Fungal Diversity
https://doi.org/10.1007/s13225-019-00433-6
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One stop shop III: taxonomic update with molecular phylogeny
for important phytopathogenic genera: 51–75 (2019)
Ruvishika S. Jayawardena1,2 • Kevin D. Hyde1,2,3 • Eric H. C. McKenzie4 • Rajesh Jeewon5 •
Alan J. L. Phillips6 • Rekhani H. Perera2,7 • Nimali I. de Silva2,8 • Sajeewa S. N. Maharachchikumburua9
Milan C. Samarakoon2,8 • Anusha H. Ekanayake2 • Danushka S. Tennakoon2,7 • Asha J. Dissanayake2 •
Chada Norphanphoun2,7 • Chuangen Lin2,7 • Ishara S. Manawasinghe2,7,10 • Qian Tian2,7 •
Rashika Brahmanage2,7,10 • Putarak Chomnunti2,7 • Sinang Hongsanan11 • Subashini C. Jayasiri2,7 •
F. Halleen12,13 • Chitrabhanu S. Bhunjun2,7 • Anuruddha Karunarathna2,8 • Yong Wang1
•
Received: 3 June 2019 / Accepted: 23 July 2019
Ó School of Science 2019
Abstract
This is a continuation of a series focused on providing a stable platform for the taxonomy of phytopathogenic fungi and
organisms. This paper focuses on 25 phytopathogenic genera: Alternaria, Capnodium, Chaetothyrina, Cytospora,
Cyphellophora, Cyttaria, Dactylonectria, Diplodia, Dothiorella, Entoleuca, Eutiarosporella, Fusarium, Ilyonectria, Lasiodiplodia, Macrophomina, Medeolaria, Neonectria, Neopestalotiopsis, Pestalotiopsis, Plasmopara, Pseudopestalotiopsis, Rosellinia, Sphaeropsis, Stagonosporopsis and Verticillium. Each genus is provided with a taxonomic background,
distribution, hosts, disease symptoms, and updated backbone trees. A new database (Onestopshopfungi) is established to
enhance the current understanding of plant pathogenic genera among plant pathologists.
Keywords Classification Database Plant pathology Phylogeny Taxonomy Symptoms Systematics
& Yong Wang
yongwangbis@aliyun.com
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
8
Department of Biology, Faculty of Science, Chiang Mai
University, Chiang Mai 50200, Thailand
9
School of Life Science and Technology, University of
Electronic Science and Technology of China,
Chengdu 611731, People’s Republic of China
10
Institute of Plant and Environment Protection, Beijing
Academy of Agriculture and Forestry Sciences, No. 9 of
Shuguanghuayuanzhonglu, Haidian District, Beijing 100097,
People’s Republic of China
11
College of Life Science and Oceanography, Shenzhen
University, 1068, Nanhai Avenue, Nanshan,
Shenzhen 518055, China
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
Landcare Research-Manaaki Whenua,
Private Bag 92170, Auckland, New Zealand
5
Department of Health Sciences, Faculty of Science,
University of Mauritius, Reduit, Mauritius
12
Plant Protection Division, ARC Infruitec-Nietvoorbij,
Private Bag X5026, Stellenbosch 7599, South Africa
6
Faculdade de Ciéncias, Biosystems and Integrative Sciences
Institute (BioISI), Universidade de Lisboa, Campo Grande,
1749-016 Lisbon, Portugal
13
Department of Plant Pathology, University of Stellenbosch,
Private Bag X1, Matieland 7602, South Africa
7
School of Science, Mae Fah Luang University,
Chiang Rai 57100, Thailand
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Fungal Diversity
Contents and contributors (main
contributors underlined)
51. Capnodium–P Chomnunti, RS Jayawardena
52. Chaetothyrina–S Hongsanan, RS Jayawardena
53. Cytospora–C Norphanphoun, RS Jayawardena, KD
Hyde
54. Cyphellophora–Q Tian, RS Jayawardena
55. Cyttaria–AH Ekanayake
56. Dactylonectria–RH Perera
57. Entoleuca–MC Samarakoon
58. Eutiarosporella–RS Brahmanage, AJL Phillips, RS
Jayawardena
59. Ilyonectria–RH Perera
60. Macrophomina–DS Tennakoon, AJL Phillips
61. Medeolaria–AH Ekanayake
62. Neonectria–RH Perera, F. Halleen
63. Neopestalotiopsis–NI de Silva, SSN
Maharachchikumbura, RS Jayawardena
64. Plasmopara–IS Manawasinghe, EHC McKenzie
65. Pseudopestalotiopsis–NI de Silva, SSN
Maharachchikumbura, RS Jayawardena
66. Rosellinia–MC Samarakoon
67. Sphaeropsis–DS Tennakoon, AJL Phillips
Updated genera
68. Alternaria–RS Jayawardena, KD Hyde
69. Diplodia–AJ Dissanayake, AJL Phillips
70. Dothiorella–RS Jayawardena, AJL Philips
71. Fusarium–RH Perera
72. Lasiodiplodia–AJL Phillips, RS Jayawardena
73. Pestalotiopsis–NI de Silva, SSN
Maharachchikumbura
74. Stagonosporopsis–SC Jayasiri, RS Jayawardena
75. Verticillium–CG Lin
Introduction
One stop shop (OSS) is a series of papers focused on
providing a stable platform for the taxonomy of plant
pathogenic fungi and organisms. Genera included in these
paper series are associated with plant diseases. However,
some may not be well-known plant pathogens and Kochs’
postulates might have not been conducted in order to
establish their pathogenicity. When this series was launched in 2014, its specific aims were mentioned (Hyde et al.
2014). Two issues of OSS have been published in which 50
genera were treated (Hyde et al. 2014; Jayawardena et al.
2019). In this study we treat 25 genera of plant pathogens
as well as establish a new website, www.onestopshopfungi.
org, to host a database for plant pathogenic fungi and
123
organisms. This fungal database allows mycologists and
plant pathologists to understand disease symptoms, host
distribution, classification, morphology and provides an
updated phylogeny which will enhance current understanding of plant pathogens and gain better insights into the
current fungal classification system. The Onestopshopfungi
webpage is an output funded by the Mushroom Research
Foundation, Thailand, which is a non-government and nonprofit organization. We invite all mycologists to contribute
to make this a success. The outcome of this series provides
a stable taxonomy and phylogeny for plant pathogens that
can provide a reliable platform for mycologists and plant
pathologists to accurately identify causal organisms.
Material and methods
Photo plates of the symptoms of the disease and morphological characters are given, when available. Classification
follows Wijayawardene et al. (2018).
Sequence data from ex-type, ex-epitype or authentic
strains for each species were retrieved from GenBank.
Sequence data from single gene regions were aligned using
Clustal X1.81 (Thompson et al. 1997) and further alignment of the sequences were carried out by 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 for each genus.
Phylogenetic analyses consisted of maximum likelihood
(ML), maximum parsimony (MP) and Bayesian inference
(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 2012) or
RAxML-HPC2 on XSEDE (8.2.8) in the CIPRES science
gateway platform (Miller et al. 2010) using GTR?I?G
model of evolution. Bayesian inference was used to construct the phylogenies using Mr. Bayes v.3.1.2 (Ronquist
and Huelsenbeck 2003). MrModeltest v. 2.3 (Nylander
et al. 2008) was used for statistical selection of best-fit
model of nucleotide substitution and was incorporated into
the analyses.
Results
Capnodium Mont., Annls Sci. Nat., Bot, sér. 3, 11: 233
(1849)
Fungal Diversity
The genus Capnodium was introduced by Montagne
(1849) to accommodate C. salicinum. Capnodium is one of
the most commonly found sooty moulds in gardens and
landscapes (Laemmlen 2011). Capnodium has a saprobic
association with sap-feeding insects in the Order Homoptera, which includes aphids, whiteflies, soft scale, mealy
bugs, leafhoppers and psyllids (Barr 1987). Gavrilov-Zimin
(2017) reported that the larvae and female of a new species
and a new monotypic genus of legless mealybug, Orbuspedum machinator, from bamboo twigs in southern
Thailand are covered with densely packed fungal hyphae of
the sooty mould Capnodium sp. Herath et al. (2012)
reported that a tropical sooty mould (Capnodium sp.) is
known to produce antibiotics such as tetramic acid,
methiosetin and epicorazin A.
Capnodium species grow on honeydew, gradually covering the surface of the plant part affected by insects,
colouring it with various shades of black. These fungi do
not colonize the plant tissues or trigger symptoms. However, they alter the ability of the plant to perform photosynthesis and exchange of gases with the atmosphere.
Severely affected leaves may die and fall, thereby affecting
plant growth and survival. Therefore, we treat Capnodium
as a main plant pathogenic group.
Classification—Dothideomycetes,
Dothideomycetidae,
Capnodiales, Capnodiaceae
Type species—Capnodium salicinum Mont., Annls Sci.
Nat., Bot, sér. 3 11:234 (1849)
Distribution—Species of Capnodium have a wide distribution but are most common in tropical and subtropical
regions (Chomnunti et al. 2014). They can be found on
plants that have been previously fed upon by insects.
Disease symptoms—Dark mycelium coating surface of
host can cause chlorosis and reduce photosynthetic ability
of plants, which effects plant growth, reduces yield, and
leading to marketability problems (Chomnunti et al. 2014;
Fig 1). In higher latitudes, Capnodium spp. are scarce
during the winter; the most common being C. salicinum in
the UK (Cannon et al. 1985; Royal Botanic Gardens, Kew,
UK National Collection of Dried Fungi, unpublished data).
Warm-temperate climates in Australia and the Mediterranean countries provide an abundance of perennial foliage
on which sooty moulds are able to establish themselves
during the winter, and so persist from one season to the
next (Fraser 1935; Reynolds and Gilbert 2005). In northern
Thailand, most of the sooty mould infections are caused by
Capnodium species (Chomnunti et al. 2014).
Hosts—Many plants when colonised by insects that
produce honeydew. Species of Annona, Camellia, Citrus,
Coffea, Chrysophyllum, Ficus, Malus, Mangifera, Olea,
Populus, Prunus, Psidium, Rhododendron and Salix (Farr
and Rossman 2019)
Morphological based identification and diversity
The asexual morph forms elongated pycnidia that develop
from a superficial mycelium on living plant surfaces and
produce tiny, hyaline conidia on top of the pycnidia
(Chomnunti et al. 2011). Persoon (1822) mention that
Fumago citri is the sooty mould but it was not well
described and completed; therefore it was transferred to
genus Polychaeton by Léveillé (1847). Later, Berkeley-
Fig. 1 Sooty moulds on various
host plants associated with
insects. a On a hardwood tree,
b on guava, c on coffee, d–f on
mango
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Fungal Diversity
Desmazieres (1849) transferred all species once known in
the genus Fumago to Capnodium. Molecular evidence
revealed that Polychaeton is an asexual stage of Capnodium, therefore, both are the same organism. According to
‘‘one fungus one name’’ and the Melbourne Code under
Art. 57.2, Capnodium was considered for conservation as it
has a larger number of epithets and is more widely used in
this group of fungi, even though Polychaeton is the older
name (Chomnunti et al 2011, 2014; McNeill et al. 2012;
Hyde et al. 2013; Wijayawardene et al. 2014, 2017, 2018;
Liu et al. 2015; Hongsanan et al. 2015).
The morphology of Capnodium species can be recognised by black mycelial growth spreading on the host
surface, which produces superficial colonies with septate,
dark brown hyphae and cylindrical and bitunicate asci. On
host surface Capnodium species share the same ecological
niche and are similar in appearance to other genera and
families of sooty moulds; often found with sexual and
asexual states growing together and living in complex
communities (Faull et al. 2002; Hughes 2003; Hughes and
Seifert 2012; Chomnunti et al. 2014; Hongsanan et al.
2015).
Table 1 Details of Capnodium isolates used in the phylogenetic
analyses
Species
Isolate/voucher no
ITS
C. coffeae
AFTOL-ID 939
DQ491515
C. coffeae
CBS 147.52
AJ244239
Capnodium coffeae
CTQE057
KX893384
Capnodium coffeicola
MFLUCC 15-0206*
KU358921
Capnodium salicinum
CBS 131.34
AJ244240
Capnodium sp.
SZ-F22
KT443921
Capnodium sp.
Capnodium sp.
S80
CP1
MH633887
MH629975
Capnodium sp.
OUCMBI101100
HQ914834
Capnodium sp.
ELM115
KU556052
Capnodium sp.
GPO-CO-02
KC180729
Capnodium sp.
agrFF1633
HE584839
Capnodium sp.
agrFF1683
HE584838
Capnodium sp.
agrFF1681
HE584837
Capnodium sp.
agrFF1679
HE584836
Capnodium sp.
agrFF1678
HE584835
Capnodium sp.
agrFF1639
HE584834
Capnodium sp.
agrFF1638
HE584833
Molecular based identification and diversity
Capnodium sp.
agrFF1614
HE584832
Capnodium sp.
agrFF1613
HE584831
DNA sequencing data of Capnodium coffeae, C. coartatum, C. salicinum, C. coffeicola and C. dematum and eleven unidentified Capnodium spp. are available in GenBank,
including sequence data for LSU, SSU and ITS (4/7/2019).
Hongsanan et al. (2015) introduced a new species Capnodium coffeicola. It differs from other Capnodium species
in having pycnidia with short and black stalks at the base
and is swollen at the central part, and it has cylindrical to
oblong conidia, but its placement is supported with phylogenetic analysis using LSU and ITS sequence data.
Sooty moulds often grow in colonies of more than one
species, and taxonomic descriptions thus often unknowingly combine elements of different genera and species.
Identification based on morphology only is difficult as
there are overlapping morphological characters among
many taxa (Chomnunti et al. 2011, 2014). To achieve
accurate generic and species identification and taxonomic
placements, phylogenetic studies using large subunit ribosomal RNA (LSU rRNA) gene sequences and the internal
transcribed spacer regions and 5.8S nrDNA gene (ITS)
were performed (Crous et al. 2009; Chomnunti et al.
2011, 2014; Liu et al. 2015; Hongsanan et al. 2015).
This study reconstructs the phylogeny of Capnodium
based on analyses of ITS sequence data (Table 1, Fig. 2)
and corresponds with previous studies (Chomnunti et al.
2011, 2014; Hongsanan et al. 2015). This can be used as a
backbone tree in the identification of Capnodium species
(Fig. 3).
Capnodium sp.
agrFF0153
HE584830
Capnodium sp.
Capnodium sp.
agrFF1634
agrFF1631
HE584829
HE584828
Capnodium sp.
agrFF0180
HE584822
Capnodium sp.
agrFF1690
HE584823
Species
Isolate/Voucher no
ITS
Capnodium sp.
agrFF0045
HE584825
Capnodium sp.
agrFF0207
HE584826
Capnodium sp.
TMS-2011
HQ631045
Capnodium sp.
TTI-247
KU985278
Conidiocarpus plumeriae
MFLUCC 15-0205
KU358919
Conidiocarpus siamensis
MFLUCC 10-0053
KU358922
Co. siamensis
MFLUCC 10-0061
KU358923
Co. siamensis
MFLUCC 10-0062
KU358924
Co. siamensis
MFLUCC 10-0063
KU358925
Co. siamensis
MFLUCC 10-0064
KU358926
Co. siamensis
MFLUCC 10-0065
KU358927
Co. siamensis
Scoria leucadendri
MFLUCC 10-0074
CBS 131318
KU358928
JQ044437
123
Ex-type (or ex-epitype) strains are in bold and marked with an
asterisk* and voucher strains are in bold
Recommended genetic marker (genus level)—LSU
Recommended genetic markers (species level)—LSU, ITS
Sequence data of LSU, SSU and ITS are available for
five species of Capnodium in GenBank but none of them
has complete sequence data. LSU is useful for preliminary
Fungal Diversity
Fig. 2 Morphology of Capnodium sp. a pycnidia on the host. b, d, e, f stalked pycnidia c mycelium network, g conical pycnidium and pycnidial
wall, h ostiole surrounded by hyaline hyphae, i conidia. Scale bars: b, d–f = 100 lm, c, g = 50 lm, h, = 20 lm, i = 10 lm
identification at the generic level (Chomnunti et al
2011, 2014; Quaedvlieg et al 2014). Hongsanan et al.
(2015) recommended the use of combined LSU and ITS
sequence data to identify the species. More protein-coding
gene loci should be sequenced to clarify the taxonomic
problems in this genus. In the current analyses, C. cortatum
was not included due to lack of ITS sequences in GenBank.
A revision of this genus is needed as it may reveal many
new species. Re-sequencing of species as well as designating epitypes or representative species is also important.
Accepted number of species: There are 140 epithets in
Index Fungorum (2019), however only four species have
DNA sequence data.
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Fungal Diversity
Fig. 3 Phylogenetic tree generated by maximum likelihood analysis
of ITS sequence data of Capnodium species. Related sequences were
obtained from GenBank. Thirty-eight strains are included in the
analyses, which comprise 512 characters including gaps. The tree was
rooted with Scoria leucadendri (CBS 131318). Tree topology of the
ML analysis was similar to the MP analysis. The best scoring RAxML
tree with a final likelihood value of - 2398.970137 is presented. The
matrix had 236 distinct alignment patterns, with 16.01% of undetermined characters or gaps. Estimated base frequencies were as follows;
A = 0.285338, C = 0.285338, G = 0.241464, T = 0.238894;
123
substitution rates AC = 1.204962, AG = 1.857184, AT = 2.642904,
CG = 1.319860, CT = 4.051266, GT = 1.000000; gamma distribution shape parameter a = 0.287147. The maximum parsimonious
dataset consisted of constant 327, 125 parsimony-informative and 60
parsimony-uninformative characters. The parsimony analysis of the
data matrix resulted in the maximum of two equally most parsimonious trees with a length of 358 steps (CI = 0.735, RI = 0.875,
RC = 0.630, HI = 0.265) in the first tree. RAxML and maximum
parsimony bootstrap support value C 50% are shown, respectively,
near the nodes. Ex-type strains are in bold
Fungal Diversity
References: Chomnunti et al 2011, 2014; Quaedvlieg et al
2014; Hongsanan et al. 2015 (morphology, phylogeny).
Chaetothyrina Theiss., Annls mycol. 11(6):495 (1913)
The genus Chaetothyrina was established by Theissen
(1913), with C. musarum (Speg.) Theiss as the type species. Chaetothyrina was placed in Micropeltidaceae based
on its superficial, flattened base, poorly developed thyriothecium and irregular meandering arrangement of compact
hyphae of walled cells. Singtripop et al. (2016) provided
molecular data of one reference specimen and one new
species. Hongsanan et al. (2017) established a new species
of Chaetothyrina and introduced a new family Phaeothecoidiellaceae to accommodate species of Chaetothyrina,
Houjia and Phaeothecoidiella in Capnodiales. Based on its
placement in phylogenetic trees and the morphological
uniqueness, Micropeltidaceae was excluded from
Microthyriales and treated as family incertae sedis in
Lecanoromycetes (Hongsanan et al. 2017; Zeng et al.
2019) (Fig. 4).
Classification—Dothideomycetes, incertae sedis, Capnodiales, Phaeothecoidiellaceae
Type species—Chaetothyrina musarum (Speg.) Theiss.,
Annls mycol. 11(6):495 (1913)
Distribution—Known from Brazil, Cook Islands, Dominican
Republic, India, Mexico, Pakistan, Panama, Thailand, US
Disease symptoms—Sooty blotch and flyspeck
Species in this genus cause flyspeck disease on various
plants, such as C. musarum on Musa sp. and C. panamensis
(F. Stevens & Dorman) Arx on Oncoba laurina. Sooty
blotch and flyspeck (SBFS) is a disease complex caused by
nearly 80 fungal species (Singtripop et al. 2016) that are
epiphytes which blemish the epicuticular wax layer of
several fruit crops, such as apple, pear, orange, persimmon,
banana and grape worldwide (Gleason et al. 2011; Gao
et al. 2014), cutting sale price and limiting the growth rate
of fruit production (Williamson and Sutton 2000; Gao et al.
2014). ‘Sooty blotch’ is characterized by colonies produced
on host tissues from superficial, spreading, dark irregular
blotches of mycelium with or without sclerotium-like
structures or fruiting bodies. On the other hand, ‘flyspeck’
defines clusters of shiny, small, black sclerotium-like
structures or fruiting bodies, lacking visible intercalary
mycelium (Gleason et al. 2011; Mayfield et al. 2012;
Singtripop et al. 2016).
Hosts—Species of Anacardium, Anodendron, Anogeissus, Carallia, Cassia, Chonemorpha, Dalbergia, Dianella,
Euonymus, Hevea, Iiana, Magnifera, Magnolia, Mammea,
Maytenus, Memecylon, Mitragyna, Musa, Myrcia, Ochrocarpos, Olea, Oncoba, Phoebe, Similax, Streblus and
Vochysia.
Morphological based identification and diversity
Chaetothyrina is characterized by superficial, flattened
thyriothecia, with base poorly developed, with thyriothecial setae and 1-septate ascospores (Reynolds and Gilbert
2005; Singtripop et al. 2016; Hongsanan et al. 2017).
Chaetothyrina can be distinguished from other species in
Micropeltidaceae on the basis of thyriothecial setae
appearance, shape and septation of the ascospores (Singtripop et al. 2016; Hongsanan et al. 2017). Twenty-three
species of Chaetothyrina epithets are listed in Index Fungorum (2019), but sequence data are available for only two
species (4/7/2019). Chaetothyrina is a poorly studied
genus. Fresh collections and sequence data are needed for
this genus. The disease cycle of this genus is yet to be
established (Fig. 5).
Fig. 4 Disease symptoms caused by Chaetothyrina spp. a on mango, b, d appearance of thyriothecia on hosts, c on a banana, e on mango leaves
123
Fungal Diversity
Molecular based identification and diversity
Singtripop et al. (2016) provided a reference type specimen
of C. musarum with sequence data. Using combined LSU,
SSU and ITS sequence data, Chaetothyrina clustered as a
sister genus to Houjia and Phaeothecoidiella within
Capnodiales (Hongsanan et al. 2017; Table 2, Fig. 6).
Fig. 5 Chaetothyrina guttulata a Thyriothecium when viewed in squash mount. b Surface of thyriothecium. c Section through thyriothecium.
d Ascus when immature. e Asci at maturity. f Ascospores. Scale bars: a = 50 lm, b, d, e = 10 lm, c = 100 lm, f = 5 lm
123
Fungal Diversity
Recommended genetic markers (genus level)—LSU and
SSU
Recommended genetic markers (species level)—ITS and
RPB2
Accepted number of species: There are 23 epithets in Index
Fungorum (2019). However, only two species have
molecular data.
Table 2 Details of
Chaetothyrina isolates used in
the phylogenetic analyses
References: Reynolds and Gilbert 2005; Singtripop et al.
2016; Hongsanan et al. 2017 (morphology, phylogeny)
Cytospora Ehrenb., Sylv. mycol. berol.: 28 (1818)
Cytospora was introduced by Ehrenberg (1818) as the
type genus of the family Cytosporaceae in Diaporthales
(Wehmeyer 1975; Barr 1978; Eriksson et al. 2001;
Castlebury et al. 2002). The genus is an important
Species
Isolate/voucher no
LSU
SSU
ITS
Austroafricana associata
CBS 120732
KF901829
–
KF901512
Capnobotryella renispora
CBS 215.90
GU214399
AY220613
AY220613
Capnodium coffeae
CBS 147.52
GU214400
DQ247808
AJ244239
Chaetothyrina guttulata
MFLUCC15-1080
KU358917
KU358916
KX372277
C. guttulata
MFLUCC15-1081*
KU358914
KU358915
KX372276
C. musarum
MFLUCC15-0383
KU710171
KU710174
KX372275
C. musarum
MFLUCC15-0383
KU710171
KU710174
KX372275
Devriesia strelitziae
CBS 122379
GU301810
GU296146
EU436763
Dissoconium aciculare
CBS 204.89
GU214419
GU214523
AY725520
D. dekkeri
CBS 342.86
JN232431
–
–
Dothistroma septosporum
CBS:112498
GQ852597
JX901744
JX901744
Hortaea werneckii
4263
JX141471
JX141470
DQ336709
Houjia yanglingensis
YHLB20
GQ433630
–
GQ433629
H. yanglingensis
YHJN13*
GQ433631
–
GQ433628
Leptoxyphium cacuminum
Mycosphaerella ellipsoidea
MFLUCC10-0049*
CBS:110843*
JN832602
GQ852602
JN832587
AY725545
AY725545
M. endophytica
CBS:114662*
GQ852603
DQ302953
DQ302953
–
M. keniensis
CBS:111001*
GQ852610
–
Myriangium duriaei
CBS 260.36
NG027579
AF242266
–
M. hispanicum
CBS 247.33
GU301854
GU296180
–
Phaeothecoidiella illinoisensis
CBS:125223
GU117901
–
GU117897
P. missouriensis
CBS:118959
GU117903
–
GU117899
Phragmocapnias asiticus
MFLUCC10-0062
JN832612
JN832597
–
P. betle
MFLUCC10-0053
JN832606
JN832591
–
P. betle
MFLUCC10-0050
JN832605
JN832590
–
Pseudoveronaea ellipsoidea
MI3 34F1a*
JQ622103
–
FJ425205
P. obclavata
UIF3
AY598916
–
AY598877
Ramichloridium apiculatum
CBS 400.76
EU041851
EU041794
EU041794
Rasutoria pseudotsugae
rapssd
EF114704
EF114729
EF114687
R. tsugae
ratstk
EF114705
EF114730
EF114688
Schizothyrium pomi
S. pomi
CUA1a
Flyspeck1924-Zj001
AY598895
AY598894
–
–
EF164898
AY598848
Scorias spongiosa
MFLUCC10-0084
JN832586
JN832601
–
S. spongiosa
AFTOL-ID 1594
DQ678075
DQ678024
–
Stomiopeltis versicolor
GA3 23C2b
FJ147163
–
FJ438375
Zygophiala cryptogama
KY1 1.2A1c*
EF164902
–
EF164900
Z. tardicrescens
MWA1a*
EF164901
–
AY598856
Z. wisconsinensis
MSTA8a*
AY598897
–
AY598853
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
123
Fungal Diversity
Fig. 6 Phylogenetic tree generated by maximum parsimony analysis
of combined LSU, SSU and ITS sequence data. Thirty-nine strains are
included in the analyses, which comprised 2225 characters including
gaps. The tree was rooted with Myriangium duriaei (CBS 260.36) and
M. hispanicum (CBS 247.33). The maximum parsimonious dataset
consisted of 1645 constant, 461 parsimony-informative and 119
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 = 0.549, RI 0.736,
RC = 0.404, HI = 0.451) in the first tree. MP and ML bootstrap
values C 50% and bayesian posterior probabilities C 0.90 (BYPP)
are shown respectively near the nodes. Ex-type strains are in bold
pathogenic fungus, causing canker and dieback on branches of a wide range of hosts with a wide distribution
(Adams et al. 2005, 2006; Hyde et al. 2017, 2018; Norphanphoun et al. 2017, 2018).
Classification—Sordariomycetes,
Diaporthomycetidae,
Diaporthales, Valsaceae
Type species—Cytospora chrysosperma (Pers.) Fr. 1823
Distribution—Worldwide
Disease symptoms—Canker and dieback disease on
branches
Hosts—Species of Abies, Acer, Berberis, Betula, Ceratonia, Cornus, Cotinus, Crataegus, Elaeagnus, Eriobotrya,
Eucalyptus, Juniperus, Lumnitzera, Malus, Picea, Pinus,
Platanus, Platycladus, Populus, Prunus, Pyrus, Quercus,
Rosa, Salix, Sequoia, Sibiraea, Sorbaronia, Sorbus,
123
Fungal Diversity
Spiraea, Styphnolobium, Syringa, Syzygium, Tibouchina,
Ulmus, Vitis and Xylocarpus (Norphanphoun et al. 2018).
Morphological based identification and diversity
Cytospora is characterized by multi-loculate conidiomata
with ostiolar necks and unicellular, elongate-allantoid to
subcylindrical, hyaline conidia (Fan et al. 2015a, b; Norphanphoun et al. 2017, 2018; Fig. 7). The genus which was
reported as causing canker diseases in many woody plants
was established in 1818 and studied in detail by taxonomists (Fries 1823; Saccardo 1884). Valsa Fr. was
reported as the sexual stage of this genus and therefore,
Valsa was treated as a synonym of Cytospora (1818) based
on The International Code of Nomenclature for Algae,
Fungi, and Plants (ICN, McNeill et al. 2012), with Cytospora being the oldest and most widely used name
(Adams et al. 2005; Fotouhifar et al. 2010; Fan et al. 2014;
Rossman et al. 2015). Previously, the conventional identification of species in Cytospora was based on their host
association, often with vague morphological descriptions.
Mycologists began to elucidate the relationships between
Cytospora species and their hosts, with morphological
observations combined with phylogenetic analyses using
internal transcribed spacer (ITS) regions as an effective
fungal DNA barcode (Adams et al. 2005, 2006; Fotouhifar
et al. 2010; Schoch et al. 2012). The establishment of
multi-gene analyses using ITS, LSU, ACT, RPB2, TUB2
has proved comprehensive for the species level (Fan et al.
2015a, b, 2020; Liu et al. 2015; Yang et al. 2015; Hyde
et al. 2016; Li et al. 2016; Norphanphoun et al. 2017, 2018;
Phookamsak et al. 2019).
Molecular based identification and diversity
Comprehensive multigene phylogenetic analyses for this
genus were performed by Fan et al. (2015a, b, 2020) and
Norphanphoun et al. (2017, 2018).
This study reconstructs the phylogeny of Cytospora
based on analyses of a combined ITS, LSU, ACT and
RPB2 sequence data (Table 3, Fig 8). The phylogenetic
tree is updated with recently introduced Cytospora species
and corresponds to previous studies (Norphanphoun et al.
2018).
Recommended genetic markers (genus level)—LSU, ITS
Recommended genetic markers (species level)—ITS, ACT
and RPB2
Accepted number of species: There are 630 species in
Index Fungorum (2019) and 110 species have molecular
data.
References: Fan et al. 2015a, b, Lawrence et al. 2016,
Senanayake et al. 2017, 2018 (morphology), Norphanphoun et al. 2017, 2018 (morphology, phylogeny).
Cyphellophora G.A. de Vries, Mycopath. Mycol. appl.
16(1):47(1962)
Cyphellophora is cosmopolitan, comprising species
distributed from a broad range of environmental sources as
human and animal disease, saprobes, epiphytes and plant
pathogens (de Hoog et al. 1999, 2000; Jacob and Bhat
2000; Decock et al. 2003; Crous et al. 2007; Zhuang et al.
2010; Feng et al. 2014; Mayfield et al. 2012; Gao et al.
2014; Phookamsak et al. 2019). Most species, including the
type species, C. laciniata, were isolated from nails or skin
of humans, resulting in clinical symptoms (Feng et al.
2014). Phylogenetically, C. phyllostachysdis clustered with
C. europaea, a human or mammal infection of hyperkeratosis (de Hoog et al. 2000). In contrast, C. phyllostachysdis causes sooty blotch and flyspeck (SBFS) of
bamboo and is not found on humans (Gao et al. 2014). The
sooty mould species C. jingdongensis was introduced with
a sexual morph; it reduces plant photosynthesis but does
not damage or cause disease of the plant (Chomnunti et al.
2014; Yang et al. 2018).
Classification—Eurotiomycetes, Chaetothyriomycetidae,
Chaetothyriales, Cyphellophoraceae
Type species—Cyphellophora laciniata G.A. de Vries,
Mycopath. Mycol. appl. 16(1):47(1962)
Distribution—Australia, Brazil, China, Germany, India,
Israel, Korea, Taiwan
Disease symptoms—Sooty blotch and flyspeck (main
symptoms of this disease are given under Chaetothyrina).
To date, C. artocarpi, C. guyanensis, C. jingdongensis,
C. musae, C. olivacea, C. oxyspora, C. phyllostachydis and
C. sessilis have been isolated from plant materials (Gams
and Holubová-Jechová 1976; de Hoog et al. 1999; Decock
et al. 2003; Gao et al. 2014; Yang et al. 2018). Cyphellophora artocarpi, C. musae, C. phyllostachydis and C.
sessilis were reported to cause sooty blotch and flyspeck
from apple, jackfruit (Artocarpus heterophyllus) and
bamboo (Phyllostachys heterocycla, Sinobambusa tootsik),
resulting in significant economic damage (Zhuang et al.
2010; Mayfield et al. 2012; Gao et al. 2014).
Hosts—Artocarpus heterophyllus, Dendrocalamus strictus,
Eucalyptus sp., Helomeco velane, Hylomecon verlance,
Malus domestica, Musa sp., Phyllostachys sp., Sinobasmbusa tootsik and Stenocalyx uniflorus.
Morphological based identification and diversity
It is difficult to identify this black yeast-like genus based
solely on morphological characters since the characters are
very similar to those of other black yeast-like fungi, such as
Phialophora and Pseudomicrodochium. Species of
Cyphellophora resemble those of Phialophora in having
melanized thalli with intercalary or terminal phialides
bearing collarettes, but Phialophora has aseptate conidia
whereas Cyphellophora produces larger, fusiform to
123
Fungal Diversity
Fig. 7 Cytospora ampulliformis a stromatal habit in wood. b fruiting
bodies on the substrate. c Surface of fruiting bodies. d Cross-section
of the stroma showing conidiomata. e Peridium, f ostiolar neck. g–i
Conidiogenous cells with attached conidia. j Mature conidia. k,
l Colonies on MEA (k-from above, l-from below). Scale bars:
a = 2 mm, b = 1 mm, c = 500 lm, d, f = 200 lm, e = 50 lm, g,
h = 10 lm, i, j = 5 lm
sigmoid, aseptate to multi-septate conidia (Réblová et al.
2013). Cyphellophora can also be compared to Pseudomicrodochium, the former having melanized thalli while
they are hyaline in Pseudomicrodochium (Decock et al.
2003; de Hoog et al. 2000, 2011). Yang et al. (2018)
introduced C. jingdongensis as the first sexual morph,
which is characterized by subglobose to globose, non-ostiolate ascomata, ellipsoidal to cylindrical asci and fusoid,
1–3 septate ascospores. However, the asexual morph of C.
jingdongensis was difficult to observe in culture to
123
Fungal Diversity
Table 3 Details of Cytospora isolates used in the phylogenetic analyses
Species
Isolate no
GenBank accession numbers
ITS
LSU
ACT
RPB2
tef1
TUB2
Cytospora acacia
CBS 468.69
DQ243804
–
–
–
–
–
C. ailanthicola
CFCC 89970*
MH933618
MH933653
MH933526
MH933592
MH933494
MH933565
C. abyssinica
CMW 10181*
AY347353
–
–
–
–
–
C. ampulliformis
MFLUCC 16-0583*
KY417726
KY417760
KY417692
KY417794
–
–
C. amygdali
CBS 144233*
MG971853
–
MG972002
–
–
–
C. atrocirrhata
CFCC 89615
KR045618
KR045700
KF498673
KU710946
KP310858
KR045659
C. austromontana
C. beilinensis
CMW 6735*
CFCC 50493*
AY347361
MH933619
–
MH933654
–
MH933527
–
–
–
MH933495
–
MH933561
C. berberidis
CFCC 89927*
KR045620
KR045702
KU710990
KU710948
KU710913
KR045661
C. berkeleyi
StanfordT3*
AY347350
–
–
–
–
–
C. brevispora
CBS 116811*
AF192315
–
–
–
–
–
C. bungeanae
CFCC 50495*
MH933621
MH933656
MH933529
MH933593
MH933497
MH933563
C. californica
CBS 144234*
MG971935
-
MG972083
–
MG971645
–
C. carbonacea
CFCC 89947
MH933622
MH933657
MH933530
MH933594
MH933498
MH933564
C. carpobroti
CMW 48981*
MH382812
MH411216
–
–
MH411212
MH411207
C. cedri
CBS 196.50
AF192311
–
–
–
–
–
C. celtidicola
CFCC 50497*
MH933623
MH933658
MH933531
MH933595
MH933499
MH933566
C. centravillosa
MFLUCC 16-1206*
MF190122
MF190068
–
MF377600
–
–
C. ceratosperma
CBS 116.21
AY347335
–
–
–
–
–
C. ceratospermopsis
CFCC 89626*
KR045647
KR045726
KU711011
KU710978
KU710934
KR045688
C. chrysosperma
CFCC 89981
MH933625
MH933660
MH933533
MH933597
MH933501
MH933568
C. cinereostroma
C. cotini
CMW 5700*
MFLUCC 14-1050*
AY347377
KX430142
–
KX430143
–
–
–
KX430144
–
–
–
–
C. curvata
MFLUCC 15-0865*
KY417728
KY417762
KY417694
KY417796
–
–
C. davidiana
CXY 1350*
KM034870
–
–
–
–
–
C. diatrypelloidea
CMW 8549*
AY347368
–
–
–
–
–
C. elaeagni
CFCC 89632
KR045626
KR045706
KU710995
KF765708
KU710918
KR045667
C. eriobotryae
IMI 136523*
AY347327
–
–
–
–
–
C. erumpens
MFLUCC 16-0580*
KY417733
KY417767
KY417699
KY417801
–
–
C. eucalypti
LSEQ
AY347340
–
–
–
–
–
C. eucalypticola
ATCC 96150*
AY347358
–
–
–
–
–
C. eucalyptina
CMW 5882
AY347375
–
–
–
–
–
C. eugeniae
CMW 7029
AY347364
–
–
–
–
–
C. euonymicola
CFCC 50499*
MH933628
MH933662
MH933535
MH933598
MH933503
MH933570
C. euonymina
CFCC 89993*
MH933630
MH933664
MH933537
MH933600
MH933505
MH933590
C. fraxinigena
MFLUCC 14-0868*
MF190133
MF190078
–
–
–
–
C. friesii
CBS 194.42
AY347328
–
–
–
–
–
C. fugax
C. germanica
CBS 203.42
CXY 1322
AY347323
JQ086563
–
JX524617
–
–
–
–
–
–
–
–
C. gigalocus
CFCC 89620*
KR045628
KR045708
KU710997
KU710957
KU710920
KR045669
MG971664
C. granati
CBS 144237*
MG971799
–
MG971949
–
MG971514
C. hippophaës
CFCC 89639
KR045632
KR045712
KU711001
KU710961
KU710924
KR045673
C. japonica
CBS 375.29
AF191185
–
–
–
–
–
C. joaquinensis
CBS 144235*
MG971895
–
MG972044
–
MG971605
MG971761
C. junipericola
MFLU 17-0882*
MF190125
MF190072
–
–
MF377580
–
C. juniperina
CFCC 50501*
MH933632
MH933666
MH933539
MH933602
MH933507
–
C. kantschavelii
CXY 1383
KM034867
–
–
–
–
–
123
Fungal Diversity
Table 3 (continued)
Species
Isolate no
GenBank accession numbers
ITS
LSU
ACT
RPB2
tef1
TUB2
C. kunzei
CBS 118556
DQ243791
–
–
–
–
–
C. leucosperma
CFCC 89622
KR045616
KR045698
KU710988
KU710944
KU710911
KR045657
C. longiostiolata
MFLUCC 16-0628*
KY417734
KY417768
KY417700
KY417802
–
–
C. longispora
C. lumnitzericola
CBS 144236*
MFLUCC 17-0508*
MG971905
MG975778
–
MH253453
MG972054
MH253457
–
MH253461
MG971615
–
MG971764
–
C. mali
CFCC 50028
MH933641
MH933675
MH933548
MH933606
MH933513
MH933577
C. melnikii
MFLUCC 15-0851*
KY417735
KY417769
KY417701
KY417803
–
–
C. mougeotii
ATCC 44994
AY347329
–
–
–
–
–
C. multicollis
CBS 105.89*
DQ243803
–
–
–
–
–
C. myrtagena
CBS 116843*
AY347363
–
–
–
–
–
C. nitschkii
CMW 10180*
AY347356
–
–
–
–
–
C. nivea
MFLUCC 15-0860
KY417737
KY417771
KY417703
KY417805
–
–
C. oleicola
CBS 144248*
MG971944
–
MG972098
–
MG971660
MG971752
C. palm
CXY 1280*
JN411939
–
–
–
KJ781297
–
C. parakantschavelii
MFLUCC 15-0857*
KY417738
KY417772
KY417704
KY417806
–
–
C. parapersoonii
T28.1*
AF191181
–
–
–
–
–
C. parapistaciae
CBS 144506*
MG971804
–
MG971954
–
MG971519
MG971669
C. paratranslucens
MFLUCC 16-0506*
KY417741
KY417775
KY417707
KY417809
–
–
C. pini
C. pistaciae
CBS 224.52*
CBS 144238*
AY347316
MG971802
–
–
–
MG971952
–
–
–
MG971517
–
MG971667
C. platanicola
MFLU 17-0327*
MH253451
MH253452
MH253449
MH253450
–
–
C. platycladi
CFCC 50504*
MH933645
MH933679
MH933552
MH933610
MH933516
MH933581
C. platycladicola
CFCC 50038*
KT222840
MH933682
MH933555
MH933613
MH933519
MH933584
C. plurivora
CBS 144239*
MG971861
–
MG972010
–
MG971572
MG971726
C. populicola
CBS 144240*
MG971891
–
MG972040
–
MG971601
MG971757
C. populina
CFCC 89644
KF765686
KF765702
KU711007
KU710969
KU710930
KR045681
C. predappioensis
MFLUCC 17-2458*
MG873484
MG873480
–
–
–
–
C. predappioensis
MFLU 17-0327
MH253451
MH253452
MH253449
MH253450
–
–
C. prunicola
MFLU 17-0995*
MG742350
MG742351
MG742353
MG742352
–
–
C. pruinopsis
CFCC 50034*
KP281259
KP310806
KP310836
KU710970
KP310849
KP310819
C. pruinosa
CBS 201.42
DQ243801
–
–
–
–
–
C. punicae
CBS 144244
MG971943
–
MG972091
–
MG971654
MG971798
C. quercicola
MFLUCC 14-0867*
MF190129
MF190073
–
–
–
–
C. rhizophorae
MUCC302
EU301057
–
–
–
–
–
C. ribis
C. rosae
CBS 187.36
MFLUCC 14-0845*
DQ243810
MF190131
–
MF190075
–
–
–
–
–
–
–
–
C. rostrata
CFCC 89909*
KR045643
KR045722
KU711009
KU710974
KU710932
KR045684
C. rusanovii
MFLUCC 15-0854*
KY417744
KY417778
KY417710
KY417812
–
–
C. salicacearum
MFLUCC 16-0509*
KY417746
KY417780
KY417712
KY417814
–
–
C. salicicola
MFLUCC 14-1052*
KU982636
KU982635
KU982637
–
–
–
C. salicina
MFLUCC 15-0862*
KY417750
KY417784
KY417716
KY417818
–
–
C. salicina
MFLUCC 15-0862*
KY417750
KY417784
KY417716
KY417818
–
–
C. schulzeri
CFCC 50040
KR045649
KR045728
KU711013
KU710980
KU710936
KR045690
C. sibiraeae
CFCC 50045*
KR045651
KR045730
KU711015
KU710982
KU710938
KR045692
C. sophorae
CFCC 89598
KR045654
KR045733
KU711018
KU710985
KU710941
KR045695
C. sophoricola
CFCC 89595*
KR045655
KR045734
KU711019
KU710986
KU710942
KR045696
C. sophoriopsis
CFCC 89600*
KR045623
KP310804
KU710992
KU710951
KU710915
KP310817
123
Fungal Diversity
Table 3 (continued)
Species
Isolate no
GenBank accession numbers
ITS
LSU
ACT
RPB2
tef1
TUB2
C. sorbi
MFLUCC 16-0631*
KY417752
KY417786
KY417718
KY417820
–
–
C. sorbicola
MFLUCC 16-0584*
KY417755
KY417789
KY417721
KY417823
–
–
C. spiraeae
CFCC 50049*
MG707859
MG707643
MG708196
MG708199
–
–
C. tamaricicola
C. tanaitica
CFCC 50508*
MFLUCC 14-1057*
MH933652
KT459411
MH933687
KT459412
MH933560
KT459413
MH933617
–
MH933523
–
MH933588
–
C. thailandica
MFLUCC 17-0262*
MG975776
MH253455
MH253459
MH253463
–
–
C. tibouchinae
CPC 26333*
KX228284
KX228335
–
–
–
–
C. translucens
CXY 1351
KM034874
–
–
–
–
KM034895
C. ulmi
MFLUCC 15-0863*
KY417759
–
–
–
–
–
C. valsoidea
CMW 4309*
AF192312
–
–
–
–
–
C. variostromatica
CMW 6766*
AY347366
–
–
–
–
–
C. vinacea
CBS 141585*
KX256256
–
–
–
KX256277
KX256235
C. viticola
CBS 141586*
KX256239
–
–
–
KX256260
KX256218
C. xylocarpi
MFLUCC 17-0251*
MG975775
MH253462
MH253462
MH253462
–
–
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
compare with other species in Cyphellophora (Yang et al.
2018). There are 26 epithets of Cyphellophora in Index
Fungorum (2019). Yang et al. (2018) clarified 23 species in
this genus. To properly delineate these species, phylogenetic studies using multi-loci sequences (ITS, LSU, RPB1
and TUB2) and the secondary structures of ITS analyses
are needed (Réblová et al. 2013; Feng et al. 2014; Gao
et al. 2014; Yang et al. 2018).
Molecular based identification and diversity
Based on SSU and LSU sequence data, Cyphellophora
clustered in a well-supported clade within the
Chaetothyriales (Feng et al. 2014). Generic and species
delimitation with morphological characters, ecological
traits, host distribution and phylogenetic analyses using the
internal transcribed spacer region (ITS), the partial btubulin gene (TUB2), the nuclear large subunit rDNA gene
(LSU) and the DNA dependent RNA polymerase II largest
subunit (RPB1) were recently performed (Feng et al. 2014;
Gao et al. 2014). The present study reconstructs the phylogeny of Cyphellophora based on analyses of a combined
ITS, TUB2, LSU and RPB1 sequence data (Table 4,
Fig. 9). The phylogenetic tree in this study is updated with
recently introduced Cyphellophora species and corresponds to previous studies (Feng et al. 2014; Gao et al.
2014). Cyphellophoroa indica and C. taiwanensis lack
sequences in GenBank (4/7/2019). Cyphellophoroa
hylomeconis was synonymized as Camptophora hylomeconis and C. eugeniae was synonymized as Aphanophora
eugeniae (Réblová et al. 2013). Cyphellophoroa eucalypti
were synonymized as C. guyanensis (Feng et al. 2014).
Therefore, these species were not included in the present
phylogenetic analyses (Fig. 9).
Recommended genetic markers (genus level)—LSU and
SSU
Recommended genetic markers (species level)—ITS, LSU,
TUB2, RPB1 and secondary (2D) structure of ITS analyses
LSU is useful for preliminary identification at the generic level (Feng et al. 2014). Réblová et al. (2013) resolved
Cyphellophora and Phialophora as close relatives within
the Chaetothyriales, although both genera were paraphyletic based on analysis of ITS, TUB2 and nuc28S
rDNA sequence data. It is recommended to use a combination of ITS, LSU, TUB2, RPB1 and secondary (2D)
structure of ITS analyses (Réblová et al. 2013; Feng et al.
2014; Gao et al. 2014) in order to identify to the species
level.
Accepted number of species: 24 species
References: Vries 1962, 1986; Matsushima 1987; Walz and
de Hoog 1987; Decock et al. 2003; Crous et al. 2013, 2016;
Réblová et al. 2013; Feng et al. 2014; Gao et al. 2014;
Madrid et al. 2016; Yang et al. 2018 (morphology,
phylogeny)
Cyttaria Berk., Trans. Linn. Soc. London 19:40 (1842)
This genus is geographically restricted to South America
(Argentina and Chile) and Southeastern Australasia (including Tasmania, and New Zealand) (Peterson and Pfister
2010). Cyttaria species are found in the secondary phloem
and xylem, cambium and cortex of the hosts. They produce
123
Fungal Diversity
Fig. 8 Phylogenetic tree generated by maximum parsimony analysis
of combined ITS, LSU, ACT and RPB2 sequence data of Cytospora
species. Related sequences were obtained from GenBank. One
hundred and eleven strains are included in the analyses, which
comprised 2266 characters including gaps. The tree was rooted with
Diaporthe vaccinii (CBS 160.32). The maximum parsimonious
dataset consisted of 1358 constant, 596 parsimony-informative and
123
312 parsimony-uninformative characters. The parsimony analysis of
the data matrix resulted in the maximum of ten equally most
parsimonious trees with a length of 3836 steps (CI = 0.364, RI 0.649,
RC = 0.236, HI = 0.636) in the first tree. MP and ML bootstrap values
C 50% and Bayesian posterior probabilities C 0.90 are shown
respectively near the nodes. The scale bar indicates 10 changes per
site. Ex-type strains are in bold
Fungal Diversity
Fig. 8 continued
trunk and branch cankers that arise due to localized,
stimulated cambial activity attributed to the presence of
hyphae of Cyttaria (Wilson 1907; Gutierrez de Sanguinetti
1988). Cyttaria species are considered as weak parasites
(Gamundı́ and De Lederkremer 1989).
Classification—Leotiomycetes, Leotiomycetidae, Cyttariales, Cyttariaceae
Type species—Cyttaria darwinii Berk., Trans. Linn. Soc.
London 19:40 (1842)
Distribution—Argentina, Australia, Chile, New Zealand,
Tasmania.
Disease symptoms—Canker, galls
These species are known to cause two types of cankers:
globose and longitudinal. Globose cankers arise from
123
Fungal Diversity
Table 4 Details of the Cyphellophora isolates used in the phylogenetic analyses
Species
Isolate/voucher no
ITS
LSU
RPB1
TUB2
Cyphellophora ambigua
CBS 235.93*
JQ766431
JQ766480
JQ766386
JQ766340
C. artocarpi
CGMCC3.17496*
KP010367
KP122930
KP122920
KP122925
C. catalaunica
CPC 22929*
HG003670
HG003673
–
–
C. chlamydospora
CBS 127581 (= FMR 10878) *
HG003674
HG003675
–
–
C. europaea
CBS 101466*
JQ766443
KC455259
JQ766395
JQ766365
C. europaea
CBS 218.78
JQ766441
JQ766488
JQ766393
JQ766366
C. europaea
CBS 129.96
JQ766440
JQ766487
JQ766392
JQ766364
C. filicis
KUMCC 18-0144
MK404056
MK404052
–
–
C. fusarioides
CBS 130291*
JQ766439
KC455252
JQ766391
JQ766363
C. gamsii
CPC 25867*
KX228255
KX228307
–
KX228381
C. guyanensis
C. guyanensis
MUCL 43737*
CBS 124764
KC455240
GQ303274
KC455253
GQ303305
–
–
KC455223
–
C. guyanensis
CBS 126014
JQ766434
JQ766483
JQ766389
JQ766339
C. jingdongensis
IFRDCC 2659*
MF285234
MF285236
–
–
C. laciniata
CBS 190.61*
JQ766423
JQ766472
JQ766378
JQ766329
C. laciniata
CBS 174.79
JQ766422
JQ766471
JQ766377
JQ766328
C. laciniata
CBS 239.91
JQ766424
JQ766473
JQ766379
JQ766330
C. livistonae
CPC19433
KC005774
KC005796
–
–
C. musae
CGMCC3.17497*
KP010370
KP122932
KP122922
KP122927
C. musae
GLGZXJ9B
KP010368
KP122931
KP122923
KP122926
C. musae
GLMMZZ4
KP010369
KP122934
KP122921
KP122928
C. olivacea
CBS 123.74*
KC455248
KC455261
–
KC455231
C. olivacea
CBS 122.74
KC455247
KC455260
–
KC455230
C. oxyspora
CBS 698.73*
JQ766450
KC455262
JQ766402
KC455232
C. oxyspora
CBS 416.89
JQ766449
JQ766497
JQ766401
JQ766374
C. pauciseptata
CBS 284.85*
JQ766466
JQ766515
JQ766415
JQ766360
C. phyllostachidis
C. pluriseptata
CGMCC3.17495*
CBS 286.85*
KP010371
JQ766429
KP122933
KC455255
KP122924
JQ766384
KP122929
JQ766335
C. pluriseptata
CBS 109633
JQ766430
JQ766479
JQ766385
JQ766336
C. reptans
CBS 113.85*
JQ766445
JQ766493
JQ766397
JQ766370
C. reptans
CBS 152.90
JQ766446
JQ766494
JQ766398
JQ766371
C. reptans
CBS 458.92
JQ766447
JQ766495
JQ766399
JQ766372
C. reptans
CBS120903
JQ766448
JQ766496
JQ766400
JQ766373
C. sessilis
CBS 243.85*
EU514700
EU514700
–
KC455234
C. sessilis
CBS 238.93
AY857541
KF928523
–
KF928587
C. suttonii
CBS 449.91*
JQ766459
KC455256
–
KC455226
C. suttonii
FMR 10589
KU705828
KU705845
–
–
C. vermispora
CBS 228.86*
KC455244
KC455257
JQ766381
JQ766332
C. vermispora
CBS 122852
JQ766427
JQ766476
JQ766382
JQ766333
C. vermispora
CBS 227.86
JQ766425
JQ766474
JQ766380
JQ766331
Cladophialophora immunda
CBS 834.96
EU137318
KC809990
–
EU137203
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
123
Fungal Diversity
Fig. 9 Phylogram generated
from RAxML analysis based on
combined sequences of ITS,
LSU, RPB1 and TUB2
sequences of all accepted
species of Cyphellophora.
Forty-one strains are included in
the analyses, which comprise
2514 characters including gaps.
The tree was rooted with
Cladophialophora immunda
(CBS 834.96). Tree topology of
the ML analysis was similar to
the MP and BYPP analyses. The
best scoring RAxML tree with a
final likelihood value of
- 5928.387430 is presented.
The matrix had 337 distinct
alignment patterns, with 12.44%
of undetermined characters or
gaps. Estimated base
frequencies were as follows;
A = 0.234866, C = 0.250597,
G = 0.284325, T = 0.230211;
substitution rates
AC = 1.492532,
AG = 2.025910,
AT = 2.769660,
CG = 1.674732,
CT = 8.545312,
GT = 1.000000; gamma
distribution shape parameter
a = 0.136482. RAxML and
maximum parsimony bootstrap
support value C 50% are shown
respectively near the nodes.
Bayesian posterior
probabilities C 0.95 (BYPP)
indicated as thickened black
branches. Ex-type strains are in
bold
growth mainly in the transverse axis of the branch while
longitudinal cankers arise from growth mainly along the
long axis (Rawlings 1956; Gamundi 1971). Development
of perennial galls on branches and stems may lead to
malformation and occasional death of branches (Gadgil
1985).
Hosts—Nothofagus spp.
Morphological based identification and diversity
Ascomata of Cyttaria species are orange, pitted apothecia
similar to deeply dimpled golf balls. Each fruiting body is
composed of 1–200 apothecia immersed in a sterile fleshygelatinous stroma. Asci are 8-spored, inoperculate and
amyloid. Ascospores are uninucleate, subglobose to ovoid,
smooth to rugulose, at first hyaline to yellowish but later
becoming pigmented (Mengoni 1986; Peterson et al 2010).
Molecular based identification and diversity
The first phylogenetic analysis which included Cyttaria
was done by Gargas and Taylor (1995) showing its relationship with other discomycetes. Wang et al. (2006)
showed its placement within Leotiomycetes using combined analysis of SSU, LSU and 5.8S rDNA gene sequence
data and then confirmed by Ekanayaka et al. (2017).
Peterson and Pfister (2010) did large scale phylogeny for
Cyttaria including all accepted 12 species in the genus
using sequence data of partial nucSSU, nucLSU and
mtSSU rRNA, as well as tef1. They found Cyttaria to be a
strongly supported clade and suggested a close relationship
between Cyttaria and some members of the Helotiales
(Cordierites, Encoelia, Ionomidotis and Chlorociboria)
(Peterson and Pfister 2010). The present study reconstructs
the phylogeny of Cyttaria based on analyses of a combined
123
Fungal Diversity
Table 5 Details of Cyttaria
isolates used in the phylogenetic
analyses
Species
Isolate/voucher no
LSU
SSU
mtSSU
C. berteroi
Isolate 16
EU107205
EU107178
EU10723
C. darwinii
Isolate 40
EU107207
EU107180
EU107236
C. darwinii
Isolate 14
EU107208
EU107181
–
C. darwinii
Isolate 57
EU107206
EU107179
EU107235
C. darwinii
Isolate 45
EU107209
–
–
C. darwinii
Isolate 50
EU107211
–
–
C. darwinii
Isolate 49
EU107210
–
–
C. espinosae
Isolate 187
–
EU107183
EU107238
C. espinosae
Isolate 92
EU107212
EU107182
EU107237
C. exigua
Isolate 77
EU107214
EU107185
EU107240
C. exigua
Isolate 76
EU107213
EU107184
EU107239
C. gunnii
Isolate 138
–
EU107189
EU107242
C. gunnii
Isolate 127
EU107215
EU107186
EU107241
C. gunnii
Isolate 136
–
EU107188
–
C. gunnii
C. hariotii
Isolate 132
Isolate 44
–
EU107217
EU107187
EU107194
–
EU107245
C. hariotii
Isolate 55
EU107218
EU107195
EU107246
C. hariotii
Isolate 65
EU107223
–
–
C. hariotii
Isolate 64
EU107222
–
–
C. hariotii
Isolate 63
EU107221
–
–
C. hariotii
Isolate 62
EU107220
–
–
C. hariotii
Isolate 51
EU107219
–
–
C. hookeri
Isolate 60
EU107227
–
–
C. hookeri
Isolate 59
EU107226
–
–
C. hookeri
Isolate 80
EU107228
–
–
C. hookeri
Isolate 61
EU107225
EU107197
–
C. hookeri
Isolate 58
EU107224
EU107196
–
C. johowii
Isolate 73
EU107229
EU107198
–
C. johowii
Isolate 74
EU107230
EU107199
–
C. nigra
Isolate 100
EU107232
EU107201
EU107248
C. nigra
C. septentrionalis
Isolate 97
Isolate 199
EU107231
–
EU107200
EU107203
EU107247
EU107249
C. septentrionalis
Isolate 85
–
EU107202
–
LSU, SSU and mtSSU sequence data (Table 5, Fig. 10).
The phylogenetic tree is updated with recently introduced
Cyttaria species and corresponds to previous studies (Feng
et al. 2014; Gao et al. 2014).
Recommended genetic markers (genus level)—ITS, LSU
Recommended genetic markers (species level)—nucSSU,
nucLSU, mitSSU rRNA, and tef1
Combined nucSSU, nucLSU, mitSSU rRNA, and tef1
can resolve almost all species of Cyttaria currently known
from sequence data (Peterson et al 2010).
Accepted number of species: There are 21 epithets in Index
Fungorum (2019). However, 12 species have molecular
data and are treated as accepted.
123
References: Mengoni 1986, Peterson et al 2010 (morphology); Peterson and Pfister (2010), Ekanayaka et al.
2017 (morphology, phylogeny).
Dactylonectria L. Lombard & Crous, in Lombard et al.,
Phytopath. Mediterr. 53(3): 523 (2014)
The genus Dactylonectria was introduced by Lombard
et al. (2014) for a group of species which were previously
treated in Ilyonectria (Chaverri et al. 2011; Cabral et al.
2012a, b, c). In morphology, Dactylonectria resembles
Ilyonectria and Neonectria but can be distinguished by
their characteristic ovoid to obpyriform, smooth to finely
warted, dark-red ascomata with a papillate ostiolar region
at the apex (Lombard et al. 2014; Gordillo and Decock
Fungal Diversity
Fig. 10 Phylogram generated from RAxML analysis based on
combined sequences of LSU, SSU and mtSSU sequences of all the
accepted species of Cyttaria. Related sequences were obtained from
GenBank. Thirty-four strains are included in the analyses, which
comprise 3480 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 Chlorociboria
cf. aeruginosa (OSC 100056). The best scoring RAxML tree with a
final likelihood value of - 7505.900855 is presented. The matrix had
360 distinct alignment patterns, with 39.17% of undetermined
characters or gaps. Estimated base frequencies were as follows;
A = 0.256, C = 0.214, G = 0.280, T = 0.250; substitution rates
AC = 1.190197, AG = 1.207782, AT = 0.373130, CG = 0.681125,
CT = 3.724394, GT = 1.000000; gamma distribution shape parameter a = 0.020000. RAxML and maximum parsimony bootstrap
support value C 50% (BT) are shown respectively near the nodes
2018). Species of this genus are mostly associated with
Vitis sp., while some species are also recorded from other
hosts (Farr and Rossman 2019).
Classification—Sordariomycetes,
Hypocreomycetidae,
Hypocreales, Nectriaceae
Type species—Dactylonectria macrodidyma (Hallen,
Schroers & Crous) L. Lombard & Crous, in Lombard et al.,
Phytopath. Mediterr. 53(3): 527 (2014)
Distribution—Worldwide
Disease symptoms—Black foot disease, black root rot
Characteristic symptoms of black foot disease include a
reduction in root biomass and root hairs with sunken and
necrotic lesions (Halleen et al. 2006). Severe necrosis of
the root system results in stunting, wilting, leaf chlorosis,
browning and leaf drop prior to death (Parkinson et al.
2017). Dactylonectria alcacerensis, D. estremocensis, D.
macrodidyma, D. novozelandica, D. pauciseptata, D.
pinicola, D. torresensis and D. vitis are associated with
black foot disease of grapevine (Cabral et al. 2012a;
Lombard et al. 2014) (Fig. 11).
Hosts—Abies sp., Annona cherimola, Anthrium sp., Arbutus unedo, Cistus albidus, Crataegus azalous, Erica
melanthera, Eriobotrya japonica, Ficus sp., Fragaria sp.,
Hordeum vulgare, Ilex aquifolium, Juglans regia, Juniperus phoenicea, Lonicera sp., Myrtus communis, Persea
americana, Picea glauca, Pinus sp., Pistacia lentiscus,
123
Fungal Diversity
Fig. 11 Symptoms of black foot disease on Vitis spp. a, b dead plants and stunted growth of grapevine. c, e Infection of rootstock. d Blocked
xylem vessels. f Black streak (Courtesy of Halleen)
Prunus domestica, Pyracantha sp., Quercus sp., Rosmarinus officinalis, Santolina chamaecyparissus and Vitis sp.
Morphological based identification and diversity
Lombard et al. (2014) accepted ten species in Dactylonectria based on ITS, LSU, TUB2 and tef1 sequence data
and morphological characters. Later, Gordillo and Decock
(2018) introduced another four species to the genus based
on morphology and sequence data.
Fourteen Dactylonectria species have been described
with DNA sequence data in GenBank. Dactylonectria
species produce cylindrocarpon-like asexual morphs, several of which were previously treated in Ilyonectria
(Lombard et al. 2014). Dactylonectria species were distinguished mainly by phylogenetic inference and using
unique fixed single nucleotide polymorphisms (SNP’s)
rather than morphological characters (Lombard et al. 2014;
Gordillo and Decock 2018).
Molecular based identification and diversity
Lombard et al. (2014) re-evaluated genera with cylindrocarpon-like asexual morphs based on multi-gene phylogeny
of ITS, LSU, TUB2 and tef1 genes. Gordillo and Decock
(2018) analysed His3 together with latter gene regions, for
delimiting the species in Dactylonectria. Lombard et al.
(2015) also supported the fact that Dactylonectria is
monophyletic and distinct from Ilyonectria. In this study,
we reconstruct the phylogeny of Dactylonectria based on
analyses of a combined ITS, LSU, TUB2 and tef1 sequence
123
data (Table 6, Fig. 12). The phylogenetic tree is updated
with recently introduced Dactylonectria species and corresponds to previous studies (Lombard et al. 2014, 2015;
Gordillo and Decock 2018).
Recommended genetic markers (genus level)—ITS, LSU,
TUB2, tef1
Recommended genetic markers (species level)—TUB, tef1
Accepted number of species: 14 species
References: Cabral et al. 2012a, b; Halleen et al. 2004,
Schroers et al. 2008; Lombard et al. 2014; Gordillo and
Decock 2018 (morphology, phylogeny).
Entoleuca Syd., Annls mycol. 20(3/4):186 (1922)
The genus Entoleuca Syd. (Xylariaceae) consists of
saprobic and plant pathogenic species distributed in Europe. Entoleuca mammata causes canker diseases (commonly known as Hypoxylon canker) on Malus sp.
(Rosaceae), Populus sp., Salix sp. (Salicaceae) and Sorbus
sp. (Rosaceae) (Shaw 1973; Callan 1998; Kasanen et al.
2004; Eriksson 2014) and also occurs as a saprobe on
decaying tree trunks. The species are distributed in terrestrial habitats in temperate regions. The genus is characterized by its known sexual morph. It is characterized by
partially embedded solitary or aggregated orbicular stroma,
that has a whitish surface when young and dark surface at
maturity, papillate ostiole; multiple, monostichous and
embedded ascomata in stromata; 8-spored, unitunicate asci
that are cylindrical, long pedicellate, with J? apical ring
bluing in Melzer’s reagent and uniseriate, unicellular,
Fungal Diversity
Table 6 Details of the
Dactylonectria isolates used in
the phylogenetic analyses
Species
Isolate/voucher no
ITS
LSU
TUB2
tef1
Campylocarpon fasciculare
CBS 112613*
AY677301
HM364313
AY677221
JF735691
Dactylonectria alcacerensis
CBS 129087*
JF735333
KM231629
AM419111
JF735819
D. anthuriicola
CBS 564.95*
JF735302
KM515897
JF735430
JF735768
D. amazonica
MUCL55433*
MF683707
MF683727
MF683644
MF683665
D. ecuadoriense
MUCL55424*
MF683704
MF683724
MF683641
MF683662
D. estremocencis
CBS 129085*
JF735320
KM231630
JF735448
JF735806
D. hordeicola
CBS 162.89*
AM41906
KM515898
AM419084
JF735799
D. macrodidyma
CBS 112615*
AY677290
KM515900
AY677233
JF735836
D. novozelandica
CBS 112608*
AY677288
KM515901
AY677235
JF735821
D. palmicola
MUCL55426*
MF683708
MF683728
MF683645
MF683666
D. pauciseptata
CBS 120171*
EF607089
KM515903
EF607066
JF735776
D. pinicola
CBS 173.37*
JF735319
KM515905
JF735447
JF735803
D. polyphaga
MUCL55209*
MF683689
MF683710
MF683626
MF683647
D. torresensis
CBS 129086*
JF735362
KM231631
JF735492
JF735870
D. vitis
CBS 129082*
JF735303
KM515907
JF735431
JF735769
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
Fig. 12 Phylogram generated from RAxML analysis based on
combined sequences of ITS, LSU, TUB and tef1 sequences of all
the accepted species of Dactylonectria. Related sequences were
obtained from GenBank. Fifteen 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
Campylocarpon fasciculare (CBS 112613). Tree topology of the ML
analysis was similar to the BI. 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. RAxML and maximum parsimony
bootstrap support value C 50% are shown respectively near the
nodes. Bayesian posterior probabilities C 0.95 (BYPP) indicated as
thickened black branches. Ex-type strains are in bold
ellipsoidal inequilateral, brown, with straight to oblique
germ slit ascospores (Rogers and Ju 1996; Daranagama
et al. 2018). Daranagama et al. (2018) provided an identification key with emphasis on the coarsely papillate
ostiole in Entoleuca.
Sydow and Petrak (1922) introduced the genus with E.
callimorpha as the type species. Until 1994, Hypoxylon
mammatum was considered a similar taxon to E. callimorpha. However, Læssøe and Spooner (1994) and
Læssøe (1994) treated H. mammatum as a separate,
synonym to Rosellinia. Based on these taxonomic confusions, Rogers and Ju (1996) revised the type, authentic and
other specimens and re-established the genus Entoleuca.
Classification—Sordariomycetes, Xylariomycetidae, Xylariales, Xylariaceae
Type species—Entoleuca callimorpha Syd., in Sydow &
Petrak, Annls mycol. 20(3/4):186 (1922)
Distribution—Austria, Canada, Poland, Sweden, USA
Disease symptoms—Canker
123
Fungal Diversity
Symptoms may vary on the stage of disease development. Young cankers appear as slightly sunken, yellowish
orange areas with irregular margins. Later, the outer-most
bark within the canker breaks out in blisters exposing a
powdery grey mat of fungal tissue and conidia. Then the
patches of bark start to flake off making the canker rough
and black in the centre. Advancing margins of the
enlarging cankers become yellowish orange (Ostry 2013).
Hosts—Known from Malus sylvestris, Populus sp., Salix
sp. and Sorbus aucuparia.
Recommended genetic markers (genus level)—LSU and
ITS
Recommended genetic markers (species level)—RPB2 and
TUB2
Combined LSU, ITS, RPB2 and TUB2 provide a satisfactory resolution for resolving species.
Accepted number of species: Three species
References: Sydow and Petrak 1922; Rogers and Ju 1996;
Ju et al. 2004 (morphology), Daranagama et al. 2018
(morphology, phylogeny).
Morphological based identification and diversity
Eutiarosporella Crous, in Crous et al., Phytotaxa 202(2):
85 (2015)
Eutiarosporella was introduced by Crous et al. (2015) and
is typified by Eutiarosporella tritici (B. Sutton & Marasas)
Crous on Triticum aestivum from South Africa. The genus
was named on account of its similarity to Tiarosporella
Höhn. (Crous et al. 2006). Eutiarosporella species are coelomycetes that are saprobes or pathogens which occur in
terrestrial habitats (Crous et al. 2015; Thynne et al. 2015; Li
et al. 2016). Eutiarosporella species have been reported from
Celtis africana (Rosales), Triticum aestivum (Poales), Acacia karroo (Fabales) and Dactylis glomerata (Poales)
(Thambugala et al. 2014; Crous et al. 2015). On wheat, it
causes the economically important disease known as white
grain disorder (Thynne et al. 2015). Several studies have
reported this genus on woody hosts as a saprobe (Jami et al.
2012, 2014; Dissanayake et al. 2016).
Classification—Dothideomycetes,
incertae
sedis,
Botryosphaeriales, Botryosphaeriaceae
Type species—Eutiarosporella tritici (B. Sutton & Marasas) Crous, in Crous et al., Phytotaxa
202(2):85 (2015)
Distribution—Worldwide
Disease symptoms—White grain disorder of wheats
White grain disorder shrivels and discolours (white to
light grey) wheat grain (Thynne et al. 2015). Affected
grains are more brittle and can break during harvesting.
Infected spikelets of green heads may show bleaching
appreance or grey discolouration. At first, the bleached
florets may show blue-gray ‘highlights’. Rachis of affected
heads and the upper peduncle may show a brownish discolouration (Thynne et al. 2015).
Even though species of this genus have been found to be
associated with several hosts other than wheat, their diseases have not been described.
Hosts—Acacia karroo, Arrhenatherum elatius, Avenella
flexuosa, Celtis africana, Dactylis glomerata, Triticum
aestivum and Vachelloa karroo (Farr and Rossman 2019).
Currently, the genus comprises three species: E. callimorpha, E. ellisii and E. mammata (Sydow and Petrak 1922;
Rogers and Ju 1996; Ju et al. 2004; Index Fungorum 2019).
Due to the presence of clear papillate ostioles, they have
been distinguished from closely related genera such as
Amphirosellinia, Nemania, and Rosellinia. Molecular data
are only available for E. mammata, which is the most
important species in the genus as a pathogen. Rogers and Ju
(1996) observed that there are no distinguishing morphological differences among E. mammata isolates from different hosts. However, there is a high polymorphism, but
no major phylogenetic differences among the isolates from
Europe (Kasanen et al. 2004). Ju et al. (2004) introduced E.
ellisii based on characterizations of ascospore and germ
slit. Therefore, a combination of morphological and phylogenetic analyses are needed for species delimitation of
Entoleuca.
Molecular based identification and diversity
Several recent studies have focused on the molecular
phylogeny of Entoleuca, especially E. mammata. Phylogenetic based population studies revealed that higher
polymorphism occurs in North American than in Europe
(Kasanen et al. 2004). The sterile mycelia associated with
Pinus tabulaeformis and its ITS-based phylogenetic analyses revealed that the genus Entoleuca clusters in Xylariaceae and is closely related to Nemania (Guo et al. 2003).
Daranagama et al. (2018) revisited the family Xylariaceae
and due to the morphological differences and conidial state
characters, they suggested that it is useful to maintain the
taxa as distinct genera. Daranagama et al. (2018) and
Wendt et al. (2018) conducted multi-gene phylogenetic
analyses using ITS, LSU, RPB2 and TUB2 and revealed
that E. mammata clusters with Rosellinia corticium with
high support. Due to the lack of molecular data from other
species and other gene regions, it is difficult to place Entoleuca in an appropriate family.
In this study, we included the available sequences of
Entoleuca in the analysis done for Rosellinia (Table 7,
Fig 13).
123
Morphological based identification and diversity
Eutiarosporella is characterized by hairy conidiomata with
long necks, and holoblastic conidiogenesis, features which
Fungal Diversity
Table 7 Details of the
Entoleuca and Rosellinia
isolates used in the phylogenetic
analyses
Species
Isolate/voucher no
ITS
LSU
RPB2
Coniolariella gamsii
CBS 114379*
GU553325
GU553329
N/A
C. hispanica
ATCC MYA4453*
GU553323
GU553353
N/A
C. limonispora
CBS 382.86
KF719199
KF719211
N/A
C. limonispora var. australis
AV1L2-3
KP101193
N/A
N/A
C. limonispora var. australis
AH24323
AY908997
N/A
N/A
Entoleuca mammata
JDR 100
GU300072
N/A
GQ844782
E. mammata
ATCC 58108
AF201713
N/A
N/A
E. mammata
Osterby 1
AF176983
N/A
N/A
Rosellinia abscondita
CBS 447.89
FJ175180
KF719208
N/A
R. aquila
MUCL 51703
KY610392
KY610460
KY624285
R. arcuate
CBS347.29
AB017660
N/A
N/A
R. asperata var. minor
CBS 138641*
KY941107
N/A
N/A
R. australiensis
CBS 142160*
KY979742
KY979797
N/A
R. britannica
CBS 446.89
FJ175182
KF719209
N/A
R. bunodes
R. buxi
CBS 347.36
JDR 99
AB609598
GU300070
KF719205
N/A
N/A
GQ844780
R. buxi
ATCC 32869
AY909000
EF489467
N/A
R. capetribulensis
HKU(M) 17499*
AY862570
N/A
N/A
R. acutispora
CBS 138730
KY941108
N/A
N/A
R. chiangmaiensis
MFLU 15-3524*
KU246226
KU246227
N/A
R. compacta
NIAES:20565*
AB430457
N/A
N/A
R. convexa
GZUCC 13005*
KF614036
N/A
KP876561
R. convexa
ZG-1-2-1
KR822145
N/A
N/A
R. corticium
MUCL 51693
KC477236
KY610461
KY624229
R. desmazieri
olrim153
AY805591
N/A
N/A
R. lamprostoma
HAST 89112602
EF026118
N/A
GQ844778
R. mammiformis
CBS 445.89
KF719200
KF719212
N/A
R. mearnsii
MFLU 16-1382*
KY514059
KY514060
KY514061
R. merrillii
HAST 89112601*
GU300071
N/A
GQ844781
R. necatrix
HAST 89062904
EF026117
AY083824
GQ844779
R. necatrix
R. nectrioides
CBS 349.36
CBS 449.89
AY909001
FJ175181
KF719204
KF719213
N/A
N/A
R. quercina
ATCC 36702
AB017661
N/A
N/A
R. sanctaecruciana
HAST 90072903
GU292824
N/A
GQ844777
R. subiculata
ATCC 58850
AY909002
EF489468
N/A
R. thelena
CBS 400.61
KF719202
KF719215
N/A
R. truncatispora
CBS 138732*
KY941109
N/A
N/A
Xylaria bambusicola
WSP 205*
EF026123
AB376825
GQ844802
X. grammica
HAST 479
GU300097
N/A
GQ844813
X. hypoxylon
CBS 122620*
AM993141
KM186301
KM186302
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
are clearly distinguishable from Tiarosporella (Höhnel
1919; Crous et al. 2015). This genus is morphologically
similar to Marasasiomyces (long-necked, hairy conidiomata, and holoblastic conidiogenesis), except that it
forms conidiomata in clusters, which are not found in
Marasasiomyces (Crous et al. 2015). Li et al. (2016)
reported the sexual morph of Eutiarosporella in E.
dactylidis for the first time from Avenella flexuosa (Poales).
The sexual morph is characterised by globose ascomata,
with a central ostiole, a two-layered peridium, hyphae-like
pseudoparaphyses and hyaline, aseptate, fusoid to ovoid
ascospores, with a mucilaginous sheath (Thambugala et al.
2014).
123
Fungal Diversity
Fig. 13 Phylogenetic tree generated by maximum likelihood analysis
of combined ITS, LSU and RPB2 sequence data of Entoleuca and
Rosellinia species. Related sequences were obtained from GenBank.
Forty strains are included in the analyses, which comprise 2336
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 Xylaria bambusicola (WSP
205), X. grammica (HAST 479) and X. hypoxylon (CBS 122620).
Tree topology of the ML analysis was similar to the MP. The best
scoring RAxML tree with a final likelihood value of - 12521.202450
is presented. The matrix had 793 distinct alignment patterns, with
51.67% of undetermined characters or gaps. Estimated base
123
frequencies were as follows; A = 0.241655, C = 0.263843,
G = 0.260086, T = 0.234416; substitution rates AC = 1.764265,
AG = 4.237635, AT = 0.953946, CG = 1.541272, CT = 8.643978,
GT = 1.000000; gamma distribution shape parameter a = 1.105097.
The maximum parsimonious dataset consisted of constant 1567, 629
parsimony-informative and 140 parsimony-uninformative characters.
The parsimony analysis of the data matrix resulted in the maximum of
two equally most parsimonious trees with a length of 2112 steps
(CI = 0.545, RI = 0.668, RC = 0.364, HI = 0.455) in the first tree.
RAxML and maximum parsimony bootstrap support value C 50%
are shown respectively near the nodes. Ex-type strains are in bold
Fungal Diversity
Based on ITS and LSU sequence data, three species
were initially included in this genus, E. africana (Jami
et al.) Crous, E. tritici (B. Sutton & Marasas) Crous and E.
urbis-rosarum (Jami et al.) Crous by Crous et al. (2015).
Subsequently, E. darliae E. Thynne et al., E. tritici-australis E. Thynne, et al. and E. dactylidis (Thambug.,
Camporesi & K.D. Hyde) Dissan., Camporesi & K.D.
Hyde were accommodated in the genus (Crous et al. 2015;
Thynne et al. 2015; Li et al. 2016), which now comprises
seven species (Dissanayake et al. 2016; Wijayawardene
et al. 2017).
Colony and conidial morphology are the primary characters to identify species within this genus. Colonies on
nutrient-rich media (PDA or V8-OMA) grow rapidly
(Thynne et al. 2015). However, we consider morphological
characters alone are inadequate to identify species due to
plasticity and overlapping of conidial dimensions. Therefore, incorporation of molecular data together with morphology is recommended.
disease symptoms of their original plant hosts (Chaverri
et al. 2011; Cabral et al. 2012a,c; Lombard et al.
2013, 2014; Aiello et al. 2014). Ilyonectria is a well-known
genus causing black foot rot of grapevines in various
countries (Halleen et al. 2003, 2004, 2006; Chaverri et al.
2011; Cabral et al. 2012a, b, c; Lombard et al. 2014).
Classification—Sordariomycetes,
Hypocreomycetidae,
Hypocreales, Nectriaceae
Type species—Ilonectria radicicola (Gerlach & L. Nilsson) P. Chaverri & Salgado, in Chaverri et al., Stud. Mycol.
68:71 (2011)
Distribution—Worldwide
Disease symptoms—Black foot disease, black root rot
Symptoms are given under the genus Dactylonectria
Hosts—Wide host range including plant genera in
Amaryllidaceae, Aracaceae, Araliaceae, Cupressaceae,
Fagaceae, Liliaceae, Myrtaceae, Pinaceae, Proteaceae,
Rosaceae, Strelitziaceae and Vitaceae (Farr and Rossman
2019).
Molecular based identification and diversity
Morphological based identification and diversity
Taxonomy of Eutiarosporella is largely based on DNA
sequence data to reveal the phylogenetic relationships
between the species (Crous et al. 2015; Thynne et al. 2015;
Dissanayake et al. 2016; Li et al. 2016). According to
studies by Crous et al. (2015), Thynne et al. (2015) and Li
et al. (2016), ITS and LSU are the most suitable loci for
delineation of species within the genus. The phylogram
generated with sequences available in GenBank including
ex-epitype sequences is provided in Fig. 14 (Table 8). Our
phylogenetic analyses are in accordance with previous
studies by Crous et al. (2015), Thynne et al. (2015), Dissanayake et al. (2016) and Li et al. (2016).
The genus Ilyonectria was introduced based on I. radicicola as the type species, to accommodate Neonectria species belonging to the ‘‘N. radicicola’’ group (Booth 1959).
This genus has asexual morphs and belonged to Booth’s
Group 3 (chlamydospores and microconidia present, Booth
1966; Chaverri et al. 2011; Lombard et al. 2014). Molecular phylogenetic studies revealed that Ilyonectria, as
originally conceived, was paraphyletic (Cabral et al.
2012a, c; Lombard et al. 2013, 2014). Conidial size, culture
characters and molecular data enabled the separation of
Ilyonectria species (Cabral et al. 2012a, c; Lombard et al.
2013, 2014).
Recommended genetic markers (genus level)—LSU and
SSU
Recommended genetic markers (species level)—ITS and
LSU
Accepted number of species: Seven species.
References: Crous et al. (2015), Thynne et al. (2015),
Dissanayake et al. (2016), Li et al. 2016 (morphology,
phylogeny).
Molecular based identification and diversity
Ilyonectria P. Chaverri & Salgado, in Chaverri et al., Stud.
Mycol. 68:69 (2011)
Species of Ilyonectria (Nectriaceae, Hypocreales) are
important soil-borne pathogens of various woody and
herbaceous plant hosts. Ilyonectria species are cosmopolitan and are found on a wide range of hosts (Chaverri
et al. 2011). They are mostly associated with root diseases
and stem cankers (Seifert et al. 2003; Halleen et al.
2004, 2006; Chaverri et al. 2011; Cabral et al. 2012a, b, c;
Vitale et al. 2012; Lombard et al. 2013; Aiello et al. 2014).
There are 23 species of Ilyonectria, all associated with
Delineating between species of Ilyonectria can be achieved
with histone (His3) gene region. The topologies of the
phylogenetic tree (Fig. 15, Table 9) is similar to previous
studies done on this genus (Cabral et al. 2012a; Lombard
et al. 2014).
Recommended genetic markers (genus level)—ITS, LSU,
tef1, TUB2
Recommended genetic markers (species level)—tef1,
TUB2, His3
Accepted number of species: 23 species
References: Booth 1959, 1966 (morphology), Cabral et al.
2012a, b, c; Lombard et al. 2013, 2014 (morphology,
phylogeny).
Macrophomina Petr., Annls mycol. 21: 314 (1923)
Species of Macrophomina are mostly pathogens that
cause damping-off, seedling blight, collar rot, stem rot,
charcoal rot, basal stem rot and root rot in many plant
123
Fungal Diversity
species (Arora et al. 2001; Pal et al. 2001; Gupta et al.
2002; Sarr et al. 2014; Wijayawardene et al. 2017). The
type species, Macrophomina phaseolina (Tassi) Goid., is a
seed-borne polyphagous pathogen that affects more than
500 crop and non-crop species, including economically
important crops, such as soybean, sunflower, common
bean, peanut, corn, sorghum, cowpea and cotton (Gupta
et al. 2002; Ndiaye et al. 2010; Sarr et al. 2014).
Classification—Dothideomycetes,
incertae
sedis,
Botryosphaeriales, Botryosphaeriaceae
Type species—Macrophomina phaseolina (Tassi) Goid.,
Annali Sper. agr., N.S. 1(3): 457 (1947)
Distribution—Worldwide
Disease symptoms—Charcoal rot, collar rot, damping off,
root rot, seedling blight, stem rot, wilt
Seedling damage can occur when infected seeds are
planted. Infected plants may produce slightly smaller
Fig. 14 Phylogram generated
from maximum likelihood
analysis based on combined
LSU and ITS sequence data
retrieved from GenBank. The
tree is rooted in Tiarosporella
paludosa (CPC 22701 and CBS
114650). Tree topology of the
ML analysis was similar to the
Bayesian analysis. The best
scoring RAxML tree with a final
likelihood value of
- 7055.996836 is presented.
The matrix had 380 distinct
alignment patterns, with 40.12%
of undetermined characters or
gaps. Estimated base
frequencies were as follows;
A = 0.229604, C = 0.264209,
G = 0.282595, T = 0.223593;
substitution rates
AC = 1.357965,
AG = 1.612491,
AT = 0.913118,
CG = 2.194420,
CT = 5.121479,
GT = 1.000000; gamma
distribution shape parameter
a = 0.137391. Maximum
likelihood bootstrap support
values greater than 60% are
indicated above the nodes. Extype (ex-epitype) and voucher
strains are in bold
123
leaflets than healthy plants and have reduced vigour. As the
disease advances, leaflets turn yellow, wilt and turn brown
(Adorada et al. 2018). A grey/silver discolouration can be
observed in the roots and lower stem when the plants split
open (Romero Luna et al. 2017; Koehler and Shew 2018;
Meena et al. 2018). In charcoal rot, the abundant production of minute black sclerotia by the fungus causes the
rotted tissues to become blackened. Infections on soybean
lead to early maturation and incomplete pod filling
(ElAraby et al. 2003; Yang and Navi 2005; Sarr et al.
2014). In peanut, it causes seed and seedling rots, wilt, root
and stem rots, leaf spot and rotting of developing pods and
seeds (Gupta et al. 2002; Deshwal et al. 2003).
Hosts—This soil-borne fungus can infect more than 500
agricultural crops and weed species including, Fragaria,
Glycine, Helianthus, Sorghum and Zea.
Fungal Diversity
Table 8 Details of the
Eutiarosporella isolates used in
the phylogenetic analyses
Species
Isolate/voucher no
LSU
ITS
Botryobambusa fusicoccum
MFLUCC 11-0657
JX646810
JX646793
B. fusicoccum
MFLUCC 11-0143*
JX646809
NR111793
Eutiarosporella africana
CMW 38423*
KC769990
KC769956
E. dactylidis
MFLUCC 15-0915
KU246380
NR148093
Eutiarosporella dactylidis
MFLUCC 13-0874
KM978948
KM978945
E. dactylidis
MFLUCC 13-0276*
KM978949
KM978944
E. urbis
CMW 36477*
JQ239420
NR111705
E. urbis-rosarum
CMW 36479
JQ239422
JQ239409
E. urbis-rosarum
CMW 36478
JQ239421
JQ239408
Marasasiomyces karoo
CBS 1187.18*
DQ377939
KF531828
Mucoharknessia anthoxanthi
MFLUCC 15-0904*
KU246379
NR148092
M. cortaderiae
CPC 22208
KM108402
KM108375
M. cortaderiae
CPC 19974*
KM108401
NR148075
Sakireeta madreeya
CBS 532.76*
DQ377940
KC769960
Tiarosporella africana
T. africana
CMW 38425
CMW 38424
KC769992
KC769991
KC769958
KC769957
T. paludosa
CPC 22701
KM108404
NR132907
T. paludosa
CBS 114650*
KM108403
KM108377
T. tritici
CBS 118719*
DQ377941
KC769961
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
Fig. 15 Phylogenetic tree generated by maximum likelihood analysis
of combined ITS, TEF, TUB, and His3 sequence data of Ilyonectria
species. Twenty-three strains are included in the analyses, which
comprise 2242 characters including gaps. The tree is rooted in
Campylocarpon fasciculare. Tree topology of the ML analysis was
similar to the one generated from BI (Figure not shown). The best
scoring RAxML tree with a final likelihood value of - 9669.617830
is presented. The matrix had 507 distinct alignment patterns, with
5.11% of undetermined characters or gaps. Estimated base frequencies were as follows; A = 0.219321, C = 0.325516, G = 0.222910,
T = 0.230587; substitution rates AC = 0.215721, AG = 0.328038,
AT = 0.225653, CG = 0.615208, CT = 5.798530, GT = 1.000000;
gamma distribution shape parameter a = 0.518017. Maximum likelihood bootstrap support values C 60% and bayesian posterior
probabilities C 95 (BYPP) are indicated above or near the nodes.
Ex-type strains are in bold
Morphological based identification and diversity
species Macrophomina phaseolina and M. pseudophaseolina (Sarr et al. 2014). Morphological characteristics of M.
Eight species names are recorded in Index Fungorum
(2019), however, sequences are available for only two
123
Fungal Diversity
phaseolina are mostly similar to M. pseudophaseolina,
except that conidia of the latter are shorter.
Colony and conidial morphology are the primary characters used to identify species within this genus (Ellis
1971, 1976; Simmons 1992). However, the connectivity of
sexual and asexual morphs is not proven, as no sexual
morph has been obtained from nature or culture (Crous
et al. 2006; Wijayawardene et al. 2017, 2018). According
to the morphological identifications, Macrophomina
phaseolina has conidia with apical mucoid appendages as
found in Tiarosporella (Sutton and Marasas 1976). Nevertheless, it can be distinguished from Tiarosporella in
having conidia with apical mucoid appendages, per currently proliferating conidiogenous cells and dark brown (at
maturity) conidia (Crous et al. 2006; Phillips et al. 2013).
Morphologically M. phaseolina is similar to M. pseudophaseolina, except that conidia of the latter are shorter.
sample of Macrophomina isolates from many hosts.
According to the multi-gene analysis of SSU, LSU, ITS,
tef1 and TUB2 genes in this study (Fig. 16, Table 10), the
two species cluster in a well-supported clade with high
bootstrap values (100% ML, 1.00 BYPP). The overall
topology of our phylogeny tree is similar to previous
studies.
Recommended genetic markers (genus level)cosmopolitan
genus, and—LSU and SSU
Recommended genetic markers (species level)—ITS, tef1,
ACT, CAL and TUB2
Accepted number of species: There are eight epithets in
Index Fungorum (2019) However, two species have
molecular data.
Molecular based identification and diversity
References: Crous et al. 2006; Phillips et al. 2013; Sarr
et al. 2014, Wijayawardene et al. 2017 (morphology,
phylogeny).
Phillips et al. (2013) suggested that phylogenetic analysis
of a combined SSU, LSU, ITS, tef1 and TUB2 genes
provide better resolution. Sarr et al. (2014) used ITS, tef1,
ACT, CAL and TUB2 sequence data representing a large
Medeolaria Thaxt., Proc. Amer. Acad. Arts & Sci. 57(17):
432 (1922)
The genus Medeolaria belongs to the family Medeolariaceae (Medeolariales, Leotiomycetes, Ascomycota).
Table 9 Details of the
Ilyonectria isolates used in the
phylogenetic analyses
Species
Isolate/voucher no
ITS
Campylocarpon fasciculare
CBS 112613
AY677301
Ilyonectria capensis
CBS 132815*
JX231151
I. coprosmae
CBS 119606*
JF735260
I. crassa
CBS 139.30*
I. cyclaminicola
CBS 302.93*
I. destructans
tef1
tub2
His3
JF735691
AY677221
JF735502
JX231119
JX231103
JX231135
JF735694
JF735373
JF735505
JF735275
JF735723
JF735393
JF735534
JF735304
JF735770
JF735432
JF735581
CBS 264.65*
AY677273
JF735695
AY677256
JF735506
I. europaea
CBS 129078*
JF735294
JF735756
JF735421
JF735567
I. gamsii
I. leucospermi
CBS 940.97
CBS 132809*
AM419065
JX231161
JF735766
JX231129
AM419089
JX231113
JF735577
JX231145
I. liliigena
CBS 189.49*
JF735297
JF735762
JF735425
JF735573
I. liriodendri
CBS 110.81*
DQ178163
JF735696
DQ178170
JF735507
I. lusitanica
CBS 129080
JF735296
JF735759
JF735423
JF735570
I. macroconidialis
CBS 112615
AY677290
JF735836
AY677233
JF735647
I. mors-panacis
CBS 306.35*
JF735288
JF735746
JF735414
JF735557
I. palmarum
CBS 135754*
HF937431
HF922614
HF922608
HF922620
I. panacis
CBS 129079*
AY295316
JF735761
JF735424
JF735572
I. protearum
CBS 132811*
JX231157
JX231125
JX231109
JX231141
I. pseudodestructans
CBS 129081
AJ875330
JF735752
AM419091
JF735563
I. robusta
CBS 308.35*
JF735264
JF735707
JF735377
JF735518
I. rufa
CBS 156.47
AY677272
JF735730
AY677252
JF735541
I. strelitziae
CBS 142253 *
KY304649
KY304727
KY304755
KY304621
I. venezuelensis
CBS 102032 *
AM419059
JF735760
AY677255
JF735571
I. vredenhoekensis
CBS 132807*
JX231155
JX231123
JX231107
JX231139
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
123
Fungal Diversity
Medeolaria was introduced by Thaxter (1922) and typified
with Medeolaria farlowii. Medeolaria species are pathogens of Medeola virginiana (Liliaceae). Currently, the
known distribution of this genus is only from America.
Classification—Leotiomycetes,
Medeolariales,
Medeolariaceae
Type species—Medeolaria farlowii Thaxt., Proc. Amer.
Acad. Arts & Sci. 57(17): 432 (1922)
Distribution—America
Disease symptoms—This fungus causes gall-like deformations on thickened, hypertrophic 9 parts below leaf whorls
of herbaceous stems of the host tissue, in autumn. However, they are present not only in stem lesions of the host
plant but in uninfected leaves, stems and rhizomes (Pfister
et al 2013). Pfister et al. (2013) also showed the long-term
perpetuation of the fungus in populations of the plant. They
suggested the fungus remains as a systemic infection of
vegetative plant parts and when the plant reproduces
clonally, this infection is carried in populations of the host
plant (Pfister et al 2013).
Hosts—Magnolia spp.
Morphological based identification and diversity
This genus contains only a single species, Medeolaria
farlowii Thaxter (1922), described from material collected
from Magnolia. It produces erumpent, indefinite apothecia
with a palisade layer of asci and paraphyses. An excipulum
is absent or is a very thin layer. The hymenium layer forms
fusiform swellings below and/or between the shortened
internodes of the host plant. Ascospores are large, fusiform
to naviculate, with a dark, striate outer wall. The asexual
morph of this fungus is unknown (Korf 1973; Pfister and
LoBuglio 2009; Ekanayaka et al 2017).
Molecular based identification and diversity
The first stable taxonomic placement for this genus was
provided by Korf (1973) under the family Medeolariaceae,
order Medeolariales within Leotiomycetes, according to its
morphology. Recent phylogenetic studies (LoBuglio and
Pfister 2010; Pfister et al 2013; Ekanayaka et al. 2017)
confirmed its phylogenetic relationship with Leotiomycetes
(Fig. 10), but the phylogenetic position within the class is
unresolved.
Recommended genetic marker (genus level)—ITS
Recommended genetic marker (species level)—ITS
ITS is the best single genetic marker for the genus
Medeolaria (Pfister et al 2013). Pfister et al. (2013) provided primers, designed to specifically amplify ITS rDNA
regions of Medeolaria farlowii.
Accepted number of species: One species
References: Korf 1973; LoBuglio and Pfister 2010; Pfister
et al. 2013(morphology, phylogeny).
Neonectria Wollenw., Annls mycol. 15(1/2):52 (1917)
Neonectria is a cosmopolitan genus, and their asexual
morphs are common in tropical and temperate regions
(Chaverri et al. 2011). Neonectria species can be found on
the bark of recently dead woody plants and sometimes on
decaying herbaceous material (Samuels and Brayford
1990; Samuels and Brayford 1990, 1993, 1994; Rossman
et al. 1999; Castlebury et al. 2006; Chaverri et al. 2011).
Some species of Neonectria are plant pathogens causing
cankers and other diseases on hardwood and coniferous
trees (Castlebury et al. 2006; Rossman and Palm-Hernández 2008; Crane et al. 2009; Chaverri et al. 2011; Schmitz
et al. 2017; Wenneker et al. 2017). Neonectria neomacrospora has been added to the European and
Mediterranean Plant Protection Organization (EPPO) alert
list (EPPO, 2019).
Classification—Sordariomycetes,
Hypocreomycetidae,
Hypocreales, Nectriaceae
Type species—Neonectria ramulariae Wollenw., Annls
mycol. 15(1/2):52 (1917)
Distribution—Worldwide
Disease symptoms—Canker
Dead shoots can be observed in the lower branches or all
over the affected tree. Affected branches or trunks show
canker and some may have abundant resin flow. When the
canker girdles the affected area, part of the tree above the
canker dies. Under humid conditions characteristic small,
red fruiting bodies will be formed. Badly affected trees will
eventually die (Castlebury et al. 2006).
Beech (Fagus) bark disease is caused by N. coccinea, N.
ditissima, N. fuckeliana and N. faginata. Cankers of fruit trees
are caused by N. rugulosa and N. ditissima. Shoot dieback of
Abies species are caused by N. neomacrospora (Castlebury
et al. 2006; Rossman et al. 2008; Crane et al. 2009; Chaverri
et al. 2011; Schmitz et al. 2017; Wenneker et al. 2017).
Hosts—Wide host range including plant genera in
Amaryllidaceae, Aracaceae, Araliaceae, Betulaceae, Ericaceae, Fagaceae, Lauraceae, Myrtaceae, Pinaceae, Proteaceae, Rosaceae, Sapindaceae and Vitaceae (Farr and
Rossman 2019).
Morphological based identification and diversity
The genus Neonectria was established by Wollenweber
(1917). The generic concept of Neonectria has been revised
by different authors (Booth 1959; Samuels and Brayford
1994; Rossman et al. 1999). Rossman et al. (1999)
accepted only three species (N. coccinia, N. galligena and
N. ramulariae) in Neonectria. Subsequently, species were
added to the genus based on morphology and/or phylogeny
(Hirooka et al. 2005; Castlebury et al. 2006; Luo and
Zhuang 2010a, b; Zhao et al. 2011; Lombard et al.
2014, 2015). However, some unrelated species were
transferred to other genera based on molecular analyses
123
Fungal Diversity
123
Fungal Diversity
b Fig. 16 Phylogenetic tree generated by maximum likelihood analysis
of combined ITS, LSU, SSU, tef1 and TUB2 sequences. Related
sequences were obtained from GenBank. Forty-four strains are
included in the analyses, which comprise 3477 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 Dothiorella iberica (CBS 113188 and CBS
115041). Tree topology of the ML analysis was similar to the MP and
BI. The best scoring RAxML tree with a final likelihood value of
- 12764.659013 is presented. The matrix had 898 distinct alignment
patterns, with 28.31% of undetermined characters or gaps. Estimated
base frequencies were as follows; A = 0.238049, C = 0.253522,
G = 0.272022, T = 0.236408; substitution rates AC = 1.121500,
AG = 2.393284, AT = 1.053637, CG = 1.711098, CT = 4.682724,
GT = 1.000000; gamma distribution shape parameter a = 0.545763.
The maximum parsimonious dataset consisted of constant 2820, 575
parsimony-informative and 82 parsimony-uninformative characters.
The parsimony analysis of the data matrix resulted in the maximum of
two equally most parsimonious trees with a length of 1490 steps
(CI = 0.626, RI = 0.861, RC = 0.539, HI = 0.374) in the first tree.
RAxML, maximum parsimony bootstrap support values C 65% and
Bayesian posterior probabilities C 0.95 (BYPP) are shown respectively near the nodes. Ex-type strains are in bold
and morphological data (Lombard et al. 2014, 2015). There
are 31 species recognised in the genus, while 23 species
have sequence data in GenBank (4/7/2019). Morphological
characters (perithecial morphology, ascospore size,
macroconidial morphology, presence or absence of
microconidia and chlamydospores) along with DNA
sequence analysis are appropriate for identification of
Neonectria species (Brayford et al. 2004).
Molecular based identification and diversity
Since 2001, DNA sequence analysis has been used to
clarify the taxonomy of Neonectria (Mantiri et al. 2001;
Brayford et al. 2004; Halleen et al. 2004; Hirooka et al.
2005; Chaverri et al. 2011). Mantiri et al. (2001) and
Brayford et al. (2004) used mtSSU rDNA sequence data to
infer intrageneric relationships of some Neonectria and
Cylindrocarpon species. Later, Halleen et al. (2004) used
mtLSU rDNA, TUB2 and nrDNA ITS regions to separate
some Cylindrocarpon species included in the N. mammoidea group. Chaverri et al. (2011) approached a comprehensive treatment of Cylindrocarpon and Neonectria
based on combined loci analyses and morphological data.
Chaverri et al. (2011) defined Neonectria sensu stricto
within Nectriaceae with Cylindrocarpon sensu stricto
based on multi-gene phylogeny of ITS, LSU, tef1, TUB2,
ACT, and RPB1. The ITS, tef1 and TUB2 loci possess
highly variable regions (Chaverri et al. 2011) and are
important in species delimitation of Neonectria. Rossman
et al. (2013) proposed to protect generic name Neonectria
over Cylindrocarpon. Maharachchikumbura et al. (2015)
considered Cylindrodendrum not to be congeneric with
Neonectria and accepted Neonectria over Cylindrocarpon.
This study reconstructs the phylogeny of Neonectria
based on analyses of a combined ITS, LSU, tef1 and TUB2
sequence data (Table 11, Fig. 17). The phylogenetic tree is
updated with recently introduced Neonectria species and
corresponds to previous studies (Chaverri et al. 2011;
Lombard et al. 2014; Mantiri et al. 2001).
Recommended genetic markers (genus level)—LSU, ITS,
tef1 and TUB2
Recommended genetic markers (species level)—ITS, tef1
and TUB2
Accepted number of species: 28 species
References: Rossman et al. 1999 (morphology), Brayford
et al. 2004; Hirooka and Kobayashi 2007; Chaverri et al.
2011; Lombard et al. 2014 (morphology, phylogeny).
Neopestalotiopsis Maharachch., K.D. Hyde & Crous
(2014), in Maharachchikumbura et al., Stud. Mycol. 79:147
(2014a)
Neopestalotiopsis is an important plant pathogenic, saprobic
and endophytic genus commonly present in tropical and
subtropical ecosystems. The genus was introduced by
Maharachchikumbura et al. (2014b). Species of
Neopestalotiopsis are appendage-bearing asexual coelomycetes in the family Sporocadaceae (Jayawardena et al. 2016).
Classification—Sordariomycetes, Xylariomycetidae, Amphisphaeriales, Sporocadaceae
Type species—Neopestalotiopsis protearum (Crous & L.
Swart) Maharachch. et al., in Maharachchikumbura et al.,
Stud. Mycol. 79:147 (2014a)
Distribution—Worldwide
Disease symptoms—Canker, dieback, fruit rots, leaf spot
Pathogenic Neopestalotiopsis are recorded in post-harvest fruit rots of grapes, trunk diseases in grapevine in
China, India and France, leaf spot disease of grapevine in
China and leaf blights in many plant species worldwide
(Hyde et al. 2014; Jayawardena et al. 2015, 2016;
Maharachchikumbura et al. 2017).
Neopestalotiopsis species infect a variety of grapevine
cultivars, causing diseases including grapevine dieback,
fruit rot, postharvest disease and severe defoliation. Initial
symptoms of fruit rot disease are mostly observed at the
splits between the pedicel and the berry and at the wounds
of the fruits and severely infected fruits become rotten and
separate completely from the pedicel (Jayawardena et al.
2015). Neopestalotiopsis asiatica and N. javaensis are
associated with grapevine trunk disease (Maharachchikumbura et al. 2017). Grapevine trunk diseases
reduce the yield and quality of grapes, even leading to
partial or total death of individual plants.
Neopestalotiopsis clavispora and N. surinamensis cause
guava scab (Solarte et al. 2018). Neopestalotiopsis ellipsospora causes leaf spot on sweet potatoes
123
Fungal Diversity
Table 10 Details of Macrophomina and Sphaeropsis isolates used in the phylogenetic analyses
Species
Isolate/voucher no
SSU
ITS
LSU
tef1
TUB2
Barriopsis fusca
CBS 174.26*
EU673182
EU673330
DQ377857
EU673296
EU673109
Botryobambusa fusicoccum
CBS 134113*
JX646826
JX646792
JX646809
JX646857
N/A
MFLUCC 11-0657
JX646827
JX646793
JX646810
JX646858
N/A
CBS 133992*
JX646825
JX646791
JX646808
JX646856
JX646841
MFLUCC 10-0051
JX646824
JX646790
JX646807
JX646855
JX646840
CBS 119047*
EU673175
DQ299245
EU673244
EU017539
EU673107
Botryosphaeria agaves
B. corticis
ATCC 22927
EU673176
DQ299247
EU673245
EU673291
EU673108
CBS 115476 *
EU673173
AY236949
AY928047
AY236898
AY236927
CBS 110302
EU673174
AY259092
EU673243
AY573218
EU673106
Cophinforma atrovirens
MFLUCC 11-0425*
JX646833
JX646800
JX646817
JX646865
JX646848
Dothiorella iberica
MFLUCC 11-0655
CBS 115041*
JX646834
EU673155
JX646801
AY573202
JX646818
AY928053
JX646866
AY573222
JX646849
EU673096
B. dothidea
Diplodia allocellula
CBS 113188
EU673156
AY573198
EU673230
EU673278
EU673097
CBS 130408*
N/A
JQ239397
JQ239410
JQ239384
JQ239378
CBS 130410
N/A
JQ239399
JQ239412
JQ239386
JQ239380
CBS 132777*
N/A
JN693507
N/A
JQ517317
JQ411459
UCROK 1429
N/A
JQ411412
N/A
JQ512121
JQ411443
CBS 115812*
EU673193
AY639595
DQ377902
DQ103566
DQ458860
CBS 116355
EU673194
AY639594
EU673252
DQ103567
EU673126
CBS 134112*
JX646830
JX646797
JX646814
JX646862
JX646845
MFLUCC 11-0656
JX646831
JX646798
JX646815
JX646863
JX646846
CBS 499.66
KF531818
KF531820
DQ377925
KF531798
KF531800
CBS 251.49
KF531817
KF531819
DQ377923
KF531797
KF531799
Neodeightonia subglobosa
CBS 448.81*
EU673202
EU673337
DQ377866
EU673306
EU673137
N. phoenicum
CBS 122528*
EU673205
EU673340
EU673261
EU673309
EU673116
Macrophomina phaseolina
CBS 227.33
KF531823
KF531825
DQ377906
KF531804
KF531806
M. pseudophaseolina
CBS 162.25
CPC 21422
KF531824
N/A
KF531826
KF951792
DQ377905
N/A
KF951996
KF952154
KF531805
KF952234
D. agrifolia
Lasiodiplodia gonubiensis
L. lignicola
Neoscytalidium hyalinum
Phaeobotryon mamane
Oblongocollomyces variabilis
Sphaeropsis citrigena
S. eucalypticola
CPC 21417*
N/A
KF951791
N/A
KF952153
KF952233
CPC 21524
N/A
KF951799
N/A
KF952161
KF952240
CBS 122980*
EU673184
EU673332
EU673248
EU673298
EU673121
CPC 12442
EU673185
EU673333
DQ377899
EU673299
EU673124
CMW 25420
N/A
EU101313
N/A
EU101358
N/A
CMW 25421, CBS 121775
N/A
EU101314
N/A
EU101359
N/A
CMW 25422, CBS 121776
N/A
EU101326
N/A
EU101371
N/A
CMW 25423
N/A
EU101327
N/A
EU101372
N/A
ICMP 16812*
EU673180
EU673328
EU673246
EU673294
EU673140
ICMP 16818
EU673181
EU673329
EU673247
EU673295
EU673141
CBS 133993*
JX646835
JX646802
JX646819
JX646867
JX646850
MFLUCC 11-0654
JX646836
JX646803
JX646820
JX646868
JX646851
S. porosa
CBS 110496*
EU673179
AY343379
DQ377894
AY343340
EU673130
S. visci
CBS 110574
CBS 122526 *
N/A
N/A
AY343378
EU673324
N/A
N/A
AY343339
EU673292
N/A
N/A
CBS 186.97
EU673178
EU673325
DQ377868
EU673293
EU673128
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
123
Fungal Diversity
Table 11 Details of the Neonectria isolates used in the phylogenetic analyses
Species
Isolates/voucher no
ITS
LSU
TUB
tef1
Neonectria austroradicicola
PDD 46334 G.J.S. 83-154
EF607077
–
–
–
N candida
CBS 151 29 IMI 113894/MUCL 28083
AY677291
AY677333
DQ789863
DQ789723
N. coccinea
CBS 119158/GJS 98-114
JF268759
KC660620
KC660727
JF268734
N. confusa
CBS 127485/HMAS 99197*
FJ560437
KM515934
FJ860054
–
N. confusa
CBS 127484/HMAS 99198
KM515889
KM515933
KM515886
–
N. ditissima
CBS 100318
KM515890
KM515935
DQ789858
KM515944
N. ditissima
CBS 100317
KM515891
KM515936
KM515887
KM515945
N. ditissimopsis
HMAS 98329*
JF268764
–
JF268729
JF268745
N. faginata
CBS 217.67/IMI 105738/ATCC 16547*
HQ840385
HQ840382
JF268730
JF268746
N. faginata
CBS 119160/GJS 04-159
HQ840384
HQ840383
DQ789883
DQ789740
N. fuckeliana
N. hederae
CBS 239.29/IMI 039700
IMI 058770a/ATCC 16543*
HQ840386
–
HQ840377
KC660617
DQ789871
DQ789895
JF268748
DQ789752
N. hederae
CBS 714.97/PD 97/1932
–
KC660616
DQ789878
KC660461
N. lugdunensis
CBS 125485/DAOM 235831/TG 2008-07
KM231762
KM231625
KM232019
KM231887
N. major
CBS 240.29/IMI 113909*
JF735308
KM515942
DQ789872
JF735782
N. microconidia
HMAS 98294
KC660530
KC660587
–
–
N. neomacrospora
CBS 198.62/BBA 9628/IMI 113890
AJ009255
HM364316
HM352865
HM364351
N. neomacrospora
CBS 324.61/DSM 62489/IMB 9628
JF735312
HM364318
DQ789875
–
N. obtusispora
CBS 183.36/IMI 113895
AM419061
KM515943
AM419085
JF735796
N. punicea
CBS 242.29
KC660522
KC660565
DQ789873
DQ789730
N. shennongjiana
HMAS 183185
FJ560440
–
FJ860057
–
N. tsugae
CBS 788.69*
KM231763
HQ232146
KM232020
–
Thelonectria gongylodes
CBS 12511/GJS 90-48
JQ403330
JQ403369
HM352870
HM364357
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
(Maharachchikumbura et al. 2016). Neopestalotiopsis
clavispora causes crown and root rot of strawberry
worldwide while N. iranensis infects leaves and fruits of
strawberry (Ayoubi and Soleimani 2016), with the pathogen initially developing circular, black, and slightly sunken
spots that expand outwards on the surface. Droplets of
spores are scattered over the white aerial mycelial area and
later cause soft decay of the fruit flesh (Ayoubi and
Soleimani 2016). Canker and dieback on blueberry in Chile
and Uruguay are also caused by N. clavispora (Espinoza
et al. 2008; González et al. 2012; Chamorro et al. 2016).
Neopestalotiopsis samarangensis has been described from
wax apple fruit rot in Thailand (Maharachchikumbura et al.
2013a, b). In fruit rots, the initial symptom is small, circular, black, slightly sunken spots on fruits. Later, the spots
enlarged rapidly, become sunken and result in a soft decay
of the fruit flesh (Maharachchikumbura et al. 2013a, b).
Hosts—Species of Fragaria 9 ananassa, Ipomoea, Malus,
Psidium, Vaccinium and Vitis
Morphological based identification and diversity
Neopestalotiopsis species can be differentiated using morphology and molecular phylogeny (Maharachchikumbura
et al. 2014b). There are 36 species epithets listed in Index
Fungorum (2019). Neopestalotiopsis species differ from
Pestalotiopsis and Pseudopestalotiopsis in having somewhat
versicolorous median cells (Maharachchikumbura et al.
2014b) whereas both Pestalotiopsis and Pseudopestalotiopsis have concolourous median cells (Maharachchikumbura et al. 2014b) as well as its conidiophores which are
indistinct and often reduced to conidiogenous cells (Maharachchikumbura et al. 2014b).
Conidial morphology is widely used in taxonomy in
pestalotioid fungi (Steyaert 1949; Guba 1961; Nag Raj
1993; Maharachchikumbura et al. 2012, 2014b). Species
delimitation based on morphological characters is limited
as these characters are plastic and vary between hosts and
environments (Maharachchikumbura et al. 2011, 2016).
Therefore, phylogenetic species recognition is an effective
method to identify different pestalotioid species (Maharachchikumbura et al. 2016).
Molecular based identification and diversity
Neopestalotiopsis species can be roughly separated from
Pestalotiopsis and Pseudopestalotiopsis based on the total
number of base pairs in the ITS region
123
Fungal Diversity
Fig. 17 Phylogenetic tree generated by maximum likelihood analysis
of combined ITS, LSU, tef1 and TUB sequence data of Neonectria
species. Related sequences were obtained from GenBank. Twentythree strains are included in the analyses, which comprise 2336
characters including gaps. Tree topology of the ML analysis was
similar to the one generated from BI (figure not shown). The best
scoring RAxML tree with a final likelihood value of - 7942.756270
is presented. The matrix had 525 distinct alignment patterns, with
18.13% of undetermined characters or gaps. Estimated base
frequencies were as follows; A = 0.223071, C = 0.285136,
G = 0.261197, T = 0.230596; substitution rates AC = 1.213729,
AG = 2.500008, AT = 1.727890, CG = 0.720430, CT = 6.191594,
GT = 1.000000; gamma distribution shape parameter a = 0.749195.
Maximum likelihood bootstrap support (C 55%) and posterior
probabilities (BYPP C 0.90) from Bayesian inference analysis are
indicated respectively near the nodes. Ex-type strains are in bold. The
tree is rooted in Thelonectria gongylodes
(Maharachchikumbura et al. 2014b). However, the use of
ITS sequences alone does not resolve Neopestalotiopsis
species (Maharachchikumbura et al. 2012). Therefore,
Maharachchikumbura et al. (2014b) suggested using combined ITS, TUB2 and tef1 genes to provide a better resolution in phylogenetic analyses. This study reconstructs the
phylogeny of Neopestalotiopsis based on a combined ITS,
TUB2 and tef1 sequence data (Fig 18, Table 12) and
reveals similar phylogenetic relationships to previous
studies by Maharachchikumbura et al. (2014b, 2016).
Schröter (1886), but no species was assigned as a type for
the genus (Constantinescu et al. 2005). Plasmopara nivea
is considered as the type species of this genus (Constantinescu et al. 2005). Plasmopara species are commonly
known as downy mildew pathogens. There are 2064
records in USDA fungal database under genus Plasmopara
(Farr and Rosman 2019). Downy mildew has become one
of the most troublesome diseases in agriculture including
P. viticola on grape, P. geranii on geranium and P. halstedii on sunflower (McTaggart et al. 2015). Kamoun et al.
(2015) categorized P. viticola among the top ten Oomycetes pathogens in plant pathology. Current interest in this
genus is to understand the co-evolution with the host and
effective disease management (Thines and Kamoun 2010).
Taxonomically useful morphological or ecological characters are few for the downy mildews and this makes
identification of synapomorphic states impossible (Göker
et al. 2003).
Classification—Oomycota incertae sedis, Peronosporea,
Peronosporidae, Peronosporales, Peronosporaceae
Type species—Plasmopara nivea (Unger) J. Schröt.
Distribution—Worldwide
Disease symptoms—Downy mildew
Hosts—Species belonging to this genus are obligate biotrophs on a wide range of hosts including Acanthaceae,
Asteraceae, Balsaminaceae, Geraniaceae, Malvaceae,
Onagraceae, Orobanchaceae, Violaceae and Vitaceae
Recommended genetic marker (genus level)—LSU
Recommended genetic markers (Species level)—ITS,
TUB2 and tef1
Accepted number of species: 41 species.
References: Maharachchukumbura 2012, 2014b (morphology, phylogeny); Maharachchukumbura et al. 2016
(morphology, phylogeny); Jayawardena et al. 2015, 2016
(morphology, phylogeny, pathogenicity)
Plasmopara J. Schröt., in Cohn, Krypt.-Fl. Schlesien
3.1(9–16): 236 (1886) [1889]
The genus Plasmopara belongs to the family Peronosporaceae of the Peronosporales in Oomycetes (Riethmüller
et al. 2002; Görg et al. 2017). This genus is included in this
study as it is an important plant pathogen on many economically important crops. Plasmopara was introduced by
123
Fungal Diversity
Fig. 18 Phylogram generated from maximum likelihood analysis
based on combined ITS, TUB2 and tef1 sequence data of Neopestalotiopsis species. Related sequences were obtained from GenBank.
Forty-three strains are included in the combined sequence analyses,
which comprise 1391 characters with gaps. Pestalotiopsis diversiseta
(MFLUCC 12-0287) is used as the outgroup taxa. The best scoring
RAxML tree with a final likelihood value of - 5457.035085 is
presented. The matrix had 409 distinct alignment patterns, with 6.30%
of undetermined characters or gaps. Estimated base frequencies were
as
follows;
A = 0.231067,
C = 0.270889,
G = 0.213946,
T = 0.284098; substitution rates AC = 0.847461, AG = 2.876343,
AT = 1.282349, CG = 0.723831, CT = 3.850003, GT = 1.000000;
gamma distribution shape parameter a = 0.235476. The maximum
parsimonious dataset consisted of 1026 constant, 177 parsimonyinformative and 188 parsimony-uninformative characters. The parsimony analysis of the data matrix resulted in the maximum of ten
equally most parsimonious trees with a length of 650 steps
(CI = 0.688, RI = 0.609, RC = 0.419, HI = 0.312) in the first tree.
RAxML and maximum parsimony bootstrap support value C 50%
and posterior probabilities BYPP C 0.90 from Bayesian inference
analysis are indicated respectively near the nodes, are shown
respectively near the nodes. Ex-type strains are in bold
(Voglmayr et al. 2004; Thines and Kamoun 2010;
McTaggart et al. 2015).
discussion of nomenclatural and taxonomic problems of
this genus, Plasmopara was segregated in two different
groups by morphology and phylogeny (Constantinescu
et al. 2005). Constantinescu et al. (2005) proposed to
introduce a new generic name for P. pygmaea and for six
Morphological based identification and diversity
Wilson (1907) was the first to consider P. pygmaea as the
type of Plasmopara. However, even after a century of
123
Fungal Diversity
Table 12 Details of the
Neopestalotiopsis isolates used
in the phylogenetic analyses
Species
Isolate no
ITS
TUB2
tef1
Neopestalotiopsis acrostichum
MFLUCC 17-1754*
MK764272
MK764338
MK764316
N. alapicalis
MFLUCC 17-2544*
MK357772
MK463545
MK463547
N. aotearoa
MFLUCC 17-1754
MK764272
MK764338
MK764316
N. asiatica
MFLUCC12-0286*
JX398983
JX399018
JX399049
N. australis
CBS 114159*
KM199348
KM199432
KM199537
N. brachiata
MFLUCC 17-1555*
MK764274
MK764340
MK764318
N. chrysea
MFLUCC12-0261*
JX398985
JX399020
JX399051
N. clavispora
MFLUCC 12-0281*
JX398979
JX399014
JX399045
N. cocoes
MFLUCC 15-0152*
KX789687
–
KX789689
N. coffeae-arabicae
HGUP 4019*
KF412647
–
–
N. cubana
CBS 600 96*
KM199347
KM199438
KM199521
N. egyptiaca
CBS 140162*
KP943747
KP943746
KP943748
N. ellipsospora
MFLUCC 12-0283*
JX398980
JX399016
JX399047
N. eucalypticola
CBS 264 37*
KM199376
KM199431
KM199551
N. foedans
N. formicarum
CGMCC3 9123*
CBS 362 72*
JX398987
KM199358
JX399022
KM199455
JX399053
KM199517
N. honoluluana
CBS 114495*
KM199364
KM199457
KM199548
N. iraniensis
CBS 137768*
KM074048
KM074057
KM074051
N. javaensis
CBS 257 31*
KM199357
KM199437
KM199543
N. keteleeria
MFLUCC 13-0915*
KJ503820
KJ503821
KJ503822
N. macadamiae
BRIP 63738B*
KX186604
KX186654
KX186627‘
N. magna
MFLUCC12-652*
KF582795
KF582793
KF582791
N. mesopotamica
CBS 336 86*
KM199362
KM199441
KM199555
N. musae
MFLUCC 15-0776*
KX789683
KX789686
KX789685
N. natalensis
CBS 138 41*
KM199377
KM199466
KM199552
N. pernambucana
GS-2014 strain RV01*
KJ792466
–
KU306739
N. petila
MFLUCC 17-1738*
MK764275
MK764341
MK764319
N. piceana
CBS 394 48*
KM199368
KM199453
KM199527
N. protearum
CBS 114178*
JN712498
KM199463
KM199542
N. rhisophorae
MFLUCC 17-1550*
MK764277
MK764343
MK764321
N. rosae
N. rosicola
CBS 101057*
CFCC 51992
KM199359
KY885239
KM199429
KY885245
KM199523
KY885243
N. samarangensis
MFLUCC 12-0233*
JQ968609
JQ968610
JQ968611
N. saprophytica
MFLUCC 12-0282*
KM199345
KM199433
KM199538
N. sonneratae
MLFUCC 17-1745*
MK764279
MK264345
MK264323
N. steyaertii
IMI192475*
KF582796
KF582794
KF582792
N. surinamensis
CBS 450.74*
KM199351
KM199465
KM199518
N. thailandica
MFLUCC 17-1730*
MK764281
MK764347
MK754325
N. umbrinospora
MFLUCC 12-0285*
JX398984
JX399019
JX399050
N. vitis
MFLUCC 15-1265*
KU140694
KU140685
KU140676
N. zimbabwana
CBS 111495*
–
KM199456
KM199545
Ex-type (or ex-epitype) strains are in bold and marked with an asterisk* and voucher strains are in bold
other related species and they have established the current
classification for Plasmopara.
123
Species belonging to Plasmopara have the following
characters. Hyphae are intercellular, haustoria are intracellular, as obpyriform, globose, or slightly elongated
Fungal Diversity
vesicles (Göker et al. 2003; Voglmayr et al. 2004; Constantinescu et al. 2005). A callose sheath often surrounds
haustoria. Sporangiophores are mostly present on the under
leaf surface of the host, but sometimes also on other parts
of the plant (eg. P. viticola produces sporangiophores on
inflorescences and young berries, Zhang et al. 2017).
Sporangiophores are colourless, branched in the upper part.
They branch monopodially, in two to more orders (Göker
et al. 2003; Constantinescu et al. 2005). Branches are more
or less divergent, ending in a number of elongated ultimate
branchlets. The newly formed wall closing the tip after
sporangium discharge (Constantinescu et al. 2005). Callose
plugs usually present in trunk and/or branches. Sporangiogenesis is holoblastic. These species produce sporangia
synchronously, which vary in shape, sporangia wall is
colourless, appearing smooth in light microscopy but
showing various types of ornamentations in the electron
microscope (Constantinescu et al. 2005). There are 199
epithets listed in Index Fungorum (2019), however, 40 of
them do not belong to Plasmopara based on phylogenetic
evidence (Figs. 19, 20).
Oospores develop a single germ tube, terminating with
sporangium, once a sporangium disseminated, by rain flash
or wind, it releases zoospores (Ash 2000; Rossi et al. 2008;
Carisse 2016; Kamoun et al. 2015; Wilcox et al. 2015).
Molecular based identification and diversity
Molecular and phylogenetic studies have shown that
Plasmopara is polyphyletic (Riethmüller et al. 2002; Göker
et al. 2003, 2007; Voglmayr et al. 2004; Voglmayr and
Constantinescu 2008). Even though Wilson (1907) proposed P. pygmaea as the type species of the genus Plasmopara, it has a close relationship with Bremia,
Paraperonospora and Basidiophora (Göker et al. 2003).
With these morphological and phylogenetic aspects, many
species that are traditionally included in Plasmopara have
moved into new genera. The newly introduced genera are
Viennotia (Göker et al. 2003), Protobremia (Voglmayr
et al. 2004), and Plasmoverna (Constantinescu et al. 2005).
Constantinescu et al. (2005) resolved Plasmopara phylogeny, introducing Plasmoverna as a new genus to
accommodate the morphologically dissimilar and polyphyletic taxa belonging to previous classifications. Voglmayr and Constantinescu (2008) re-classified three species
of Plasmopara into new genus Novotelnova Voglmayr &
Constant. The species belonging to Novotelnova were
identical in the analyses of the nuLSU and nuSSU-ITS15.8S datasets. Therefore, in the present study, we follow
Voglmayr and Constantinescu (2008) to provide a backbone tree for Plasmopara using combined nuLSU sequence
data (Fig. 21, Table 13).
The downy mildew pathogens have been studied
extensively to understand their host specificity and co-
evolution with the host plants. The grape downy mildew
has been identified as a host-specific cryptic species
(Rouxel et al 2013; Zhang et al. 2017). Rouxel et al. (2013)
considered the cryptic species as formae speciales: P.
viticola f. sp. riparia (lineage A occurring on V. riparia and
some hybrids); P. viticola f. sp. aestivalis (lineage B found
on V. aestivalis, V. labrusca, V. vinifera and some hybrids);
P. viticola f. sp. vinifera (lineage C occurring on V. vinifera
and some hybrids); P. viticola f. sp. quinquefolia (lineage
D found on V. quinquefolia). To understand the cryptic
lineages genealogical concordance phylogenetic species
recognition (GCPSR) approach is currently accepted
(Taylor et al. 2000; Rouxel et al. 2013). GCPSR facilitate
the most convenient analysis for species that cannot be
cultivated or mate in control conditions (O’Donnell et al.
2000; Steenkamp et al. 2002; Rouxel et al. 2013).
Recommended genetic marker (genus level)—LSU
Recommended genetic marker (species level)—LSU
The universal barcode for the Oomycetes, the cytochrome oxidase subunit 1 and 2 genes (cox 1 and cox 2) are
used. However Choi et al. (2015) suggested cox2 is better
suited to this because of its ease of amplification among
oomycete lineages, better performance on herbarium
specimens, higher discriminatory power at the species level
and the availability of a large taxonomically diverse database that already includes many species of oomycetes,
especially the downy mildew. In previous studies, nuLSU
gene regions (D1–D3 and D7–D8 sequences) were widely
used (Riethmüller et al. 2002; Göker et al. 2003, 2007;
Voglmayr et al. 2004; Voglmayr and Constantinescu
2008). Branch supports of the backbone tree was often
higher in the nuLSU data, which resulted in a larger data
matrix and a higher number of parsimony-informative
characters than when ITS was used (Voglmayr and Constantinescu 2008). No study has combined these gene
regions or any other gene regions as the marker to understand the phylogenetic relationship within the genus.
Accepted number of species: There are 199 species in
Index Fungorum (2019) and only 19 species have molecular data in this genus.
References: Riethmüller et al. 2002; Göker et al. 2003;
2007; Voglmayr et al. 2004; Voglmayr and Constantinescu
2008; Rouxel et al 2013; Zhang et al. 2017 (morphology,
phylogeny).
Pseudopestalotiopsis Maharachch., K.D. Hyde & Crous
(2014), in Marachchikumbura et al., in Maharachchikumbura et al., Stud. Mycol. 79:180 (2014a)
The genus was introduced by Maharachchikumbura
et al. (2014b) with Pseudopestalotiopsis theae (Sawada)
Maharachch., K.D. Hyde & Crous as the type species.
Species of Pseudopestalotiopsis are appendage-bearing
phenotypically diverse coelomycetes in the family
123
Fungal Diversity
Fig. 19 Grape downy mildew disease symptoms. a Infected grapevines, b–c appearance of oil spot on the upper leaf surface. d Sporulation on
the lower leaf surface. e Young infected berries with sporulation. f Infection on fruits
Sporocadaceae and are commonly found in tropical and
subtropical ecosystems (Jaklitsch et al. 2016;
Maharachchikumbura et al. 2016). Pseudopestalotiopsis is
characterized by brown to dark brown or olivaceous
median cells and knobbed or not knobbed apical appendages (Maharachchikumbura et al. 2014b, 2016). The
epitype of Pseudopestalotiopsis theae (Sawada) Steyaert
was designated from fresh leaves of Camellia sinensis
collected in Thailand (Maharachchikumbura et al.
2013a, b). Pseudopestalotiopsis has been studied for the
production of various secondary metabolites with diverse
structural features, with antitumour, antifungal, antimicrobial and other activities (Ding et al. 2008;
Maharachchikumbura et al. 2011, 2016).
Pseudopestalotiopsis theae is economically significant
as it has been identified as a pathogen in major tea-growing
areas in the world (Maharachchikumbura et al. 2016).
Pseudopestalotiopsis theae causes grey blight of tea and
reduces
yield
(Maharachchikumbura
et
al.
2011, 2013a, b, 2016). Pseudopestalotiopsis theae was also
isolated as an endophyte from different hosts (Camellia
nitidissima, C. sinensis, Holarrhena antidysenterica,
Podocarpus macrophyllus, Terminalia arjuna) or as a
saprobe (seeds of Diospyros crassiflora) (Maharachchikumbura et al. 2011, 2013a, b, 2016).
123
Classification—Sordariomycetes, Xylariomycetidae, Amphisphaeriales, Sporocadaceae
Type species—Pseudopestalotiopsis theae (Sawada)
Maharachch., in Maharachchikumbura et al., Stud. Mycol.
79:183 (2014a)
Distribution—China, India, Indonesia, Malaysia, Thailand
(Maharachchikumbura et al. 2016)
Disease symptoms—Pseudopestalotiopsis theae causes
grey blight in major tea growing areas in the world (Horikawa 1986, Maharachchikumbura et al. 2013a, b, 2016).
The pathogen develops circular to irregular leaf spots initially and grey, brown margins when mature, covering up
to half of the leaf with acervuli (Maharachchikumbura
et al. 2016). Pseudopestalotiopsis ixorae and P. taiwanensis cause a leaf spot which initially develops small,
circular, ash-coloured spots which later turn into brown
spots (Tsai et al. 2018).
Hosts—Averrhoa carambola, Camellia sp., Cinnamomum
sp., Cocos nucifera, Diospyros crassiflora, Fragaria sp.,
Hibiscus rosa-sinensis, Holarrhena antidysenterica, Ixora
sp., Kandelia obovate, Macaranga sp., Pandanus odoratissimus, Podocarpus macrophyllus, Prunus sp., Terminalia arjuna and Thea sinensis
Fungal Diversity
Fig. 20 Disease cycle of grape downy mildew. Redrawn from Kassemeyer (2017)
Morphological based identification and diversity
Molecular based identification and diversity
Pseudopestalotiopsis can be distinguished from
Neopestalotiopsis and Pestalotiopsis by dark concolourous
median cells with indistinct conidiophores (Maharachchikumbura et al. 2014b, 2016). However, there
could be a wide host range for Pseudopestalotiopsis species
and the actual number of species could be much higher
than presently known (Maharachchikumbura et al.
2011, 2016).
Conidial morphology is widely used in taxonomy in
pestalotioid fungi (Steyaert 1949; Guba 1961; Nag Raj
1993; Maharachchikumbura et al. 2011, 2012, 2014b).
Species delimitation based on morphological characters is
limited as these characters are plastic and vary between
hosts and environments (Maharachchikumbura et al.
2011, 2016). Therefore, phylogenetic species recognition is
an effective method to identify different pestalotioid species (Maharachchikumbura et al. 2016).
ITS sequence data alone is not sufficient for species
delimitation
of
Pseudopestalotiopsis.
Therefore,
Maharachchikumbura et al. (2012) suggested a phylogenetic analysis of combined ITS, TUB2 and tef1 genes
provide better resolution as compared to single gene phylogeny (Fig. 22, Table 14).
Recommended genetic markers (genus level)—LSU (as
outlined in Maharachchikumbura et al. 2012)
Recommended genetic markers (species level)—ITS,
TUB2 and tef1 (as outlined in Maharachchikumbura et al.
2012)
Accepted number of species: 20 species
References: Maharachchukumbura 2013a, b, 2014b, 2016b
(morphology, phylogeny)
Rosellinia De Not., G. bot. ital.1 (1): 334(1844)
Rosellinia (Xylariaceae) species are characterized
mainly as saprobes, some endophytes and occasionally as
pathogens. They have a worldwide distribution and common in both temperate and tropical regions (Petrini
123
Fungal Diversity
Fig. 21 Phylogenetic tree generated by maximum parsimony analysis
of LSU sequence data of Plasmopara species. Related sequences
were obtained from GenBank. Nineteen strains are included in the
analyses, which comprise 1263 characters including gaps. The tree
was rooted with Phytophthora arece (AR 234). Tree topology of the
MP analysis was similar to the ML. The maximum parsimonious
dataset consisted of constant 1053, 110 parsimony-informative and
100 parsimony-uninformative characters. The parsimony analysis of
the data matrix resulted in the maximum of two equally most
parsimonious trees with a length of 365 steps (CI = 0.641, RI =
0.539, RC = 0.345, HI = 0.359) in the first tree. The best scoring
RAxML tree with a final likelihood value of - 3660.849005 is
presented. The matrix had 254 distinct alignment patterns, with
30.91% of undetermined characters or gaps. Estimated base frequencies were as follows; A = 0.229156, C = 0.177763, G = 0.308486,
T = 0.284595; substitution rates AC = 0.706031, AG = 4.368078,
AT = 1.048734, CG = 0.141039, CT = 7.063364, GT = 1.000000;
gamma distribution shape parameter a = 0.163551. RAxML and
maximum parsimony bootstrap support value C 50% (BT) are shown
respectively near the nodes
1993, 2013; ten Hoopen and Krauss 2006). Plant pathogenic Rosellinia species play a vital role in economically
important crops, trees and ornamental plants. Rosellinia
desmazieresii and R. necatrix are mostly known from
temperate regions, while R. bunodes is known only from
the tropics causing root rot on fruit trees and vines (Agrios
2005; ten Hoopen and Krauss 2006). Among the root
diseases cause by Rosellinia species, R. bunodes is
responsible for black root rot, R. necatrix for white root rot
and R. pepo for stellate root rot (Castro et al. 2013). Species of this genus can survive as microslerotia in wood,
roots and soil and the infection spreads through feeder
roots when they contact hyphae or microsclerotia (Ploetz
et al. 2003).
123
Fungal Diversity
Table 13 Details of the
Plasmopara isolates used in the
phylogenetic tree
Species
Isolate/voucher no
Host
LSU
Plasmopara australis
HV 2867
Luffa cylindrica
KT159461
P. baudysii
HV 571
Berula erecta
AY035517
P. densa
HV 2232
Rhinanthus minor
EF553463
P. epilobii
HV988
Epilobium parviflorum
AY250178
P. euphrasiae
EV 301
Euphrasia rostkoviana
EF553467
P. geranii
PA5
Geranium maculatum
DQ148397
P. geranii-sylvatici
HV411
Geranium sylvaticum
DQ148398
P. halstedii
RDM TC14
Rudbeckia fulgida
KP164999
P. laserpitii
HV2051
Laserpitium latifolium
KC495034
P. mei-foeniculi
AR284
Meum athamanticum
AY250160
P. pastinacae
HV1090
Pastinaca sativa
AY250157
P. peucedani
AR277
Peucedanum palustre
AY250154
P. praetermissa
HV2061
Geranium sylvaticum
DQ148396
P. skvortzovii
AR306
Abutilon theophrasti
AY250179
P. solidaginis
P. sphagneticolae
R409
BRIP
Solidago virgaurea
Sphagneticola trilobata
AY250144
KM085176
P. viticola
AR 160
Vitis vinifera
AY035524
P. wildemaniana
AR324
Hypoestes sp.
AY250180
P. wilsonii
HV2065
Geranium nepalense
DQ148408
Phytophthora arecae
AR 243
Unknown
AY035530
Rosellinia was introduced to accommodate species
which are characterized by uniascomatal and carbonaceous
stromata that develop within a subiculum. There have been
different contradiction placements of Rosellinia. Miller
(1928) placed it in the family Xylariaceae and this was
confirmed in morphology and phylogeny-based studies
later (Hsieh et al. 2010; Daranagama et al. 2015). Daranagama et al. (2018) and Wendt et al. (2018) revealed that
Rosellinia is closely related to Entoleuca and Nemania.
Classification—Sordariomycetes, Xylariomycetidae, Xylariales, Xylariaceae
Type species—Rosellinia aquila (Fr.) Ces. & De Not., G.
bot. ital.1 (1): 334(1844)
Distribution—Worldwide
Disease symptoms—Root rots
Black root rot is characterized by the occurrence in
patches that extend in a circular pattern. Rosellinia bunodes
the main causal agent of black root rot typically shows
black branching strands that are firmly attached to the roots
and may form condensed irregular knots and chlorotic
leaves may shed gradually (Sivanesan and Holiday 1972;
Oliverira et al. 2008).
The symptoms of white root rot caused by R. necatrix in
the upper parts of the plants (such as yellow foliage,
shrivelled fruits, no new growth) cannot be recognized in
early stages of root infection. Cottony, white mycelia cover
feeder roots of a tree and decay sets in. Mycelia grow into
the soil and upward in the tree forming small, pale patches
under or in the bark of major roots, root crown and lower
trunk which eventually decay. A purple canker in wood at
the root crown of young trees can also be caused by the
fungus. Diseased trees will defoliate and premature death
may occur (Pérez-Jiménez 2006; Pasini et al. 2016).
Hosts—This genus has a wide range of hosts including
Adoxaceae, Annonaceae, Apiaceae, Asteraceae, Betulaceae, Celastraceae, Convolvulaceae, Euphorbiaceae,
Fabaceae, Fagaceae, Grossulariaceae, Juglandaceae,
Lauraceae, Moraceae, Myrtaceae, Oleaceae, Pinaceae,
Poaceae, Rosaceae, Rutaceae, Salicaceae, Sapindaceae,
Scrophulariaceae, Tamaricaceae, Verbenaceae, Vitaceae
and Zingiberaceae.
Morphological based identification and diversity
The genus is characterized by globose-subglobose, uni- to
multiloculate, often collapsed ascomata, mostly detached
from the stroma wall,; septate, hyaline paraphyses, asci that
are 8-spored, unitunicate, cylindrical to clavate, long
pedicellate, rounded at the apex, with J ? apical ring
bluing in Melzer’s reagent, massive barrel-shaped with
distinctive rings ascospores that are uniseriate, unicellular,
elongated ellipsoidal-fusiform, light to dark brown, with
germ slits, cellular appendages and/or may be slimy
sheaths or caps and a dematophora-like or geniculosporium-like asexual morphs (Daranagama et al. 2018).
Rosellinia is a large genus with 483 epithets in Mycobank, 517 in Index Fungorum and 311 in Global Biodiversity Information Facility (GBIF); there are currently 158
accepted species (Petrini 2013; Li and Guo 2015; Li et al.
123
Fungal Diversity
Fig. 22 Phylogram generated from maximum likelihood analysis
based on combined ITS, TUB2 and tef1 sequence data of Pseudopestalotiopsis species. Related sequences were obtained from
GenBank. Twenty-five strains are included in the combined sequence
analyses, which comprise 1404 characters with gaps. Neopestalotiopsis natalensis (CBS 138.41) was used as the outgroup taxa. The best
scoring RAxML tree with a final likelihood value of - 4028.799660
is presented. The matrix had 274 distinct alignment patterns, with
6.34% of undetermined characters or gaps. Estimated base frequencies were as follows; A = 0.235765, C = 0.270775, G = 0.213073,
T = 0.280387; substitution rates AC = 1.242401, AG = 3.217138,
AT = 1.272343, CG = 0.837226, CT = 4.463116, GT = 1.000000;
gamma distribution shape parameter a = 0.229606. The maximum
parsimonious dataset consisted of 1122 constant, 79 parsimonyinformative and 203 parsimony-uninformative characters. The parsimony analysis of the data matrix resulted in the maximum of four
equally most parsimonious trees with a length of 386 steps
(CI = 0.832, RI = 0.737, RC = 0.613, HI = 0.168) in the first tree.
RAxML and maximum parsimony bootstrap support value C 50%
are shown respectively near the nodes. Bayesian posterior probabilities C 0.95 (BYPP) indicated as thickened black branches. Ex-type
strains are in bold
2015, 2016; Su et al. 2016; Crous et al. 2017; Fournier
et al. 2017a, b; Tibpromma et al. 2017). Petrini (2013)
found seven morphologically distinct groups with distinguishing morphological characters associated with the
shape, size and orientations of stroma, ostiole, ascospores
and germ slit, which can be used for species delimitation
(Fig. 23).
Molecular based identification and diversity
123
Protein coding gene sequences are available for nine species of Rosellinia, mostly with only ITS and LSU sequence
data. However, with the limited data, Daranagama et al.
(2018) provided an updated backbone tree for genera in
Xylariaceae, and Rossellinia clustered with Nemania and
Entoleuca. Several phylogenetic studies have focused on
Fungal Diversity
Table 14 Details of the
Pseudopestalotiopsis isolates
used in the phylogenetic
analyses
Species
Isolates
ITS
TUB2
tef1
Pseudopestalotiopsis ampullacea
LC6618*
KX895025
KX895358
KX895244
P. avucenniae
MFLUCC 17-0434*
MK764287
MK764353
MK764331
P. camelliae-sinensis
LC3490*
KX894985
KX895316
KX895202
P. chinensis
LC3011*
KX894937
KX895269
KX895154
P. cocos
CBS 272.29*
KM199378
KM199467
KM199553
P. dawaina
MM14-F0015*
LC324750
LC324751
LC324752
P. curvatispora
MFLUCC 17-1722*
MK764288
MK764354
MK764332
P. ignota
NN 42909*
KU500020
–
KU500016
P. indica
CBS 459.78*
KM199381
KM199470
KM199560
P. ixorae
NTUCC 17-001.1*
MG816316
MG816326
MG816336.
P. jiangxiensis
LC 4479*
KX895034
KX895343
KX895229
P. kawthaungina
MM14-F0083
LC324753
LC324754
LC324755
P. kubahensis
UMAS KUB-P20*
KT006749
–
–
P. myanmarina
NBRC 112264*
LC114025
LC114045
LC114065
P. rhizophorae
P. smitheae
MFLUCC 17-1560*
MFLUCC 12-0121*
MK764291
KJ503812
MK764357
KJ503815
MK764335
KJ503818
P. thailandica
MFLUCC 17-1724*
MK764292
MK764358
MK764336
P. taiwanensis
NTUCC 17-002.1*
MG816319
MG816329
MG816339
P. theae
MFLUCC 12-0055*
JQ683727
JQ683711
JQ683743
P. vietnamensis
NBRC 112252*
LC114034
LC114054
LC114074
Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold
pathogenic species such as R. bunodes and R. pepo. Castro
et al. (2013) investigated R. bunodes and R. pepo isolated
from Coffea arabica (Rubiaceae), Hevea brasiliensis
(Euphorbiaceae), Macadamia integrifolia (Proteaceae),
Psidium guajava (Myrtaceae) and Theobroma cacao
(Malvaceae) using ITS based phylogenetic analyses from
Colombia. Another ITS-based phylogenetic study identified R. necatrix, the pathogen responsible for white root
disease on Aronia melanocarpa (Rosaceae) in Korea (Choi
et al. 2017).
This study reconstructs the phylogeny of Rosellinia
based on analyses of combined ITS, LSU and RPB2
sequence data (Table 7, Fig. 13). The phylogenetic tree is
updated with recently introduced Rosellinia species and
corresponds to previous studies (Li et al. 2015, 2016; Su
et al. 2016; Crous et al. 2017; Fournier et al. 2017a, b;
Tibpromma et al. 2017).
Recommended genetic markers (genus level)—LSU, ITS
Recommended genetic marker (species level)—ITS
Based on several studies and the availability of sequence
data, ITS based phylogenetic studies are sufficient to identify
Rosellinia to species level. There are few other studies carried out using LSU, ITS and RPB2 sequences. With a lack of
sequence data for most species, there are some contradictions
for the species and generic delimitat ion.
Accepted number of species: 158 with only 26 species with
molecular data
References: Petrini 2013; Li and Guo 2015; (morphology),
Castro et al. 2013; Li et al. 2015, 2016; Crous et al. 2017;
Fournier et al. 2017a, b; Tibpromma et al. 2017, Daranagama et al. 2018 (morphology, phylogeny), Shimizu
et al. 2012; dos Santos et al. 2017; Arjona-Girona and
López-Herrera 2018; Kleina et al. 2018 (pathogenicity).
Sphaeropsis Sacc., Michelia 2: 105. 1880.
The genus Sphaeropsis was introduced by Saccardo
(1880) (for species of Diplodia with brown, aseptate conidia),
with S. visci as the type species. Sphaeropsis is the asexual
morph of Phaeobotryosphaeria (Phillips et al. 2008, 2013;
Wijayawardene et al. 2017). Species in Sphaeropsis seem to
be cosmopolitan in distribution since they have been recorded
from both temperate and tropical countries (i.e. Germany,
New Zealand, South Africa, Thailand (Phillips et al. 2013;
Slippers et al. 2014; Farr and Rossman 2019). Host specificity
of Sphaeropsis has not yet been clarified and species have
been recorded from various plant families.
Classification—Dothideomycetes,
incertae
sedis,
Botryosphaeriales, Botryosphaeriaceae
Type species—Sphaeropsis visci (Alb. & Schwein.) Sacc.
Distribution—Worldwide
Disease symptoms—calyx-end rot, stem end rot
The decayed tissues in rot diseases are firm or spongy
and brown in colour. The skin of decayed areas generally
remains brown or dark brown but may appear dark in aged
areas (Kim et al. 2005).
123
Fungal Diversity
Fig. 23 Rosellinia bunodes (holotype, K(M) 62957, Sri Lanka,
Peradeniya, on dead wood, November 1867, G.H.K. Thwaites) a,
e Stromata (e ostiole white arrow). b–d Herbarium details.
f Paraphyses. g–j Ascospores (g germ slit black arrow). Scale bars:
e = 500 lm, g–j = 20 lm, f = 5 lm
Hosts—Broad range of hosts, including Myrtaceae, Rutaceae, Santalaceae and Vitaceae.
have been identified from culture. Sphaeropsis porosa
differs from other species in having distinct pitted conidial
walls. Sphaeropsis visci and S. citrigena can be distinguished from each other with their conidial pigmentation
and swollen paraphyses tips (Phillips et al. 2013).
Morphological based identification and diversity
Over 600 species names are listed in Index Fungorum
(2019), but few of them are currently in use and for most
species cultures are not available except for S. citrigena
(A.J.L. Phillips et al.) A.J.L. Phillips & A. Alves, S.
eucalypti Berk. & Broome, S. porosa (Van Niekerk &
Crous) A.J.L. Phillips & A. Alves, and S. visci (Alb. &
Schwein.) Sacc. Pycnidial paraphyses in Sphaeropsis species distinguish this genus from Diplodia species, which do
not have paraphyses. The aseptate, smooth-walled conidia
of Sphaeropsis species differentiate them from Lasiodiplodia species, which have 1-septate, striate conidia.
Recently, S. variabilis was transferred to a separate genus,
Oblongocollomyces due to distinct morphological differences (Yang et al. 2017).
Colony and conidial morphology are the primary characters to identify species within this genus (Ellis
1971, 1976; Simmons 1992). The sexual and asexual
morphs connection of Sphaeropsis was established by
Phillips et al. (2008) who obtained coelomycetes with
large, brown, aseptate conidia typical of Sphaeropsis from
Phaeobotryosphaeria culture. Four Sphaeropsis species
123
Molecular based identification and diversity
Phillips et al. (2013) suggested that phylogenetic analysis
of combined SSU, LSU, ITS, tef1 and TUB2 genes provide
better resolution compared to ITS alone. This study provides the phylogenetic analyses of combined ITS, LSU,
SSU, tef1 and TUB2 sequence data (Table 10, Fig. 16).
The topology of the Sphaeropsis species tree is identical to
the phylogeny tree of Phillips et al. (2013).
Recommended genetic markers (genus level)—LSU and
SSU
Recommended genetic markers (species level)—ITS, tef1
and TUB2
Accepted number of species: There are 624 species epithets
in Index Fungorum (2019) under this genus. However, only
four species have sequence data.
References: Phillips et al. 2013; Yang et al. 2017 (morphology, phylogeny).
Fungal Diversity
Updates on important phytopathogens
Alternaria Nees, Syst. Pilze (Würzburg): 72 (1816)
Species of Alternaria are saprotrophs on dead vegetation
and are frequently isolated from soil, air, dust and waterdamaged buildings (Ellis 1971, 1976; De Hoog and Horré
2002; Runa et al. 2009; Woudenberg et al. 2013; Lawrence
et al. 2016). The majority of species, however, are pathogens, infecting a vast array of host species (Jayawardena
et al. 2019). A detailed background, diseases and the
symptoms, morphological characters is discussed in
Jayawardena et al. (2019). In this paper, we provide an
update for the sections in Alternaria based on six gene
combination analyses (Al Ghafri et al. 2019; Table 15,
Fig. 24).
Diplodia Fr., in Montagne, Annls Sci. Nat., Bot., sér. 2 1:
302 (1834)
The genus Diplodia was introduced by Montagne (1834)
and comprises species with hyaline or dark brown, aseptate
or 1-septate, thick-walled conidia (Phillips et al. 2005).
Diplodia is defined by having unilocular, solitary or
aggregated conidiomata lined with conidiogenous cells that
form conidia at their tips (Phillips et al. 2005). The type
species of Diplodia is Diplodia mutila (Montagne 1834;
Fries 1849), but there are no living cultures linked to the
holotype of this species. As this has severely hampered
studies on taxonomy and phylogeny of Diplodia, Alves
et al. (2004) provided a detailed description of D. mutila
based on an isolate from grapevines in Portugal (CBS
112553). Alves et al. (2014) designated an epitype for
Diplodia mutila, with associated ex-epitype cultures. This
epitype confirmed in all ways with the isotype of D. mutila
and with the asexual morph on BPI 599153 as described by
Alves et al. (2004). Diplodia mutila has hyaline conidia
that become brown and one-septate after discharge from
the pycnidia. Species of Diplodia can be differentiated on
slight differences in conidial dimensions (Alves et al.
2014).
Classification—Dothideomycetes,
incertae
sedis,
Botryosphaeriales, Botryosphaeriaceae
Type species—Diplodia mutila (Fr. : Fr.) Fr., Summa Veg.
Scand. 2:417 (1849)
Distribution—Worldwide
Disease symptoms—Diebacks, cankers, fruit rots.
Hosts—Plurivorous on woody hosts.
Morphological based identification and diversity
Diplodia is a large genus and a search in MycoBank (2019)
revealed 1398 names while Index Fungorum (2019) has
1268 names. Cryptic speciation is common in the genus,
which makes species identification difficult if based only
on morphological characters (Phillips et al. 2012, 2013).
Dissanayake et al. (2016) included 26 Diplodia species in
their phylogeny. Recently, a novel species Diplodia eriobotryicola on Eriobotrya japonica from Spain was
introduced by González-Domı́nguez et al. (2016). Yang
et al. (2017) introduced D. pyri on Pyrus sp., the Netherlands, D. citricarpa on Citrus sp., Iran, and D. gallae on
galls of Quercus sp. However, the ITS and tef1 of the novel
species, D. citricarpa are not available in GenBank and
hence we could not include this species in our phylogeny.
The genus now comprises 30 species known from culture.
Molecular based identification and diversity
Earlier taxonomic studies on Diplodia using molecular data
employed ITS rDNA, but this single marker can underestimate species diversity among closely related or cryptic
species. Multiple gene sequence concordance phylogenies
have therefore been applied to identify cryptic or previously overlooked species of Diplodia (Slippers et al.
2004a, b, c; Burgess et al. 2006; Phillips et al.
2005, 2012, 2013; Hyde et al. 2014; Dissanayake et al.
2016). As the tef1 gene is considerably more variable than
the ITS rDNA region in these taxa, data from tef1 have
been combined with ITS sequence data. Unfortunately, no
single gene region is sufficient to distinguish all species in
this genus. The present phylogenetic analysis was performed based on up to date ex-holotype or ex-epitype
sequence data available in GenBank (Fig. 25, Table 16).
Recommended genetic markers (genus level)—SSU and
LSU
Recommended genetic markers (species level)—ITS, tef1,
TUB2
Accepted number of species: 30 species
References: Phillips et al. 2013 (morphology, phylogeny,
distribution, hosts); Dissanayake et al. 2016 (phylogeny).
Dothiorella Sacc., Michelia 2(6): 5 (1880)
Dothiorella was proposed by Saccardo to accommodate D.
pyrenophora (Hyde et al. 2014). Members of this genus are
pathogens, endophytes and saprobes (Phillips et al. 2013;
Dissanayake et al. 2016). Taxonomy of this genus has been
in a state of flux for decades (Phillips et al. 2013).
Sivanesan (1984) treated D. pyrenophora as a synonym of
Dothichiza sorbi (asexual morph of Dothiora pyrenophora). However, Sivanesan (1984) was referring to
Dothiorella pyrenophora Sacc. (1884) which, according to
Sutton (1977), is a later homonym of Dothiorella pyrenophora Sacc. (1880). Crous and Palm (1999) studied the
holotype of D. pyrenophora and considered it a synonym
of Diplodia. However, Phillips et al. (2005) based on both
morphological and molecular data revived the genus
Dothiorella for species in which the conidia become brown
and 1-septate while attached to the conidiogenous cells.
123
Fungal Diversity
Table 15 Details of the Alternaria isolates used in the phylogenetic analyses
Species name
Strain number
GenBank accession numbers
SSU
LSU
RPB2
ITS
GPDH
tef1
KC584707
Alternaria abundans
CBS 534.83
KC584581
KC584323
KC584448
JN383485
KC584154
A. alternantherae
CBS 124392
KC584506
KC584251
KC584374
KC584179
KC584096
KC584633
A. alternariae
CBS 126989
KC584604
KC584346
KC584470
AF229485
AY278815
KC584730
A. alternate
CBS 916.96
KC584507
DQ678082
KC584375
AF347031
AY278808
KC584634
A. arborescens
CBS 102605
KC584509
KC584253
KC584377
AF347033
AY278810
KC584636
A. argyranthemi
CBS 116530
KC584510
KC584254
KC584378
KC584181
KC584098
KC584637
A. arrhenatheri
A. aspera
BMP 0514
CBS 115269
–
KC584607
–
KC584349
–
KC584474
JQ693680
KC584242
JQ693629
KC584166
–
KC584734
A. atra
CBS 195.67
KC584608
KC584350
KC584475
AF229486
KC584167
KC584735
A. axiaeriisporifera
CBS 118715
KC584513
KC584257
KC584381
KC584184
KC584101
KC584640
A. bornmueller
DAOM 231361
KC584624
KC584366
KC584491
FJ357317
FJ357305
KC584751
A. botryospora
CBS 478.90
KC584594
KC584336
KC584461
AY278844
AY278831
KC584720
A. botrytis
CBS 197.67
KC584609
KC584351
KC584476
KC584243
KC584168
KC584736
A. brassicae
CBS 116528
KC584514
KC584258
KC584382
KC584185
KC584102
KC584641
A. brassicae-pekinensis
CBS 121493
KC584611
KC584353
KC584478
KC584244
KC584170
KC584738
A. brassicicola
CBS 118699
KC584515
KC584259
KC584383
JX499031
KC584103
KC584642
A. breviramosa
CBS 121331
KC584574
KC584318
KC584442
FJ839608
KC584148
KC584700
A. calycipyricola
CBS 121545
KC584516
KC584260
KC584384
KC584186
KC584104
KC584643
A. capsici-annui
CBS 504.74
C584517
KC584261
KC584385
KC584187
KC584105
KC584644
A. caricis
CBS 480.90
KC584600
KC584342
KC584467
Y278839
AY278826
C584726
A. carotiincultae
CBS 109381
KC584518
KC584262
KC584386
KC584188
KC584106
KC584645
A. cetera
A. chartarum
CBS 121340
CBS 200.67
KC584573
KC584614
KC584317
KC584356
KC584441
KC584481
JN383482
AF229488
AY562398
KC584172
KC584699
KC584741
A. cheiranthi
CBS 109384
C584519
C584263
C584387
F229457
C584107
C584646
A. chlamydospora
CBS 491.72
KC584520
KC584264
KC584388
KC584189
KC584108
KC584647
A. chlamydosporigena
CBS 341.71
KC584584
KC584326
KC584451
KC584231
KC584156
KC584710
A. cinerariae
CBS 116495
KC584521
KC584265
KC584389
KC584190
KC584109
KC584648
A. concatenate
CBS 120006
KC584613
KC584355
KC584480
KC584246
AY762950
KC584740
A. conjuncta
CBS 196.86
KC584522
KC584266
KC584390
J266475
Y562401
KC584649
A. conoidea
CBS 132.89
KC584585
KC584327
KC584452
AF348226
FJ348227
KC584711
A. consortialis
CBS 104.31
KC584615
KC584357
KC584482
KC584247
KC584173
KC584742
A. cucurbitae
CBS 483.81
KC584616
KC584358
KC584483
FJ266483
AY562418
KC584743
A. cumini
CBS 121329
KC584523
KC584267
KC584391
KC584191
KC584110
KC584650
A. daucifolii
CBS 118812
KC584525
KC584269
KC584393
KC584193
KC584112
KC584652
A. dennisii
CBS 110533
KC584586
KC584328
KC584453
KC584232
KC584157
KC584712
A. dennisii
CBS 476.90
KC584587
KC584329
KC584454
JN383488
JN383469
KC584713
A. dianthicola
CBS 116491
KC584526
KC584270
KC584394
KC584194
KC584113
KC584653
A. didymospora
A. elegans
CBS 766.79
CBS 109159
KC584588
KC584527
KC584330
KC584271
KC584455
KC584395
FJ357312
KC584195
FJ357300
KC584114
KC584714
KC584654
A. embellisia
CBS 339.71
KC584582
KC584324
KC584449
KC584230
KC584155
KC584708
A. eryngii
CBS 121339
KC584529
KC584273
KC584397
Q693661
Y562416
KC584656
A. eureka
CBS 193.86
KC584589
KC584331
KC584456
JN383490
JN383471
KC584715
A. geniostomatis
CBS 118701
KC584532
KC584276
KC584400
KC584198
KC584117
KC584659
A. gypsophilae
CBS 107.41
KC584533
KC584277
KC584401
KC584199
KC584118
KC584660
A. helianthiinficiens
CBS 117370
KC584534
KC584278
KC584402
KC584200
KC584119
KC584661
A. helianthiinficiens
CBS 208.86
KC584535
KC584279
KC584403
JX101649
KC584120
EU130548
A. heterospora
CBS 123376
KC584621
KC584363
KC584488
KC584248
KC584176
KC584748
123
Fungal Diversity
Table 15 (continued)
Species name
Strain number
GenBank accession numbers
SSU
LSU
RPB2
ITS
GPDH
tef1
A. hyacinthi
CBS 416.71
KC584590
KC584332
KC584457
KC584233
KC584158
KC584716
A. indefessa
CBS 536.83
KC584591
KC584333
KC584458
KC584234
KC584159
KC584717
A. infectoria
CBS 210.86
KC584536
KC584280
KC584404
DQ323697
AY278793
KC584662
A. japonica
A. kulundii
CBS 118390
M313
KC584537
KJ443087
KC584281
KJ443132
KC584405
KJ443176
KC584201
KJ443262
KC584121
KJ649618
KC584663
-
A. leucanthemi
CBS 421.65
KC584605
KC584347
KC584472
KC584240
KC584164
KC584732
A. leucanthemi
CBS 422.65
KC584606
KC584348
KC584473
KC584241
KC584165
KC584733
A. limaciformis
CBS 481.81
KC584539
KC584283
KC584407
KC584203
KC584123
KC584665
A. macrospora
CBS 117228
KC584542
KC584286
KC584410
KC584204
KC584124
KC584668
A. nepalensis
CBS 118700
KC584546
KC584290
KC584414
KC584207
KC584126
KC584672
A. nobilis
CBS 116490
KC584547
KC584291
KC584415
KC584208
KC584127
KC584673
A. obclavata
CBS 124120
KC584575
FJ839651
KC584443
KC584225
KC584149
KC584701
A. oudemansii
CBS 114.07
KC584619
KC584361
KC584486
FJ266488
KC584175
KC584746
A. omaniana
SQUCC 13580
MK878559
MK878556
MK880893
MK878562
MK880899
MK880896
A. omaniana
SQUCC 15560
MK878560
MK878557
MK880894
MK878563
MK880900
MK880897
A. omaniana
SQUCC 15561
MK878561
MK878558
MK880895
MK878564
MK880901
MK880898
A. panax
CBS 482.81
KC584549
KC584293
KC584417
KC584209
KC584128
KC584675
A. papavericola
CBS 116606
KC584579
KC584321
KC584446
FJ357310
FJ357298
KC584705
A. penicillata
A. penicillata
CBS 116608
116607
KC584572
KC584580
KC584316
KC584322
KC584440
KC584447
FJ357311
KC584229
FJ357299
KC584153
KC584698
KC584706
A. perpunctulata
CBS 115267
KC584550
KC584294
KC584418
KC584210
KC584129
KC584676
A. petroselini
CBS 112.41
KC584551
KC584295
KC584419
KC584211
KC584130
KC584677
A. petuchovskii
M304
KJ443079
KJ443124
KJ443170
KJ443254
KJ649616
–
A. photistica
CBS 212.86
KC584552
KC584296
KC584420
KC584212
KC584131
KC584678
A. phragmospora
CBS 274.70
KC584595
KC584337
KC584462
JN383493
JN383474
KC584721
A. porri
CBS 116698
KC584553
KC584297
KC584421
DQ323700
KC584132
KC584679
A. proteae
CBS 475.90
KC584597
KC584339
KC584464
AY278842
KC584161
KC584723
A. pseudorostrata
CBS 119411
KC584554
KC584298
KC584422
JN383483
AY562406
KC584680
A. radicina
CBS 245.67
KC584555
KC584299
KC584423
KC584213
KC584133
KC584681
A. scirpicola
CBS 481.90
KC584602
KC584344
KC584469
KC584237
KC584163
KC584728
A. septorioides
CBS 106.41
KC584559
KC584303
KC584427
KC584216
KC584136
KC584685
A. septospora
CBS 109.38
KC584620
KC584362
KC584487
FJ266489
FJ266500
KC584747
A. shukurtuzii
M307
KJ443082
KJ443127
KJ443172
KJ443257
KJ649620
-
A. simsimi
CBS 115265
KC584560
KC584304
KC584428
JF780937
KC584137
KC584686
A. slovaca
A. smyrnii
CBS 567.66
CBS 109380
KC584576
KC584561
KC584319
KC584305
KC584444
KC584429
KC584226
AF229456
KC584150
KC584138
KC584702
KC584687
A. solani
CBS 116651
KC584562
KC584306
KC584430
KC584217
KC584139
KC584688
A. soliaridae
CBS 118387
KC584563
KC584307
KC584431
KC584218
KC584140
KC584689
A. solidaccana
CBS 118698
KC584564
KC584308
KC584432
KC584219
KC584141
KC584690
A. sonchi
CBS 119675
KC584565
KC584309
KC584433
KC584220
KC584142
KC584691
Alternaria sp.
CBS 175.52
KC584577
KC584320
KC584445
KC584227
KC584151
KC584703
A. tagetica
CBS 479.81
KC584566
KC584310
KC584434
KC584221
KC584143
KC584692
A. tellustris
CBS 538.83
KC584598
KC584340
KC584465
FJ357316
AY562419
KC584724
A. thalictrigena
CBS 121712
KC584568
KC584312
KC584436
EU040211
KC584144
KC584694
A. triglochinicola
CBS 119676
KC584569
KC584313
KC584437
KC584222
KC584145
KC584695
A. vaccariae
CBS 116533
KC584570
KC584314
KC584438
KC584223
KC584146
KC584696
A. vaccariicola
CBS 118714
KC584571
KC584315
KC584439
KC584224
KC584147
KC584697
123
Fungal Diversity
123
Fungal Diversity
b Fig. 24 Phylogenetic tree generated by maximum parsimony analysis
of combined SSU, LSU, ITS, GPDH, tef1 and RPB2 sequence data of
Alternaria species. One hundred strains are included in the analyses,
which comprised 4056 characters including gaps. The tree was rooted
with Stemyphylium herbarium (CBS 191.86) and Pleospora tarda
(CBS 714.68). The maximum parsimonious dataset consisted of 3091
constant, 852 parsimony-informative and 113 parsimony-uninformative characters. The parsimony analysis of the data matrix resulted in
the maximum of ten equally most parsimonious trees with a length of
4520 steps (CI = 0.335, RI 0.708, RC = 0.237, HI = 0.665) in the
first tree. MP and ML bootstrap values C 50% and Bayesian posterior
probabilities C 0.90 are shown respectively near the nodes. Ex-type
strains are in bold
Classification—Dothideomycetes,
incertae
sedis,
Botryosphaeriales, Botryosphaeriaceae
Type species—Dothiorella pyrenophora Berk. ex Sacc.,
Michelia 2 (6): 5 (1880) (1909)
Distribution—Worldwide
Disease symptoms—Diebacks, cankers, fruit rots.
Hosts—Plurivorous on woody hosts.
Morphological based identification and diversity
Species of this genus were mostly described based on host
association, which has led to the introduction of many
species names and currently there are 393 epithets in Index
Fungorum (2019). Slippers et al. (2013) suggested that host
association cannot be considered as an important factor in
species delimitation, many names are likely to be synonyms. Phillips et al. (2008) introduced a new genus
Spencermartinsia to accommodate dothiorella-like species
with apiculate ascospores. However, Yang et al. (2017)
based on six-gene phylogeny and a broad taxon sampling
considered that Spencermartinsia should be treated as a
synonym of Dothiorella. Phillips et al. (2013) listed all
cultures available for this genus and provided a phylogenetic tree and a key to the species. In that study 13 species
names and 16 unnamed lineages were listed. Hyde et al.
(2014), Dissanayake et al. (2016) and Yang et al. (2017)
provided updates for the genus. Hyde et al. (2014) accepted
19 species and Dissanayake et al. (2016) accepted 30
species in the genus. After making Spencermartinsia a
synonym of Dothiorella Yang et al. (2017) accepted 36
species in this genus.
Phillips et al. (2013) differentiated 13 Dothiorella species on the basis of conidiomata and conidial dimensions.
However, the dimensions of these characters overlap
between species. Therefore, using morphology alone
without molecular data is not suitable to define species.
Molecular based identification and diversity
Recent studies have re-evaluated this genus based on multigene phylogeny of ITS, TUB2 and tef1 sequence data. We
reconstruct the phylogeny of Dothiorella based on analyses
of a combined ITS and tef1 sequence data (Table 17,
Fig. 26). The phylogenetic tree is updated with recently
introduced Dothiorella species and corresponds to previous
studies (Dissanayake et al. 2016; Yang et al. 2017; Hyde
et al. 2018; Phookamsak et al. 2019). In the analyses, it
appears that several species are synonyms, such as D.
parva/D. guttulata and D. rhamni/D. eriobotryae and
possibly others. Therefore, a thorough revision of the genus
is recommended to clarify the status of these dubious
species.
Recommended genetic markers (genus level)—SSU and
LSU
Recommended genetic markers (species level)—ITS and
tef1
Accepted number of species: Currently, 393 species names
are listed for Dothiorella in Index Fungorum (2019). Cultures and DNA sequences are available for 46 species,
therefore 46 species are currently accepted in
Dothiorella.
References: Phillips et al. 2013; Dissanayake et al. 2016
(morphology, phylogeny, distribution, hosts), Yang et al.
2017 (morphology and phylogeny)
Fusarium Link, Mag. Gesell. naturf. Freunde, Berlin 3(12): 10 (1809)
Fusarium is a genus with 20 monophyletic species
complexes (Rana et al. 2017).
Species formely belonged to F. solani species complex
were transferred to genus Neocosmospora based on sexual
morph characters and molecular phylogeny (Lombard et al.
2015; Sandoval-Denis and Crous (2018). Fusarium species
are saprobes, parasites, endophytes, soil-borne or isolated
from water (Rana et al. 2017). Species of Fusarium are
economically important fungi as they are responsible for
blights, cankers, rots, and wilts of horticultural, ornamental
and forest crops in both agricultural and natural ecosystems, worldwide, and also human infections (Rana et al.
2017; Varela et al. 2013; Peraldi et al. 2014; Al-Hatmi
et al. 2019; Maryani et al. 2019a, b). In nature, sexual
morphs of Fusarium occur less commonly than the asexual
morphs (Gräfenhan et al. 2011; Rossman et al. 1999).
Classification—Sordariomycetes,
Hypocreomycetidae,
Hypocreales, Nectriaceae
Type species—Fusarium sambucinum Fuckel, Hedwigia
2: 135.1863.
Distribution—Worldwide
Disease symptoms—blights, cankers, rots, and wilts
Plant pathogenic species of this genus have the capability to change their lifestyle to saprotrophic and can
survive for long periods as chlamydospores in host tissues.
Fusarium species damage their hosts by systemically colonizing and occluding the host xylem (Ploetz et al. 2003).
Hosts—Known from many host plant families.
123
Fungal Diversity
Fig. 25 Phylogenetic tree generated by maximum likelihood analysis
of combined ITS and tef1 sequence data of Diplodia species. Related
sequences were obtained from GenBank. Forty nine strains are
included in the analyses, which comprise 866 characters including
gaps. The tree was rooted with Lasiodiplodia theobromae (CBS
164.96). Tree topology of the ML analysis was similar to the BYPP.
The best scoring RAxML tree with a final likelihood value of
- 3342.903931 is presented. The matrix had 278 distinct alignment
patterns, with 9.02%. % of undetermined characters or gaps.
Estimated base frequencies were as follows; A = 0.207781,
C = 0.297582, G = 0.261770, T = 0.232868; substitution rates AC =
0.993193, AG = 3.566477, AT = 0.787748, CG = 1.607220, CT =
4.471399, GT = 1.000000; gamma distribution shape parameter
a = 1.224079. RAxML bootstrap support values C 80% (BT) are
shown respectively near the nodes. Bayesian posterior probabilities C 0.5 (PP) indicated as thickened black branches. Ex-type strains
are in bold
Morphological based identification and diversity
species concept of Fusarium much broader (Geiser et al.
2004). It leads to the incorrect and confusing application of
species names to toxigenic and pathogenic isolates (Geiser
et al. 2004). Species boundaries have been inferred using
multi-gene phylogenetic methods, reflecting the species
diversity more than morphological treatments (Aoki and
O’Donnell 1999; Geiser et al. 2004; O’Donnell 2000;
Fusarium was also known from the sexual morphic fungus
name Gibberella, which was suppressed in favour of
Fusarium by Rossman et al. (2013). Variation and mutation
in culture and lack of clear morphological characters for
separating species are the main problems which make the
123
Fungal Diversity
Table 16 Details of the
Diplodia isolates used in the
phylogenetic analyses
Species
Isolate/voucher no
ITS
tef1
Diplodia africana
CBS 120835*
EF445343
EF445382
Diplodia africana
CBS 121104
EF445344
EF445383
Diplodia agrifolia
CBS 132777*
JN693507
JQ517317
Diplodia agrifolia
UCROK1429
JQ411412
JQ512121
Diplodia alatafructa
CBS 124931*
FJ888460
FJ888444
Diplodia alatafructa
CBS 124933
FJ888478
FJ888446
Diplodia allocellula
CBS 130408*
JQ239397
JQ239384
Diplodia allocellula
CBS 130410
JQ239399
JQ239386
Diplodia arengae
MFLU 17-2769
MG762771
MG762774
Diplodia bulgarica
CBS 124254*
GQ923853
GQ923821
Diplodia bulgarica
CBS 124135
GQ923852
GQ923820
Diplodia corticola
CBS 112549*
AY259100
AY573227
Diplodia corticola
CBS 112546
AY259110
DQ458872
Diplodia crataegicola
MFLU 15-1311*
KT290244
KT290248
Diplodia cupressi
Diplodia cupressi
CBS 168.87*
CBS 261.85
DQ458893
DQ458894
DQ458878
DQ458879
Diplodia estuarina
CMW41231*
KP860831
KP860676
Diplodia estuarina
CMW41230
KP860830
KP860675
Diplodia fraxinii
CBS 136010*
KF307700
KF318747
Diplodia galiicola
MFLU 15-1310*
KT290245
KT290249
Diplodia insularis
CBS 140350*
KX833072
KX833073
Diplodia intermedia
CBS 124462*
GQ923858
GQ923826
Diplodia intermedia
CBS 124134
HM036528
GQ923851
Diplodia malorum
CBS 124130*
GQ923865
GQ923833
Diplodia malorum
CBS 112554
AY259095
DQ458870
Diplodia mutila
CBS 112553*
AY259093
AY573219
Diplodia mutila
CBS 230.30
DQ458886
DQ458869
Diplodia neojuniperi
CPC 22753*
KM006431
KM006462
EU392279
Diplodia olivarum
CBS 121887*
EU392302
Diplodia olivarum
CBS 121886
EU392297
EU392274
Diplodia pseudoseriata
Diplodia pseudoseriata
CBS 124906*
CBS 124907
EU080927
EU080922
EU863181
EU863179
Diplodia quercivora
CBS 133852*
JX894205
JX894229
Diplodia rosacearum
CBS 141915*
KT956270
KU378605
Diplodia rosulata
CBS 116470*
EU430265
EU430267
Diplodia rosulata
CBS 116472
EU430266
EU430268
Diplodia sapinea
CBS 393.84*
DQ458895
DQ458880
Diplodia sapinea
CBS 109725
DQ458896
DQ458881
Diplodia scrobiculata
CBS 118110*
AY253292
AY624253
Diplodia scrobiculata
CBS 109944
DQ458899
DQ458884
Diplodia scrobiculata
CBS 113423
DQ458900
DQ458885
Diplodia seriata
CBS 112555*
AY259094
AY573220
Diplodia seriata
CBS 119049
DQ458889
DQ458874
Diplodia subglobosa
CBS 124133*
GQ923856
GQ923824
Diplodia tsugae
CBS 418.64*
DQ458888
DQ458873
Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold
123
Fungal Diversity
Fig. 26 Phylogenetic tree generated by maximum parsimony analysis
of combined ITS and tef1 sequence data of Dothiorella species.
Related sequences were obtained from GenBank. Forty eight strains
are included in the analyses, which comprised 873 characters
including gaps. The tree was rooted with Neofusicoccum parvum
(CMW9081) and N. mangiferae (CMW7024). The maximum parsimonious dataset consisted of 572 constant, 204 parsimony-
informative and 97 parsimony-uninformative characters. The parsimony analysis of the data matrix resulted in the maximum of ten
equally most parsimonious trees with a length of 891 steps
(CI = 0.532, RI 0.738, RC = 0.393, HI = 0.468) in the first tree.
MP and ML bootstrap values C 50% and Bayesian posterior probabilities C 0.90 are shown respectively near the nodes. The scale bar
indicates 10 changes per site. Ex-type strains are in bold
O’Donnell et al. 1998a, b; Ward et al. 2002). A combined
phylogenetic analysis of LSU, ITS, RPB2 and new phylogenetic marker acl1 by Gräfenhan et al. (2011), revealed
that the early concept of Fusarium is not monophyletic.
Fusarium sensu Wollenweber divided into two large
groups, basal ‘Fusarium-like clades’, and the other one
terminal ‘Fusarium clade’ in the Nectriaceae (Gräfenhan
et al. 2011) (Fig. 27).
Molecular based identification and diversity
123
ITS and LSU are least informative in species-level identification of Fusarium (O’Donnell et al. 1998a; Hyde et al.
2014). Moreover, non-orthologous copies of the ITS2,
which can lead to wrong phylogenetic inferences, can be
detected in many species of Fusarium (Geiser et al. 2004;
O’Donnell et al. 1998a, b). Generally, for the species-level
identification of fungi intron-rich regions of protein-coding
Fungal Diversity
Table 17 Details of the
Dothiorella isolates used in the
phylogenetic analyses
Species
Isolate/voucher no
ITS
tef1
Dothiorella acacicola
CBS 141295
KX228269
KX228376
D. acericola
KUMCC 18-0137*
MK359449
MK361182
D. alpina
CGMCC 3.18001*
KX499645
KX499651
D. americana
CBS 128309*
HQ288218
HQ288262
D. brevicollis
CBS 130411*
JQ239403
JQ239390
D. californica
CBS 141587*
KX357188
KX357211
D. capri-amissi
CMW 25403*
EU101323
EU101368
D. casuarinae
CBS 120688*
DQ846773
DQ875331
D. citricola
ICMP16828*
EU673323
EU673290
D. dulcispinae
CBS 130413*
JQ239400
JQ239387
KT240262
D. eriobotryae
CBS 140852*
KT240287
D. guttulata
MFLUCC 17-0242
KY797637
–
D. iberica
CBS 115041*
AY573202
AY573222
D. iranica
IRAN1587C*
KC898231
KC898214
D. italica
D. juglandis
MFLUCC 17-0951
CBS 188.87
MG828897
EU673316
MG829267
EU673283
D. lampangensis
MFLUCC 18-0232
MK347758
MK340869
D. longicollis
CBS 122068*
EU144054
EU144069
D. magnoliae
CFCC 51563
KY111247
KY213686
D. mangifericola
IRAN1584C*
KC898221
KC898204
D. moneti
MUCC505*
EF591920
EF591971
D. neclivorem
DAR80992*
KJ573643
KJ573640
D. oblonga
CMW 25407*
EU101300
EU101345
D. omnivora
CBS 140349*
KP205497
KP205470
D. parva
IRAN1579C*
KC898234
KC898217
D. plurivora
IRAN1557C*
KC898225
KC898208
D. pretoriensis
CBS 130404*
JQ239405
JQ239392
D. prunicola
CBS 124723*
EU673313
EU673280
D. rhamni
MFLUCC 14-0902*
KU246381
–
D. rosulata
CBS 121760*
EU101290
EU101335
D. santali
D. sarmentorum
MUCC 509*
EF591924
EF591975
IMI63581b*
AY573212
AY573235
D. sempervirentis
IRAN1583C*
KC898236
KC898219
D. striata
ICMP16824*
EU673320
EU673287
D. styphnolobii
JZB3150013*
MH880849
MK069594
D. symphoricarposicola
MFULCC 13-0497*
KJ742378
KJ742381
D. tectonae
MFLUCC12-0382*
KM396899
KM409637
D. thailandica
CBS 133991*
JX646796
JX646861
D. thripsita
BRIP 51876*
FJ824738
KJ573639
D. ulmacea
CBS 138855*
KR611881
KR611910
D. uruguayensis
CBS 124908*
EU080923
EU863180
D. vidmadera
DAR78992*
EU768874
EU768881
D. vinea-gemmae
DAR81012*
KJ573644
KJ573641
D. viticola
CBS 117009*
AY905554
AY905559
D. westrale
DAR80529*
HM009376
HM800511
D. yunnana
CGMCC 3.17999*
KX499643
KX499649
Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold
a the tef1 sequence of D. guttulata in GenBank is incorrect, therefore was not included in the analyses
123
Fungal Diversity
genes are used as the markers (Geiser et al. 2004). The
translation elongation factor 1-a (tef1), which lacks nonorthologous copies of the gene, is highly informative at the
species level in Fusarium (Geiser et al. 2004). RPB1 and
RPB2 are also very informative gene regions for species
identification of Fusarium (O’Donnell et al. 2013; Hyde
et al. 2014). Lombard et al. (2018) observed that tef1 and
RPB2 genes provide better resolution of the species in the
F. oxysporum complex than cmdA and tub2 (Fig. 28,
Table 18).
Recommended genetic markers (genus level)—ATP citrate
lyase (acl1), tef1 and ITS
Recommended genetic markers (species level)—calmodulin-encoding gene (cmdA), tub2, tef1, RPB1 and RPB2
Accepted number of species: There are 1552 species epithets in Index Fungorum (2019) under this genus. More
than 175 species have DNA sequence data.
References: Booth 1971, Rossman et al. 1999 (morphology), Rana et al. 2017, Gräfenhan et al. 2011; Laurence
et al. 2014; Lombard et al. 2018, 2019; Maryani et al.
2019a, b; Wang et al. 2019; Nalim et al. 2011 (morphology, phylogeny).
Lasiodiplodia Ellis & Everh., Bot. Gaz. 21:92 (1896)
According to Clendenin (1896), a fungus causing rot of
sweet potatoes imported from Java was identified by Ellis
in 1894 as a new genus and he named the fungus Lasiodiplodia tubericola. However, Ellis (1894) did not
describe the fungus or publish the new genus. Clendenin
(1896) provided a description of the genus and the species,
attributing both to Ellis and Everhardt. Griffin and Maublanc (1909) considered that on account of the pycnidial
paraphyses, Botryodiplodia theobromae, described by
Patouillard and de Lagerheim (1892), was more suitably
accommodated in Lasiodiplodia. Since the epithet theobromae (1892) is older than tubericola (1896), L. theobromae should be regarded as the type species of
Lasiodiplodia. Neither Patouillard and de Lagerheim
(1892) nor Clendenin (1896) referred to any type or other
specimens of the genus or species. Pavlic et al. (2004)
could not locate the types, and they could not find any
specimens from the original hosts or origins. Phillips et al.
(2013) designated CBS H-21411 as neotype with CBS
164.96 as culture ex-neotype.
The sexual morph has been reported for L. theobromae,
but the connection with the asexual morph has not been
confirmed (Phillips et al. 2013). Sexual morphs have also
been reported for L. pseudotheobromae (Tennakoon et al.
2016), L. gonubiensis (Trakunyingcharoen et al. 2015) and
L. lignicola (Phillips et al. 2013) with clear evidence that
connects sexual with asexual morphs.
123
Classification—Dothideomycetes,
incertae
sedis,
Botryosphaeriales, Botryosphaeriaceae
Type species—Lasiodiplodia theobromae (Pat.) Griffon &
Maubl., Bull. Soc. mycol. Fr. 25: 57 (1909)
Distribution—Worldwide, mostly confined to tropical and
sub-tropical regions, but becoming increasingly more
common in warm temperate regions.
Disease symptoms—Diebacks, cankers, fruit rots.
Hosts—Plurivorous on woody hosts
Morphological based identification and diversity
The pigmented, 1-septate conidia with longitudinal striations together with the pycnidial paraphyses distinguish
Lasiodiplodia from all other genera in Botryosphaeriaceae
(Phillips et al. 2013). Striations on the conidia distinguish it
from Diplodia, the conidiomata paraphyses distinguish it
from Neodeightonia, which also has striate conidia.
Although Barriopsis has striate conidia and paraphyses,
Lasiodiplodia is unique in the Botryosphaeriaceae because
striations are visible on immature, hyaline conidia.
Although Phillips et al. (2013) differentiated 18 species in
Lasiodiplodia on the basis of conidial morphology (especially dimensions) and morphology of the paraphyses, in
reality, species in Lasiodiplodia cannot be identified with
any confidence from their morphology and molecular data
are necessary for definitive identifications.
Molecular based identification and diversity
Denman et al. (2000) suggested that Lasiodiplodia could be
a synonym of Diplodia. When Crous et al. (2006) re-organized Botryosphaeria on the basis of LSU phylogeny
they split the genus into 10 genera, but could not resolve
the position of Lasiodiplodia or separate it from Diplodia.
Following a multi-locus approach (SSU, ITS, LSU, tef1
and TUB2) Phillips et al. (2008) showed that Lasiodiplodia
constitutes a clear phylogenetic lineage.
For many years, only the type species of Lasiodiplodia
(L. theobromae) was mentioned in the phytopathological
and mycological literature, and it was regarded as a cosmopolitan, plurivorous pathogen restricted mainly to
tropical and sub-tropical regions (Punithalingam
1976, 1980). Soon after the widespread application of
DNA-based phylogenies, Pavlic et al. (2004) introduced L.
gonubiensis as a new species on the basis of conidial
morphology and ITS sequence data. Soon after, Burgess
et al. (2006) described three new species (L. crassispora, L.
venezuelensis and L. rubropurpurea) from the tropics based
on ITS and tef1 sequence data and morphological characters. Alves et al. (2008) also used ITS and tef1 sequence
data to reveal two cryptic species in the L. theobromae
complex. Over the years more species were introduced and
Phillips et al. (2013) listed 18 species and Dissanayake
et al. (2016) listed 31 species known from culture. Today
Fungal Diversity
Fig. 27 Sexual morph of a Fusarium sp. a Herbarium material.
b Ascomata on the host. c Section of ascomata. d Section of the
ostiolar region. e Peridium in face view. f–h Asci (h in Melzer’s
reagent). i, j Ascospores. k Germinating ascospore. l, m Colony on
MEA. Scale bars: c = 100 lm, d = 50 lm, e–k = 20 lm
the figure stands at 40 (Fig. 29). Apart from L. theobromae,
all species have been introduced almost entirely on the
basis of DNA sequence phylogenies. Although the phylogenies were derived from analysis of multiple loci (mostly
ITS, tef1 and TUB2 and sometimes RPB2) the genealogical
concordance phylogenetic species recognition concept
(Taylor et al. 2000) has not always been strictly applied
and species have been introduced on the basis of minor
differences in only one locus. The result is that some
species are not well separated phylogenetically (Fig. 29,
Table 19), such as L. hyalina and L. thailandica, L.
chinensis, L. sterculiae, L. pseudotheobromae, L. pyriformis and L. crassispora. In a detailed study of five loci of
19 Lasiodiplodia species, Cruywagen et al. (2017) concluded that several accepted species (L. viticola, L. missouriana, L. laeliocattleyae, L. brasiliense) may, in fact, be
hybrids. There has been no such study of the 16 species
introduced after the work of Cruywagen et al. (2017). In
view of the questionable status of several species in Lasiodiplodia, there is an urgent need to re-assess all of the
species currently accepted in this genus.
123
Fungal Diversity
123
Fungal Diversity
b Fig. 28 Phylogram generated from RAxML analysis based on
combined RPB1, RPB2 and tef1 sequences of accepted species of
Fusarium. Related sequences were obtained from GenBank. One
hundred sixty-five taxa are included in the analyses, which comprise
3980 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 in Fusicolla aquaeductuum
(NRRL 20696). Tree topology of the ML analysis was similar to the
BYPP. The best scoring RAxML tree with a final likelihood value of
- 63956.723151 is presented. The matrix had 2254 distinct alignment
patterns, with 25.13% of undetermined characters or gaps. Estimated
base frequencies were as follows; A = 0.257298, C = 0.251723,
G = 0.248896, T = 0.242083; substitution rates AC = 1.366599,
AG = 4.760724, AT = 1.266971, CG = 0.903914, CT = 9.564945,
GT = 1.000000; gamma distribution shape parameter a = 1.089091.
Maximum likelihood bootstrap support values C70% (BT) and
Bayesian posterior probabilities C 0.99 (PP) are given near the nodes
respectively
Recommended genetic markers (genus level)—SSU and
LSU
Recommended genetic markers (species level)—ITS, tef1,
TUB2
Accepted number of species: Currently, 51 species names
are listed for Lasiodiplodia in MycoBank and Index Fungorum (2019). Cultures and DNA sequences are available
for 43 species, three of which have been reduced to synonymy under existing names. Thus, 40 species are currently recognised in Lasiodiplodia.
References: Phillips et al. 2013 (morphology, phylogeny,
distribution, hosts); Dissanayake et al. 2016 (species).
Pestalotiopsis Steyaert, Bull. Jard. bot. État Brux. 19: 300
(1949)
Pestalotiopsis is an appendage-bearing, 5-celled conidia
(asexual coelomycetes) in the family Sporocadaceae
(Maharachchikumbura et al. 2014a, b; Jayawardena et al.
2016). The genus was introduced by Steyaert (1949).
Pestalotiopsis species are widely distributed throughout
1961;
tropical
and
temperate
regions
(Guba
Maharachchikumbura et al. 2012, 2014a). Pestalotiopsis
species have been isolated from dead leaves, bark, twigs,
soil, polluted stream water, wood, paper, fabrics, and wool
(Guba 1961; Maharachchikumbura et al. 2012, 2014a).
Some species have been associated with human and animal
infections, and others (e.g. P. guepinii and P. microspora)
have also been isolated from extreme environments (Maharachchikumbura et al. 2014b).
Classification—Sordariomycetes, Xylariomycetidae, Amphisphaeriales, Sporocadaceae
Type species—Pestalotiopsis guepinii (Desm.) Steyaert [as
‘guepini’], Bull. Jard. bot. État Brux. 19(3): 312 (1949)
Distribution—Worldwide
Disease symptoms—Species of Pestalotiopsis cause a
variety of diseases in plants including canker lesions, shoot
dieback, leaf spots, needle blight, tip blight, grey blight,
scabby canker, severe chlorosis, fruit rots and various postharvest
diseases
(Maharachchikumbura
et
al.
2013a, b, 2014a, b). These pathogens reduce production
and cause economic loss in apple, blueberry, coconut,
chestnut, ginger, grapevine, guava, hazelnut, lychee,
mango, orchid, peach, rambutan, tea and wax apple due to
diseases (Maharachchikumbura et al. 2013a, b, 2014a, b).
Grapevine trunk diseases are the most destructive diseases
of grapevines that impact the economic production and
longevity of vineyards and even leading to partial or total
death of individual plants. Therefore, the initial identification of the causal agent is essential for early control of
2015;
these
diseases
(Jayawardene
et
al.
Maharachchikumbura et al. 2017). Pestalotoid fungi have
been reported as pathogens on a variety of grapevine cultivars, causing diseases including grapevine dieback, fruit
rot, postharvest disease and severe defoliation and they
infect all plant parts including leaves, canes, wood, berries
and flowers (Jayawardene et al. 2015; Maharachchikumbura et al. 2017). Pestalotiopsis menezesiana (Bres. &
Torr.) Bissett. and P. uvicola (Spegazzini) Bissett, are the
most common species recorded from grapevine around the
world and especially P. biciliata are associated with trunk
2015;
grapevine
disease
(Jayawardene
et
al.
Maharachchikumbura et al. 2017).
Hosts—Broad range of hosts including members of Altingiaceae, Arecaceae, Bromeliaceae, Euphorbiaceae, Myrtaceae, Poaceae, Proteaceae, Rosaceae, Rutaceae,
Theaceae and Vitaceae.
Morphological based identification and diversity
There are around 250 species, most of which were named
according to their host associations (Maharachchikumbura
et al. 2014a, b). However, Pestalotiopsis species are not
hosted specific and are found on a wide range of plants and
substrates (Jeewon et al. 2003; Lee et al. 2006;
Maharachchikumbura et al. 2014a, b). They exhibit considerable diversity in phenotype, and group together based
on similarities in conidial morphology (Jeewon et al. 2003;
Maharachchikumbura et al. 2012, 2013a, b, 2014a, b).
Considering morphology, conidial length, width, median
cell length, the colour of median cells and length of the
apical appendages appear to be stable characters within
Pestalotiopsis (Jeewon et al. 2003; Maharachchikumbura
et al. 2014b).
Pestalotiopsis guepinii was considered to be the type species of the genus described from stems and leaves of
Camellia japonica collected in France, and is characterised
by 5-celled conidia with three concolourous median cells,
hyaline terminal cells and simple or unbranched
123
Fungal Diversity
Fig. 28 continued
appendages arising from the apex of the apical cell
(Steyaert 1949; Maharachchikumbura et al. 2014b). Nag
Raj (1985) regarded P. maculans as the type species of
Pestalotiopsis with P. guepinii as a synonym. Jeewon et al.
(2003) also accepted P. maculans clusters with species
having concolourous median cells based on phylogenetic
analysis of ITS sequence data and that P. karstenii might
be a synonym of P. maculans (Maharachchikumbura et al.
2014b).
Most Pestalotiopsis species lack sexual morphs. The
sexual morph of Pestalotiopsis was treated as Pestalosphaeria Barr, with the type species Pestalosphaeria concentrica collected from grey-brown spots on living leaves
123
of Rhododendron maximum in North Carolina, USA (Maharachchikumbura et al. 2014b). Pestalosphaeria concentrica is characterised by immersed, subglobose ascomata
and unitunicate, cylindrical asci with a J ? apical ring;
ascospores uniseriate in the ascus, ellipsoid, pale dull
brown and 2-septate (Maharachchikumbura et al. 2014b).
Pestalotiopsis species have the ability to switch lifemodes as endophytes, pathogens and saprobes (Hu et al.
2007; Maharachchikumbura et al. 2012). Therefore, many
endophytic and plant pathogenic Pestalotiopsis species
persist as saprobes and have been isolated from dead
leaves, bark and twigs (Maharachchikumbura et al.
2012, 2013a, b, 2014b).
Fungal Diversity
Table 18 Details of the Fusarium isolates used in the phylogenetic analyses
Species
Isolate/voucher no
RPB1
RPB2
tef1
Fusarium anguioides
NRRL 25385*; ATCC 66485
JX171511
JX171624
MH742689
F. acaciae-mearnsii
NRRL 26755
KM361640
KM361658
AF212449
F. acuminatum
NRRL 36147; CBS 109232
HM347174
GQ505484
GQ505420
F. agapanthi
NRRL 54463*
KU900620
KU900625
KU900630
F. albidum
NRRL 22152
JX171492
JX171605
–
F. albosuccineum
NRRL 20459
JX171471
JX171585
–
F. algeriense
NRRL 66647*; CBS 142638; IL-79
MF120488
MF120499
–
F. ananatum
CBS 118516*
LT996188
LT996137
KU604416
F. andiyazi
NRRL 31727; CBS 119857
LT996189
LT996138
KP662901
F. anthophilum
NRRL 13602; CBS 737.97
LT996190
LT996139
KU711685
F. arcuatisporum
F. armeniacum
CGMCC3.19493*; LC12147
NRRL 6227
MK289799
JX171446
MK289739
JX171560
MK289584
HM744692
F. asiaticum
NRRL 13818*; CBS 110257
JX171459
JX171573
AF212451
F. avenaceum
NRRL 54939
JX171551
JX171663
MH582391
F. aywerte
NRRL 25410
JX171513
JX171626
KU171717
F. babinda
NRRL 25539; CBS 396.96
JX171519
JX171632
MH742712
F. begoniae
CBS 403.97*; NRRL 25300
LT996191
LT996140
AF160293
F. beomiforme
NRRL 25174; CBS 740.97
–
JX171619
–
F. brachygibbosum
NRRL 13829
JX171460
JX171574
–
F. buharicum
NRRL 13371; CBS 796.70
JX171449
JX171563
–
F. bulbicola
NRRL 13618*; CBS 220.76
KF466394
KF466404
KF466415
F. burgessii
CBS 125537*; RBG 5319
KJ716217
HQ646393
HQ667149
F. callistephi
CBS 187.53*
–
MH484905
MH484966
F. carminascens
CBS 144738*; CPC 25800
–
MH484937
MH485028
F. celtidicola
MFLUCC 16-0751*
–
MH576580
–
F. citri
CGMCC3.19467*; LC6896
MK289828
MK289771
MK289617
F. citricola
F. coicis
CBS 142421*; CPC 27805
NRRL 66233*; RBG5368
LT746290
KP083269
LT746310
KP083274
LT746197
KP083251
F. commune
NRRL 28387
–
JX171638
KU171720
F. concentricum
NRRL 25181*; CBS 450.97
LT996192
JF741086
AF160282
F. concolor
NRRL 13459*; CBS 961.87
JX171455
JX171569
MH742681
F. contaminatum
CBS 114899*
–
MH484901
MH484992
F. continuum
F201128
KM520389
KM236780
KM236720
F. convolutans
CBS 144207*; CPC 33733
LT996193
LT996141
LT996094
F. cugenangense
InaCCF984*
LS479560
LS479308
–
F. culmorum
NRRL 25475; CBS 417.86
JX171515
JX171628
KY873384
F. cuneirostrum
NRRL 31104
–
EU329558
EF408413
F. curvatum
CBS 238.94; NRRL 26422; PD 94/184
–
MH484893
MH484984
F. cyanostomum
NRRL 53998
JX171546
JX171658
–
F. dactylidis
NRRL 29298*
KM361654
KM361672
DQ459748
F. denticulatum
NRRL 25302; CBS 735.97
LT996195
LT996143
AF160269
F. desaboruense
F. dlaminii
InaCC F950
NRRL 13164*; CBS 119860
LS479870
KU171681
LS479852
KU171701
–
MK639039
F. duoseptatum
InaCC F916*
LS479495
LS479239
–
F. elaeidis
CBS 217.49*; NRRL 36358
–
MH484870
MH484961
F. enterolobii
CPC 27190
–
LT746312
LT746199
F. equiseti
NRRL 13405
–
GQ915491
GQ915507
F. fabacearum
CBS 144743*; CPC 25802
–
MH484939
MH485030
123
Fungal Diversity
Table 18 (continued)
Species
Isolate/voucher no
RPB1
RPB2
tef1
F. ficicrescens
CBS 125178*
–
KT154002
KP662899
F. flocciferum
NRRL 25473
JX171514
JX171627
–
F. foetens
NRRL 38302
JX171540
JX171652
GU170559
F. fracticaudum
CMW 252374
LT996196
LT996144
KJ541059
F. fractiflexum
NRRL 28852*
–
LT575064
AF160288
F. fredkrugeri
CBS 144209*; CPC 33747
LT996199
LT996147
LT996097
F. fujikuroi
NRRL 13566
JX171456
JX171570
–
F. gaditjirrii
F. gamsi
NRRL 45417
CBS 143610*; CPC 30862; OrSaAg4
–
–
JX171654
LT970760
KU171724
LT970788
F. globosum
NRRL 26131*; CBS 428.97
KF466396
KF466406
KF466417
F. glycines
CBS 144746*; CPC 25808
–
MH484942
MH485033
F. gossypinum
CBS 116613*
–
MH484909
MH485000
F. graminearum
NRRL 31084; CBS 123657
JX171531
JX171644
HM744693
F. grosmichelii
InaCC F833*
LS479548
LS479295
LS479744
F. guilinense
CGMCC3.19495*; LC12160
MK289831
MK289747
MK289594
F. guttiforme
NRRL 22945
JX171505
JX171618
–
F. hainanense
CGMCC3.19478*; LC11638
MK289833
MK289735
MK289581
F. heterosporum
NRRL 20693; CBS 720.79
JX171480
JX171594
–
F. hexaseptatum
InaCC F866*
–
LS479359
LS479805
F. hoodiae
CBS 132474*
–
MH484929
MH485020
F. hostae
NRRL 29889
JX171527
JX171640
AY329034
F. inflexum
NRRL 20433
–
JX171583
AF008479
F. ipomoeae
F. iranicum
CGMCC3.19496*; LC12165
CBS 143608*; CPC 30860; OrSaAg2
MK289859
–
MK289752
LT970757
MK289599
LT970785
F. irregulare
CGMCC3.19489*; LC7188
MK289863
MK289783
MK289629
F. kalimantanense
InaCC F917*
LS479497
LS479241
LS479690
F. konzum
CBS 119849*
LT996200
LT996148
LT996098
F. kotabaruense
InaCC F963*
LS479875
LS479859
LS479445
F. kuroshium
CBS 142642*; UCR3641
KX262236
KX262256
KX262216
F. kyushuense
NRRL 25349
–
GQ915492
GQ915508
F. lacertarum
NRRL 20423; CBS 130185
HM347137
JX171581
GQ505593
F. lactis
NRRL 25200*; CBS 411.97
LT996201
LT996149
AF160272
F. langsethiae
NRRL 54940
JX171550
JX171662
–
F. languescens
CBS 645.78*; NRRL 36531
–
MH484880
MH484971
F. lateritium
NRRL 13622
JX171457
JX171571
AY707173
F. libertatis
CBS 144749*; CPC 28465
–
MH484944
MH485035
F. longipes
NRRL 13368
JX171448
JX171562
–
F. luffae
CGMCC3.19497*; LC12167
MK289869
MK289754
MK289601
F. lumajangense
F. lyarnte
InaCC F872*
NRRL 54252; CBS 125536
–
JX171549
LS479850
JX171661
LS479441
–
F. mangiferae
NRRL 25226*; BBA 69662
JX171509
JX171622
–
F. miscanthi
NRRL 26231
–
JX171634
KU171725
F. mundagurra
NRR L66235*; RBG5717
KP083272
KP083276
MK639058
F. nanum
CGMCC3.19498*; LC12168
MK289871
MK289755
MK289602
F. napiforme
CBS 748.97*; NRRL 13604
HM347136
EF470117
KU604409
GQ505402
F. nelsonii
NRRL 13338
JX171447
JX171561
F. newnesense
NRRL 66237; RBG5443
KP083271
KP083277
KJ397074
F. nirenbergiae
CBS 840.88*
–
MH484887
MH484978
123
Fungal Diversity
Table 18 (continued)
Species
Isolate/voucher no
RPB1
RPB2
tef1
F. nisikadoi
NRRL 25179; CBS 742.97
JX171507
JX171620
–
F. nurragi
NRRL 36452; CBS 392.96
JX171538
JX171650
–
F. nygamai
NRRL 13448*; CBS 749.97
LT996202
EF470114
AF160273
F. odoratissimum
InaCC F822*
LS479618
LS479386
–
F. oligoseptatum
NRRL 62579*; FRC S- 2581; MAFF 246283; CBS 143241
KC691596
KC691656
KC691538
F. oxysporum
CBS 144134*
–
MH484953
MH485044
F. palustre
NRRL 54056*
KT597718
KT597731
–
F. paranaense
F. parvisorum
CML1830*
CBS 137236*; FCC 5407; CMW 25267
–
–
KF680011
LT996150
KF597797
KJ541060
F. pernambucanum
MUM 1862*; URM 7559
MH668869
–
–
F. petersiae
CBS 143231*
MG386139
MG386150
MG386159
F. pharetrum
CBS 144751*; CPC 30824
–
MH484952
MH485042
F. phialophorum
InaCC F971*
LS479545
LS479292
LS479741
F. phyllophilum
NRRL 13617*; CBS 216.76
KF466399
KF466410
KF466421
F. pisi
NRRL 22278
–
EU329501
AF178337
F. poae
NRRL 13714
JX171458
JX171572
–
F. praegraminearum
NRRL 39664*
KX260125
KX260126
KX260120
F. proliferatum
NRRL 22944; CBS 217.76
JX171504
JX171617
–
F. pseudensiforme
NRRL 46517
KC691615
KC691645
KC691555
F. pseudocircinatum
NRRL 22946*; CBS 449.97
LT996204
LT996151
AF160271
F. pseudograminearum
NRRL 28062*; CBS 109956
JX171524
JX171637
AF212468
F. pseudonygamai
NRRL 13592*; CBS 417.97
LT996205
LT996152
AF160263
F. purpurascens
F. ramigenum
InaCC F886*
NRRL 25208*; CBS 418.98
–
KF466401
LS479385
KF466412
LS479827
KF466423
F. redolens
NRRL 22901; CBS 743.97
–
KU171708
KU171728
F. riograndense
HCF3*
–
KX534003
KX534002
F. roseum
NRRL 22187
JX171493
JX171606
–
F. sacchari
NRRL 13999; CBS 223.76
JX171466
JX171580
KU711669
F. salinense
CBS 142420*; CPC 26973
LT746286
LT746306
LT746193
F. sangayamense
InaCC F960*
LS479537
LS479283
–
F. sarcochroum
NRRL 20472; CBS 745.79
JX171472
JX171586
–
F. scirpi
NRRL 13402
JX171452
JX171566
GQ505592
F. sibiricum
NRRL 53430*
–
HQ154472
HM744684
F. siculi
CBS 142422*; CPC 27188
LT746299
LT746327
LT746214
F. sororula
CBS 137242*
LT996206
LT996153
–
F. sporotrichioides
NRRL 3299
JX171444
JX171558
HM744665
F. staphyleae
NRRL 22316
JX171496
JX171609
MH582426
F. stercicola
CBS 142481*; DSM 106211
–
KY556552
KY556524
F. stilboides
F. subglutinans
NRRL 20429; ATCC 15662
NRRL 22016*; CBS 747.97
JX171468
JX171486
JX171582
JX171599
–
HM057336
F. sublunatum
NRRL 13384*; CBS 189.34
JX171451
JX171565
–
F. subtropicale
NRRL 66764*; CBS 144706
MH706972
MH706973
MH706974
F. succisae
NRRL 13613; CBS 219.76
LT996207
LT996154
AF160289
F. sudanense
CBS 454.97*; NRRL 25451
LT996208
LT996155
KU711697
F. sulawesiense
InaCC F940*
–
LS479855
LS479443
F. tanahbumbuense
InaCC F965*
LS479877
LS479863
LS479448
F. tardichlamydosporum
InaCC F958*
–
LS479280
LS479729
F. tardicrescens
NRRL 36113*
LS479474
LS479217
LS479665
123
Fungal Diversity
Table 18 (continued)
Species
Isolate/voucher no
RPB1
RPB2
tef1
F. terricola
CBS 483.94*
LT996209
LT996156
KU711698
F. thapsinum
NRRL 22045; CBS 733.97
JX171487
JX171600
AF160270
F. tjaetaba
NRRL66243*; RBG5361
KP083267
KP083275
KP083263
F. tjaynera
NRRL66246*; RBG5367
KP083268
KP083279
–
F. torreyae
NRRL 54149
JX171548
HM068359
HM068337
F. torulosum
NRRL 22748; NRRL 13919
JX171502
JX171615
–
F. transvaalense
CBS 144211*; CPC 30923
LT996210
LT996157
LT996099
F. tricinctum
F. triseptatum
NRRL 25481*; CBS 393.93
CBS 258.50*; NRRL 36389
JX171516
–
HM068327
MH484873
MH582379
MH484964
F. udum
NRRL 22949; CBS 178.32
LT996220
LT996172
AF160275
F. venenatum
CBS 458.93*
–
KM232382
KM231942
F. verrucosum
NRRL 22566, BBA 64786
–
JX171613
–
F. verticillioides
NRRL 20956
JX171485
JX171598
–
F. veterinarium
CBS 109898*; NRRL 36153
–
MH484899
MH484990
F. volatile
CBS 143874*
–
LR596006
LR596007
F. witzenhausenense
CBS 142480*
–
KY556553
KY556525
F. xylarioides
NRRL 25486; CBS 258.52
JX171517
JX171630
AY707136
F. caatingaense
MUM 1859*; URM 6779
MH668845
LS398495
LS398466
F. goolgardi
NRRL 66250*; RBG5411
KP083270
KP083280
KP101123
F. humuli
CGMCC3.19374*; CQ1039
MK289840
MK289724
MK289570
Fusicolla aquaeductuum
NRRL 20686*
JX171476
JX171590
–
Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold
Pestalotiopsis species that were isolated as endophytes are
important in the discovery of novel compounds with
medicinal, agricultural and industrial applications (Maharachchikumbura et al. 2014b; Xu et al. 2010, 2014).
Pestalotiopsis species are a rich source for bioprospecting
compared to other fungal genera, and more than 100
compounds have been isolated from Pestalotiopsis (Maharachchikumbura et al. 2014b; Xu et al. 2010, 2014).
Molecular based identification and diversity
Maharachchikumbura et al. (2012) tested with 10 gene
regions to resolve species boundaries in Pestalotiopsis
(actin, calmodulin, glutamine synthase, glyceraldehyde-3phosphate dehydrogenase, ITS, LSU, 18S nrDNA, RNA
polymerase II, tef1 and TUB2). Maharachchikumbura et al.
(2014b) used phylogenetic analysis of combined ITS,
TUB2 and tef1 genes to successfully resolve Pestalotiopsis
species (Fig. 30, Table 20).
Recommended genetic marker (genus level)—LSU (as
outlined in Maharachchikumbura et al. 2012)
Recommended genetic markers (species level)—ITS,
TUB2 and tef1 (as outlined in Maharachchikumbura et al.
2012)
123
Accepted number of species: There are 360 epithets in
Index Fungorum in this genus, however, 75 species with
DNA sequence data are accepted.
References:
Maharachchikumbura
et
al.
2013a, b, 2014b, 2016 (morphology, phylogeny)
Stagonosporopsis Died. emend. Aveskamp et al., Stud.
Mycol. 65: 44. 2010
Stagonosporopsis is a coelomycetous genus in the
family Didymellaceae (de Gruyter et al. 2013), accommodating several important phytopathogenic species. Some
of the species have described sexual forms in Didymella
(Diedicke 1912; Aveskamp et al. 2010). Some
Stagonosporopsis species have quarantine importance.
Stagonosporopsis andigena is listed in Annex IAI by
European Union (EU), meaning its introduction to EU is
prohibited. This pathogen is also listed in the A1 list by the
European and Mediterranean Plant Protection Organization
(EPPO 2019). Stagonosporopsis chrysanthemi is another
species listed in A2 list by EPPO (EPPO 2019).
Classification—Dothideomycetes,
Pleosporomycetidae,
Pleosporales, Didymellaceae
Type species—Stagonosporopsis boltshauseri (Sacc.)
Died. 1912
Distribution—Worldwide
Fungal Diversity
Fig. 29 Phylogenetic tree
generated by maximum
likelihood analysis of combined
ITS and tef1 sequence data of
Lasiodiplodia species. Related
sequences were obtained from
GenBank. Forty nine strains are
included in the analyses, which
comprise 866 characters
including gaps. The tree was
rooted with Barriopsis tectonae
and B. iraniana. Tree topology
of the ML analysis was similar
to MP and BYPP. The best
scoring RAxML tree with a final
likelihood value of
- 3733.342990 is presented.
The matrix had 253 distinct
alignment patterns, with 4.41%
of undetermined characters or
gaps. Estimated base
frequencies were as follows;
A = 0.211797, C = 0.285190,
G = 0.260783, T = 0.242230;
substitution rates
AC = 0.983905,
AG = 3.303939,
AT = 1.281593,
CG = 0.950258,
CT = 5.553417,
GT = 1.000000; gamma
distribution shape parameter
a = 0.221126. RAxML
bootstrap support values C 80%
are shown respectively near the
nodes. Bayesian posterior
probabilities C 0.5 (BYPP)
indicated as thickened black
branches. Ex-type strains are in
bold
Disease symptoms—the Black blight of potato, gummy
stem blight, ray blight
All plant parts may be attacked by S. chrysanthemi and
S. inoxydabilis, however, flowers and cuttings are highly
susceptible. Death of flowers and buds, a necrotic lesion on
leaves and peduncles of unopened buds, soft rot of cortex
of roots and discolouration of bark are the main symptom
of the disease. Eventually, plant death occurs (Fox 1998;
Pethybridge et al. 2008). In gummy stem blight of cucurbits, symptoms can be observed on all above ground and
reproductive parts. Leaf spots are the main diagnostic
character of this disease. Most of the circular or triangular
shaped spots start at the margin of the leaf or extend
towards the margin. The centre of the leaf spot is a lighter
shade of brown than the surrounding portion. As leaf spots
coalesce leaf blights occur. Actively expanding lesions on
leaves, petioles, and pedicels often appear as water-soaked.
Cankers may form on crowns, main stems and vines
(Keinath 2013). Stagonosporopsis andigena the black
blight of potato causal agent affects leaves, petioles and
stems causing lesions and premature leaf drop, but does not
infect the underground parts. On leaves, the pathogen
causes small, blackish concentric lesions. The initial
symptoms can be observed on the lower leaves, however,
as the disease progresses lesions may also develop in upper
leaves as well. Lesions may coalesce and severely affected
leaves may turn blackish giving a scorched appearance
(EFSA panel on plant health 2019).
Hosts—Amaranthaceae, Asteraceae, Campanulaceae,
Caryophyllaceae, Cucurbitaceae, Fabaceae, Lamiaceae,
Pinaceae, Ranunculaceae, Solanaceae and Valerianaceae.
123
Fungal Diversity
Table 19 Details of the
Lasiodiplodia isolates used in
the phylogenetic analyses
Species
Isolate/voucher no
ITS
tef1
Lasiodiplodia avicenniae
CBS 139670*
KP860835
KP860680
L. avicenniarum
MFLUCC 17-2591*
MK347777
MK340867
L. brasiliense
CMM 4015*
JX464063
JX464049
L. bruguierae
CBS 139669*
KP860832
KP860677
L. caatinguensis
CMM 1325*
KT154760
KT008006
L. chinensis
CGMCC 3.18061*
KX499889
KX499927
L. chonburiensis
MFLUCC 16-0376*
MH275066
MH412773
L. cinnamomi
CFCC 51997*
MG866028
MH236799
L. citricola
CBS 124707*
GU945354
GU945340
L. crassispora
CBS 118741*
DQ103550
EU673303
L. euphorbiicola
CMM 3609*
KF234543
KF226689
L. exigua
CBS 137785*
KJ638317
KJ638336
L. gilanensis
CBS 124704*
GU945351
GU945342
L. gonubiensis
CBS 115812*
AY639595
DQ103566
L. gravistriata
L. hormozganensis
CMM 4564*
CBS 124709*
KT250949
GU945355
KT250950
GU945343
L. hyalina
CGMCC 3.17975*
KX499879
KX499917
L. iraniensis
CBS 124710*
GU945346
GU945334
L. laeliocattleyae
CBS 167.28*
KU507487
KU507454
L. lignicola
CBS 134112*
JX646797
KU887003
L. macrospora
CMM 3833*
KF234557
KF226718
L. mahajangana
CBS 124925*
FJ900595
FJ900641
L. margaritacea
CBS 122519*
EU144050
EU144065
L. mediterranea
CBS 137783*
KJ638312
KJ638331
L. missouriana
CBS 128311*
HQ288225
HQ288267
L. pandanicola
MFLUCC 16-0265*
MH275068
MH412774
L. parva
CBS 456.78*
EF622083
EF622063
L. plurivora
CBS 120832*
EF445362
EF445395
L. pontae
CMM 1277*
KT151794
KT151791
L. pseudotheobromae
CBS 116459*
EF622077
EF622057
L. pyriformis
L. rubropurpurea
CBS 121770*
EU101307
EU101352
CBS 118740*
DQ103553
EU673304
L. sterculiae
CBS 342.78*
KX464140
KX464634
L. subglobosa
CMM 3872*
KF234558
KF226721
L. swieteniae
MFLUCC 18-0244*
MK347789
MK340870
L. thailandica
CBS 138760*
KJ193637
KJ193681
L. theobromae
CBS 164.96*
AY640255
AY640258
L. venezuelensis
CBS 118739*
DQ103547
EU673305
L. viticola
CBS 128313*
HQ288227
HQ288269
L. vitis
CBS 124060*
KX464148
KX464642
Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold
Morphological based identification and diversity
Stagonosporopsis is characterized by ellipsoidal to subglobose, aseptate to 3 septate conidia and sexual morph
with ellipsoidal, fusiform or obovoid, 1 septate ascospore
(Aveskamp et al. 2010; Chen et al. 2015).
Stagonosporopsis was originally separated from Ascochyta
123
by Diedicke (1912) based on the occasional formation of
multi-septate (Stagonospora-like) conidia. In the phylogenetic reassessment of Didymellaceae (Aveskamp et al.
2010) based on the sequences LSU and ITS of the nrDNA
and TUB2 region, multiple Phoma species, including P.
ligulicola, were recovered in a high supported clade with
the interpretive types of the genus Stagonosporopsis; S.
Fungal Diversity
Fig. 30 Phylogram generated from RAxML analysis based on
combined ITS, TUB2 and tef1 sequences of all the accepted species
of Pestalotiopsis. Related sequences were obtained from GenBank.
Seventy-nine taxa are included in the analyses, which comprise 1581
characters including gaps. The tree was rooted in Neopestalotiopsis
cubana (CBS 600.96) and N. saprophytica (MFLUCC 12-0282). Tree
topology of the ML analysis was similar to the BYPP and MP. The
best scoring RAxML tree with a final likelihood value of
- 12269.881063 is presented. The matrix had 763 distinct alignment
patterns, with 15.79% of undetermined characters or gaps. Estimated
base frequencies were as follows; A = 0.234129, C = 0.293516,
G = 0.211518, T = 0.260837; substitution rates AC = 1.189917,
AG = 3.402399, AT = 1.153875, CG = 1.001451, CT = 4.301074,
GT = 1.000000; gamma distribution shape parameter a = 0.283001.
The maximum parsimonious dataset consisted of 948 constant, 450
parsimony-informative and 183 parsimony-uninformative characters.
The parsimony analysis of the data matrix resulted in the maximum of
ten equally most parsimonious trees with a length of 1962 steps
(CI = 0.498, RI = 0.697, RC = 0.347, HI = 0.502) in the first tree.
RAxML and maximum parsimony bootstrap support value C 50%
and BYPP C 0.90 values are shown near the nodes. The scale bar
indicates 10 changes per site. The ex-type strains are in bold
actaeae (Boerema 1997, Boerema et al. 2004). In addition,
S. tanaceti shows morphological similarity to S. inoxydabilis but can be differentiated by the faster growth rate,
larger conidia, presence of chlamydospores, and lack of
ascomata in culture (Vaghefi et al. 2012). Morphological
characters overlap between the species in this genus and
species are primarily separated based on molecular data.
Molecular based identification and diversity
Most comprehensive multigene phylogeny analyses for this
genus were performed by Aveskamp et al. (2010), Vaghefi
123
Fungal Diversity
Table 20 Details of
Pestalotiopsis the isolates used
in the phylogenetic analyses
123
Species
Isolate/voucher no
ITS
TUB2
tef1
Pestalotiopsis adusta
ICMP 6088*
JX399006
JX399037
JX399070
P. aggestorum
LC6301*
KX895015
KX895348
KX895234
P. anacardiacearum
IFRDCC 2397*
NR120255.1
KC247155
KC247156
P. arceuthobii
CBS 434.65*
NR147561
KM199427
KM199516
P. arengae
CBS 331.92*
NR147560
KM199426
KM199515
P. australasiae
CBS 114126*
NR147546
KM199409
KM199499
P. australis
CBS 114193*
KM199332
KM199383
KM199475
P. biciliata
CBS 124463*
KM199308
KM199399
KM199505
P. brachiata
LC2988*
KX894933
KX895265
KX895150
P. brassicae
CBS170.26*
NR147562
–
KM199558
P. camelliae
MFLUCC12-0277*
NR120188
JX399041
JX399074
P. chamaeropis
CBS 186.71*
KM199326
KM199391
KM199473
P. clavata
MFLUCC12-0268*
JX398990
JX399025
JX399056
P. colombiensis
CBS 118553*
NR147551
KM199421
KM199488
P. digitalis
P. dilucida
ICMP 5434*
LC3232*
KP781879
KX894961
KP781883
KX895293
–
KX895178
P. diploclisiae
CBS 115587*
NR147552
KM199419
KM199486
P. diversiseta
MFLUCC12-0287*
NR120187
JX399040
JX399073
P. dracontomelon
MFUCC 10-0149*
KP781877
–
KP781880
P. ericacearum
IFRDCC 2439*
KC537807
KC537821
KC537814
P. formosana
NTUCC 17-009*
MH809381
MH809385
MH809389
P. furcata
MFLUCC12-0054*
JQ683724
JQ683708
JQ683740
P. gaultheria
IFRD 411-014*
KC537805
KC537819
KC537812
P. gibbosa
NOF3175*
LC311589
LC311590
LC311591
P. grevilleae
CBS 114127*
NR147548
KM199407
KM199504
P. hawaiiensis
CBS 114491*
NR147559
KM199428
KM199514
P. hollandica
CBS 265.33*
KM199328
KM199388
KM199481
P. humus
CBS 336.97*
KM199317
KM199420
KM199484
P. inflexa
MFLUCC12-0270*
JX399008
JX399039
JX399072
P. intermedia
MFLUCC12-0259*
JX398993
JX399028
JX399059
P. italiana
P. jester
MFLUCC12-0657*
KP781878
KP781882
KP781881
CBS 109350*
KM199380
KM199468
KM199554
P. jiangxiensis
LC4399*
KX895009
KX895341
KX895227
P. jinchanghensis
LC6636*
KX895028
KX895361
KX895247
P. kenyana
CBS 442.67*
KM199302
KM199395
KM199502
P. knightiae
CBS 114138*
KM199310
KM199408
KM199497
P. licualacola
HGUP 4057*
KC492509
KC481683
KC481684
P. linearis
MFLUCC12-0271*
JX398992
JX399027
JX399058
P. longiappendiculata
LC3013*
KX894939
KX895271
KX895156
KX895223
P. lushanensis
LC4344*
KX895005
KX895337
P. macadamiae
BRIP 63738b*
KX186588
KX186680
KX186621
P. malayana
CBS 102220*
NR147550
KM199411
KM199482
P. monochaeta
CBS 144.97*
KM199327
KM199386
KM199479
P. montellica
MFLUCC12-0279*
JX399012
JX399043
JX399076
P. neolitseae
NTUCC 17-011*
MH809383
MH809387
MH809391
P. novae-hollandiae
P. olivaceae
CBS 130973*
PSHI2002*
NR147557
AY687883
KM199425
DQ333580
KM199511
–
P. oryzae
CBS 353.69*
KM199299
KM199398
KM199496
P. pallidotheae
MAFF 240993*
NR111022
LC311584
LC311585
P. papuana
CBS 887.96*
KM199318
KM199415
KM199492
Fungal Diversity
Table 20 (continued)
Species
Isolate/voucher no
ITS
TUB2
tef1
P. parva
CBS 265.37*
KM199312
KM199404
KM199508
P. photinicola
GZCC 16-0028*
KY092404
KY047663
KY047662
P. portugalica
CBS 393.48*
KM199335
KM199422
KM199510
P. rhizophorae
MFLUCC17-0416*
MK764283
MK764349
MK764327
P. rhododendri
IFRDCC 2399*
NR120265
KC537818
KC537811
P. rhodomyrtus
HGUP 4230*
KF412648
KF412642
KF412645
P. rosea
MFLUCC12-0258*
JX399005
JX399036
JX399069
P. scoparia
CBS 176.25*
KM199330
KM199393
KM199478
P. shorea
MFLUCC12-0314*
KJ503811
KJ503814
KJ503817
P. spathulata
CBS 356.86*
NR147558
KM199423
KM199513
P. telopeae
CBS 114161*
NR147545
KM199403
KM199500
P. thailandica
MFLUCC17-1616*
MK764285
MK764351
MK764329
P. trachicarpicola
IFRDCC 2440*
NR120109
JQ845945
JQ845946
P. unicolor
MFLUCC12-0276*
JX398999
JX399030
–
P. verruculosa
P. yanglingensis
MFLUCC12-0274*
LC4553*
NR120185
KX895012
–
KX895345
JX399061
KX895231
P. yunnanensis
HMAS 96359*
AY373375
–
–
Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold
et al. (2012), Hyde et al. (2014), Chen et al. (2015, 2017)
and Jayasiri et al. (2019). Five-marker phylogeny of the
Stagonosporopsis spp. for which these DNA sequence data
are available is shown (Table 21).
Identification of Stagonosporopsis species associated
with ray blight of Asteraceae can be achieved through
multi-locus sequence typing (Aveskamp et al. 2010;
Vaghefi et al. 2012) and also with a species-specific multiplex PCR assay developed by Vaghefi et al. (2016). This
assay is based on a four-primer PCR that targets the
intergenic spacer of the nrDNA of the ray blight pathogens,
producing species-specific amplicons of * 560 in S.
chrysanthemi, * 630 bp in S. inoxydabilis and * 400 bp
in S. tanaceti, which can be easily differentiated on an
agarose gel (Vaghefi et al. 2016).
This
study
reconstructs
the
phylogeny
of
Stagonosporopsis based on analyses of a combined ITS,
LSU, RPB2 and TUB2 sequence data (Fig. 31). The phylogenetic tree is updated with recently introduced
Stagonosporopsis species and corresponds to previous
studies (Chen et al. 2017, Jayasiri et al. 2019).
Recommended genetic marker (genus level)—ITS
Recommended genetic markers (species level)—TUB2 and
RPB2
Accepted number of species: There are 55 species in Index
Fungorum (2019) and only 24 species are accepted/ have
molecular data in this genus.
References: Chen et al. 2015, 2017, Jayasiri et al. 2019
(morphology, phylogeny).
Verticillium Nees, Syst. Pilze (Würzburg): 57 (1816)
[1816-17]
The genus Verticillium Nees was introduced by Nees
von Esenbeck (1816) for a single saprotrophic species, V.
tenerum Nees, which was proposed as the type species.
Zare et al. (2004) synonymized V. tenerum under
Acrostalagmus luteoalbus (Link) Zare, W. Gams &
Schroers, and Gams et al. (2005) proposed V. dahliae Kleb.
as the conserved type of the genus Verticillium.
Verticillium includes several plant pathogenic species
that infect trees, insects, mushrooms and, in particular,
dicotyledonous plants: V. dahliae Kleb., V. albo-atrum
Reinke et Berth., V. nigrescens Pethybr., V. nubilum
Pethybr., V. tricorpus Isaac., V. theobromae (Turc.) Mas. &
Hughes and V. fungicola (Preuss) Hassebrauk (Pegg and
Brady 2002). Zare et al. (2007) assigned V. nigrescens to
the genus Gibellulopsis and V. theobromae to Musicillium.
Zare and Gams (2008) assigned V. fungicola to the genus
Lecanillium. Verticillium dahliae and V. albo-atrum are the
two most notorious species which cause Verticillium wilt
diseases in a wide range of mainly dicotyledonous hosts
and result in billions of dollars of damage annually in crop
losses worldwide (Pegg and Brady 2002; Barbara and
Clewes 2003; Inderbitzin et al. 2011).
Verticillium species, in particular, V. dahliae and V. alboatrum, can infect a wide range of plant species. Many hosts
of Verticillium species were given by different mycologists, e.g., Van der Meer (1925); Rudolph (1931); Engelhard and Carter (1956); Parker (1959); Stark (1961);
Devaux and Sackston (1966); Himelick (1969), including
123
Fungal Diversity
growth and premature defoliation. Olive- green to black
streaks can be observed in the sapwood of infected branches. In cross sections, vascular tissue appears as a dark
ring or pinpoint dark spots. Initial symptoms can occur on
one side of the tree or the entire plant (Fradin and Thomma
2006; Blum et al. 2018).
Hosts—Species of this genus have a broad host range
including members of Amaranthaceae, Amaryllidaceae,
Asteraceae, Brassicaceae, Musaceae, Pinaceae, Rosaceae,
Rubiaceae, Sapindaceae, Solanaceae, Theaceae, Vitaceae
and Zingiberaceae (Farr and Rossman 2019).
high-value crop plants, e.g., cotton (Land et al. 2016),
lettuce (Garibaldi et al. 2007; Powell et al. 2013), mango
(Baeza-Montanez et al. 2010; Ahmed et al. 2014), gold
kiwifruit (Auger et al. 2009), bean (Berbegal and Armengol 2009; Sun et al. 2016; Blomquist et al. 2017), watermelon (Bruton et al. 2007), olive tree (Lo Giudice et al.
2010; Kaliterna et al. 2016), potato (Pace-Lupi et al. 2006),
pumpkin (Rampersad 2008). The most comprehensive
hosts’ list was provided by Pegg and Brady (2002).
Classification—Sordariomycetes,
Hypocreomycetidae,
Glomerellales, Plectosphaerellaceae
Type species—Verticillium dahliae Kleb., Mykol. Zentbl.
3: 66 (1913)
Distribution—Worldwide
Disease symptoms—Wilt
Wilt caused by Verticillium species is a serious fungal
disease that causes injury or death to many plant species.
Symptoms of this disease vary according to the host species and to environmental conditions including sudden
wilting of small branches, yellowing of foliage, stunt
There are 270 records in Index Fungorum (2019) and 288
records in MycoBank (Crous et al. 2004) in this genus.
Most of the species have been transferred to other genera,
e.g., Gibellulopsis (Zare et al. 2007), Haptocillium (Zare
and Gams 2001b), Lecanicillium (Zare and Gams 2001a),
Musicillium (Zare et al. 2007), Pochonia (Zare and Gams
2001a, b), Simplicillium (Zare and Gams 2001a). Only ten
Fig. 31 Phylogenetic tree generated by maximum likelihood analysis
of combined ITS, LSU, RPB2 and TUB2 sequence data of
Stagonosporopsis species. Related sequences were obtained from
GenBank. Thirty-two are included in the analyses, which comprise
2756 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 Heterophoma poolensis
(CBS 113.20). Tree topology of the ML analysis was similar to the
MP. The best scoring RAxML tree with a final likelihood value of
- 8386.622374 is presented. The matrix had 388 distinct alignment
patterns, with 11.83% of undetermined characters or gaps. Estimated
base frequencies were as follows; A = 0.245798, C = 0.237676,
G = 0.273178, T = 0.243348; substitution rates AC = 1.882600,
AG = 4.123164, AT = 2.015920, CG = 0.907833, CT = 12.626910,
GT = 1.000000; gamma distribution shape parameter a = 1.105097.
RAxML bootstrap support values C 50% and Bayesian posterior
probabilities C 0.95 (BYPP) are shown respectively near the nodes.
Ex-type strains are in bold
123
Morphological based identification and diversity
Fungal Diversity
Fig. 32 Phylogenetic tree generated from Bayesian analysis based on
combined ACT, tef1, GPD and TS sequence data for the genus
Verticillium. Sixteen strains are included in the combined genes
sequence analyses which comprise total of 2597 characters (609
characters for the ACT, 620 characters for tef1, 744 characters for
GPD, 624 characters for TS) after alignment. For the Bayesian
analysis, two parallel runs with six chains were run for 1,000,000
generations and trees were sampled every 100th generation, resulted
in 20,002 trees from two runs of which 15,002 trees were used to
calculate the posterior probabilities (each run resulted in 10,001 trees
of which 7501 trees were sampled). Bootstrap support values for
maximum likelihood (ML, first set) and maximum parsimony (MP,
second set) greater than 75% and Bayesian posterior probabilities
greater than 0.95 are indicated above or below the nodes. Ex-type
strains are in bold. The tree is rooted with Gibellulopsis nigrescens
(PD596)
species, V. albo-atrum, V. alfalfae, V. dahliae, V. isaacii, V.
klebahnii, V. longisporum, V. nonalfalfae, V. nubilum, V.
tricorpus and V. zaregamsianum, were accepted within
Verticillium sensu stricto (Inderbitzin et al. 2011). No
sexual states are known. Descriptions and a key to these ten
species were provided by Inderbitzin et al. (2011).
(RPB1), the cytochrome oxidase subunit III gene (cox3),
the small ribosomal rRNA subunit (rns), NADH dehydrogenase subunit genes (nad1 and nad3) were used (Barbara
and Clewes 2003; Pantou et al. 2005; Zare and Gams
2008, 2016).
Molecular based identification and diversity
The first phylogenetic analysis of Verticillium species was
made by Morton et al. (1995) to analysis the relationship
between V. alboatrum and V. dahliae based on the internal
transcribed spacer regions and intervening 5.8S rDNA
(ITS) sequences data (Fig. 32, Table 22). Subsequently,
SSU, LSU, RNA polymerase II largest subunit gene
Recommended genetic marker (genus level)—LSU
Recommended genetic marker (species level)—ITS
Accepted number of species: 10 species.
References: Inderbitzin et al. 2011 (morphology and phylogeny); Barbara and Clewes 2003, Morton et al. 1995,
Pantou et al. 2005, Zare and Gams 2008, 2016 (phylogeny); Fradin and Thomma 2006, Blum et al. 2018
(pathogenicity)
123
Fungal Diversity
Table 21 Details of the Stagonosporopsis isolates used in the phylogenetic analyses
Species
Stagonosporopsis actaeae
Culture
LSU
GenBank Accession numbers
ITS
RPB2
TUB2
CBS 106.96*
GU238166
GU237734
KT389672
CBS 114303
KT389760
KT389544
–
KT389847
MFLUCC 16-1439*
KY100874
KY100872
KY100876
KY100878
S. ajacis
CBS 177.93*
GU238168
GU237791
KT389673
GU237673
S. andigena
CBS 269.80
GU238170
GU237817
–
GU237675
CBS 101.80
GU238169
GU237714
–
GU237674
S. artemisiicola
S. astragali
CBS 102636
CBS 178.25
GU238171
GU238172
GU237728
GU237792
KT389674
–
GU237676
GU237677
S. caricae
CBS 248.90
GU238175
GU237807
–
GU237680
CBS 282.76
GU238177
GU237821
–
GU237682
CBS 500.63
GU238190
GU237871
–
GU237695
CBS 137.96
GU238191
GU237783
–
GU237696
S. crystalliniformis
CBS 713.85*
GU238178
GU237903
KT389675
GU237683
S. cucurbitacearum
CBS 133.96
GU238181
GU237780
KT389676
GU237686
S. dennisii
CBS 631.68*
GU238182
GU237899
KT389677
GU237687
S. ailanthicola
S. chrysanthemi
GU237671
S. dorenboschii
CBS 426.90*
GU238185
GU237862
KT389678
GU237690
S. helianthi
CBS 200.87*
KT389761
KT389545
KT389683
KT389848
S. heliopsidis
CBS 109182
GU238186
GU237747
KT389679
GU237691
S. hortensis
CBS 104.42
GU238198
GU237730
KT389680
GU237703
CBS 572.85
GU238199
GU237893
KT389681
GU237704
S. inoxydabilis
CBS 425.90*
GU238188
GU237861
KT389682
GU237693
S. loticola
S. lupini
CBS 562.81*
CBS 101494*
GU238192
GU238194
GU237890
GU237724
KT389684
KT389685
GU237697
GU237699
S. oculohominis
CBS 634.92*
GU238196
GU237901
KT389686
GU237701
S. pini
MFLUCC 18-1549*
MK348019
MK347800
MK434860
–
S. rudbeckiae
CBS 109180
GU238197
GU237745
–
GU237702
S. tanaceti
CBS 131484*
JQ897461
NR_111724
–
JQ897496
S. trachelii
CBS 379.71
GU238173
GU237850
KT389687
GU237678
CBS 384.68
GU238174
GU237856
–
GU237679
–
S. valerianellae
123
CBS 273.92
GU238200
GU237819
CBS 329.67*
GU238201
GU237832
GU237705
GU237706
Fungal Diversity
Table 22 GenBank accession
numbers of Verticillium isolates
included in this study
Taxa
Strains
Verticillium albo-atrum
V. alfalfa
ACT
tef1
GPD
TS
PD747
JN188144
JN188272
JN188208
JN188080
PD489
JN188097
JN188225
JN188161
JN188033
V. dahlia
PD322
HQ206921
HQ414624
HQ414719
HQ414909
V. isaacii
PD660
HQ206985
HQ414688
HQ414783
HQ414973
V. klebahnii
PD401
JN188093
JN188221
JN188157
JN188029
V. longisporum
PD348
a1
HQ206930
HQ414633
HQ414728
HQ414918
V. longisporum
PD348
d1
HQ206931
HQ414634
HQ414729
HQ414919
V. longisporum
PD356
a1
HQ206934
HQ414637
HQ414732
HQ414922
V. longisporum
PD356
d2
HQ206935
HQ414638
HQ414733
HQ414923
V. longisporum
PD687
a1
HQ206993
HQ414696
HQ414791
HQ414981
V. longisporum
PD687
d2
HQ206994
HQ414697
HQ414792
HQ414982
V. nonalfalfae
PD592
JN188099
JN188227
JN188163
JN188035
V. nubilum
PD742
JN188139
JN188267
JN188203
JN188075
V. tricorpus
PD690
JN188121
JN188249
JN188185
JN188057
V. zaregamsianum
PD736
JN188133
JN188261
JN188197
JN188069
Acknowledgements This work was funded by the grants of the project of National Natural Science Foundation of China (No.
31560489), Talent project of Guizhou science and technology cooperation platform ([2017]5788-5) and Guizhou science, technology
department international cooperation base project ([2018]5806).
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’’
(Grant No. DBG6080013), Thailand Research Fund (TRF) grant no
RSA5980068 entitled Biodiversity, phylogeny and role of fungal
endophytes on above parts of Rhizophora apiculata and Nypa fruticans and‘‘Impact of climate change on fungal diversity and biogeography in the Greater Mekong Subregion’’ (RDG6130001).
Rajesh Jeewon would like to thank Mae Fah Luang University and the
University of Mauritius for research support. Alan J.L. Phillips
acknowledges the support from Biosystems and Integrative Sciences
Institute (BioISI, FCT/UID/ Multi/04046/2013).
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