692 KJ595367
KJ595492
AY598653
AY598665
N/A
AY598654
AY598672
AY598653
AY598665
KX228103
AY598654
AY598672
KJ595453
AB511994
KX228117
AB512850
KJ595489
AY598693
AY598626
HQ643565 HQ665171 AB362325
AY598626 AY598626 KJ595352
KJ595447
N/A
AF289981
AY598647
AY598637 AY598637 KJ595391
AY598647 AY598647 AB507410
KJ595515
AB512836
AY598702
AY598648
AY598702 AY598702 GU071760
AY598648 AY598648 JX397979
GU071886
JX397965
HQ643778
N/A
HQ643671
AY598700
HQ643386
HQ643778
KJ995576
HQ643671
AY598700
HQ643386
HQ643778
KJ995605
HQ643671
HQ665259
HQ643386
KJ595406
N/A
KJ595429
KJ595389
KJ595418
KJ595530
N/A
KJ595553
KJ595513
KJ595543
HQ643679
N/A
N/A
HQ643681
HQ643682
N/A
HQ643679
KX228105
HQ643680
HQ643681
HQ643682
HQ643683
HQ665071
N/A
HQ665099
HQ643681
HQ665163
HQ665119
KJ595413
KX228130
KJ595426
KJ595415
KJ595359
KJ595343
KJ595538
KX228114
KJ595550
KJ595540
KJ595484
KJ595554
AY598646
AY598703
AY598646 AY598646 AB512916
AY598703 HQ665173 AB362325
AB512842
AB512844
N/A
N/A
AY598661
AY598689 AY598689 KJ595398
AY598699 HQ665297 KJ595401
AY598661 AY598661 KJ595378
KJ595522
KJ595525
KJ595502
HQ643388
HQ643388 HQ643388 AB690665
KJ595536
Juniperus communis
Soil
Soil
Soil
Soil
Soil
Saccharum officinarum
CBS 286.79
Decaying leaf (Zostera marina)
CBS 393.54
Rumex acetosella
CBS 286.31
Phaseolus vulgaris
079-1 - CBS 141232 Soil
CBS 450.67
Soil (Sambucus)
CBS 253.60
Unknown
(VdPN)
CBS 234.94
Soil
CBS 168.68
Saccharum offici(VdPN)
narum
CBS 574.85
Equus ferus
CBS 266.38
Agrostis stolonifera
(VdPN)
CBS 250.28
Phaseolus vulgaris
CBS 156.64
Soil (Pinus sp.)
(VdPN)
CBS 101876
Arabidopsis thaliana
UZ00732
Aquatic
CBS 122908
Soil
CBS 550.88
Soil (Viciafaba)
CBS 118360
Soil (Phragmites
australis)
CBS 112355
Soil
NRh8*
Soil
CBS 122646
Soil (Vitis sp.)
CBS 113342
Triticum
CBS 222.88
Soil
CBS 122909
Soil (Lycopersicum
esculentum)
CBS 574.80
Flower bulb
CBS 251.28
Beta vulgaris
(VdPN)
CBS 750.96
Soil
CBS 773.81
Nymphyoides peltata
CBS 375.72
Apiumgraveolens
(VdPN)
CBS 112351
Soil (Vitis sp.)
LSU
GQ244427
HQ665243
N/A
AY598691
HQ665160
HQ665097
AY598625
AY598653
AY598665
N/A
AY598654
AY598672
cox2
AB362329
DQ071377
KX228131
AB512919
KJ595364
tub2
Fungal Diversity (2020) 103:87–218
191
Table 25 (continued)
Species
P. megalacanthum
P. mercurial#
Isolate
#
P. middletonii#
P. minus#
P. monospermum#
P. montanum
P. multisporum
P. nagaii#
P. nodosum#
P. nunn#
P. oedochilum#
P. okanoganense#
P. oligandrum#
P. oopapillum#
P. ornacarpum
P. ornamentatum
P. orthogonon#
P. oryzicollum#
P. ostracodes#
P. pachycaule#
P. paddicum#
P. paroecandrum#
P. parvum
P. pectinolyticum
P. periilum#
P. periplocum#
P. perplexum#
P. phragmitis#
P. pleroticum
P. plurisporium#
P. polare#
P. polymastum#
P. porphyrae#
P. phragmiticola
P. prolatum#
P. pyrioosporum
P. pyrilobum#
P. radiosum
P. recalcitrans#
P. rishiriense
P. rhizo-oryzae#
CBS 101356
CBS 122443
Host
Chrysanthemum
Macadamia integrifolia
CBS 528.74(VdPN) Soil
CBS 226.88
Soil
CBS 158.73
Soil
(VdPN)
CBS 111349
Soil (Picea abies)
CBS 470.50
Soil
CBS 779.96
Soil
CBS 102274
Soil
CBS 808.96
Soil
CBS 292.37
Unknown
CBS 315.81
Triticum aestivum
CBS 382.34
Viola sp.
(VdPN)
CBS 124053
Cucumis sativus
CBS 112350
Soil
CBS 122665
Soil
CBS 376.72
Zea mays
Kr7
Soil
CBS 768.73
Soil
(VdPN)
CBS 227.88
Soil
CBS 698.83
Triticum and Hordeum
CBS 157.64
Soil
(VdPN)
CBS 225.88
Soil
CBS 122643
Soil
CBS 169.68
Soil
(VdPN)
CBS 289.31
Citrullus vulgaris
CBS 674.85
Viciafaba
CBS 117104
Soil (Phragmites
australis)
CBS 776.81
Nymphyoides peltata
CBS 100530
Agrostis
CBS 118203
Sanionia uncinata
CBS 811.70
Lactuca sativa
(VdPN)
CBS 369.79
Porphyrayezoensis
(VdPN)
P56
Soil
CBS 845.68
Rhododendron sp.
IRAN2382C
Soil
CBS 158.64
Pinus radiata
CBS 217.94
Soil
CBS 122440
Soil (Vitis vinifera)
GUCC0007
Aquatic
CBS 119169
Soil
SSU
ITS
LSU
N/A
KF853243
HQ643693 KJ716865
DQ916363 KF853236
cox2
tub2
KJ595435
AB690666
N/A
KJ595466
N/A
HQ643696
HQ643697
AY598640 AY598640 AB362318
HQ643696 HQ665168 AB362320
HQ643697 HQ643697 KJ595350
KJ595457
KJ595446
KJ595478
HQ643389
AY598641
AY598705
N/A
AY598709
AY598664
AY598649
AY598618
HQ643389
AY598641
AY598705
HQ643709
AY598709
AY598664
AY598649
AY598618
HQ643389
AY598641
AY598705
HQ665055
AY598709
AY598664
AY598649
AY598618
KJ595410
AB362319
KJ595402
KJ595407
AF196609
AB108011
KJ595373
KJ595381
KJ595534
KJ595455
KJ595526
KJ595531
DQ071325
EF408883
KJ595498
KJ595505
N/A
HQ643721
N/A
AY598710
N/A
AY598663
FJ655174
HQ643721
HQ643722
AY598710
KX228072
AY598663
FJ655174
HQ643721
HQ665117
HQ665221
N/A
AY598663
KJ595431
KJ595411
KJ595428
KJ595379
KX228125
AB690668
KJ595556
KJ595535
KJ595552
KJ595503
KX228108
EF408880
AY598687
AY598707
AY598687 HQ665169 KJ595362
AY598707 AY598707 JX397982
KJ595487
JX397968
AY598644
AY598644 AY598644 DQ071391
DQ071332
AY598697
HQ643739
AY598683
AY598697 AY598697 AB362322
HQ643739 HQ643739 N/A
AY598683 HQ665141 N/A
KJ595445
KJ595469
KJ595444
AY598670
AY598658
HQ643746
AY598670 AY598670 KJ595369
AY598658 AY598658 KJ595395
HQ643746 HQ665081 AJ890351
KJ595494
KJ595519
EU152854
AY598642
AY598684
KJ716858
AY598660
AY598642
AY598684
AB299390
AY598660
AB362321
KJ595405
KJ595417
KJ595403
KJ595461
KJ595529
KJ595542
KJ595527
AY598673
AY598673 AY598673 KJ595377
KJ595501
N/A
AY598652
N/A
AY598636
N/A
N/A
N/A
HQ643757
KC145165
AY598652
KT894052
AY598636
AY598695
DQ357833
AB998878
HQ643757
KC145167
KJ595462
N/A
KJ595477
N/A
EF195143
N/A
KJ595545
AY598642
AY598684
KJ716859
AY598660
N/A
AY598652
N/A
AY598636
HQ665156
KJ716861
N/A
HQ643757
KC145166
AB362330
KJ595349
KJ595356
KJ595423
KJ595420
13
192
Fungal Diversity (2020) 103:87–218
Table 25 (continued)
Species
Isolate
Host
SSU
ITS
P. rhizosaccharum
CBS 112356
N/A
HQ643760 HQ665072 AB362323
KJ595463
P. rostratifingens#
P. rostratum#
P. salpingophorum#
CBS 115464
CBS 533.74
CBS 471.50
(VdPN)
CBS 129726
CBS 294.37
CBS 112354
CBS 129728
CBS 122490
CBS 119359
CBS 275.67
(VdPN)
CBS 462.48
(VdPN)
DAOM 240293
CBS 110030
CBS 603.73
CBS 453.67
CBS 122491
LEV1534
CBS 316.33
(VdPN)
CBS 323.65
CBS 219.65
Soil (Saccharum
officinarum)
Soil (Malus sp.)
Soil
Lupinus angustifolius
Glycine max
Ipomoea batatas
Soil
Zea mays
Soil (forest)
Phaseolus vulgaris
Compost
HQ643761
AY598696
AY598630
HQ643761 HQ643761 KJ595416
AY598696 AY598696 KJ595388
AY598630 AY598630 KJ595384
KJ595541
KJ595512
KJ595508
N/A
AY598680
HQ643772
N/A
HQ643773
N/A
AY598701
JF836869
AY598680
HQ643772
JF836871
HQ643773
EF688275
AY598701
JF895530
KJ595370
KJ595412
JF895532
AB362317
KJ595421
KJ595366
KJ595470
KJ595495
KJ595537
KJ595471
KJ595467
KJ595546
KJ595491
Unknown
AY598655
AY598655 AY598655 AB512921
AB512852
Soil
Soil
Daucus carota
Soil
Soil
Turfgrass
Grass
N/A
N/A
AY598682
AY598645
HQ643854
N/A
AY598624
KJ716866
HQ643836
AY598682
AY598645
HQ643854
HQ643855
AY598624
KJ595437
KJ595408
KJ595393
KJ595383
AB362315
KJ595439
KJ595374
KJ595560
KJ595532
KJ595517
KJ595507
KJ595468
KJ595562
KJ595499
Lactuca sativa
N/A
AY598677 HQ665207 KJ595375
Chenopodium album AKYB02045405 AY598656 AY598656 KJ595357
N/A
KJ595482
P. schmitthenneri#
P. scleroteichum#
P. segnitium
P. selbyi#
P. senticosum#
P. solare
P. spinosum#
P. splendens#
P. stipitatum
P. sukuiense
P. sulcatum#
P. sylvaticum#
P. takayamanum
P. tardicrescens#
P. torulosum#
P. tracheiphilum#
P. ultimum var.
sporangiiferum#
P. ultimum var.
ultimum#
P. uncinulatum#
P. undulatum#
CBS 398.51
CBS 518.77
CBS 157.69
(VdPN)
P. urmianum
IRAN2376C
P. utonaiense
UZ00769
CBS 295.37
P. vanterpoolii#
CBS 119.80(VdPN)
P. vexans#
#
CBS 119168
P. viniferum
CBS 159.64
P. violae#
(VdPN)
P. wohlseniorum
W15-2
Pythiumsp. rooibos 2 STE-U 7550
LSU
KJ716862
AY598680
HQ643772
KJ716863
HQ643773
KJ716860
AY598701
KJ716866
HQ665059
HQ665281
AY598645
HQ643854
HQ643855
AY598624
cox2
tub2
Lepidium sativum
AY598657
AY598657 AY598657 KJ595382
KJ595506
Lactuca sativa
Soil (Pinus sp.)
AY598712
AY598708
AY598712 AY598712 KJ595385
AY598708 AY598708 KJ595348
KJ595509
KJ595476
Soil
Aquatic
Triticum aestivum
Soil
Soil (Vitis sp.)
Soil
N/A
N/A
AY598685
HQ643400
HQ643956
AY598706
KT894049
KJ995587
AY598685
HQ643400
HQ643956
AY598706
N/A
N/A
KJ595496
EF426556
KJ595544
JX397966
Aquatic
Aspalathus linearis
N/A
N/A
MH277978 MH289800 MH289798
JQ412777 N/A
JQ412813
N/A
KJ995600
AY598685
HQ643400
HQ643956
AY598706
N/A
KJ595371
GU133518
KJ595419
JX397980
MH289799
JQ412789
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains and voucher strains are in bold. Species confirmed with pathogenicity studies are marked
with #. (VdPN) are strains used by Van der Plaäts-Niterink (1981) for descriptions
different species in the same genus, but shows similarities
between Rhizopus and other mucoralean taxa. Variation of
the genome size was also noted to be approximately three-fold
within a species which are induced by changes in transposable element copy numbers and genome duplications (Gryganskyi et al. 2018). Bruni et al. (2019) successfully adapted
the CRISPR-Cas 9 technique for inducing pyrF gene-specific
13
mutations in two strains of R. delemar, the causative agent of
mucoromycosis. This new tool is suggested to be useful in
investigating the pathogenesis mechanisms of R. delemar and
also generating specific mutants of Mucorales fungi.
Classification—Mucoromycota, Mucoromycotina, Mucoromycetes, Mucorales, Rhizopodaceae
Fungal Diversity (2020) 103:87–218
193
Fig. 42 Phylogenetic tree generated by maximum likelihood
analysis of combined ITS- LSUSSU sequence data of Rhizopus,
Backusella and Mucor species.
Twenty-six taxa containing
2600 characters including gaps
were used in the phylogenetic
analysis. The tree was rooted
using Backusella circina (CBS
128.70) and Mucor indicus
(CBS 226.29). The best scoring
RAxML tree with a final likelihood value of − 11138.113172
is presented. The matrix contained 761 distinct alignment
patterns, with 41.20% of undetermined characters or gaps.
Estimated base frequencies
were as follows: A = 0.293528,
C = 0.180262, G = 0.236482,
T = 0.289728; substitution
rates AC = 0.787730, AG =
2.127667, AT = 1.579251, CG
= 0.715792, CT = 3.683423,
GT = 1.000000; gamma distribution shape parameter α =
0.181944.ML bootstrap support
values greater than 70% are
shown near the nodes. The type
species are in bold. Scale bar
indicates the number of substitutions per site
Type species—Rhizopus stolonifera (Ehrenb.) Vuill. 1902
Distribution—worldwide
Disease symptoms—Rhizopus blight, Rhizopus head rot and
Rhizopus soft rot
Rhizopus blight: Rhizopus blight can affect flowers, leaves,
and stems. When infected, the plant shows symptoms such as
soft and mushy brown rot. The rot produces white mycelia with
black sporangia and the abundant mycelia projects a ‘bearded’
appearance. Spores of the fungus can be spread by water and
air. The mode of infection is similar to bacterial soft rot in
which enzymes secreted by the fungus causes cell deterioration
of the host tissue. The fungi require high temperatures, high
humidity and weakened host tissues or wounds (Hartley 1992).
Rhizopus head rot on sunflowers: Rhizopus head rot
may be caused by several Rhizopus species such as Rhizopus arrhizus, R. microsporus and R. stolonifer (Markell
et al. 2015). Historically, Rhizopus head rot was deemed
as a minor disease. However, recent surveys have shown
their severity. Initial signs of Rhizopus head rot are dark
spots of different sizes on different types of wounds on the
plant. Soft watery rot appears on the infected fruit which
often turns dark brown and extends to the back of the flower
head, sepals and peduncles as the disease progresses. The
infected sunflower receptacle disintegrates and becomes soft
and pulpy. Infection by Rhizopus causes the head to shrivel
and dry. Morphological characteristics are mycelial strands
bearing sporangiophore and sporangia which are seen as the
disease advances (Markell et al. 2015; Zhou et al. 2018).
These whiskers are tufts of hyphae containing numerous
sporangia and generally appear around lenticels or breaks
in the periderm. Sometimes hyphae may not be visible on
the outside of the root but can be viewed by pulling apart the
infected tissue, giving it a stringy appearance (Clark et al.
2013).
13
194
Table 26 DNA barcodes
available for Rhizopus
Fungal Diversity (2020) 103:87–218
Species name
Isolate no
SSU
ITS
LSU
Rhizopus americanus
R. arrhizus#
CBS 340.62*
CBS 111231
CBS 544.80
NRRL 1469
CBS 427.87*
33515
CBS 392.95
CBS336.62*
FSU2530
EML-HO95-1*
EML-HO95-2
strain FSU10053
CBS 319.35
CBS 320.35
CBS 699.68*
CBS 337.62
IFO 4810
CBS 112.07*
CBS 130146
CBS 138.95
ATCC 96514*
CBS 336.39*
CBS 389.95
SICAUCC 19-0001
NG_062623
HM999967
JN206338
JN206337
DQ641279
NR_137056
AF115730
MH862535
HM999968
KJ408567
KU058202
KU058203
NG_057873
R. caespitosus
R. delemar
R. homothallicus
R. koreanus
R. lyococcus
R. microsporus#
R. niveus#
R. oryzae#
R. schipperae
R. sexualis#
R. stolonifer#
NG_062622
NG_062624
KJ408537
KU058194
KU058195
KJ408545
AB250177
NG_062621
NG_064824
NG_063011
MN148534
AB100449
JN206373
HM999970
JN206362
DQ641284
NR_103595
MH865585
NR077174
DQ641323
AB113017
DQ641318
MN267051
NG_057871
DQ466604
MH874170
NG_057870
KJ408554
KU058196
KU058197
KJ408562
JN206534
MH869765
NG_056282
MH877020
HM849672
NG_059417
MH867536
MN148530
Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher
strains are also in bold. Species confirmed with pathogenicity studies are marked with #
Rhizopus soft rot: Common causative agents of Rhizopus soft rot are Rhizopus stolonifer and Rhizopus oryzae.
The disease is considered as one of the most common and
destructive postharvest diseases in many plants such as sweet
potato (Ipomoea batatas), potato (Solanum tuberosum) and
tomato (Solanum lycopersicum). The most frequent mode of
infection is wounds and injuries present on the plants. Studies have also shown that the type of wounding and storage
time have a significant impact on the susceptibility of infection by Rhizopus species (Scruggs and Quesada-Ocampo
2016). Earliest symptoms of infections are soft water-soaked
lesions. The disease spreads across the wounded area and
progresses to the extremities of the substrate. Hyphae soon
develop on the rotten tissues and produce grey sporangiophores which subsequently bear sporangia (Khokhar et al.
2019). Whiskers are characteristics features of Rhizopus soft
rot and have been reported in the case of soft rot on sweet
potatoes (Clark et al. 2013; Scruggs and Quesada-Ocampo
2016) (Table 26).
Hosts—Wide range of hosts including species of Allium,
Ananas, Brassica, Cucumis, Cucurbita, Fragaria, Lycopersicon, Phaseolus, Pisum and Solanum (Farr and Rossman
2020)
13
Pathogen biology, disease cycle and epidemiology
The pathogen reproduces asexually. Spores of Rhizopus
species are commonly found in the air and can survive easily on crop debris, fruits, vegetables, and even on tools and
equipment. Factors such as the Rhizopus species, type of
fruit, stage of maturity of the plant and fruit or the storage
will have a slight difference in the disease cycle. Rhizopus
stolonifer, as well as the other species causing post-harvest
diseases such as Rhizopus soft rot, require wound injuries,
cracks or any mechanical damage for entry (Hartley 1992;
Bautista-Baños et al. 2014; Scruggs and Quesada-Ocampo
2016). Infection and colonization are highly dependent on
the enzymes produced by the fungi. To establish within the
host, Rhizopus species produce numerous enzymes, including amylase, pectinase, and cellulase that can damage cell
walls and permit host colonization (Ogundero 1988; Tang
et al. 2012). This results in the softening of the host tissue; one of the symptoms of the disease (Nelson 2009;
Kwon et al, 2012; Bautista-Baños et al. 2014; Feliziani and
Romanazzi 2016). During initial stages of infection, Rhizopus rot appears as water-soaked areas and in the case of
Rhizopus stolonifer, the rot also exudes clear leachate. In
the case of Rhizopus soft rot caused by R. oryzae in banana,
Fungal Diversity (2020) 103:87–218
the symptoms and disease cycle are similar to R. stolonifer (Kwon et al. 2012). In Okinawan sweet potatoes, the
disease causes a soft and moist appearance and a stringy
flesh during the initial stages and as the disease progresses,
the tissue of the sweet potato turns brownish and eventually
black (Nelson 2009). In the case of R. stolonifer, the fungal
mycelia quickly spread across the infection site. The sporangia formed are normally black and the whole plant is covered
by fungal mycelia (Bautista-Baños et al. 2014). The enzymes
exuded from the pathogen generally liquefy the internal tissues, for an example in sweet potato parenchyma of the root
becomes liquefied, leaving the periderm and outer fibres of
the root intact (Scruggs and Quesada-Ocampo 2016). The
disease becomes more severe in warm, humid environments
(Zoffoli and Latorre 2011). Avoidance of Rhizopus species is
difficult due to their ubiquitous nature; therefore, sanitation
and storing produce under unfavourable disease conditions
is the key to control this pathogen.
Morphology- based identification and diversity
Rhizopus is normally distinguished by rhizoids, stolons
and single or branched sporangiophores (Vebliza et al.
2018). Identification of species takes into account the growth
temperature, size of sporangiophore and sporangium and the
branching of rhizoids (Abe et al. 2007). The white mycelia
consist of coenocytic hyphae which bear the sporangiophore
with normally black sporangia. These taxa are fast-growing
and form rhizoids at the base of sporangiophores. The sporangium contains a columella and spores (Bullerman 2003).
During the sexual stage, there is the formation of zygospores
and chlamydospores can also be seen during the growth of
the fungi (Bullerman 2003; Abe et al. 2007).
Molecular identification and diversity
Traditionally, Rhizopus species were classified using morphological characters such as the shape and size of the structures (chlamydospores, rhizoids, sporangiophores and columellae) and physiological features such as optimal growth
conditions. Current classification and taxonomic grouping
follow that of Schipper (Schipper 1984). Schipper classified Rhizopus into three groups namely R. microsporus, R.
stolonifer and R. arrhizus based on the physiological factors
and morphology (Abe et al. 2010; Gryganskyi et al. 2018).
Later, studies such as Abe et al. (2006), Liu et al. (2007),
Zheng et al. (2007a, b), Abe et al. (2010) implemented
molecular phylogeny using DNA sequence data in the classification of these fungi. With novel approaches used, the
classification proposed by Schipper was found to agree with
some recent studies while others divided the genus into ten
species and seven varieties or eight species. Zheng et al.
(2007b) used zygospore formation, and molecular systematic
195
morphological characters, mating compatibility, physiology
and molecular systematic to accept the division of the genus
in ten species and seven varieties. Abe et al. (2010) also used
the rDNA ITS gene region together with actin-1 and tef1, to
reorganize the proposed taxonomy into eight species instead
of ten species. One important data provided by this study
was the problematic rDNA ITS region of R. americanus. It
was discovered that R. sexualis var. americanus has three
rDNA ITS gene regions which are distinct from each other.
However, Liu et al. (2007) were not able to obtain all three
rDNA ITS gene region instead they were able to amplify
only one ITS region which was similar to that of Rhizopus
oryzae. So, this led to the conclusion that R. americanus was
phylogenetically different from R. sexualis.
Genetic markers (species and genus level)—ITS and rpb1
Genetic markers (higher-level phylogeny)—SSU, LSU and
act
Accepted number of species—There are 152 species epithets
in Index Fungorum (2020), however only 12 species have
DNA sequence data (Table 25).
References—Bullerman (2003), Abe et al. (2007) (morphology); Abe et al. (2010), Gryganskyi et al. (2018), Vebliza
et al. (2018) (morphology and phylogeny)
Discussion
This is the fourth in the One Stop Shop series focusing on
providing a stable platform for the taxonomy of plant pathogenic fungi and fungus-like organisms. These series aim to
provide updated backbone trees and information regarding
plant pathogens in one place for ease of access. Databases
play an important role in aggregating the scattered data into
an easily accessible form and many of the pathogenic genera were annotated in the UNITE database (Nilsson et al.
2014). However, this database mainly focused on ITS region
rather than the protein-coding gene regions. There are very
few databases dedicated to identity the plant pathogens and
related fungi-like organisms. We have been trying to provide
a stable and updated taxonomy for 97 genera and three families since 2014, which are listed in Table 1. All this information is available in http://www.onestopshopfungi.org.
Acknowledgements Dr Yong Wang thanks National Natural Science
Foundation of China (No. 31972222, 31560489), Program of Introducing Talents of Discipline to Universities of China (111 Program,
D20023), Talent project of Guizhou Science and Technology Cooperation Platform ([2017]5788-5 and [2019]5641) and Guizhou Science, Technology Department International Cooperation Basic project
([2018]5806), Guizhou University cultivation project [2017]5788-33.
Kevin D. Hyde would like to thank “the future of specialist fungi in
a changing climate: baseline data for generalist and specialist fungi
associated with ants, Rhododendron species and Dracaena species”
13
196
(Grant No. DBG6080013), Thailand Research Fund (TRF) Grant no
RDG6130001 “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Subregion”. Work of Viktor Papp was
supported by the Ministry for Innovation and Technology within the
framework of the Higher Education Institutional Excellence Program
(NKFIH-1159-6/2019) in the scope of plant breeding and plant protection research of Szent István University. Sinang Honsanan would like to
thank the National Natural Science Foundation of China for supporting
the Project no. 31950410548. Our thanks are due to the Research and
Researchers for Industries Grant (PHD57I0015) for financial support
to Boontiya Chuankid. Napalai Chaiwan would like to thank the Royal
Golden Jubilee PhD Program under Thailand Research Fund (RGJ) The
scholarship no. PHD60K0147. Mingkwan Doilom thanks the 5th batch
of Postdoctoral Orientation Training Personnel in Yunnan Province
(Grant no.: Y934283261) and the 64th batch of China Postdoctoral
Science Foundation (Grant no.: Y913082271).
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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Affiliations
Ruvishika S. Jayawardena1,2,7 · Kevin D. Hyde1,2,3,18 · Yi Jyun Chen2,7 · Viktor Papp4 · Balázs Palla4 · Dávid Papp5,6 ·
Chitrabhanu S. Bhunjun2,7 · Vedprakash G. Hurdeal2,7 · Chanokned Senwanna2,8 · Ishara S. Manawasinghe2,9,18 ·
Dulanjalee L. Harischandra2,7,9 · Ajay Kumar Gautam10 · Shubhi Avasthi11 · Boontiya Chuankid2,7 ·
Ishani D. Goonasekara2,7 · Sinang Hongsanan12 · XiangYu Zeng2,7,19 · Kapila K. Liyanage2,17,20 · NingGuo Liu2 ·
Anuruddha Karunarathna2,8 · Kalani K. Hapuarachchi2 · Thatsanee Luangharn2,3 · Olivier Raspé2,7 ·
Rashika Brahmanage2,7,9 · Mingkwan Doilom3,16,17 · Hyang B. Lee13 · Liu Mei9 · Rajesh Jeewon14 ·
Naruemon Huanraluek2 · Napalai Chaiwan2,7 · Marc Stadler15 · Yong Wang1
1
Department of Plant Pathology, Agriculture College,
Guizhou University, Guiyang 550025, Guizhou, China
2
Center of Excellence in Fungal Research, Mae Fah Luang
University, Chiang Rai, Thailand
3
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
4
Department of Botany, Szent István University, Villányi út
29-43, Budapest 1118, Hungary
5
Plant Pathology and Plant-Microbe Biology Section, Cornell
University, Geneva, NY 6 14456, USA
6
Department of Pomology, Szent István University, Villányi út
29-43, Budapest 1118, Hungary
7
School of Science, Mae Fah Luang University,
Chiang Rai 57100, Thailand
8
9
Department of Entomology and Plant Pathology,
Faculty of Agriculture, Chiang Mai University, No. 9 of
Shuguanghuayuanzhonglu, Chiang Mai 50200, Thailand
Institute of Plant and Environment Protection, Beijing
Academy of Agriculture and Forestry Sciences,
Haidian DistrictHaidian District, Beijing 100097,
People’s Republic of China
10
School of Agriculture, Abhilashi University, Mandi,
Himachal Pradesh 175028, India
11
School of Studies in Botany, Jiwaji University,
Gwalior 474011, India
13
12
Guangdong Provincial Key Laboratory for Plant Epigenetics,
College of Life Sciences and Oceanography, Shenzhen
University, Shenzhen 518055, PR China
13
Environmental Microbiology Lab, Dept. of Agricultural
Biological Chemistry, College of Agriculture and Life
Sciences, Chonnam National University, Gwangju 61186,
Korea
14
Department of Health Sciences, Faculty of Science,
University of Mauritius, Reduit, Mauritius
15
Department of Microbial Drugs, Helmholtz
Centre for Infection Research, Inhoffenstraße 7,
38124 Braunschweig, Germany
16
Honghe Innovation Center for Mountain Futures, Kunming
Institute of Botany, Honghe County, Yunnan 654400,
People’s Republic of China
17
World Agroforestry Centre, East and Central Asia,
Kunming 650201, Yunnan, People’s Republic of China
18
Institute of Plant Health, Zhongkai University of Agriculture
and Engineering, Guangzhou 510225, China
19
Faculty of Agriculture, Natural Resources and Environment,
Naresuan University, Phitsanulok 65000, Thailand
20
Rubber Research Institute of Sri Lanka, Dartonfield,
Agalawatta, Sri Lanka