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Epitycation of Perisporiopsis struthanthi and Perisporiopsis lantanae,
and the taxonomic implications for Perisporiopsidaceae, Perisporiopsis
and Setophoma
Bruno W. Ferreira
Universidade Federal de Viçosa Departamento de Fitopatologia: Universidade Federal de Vicosa Departamento de Fitopatologia
Debora C Guterres
Universidade Federal de Viçosa Departamento de Fitopatologia: Universidade Federal de Vicosa Departamento de Fitopatologia
Davi M. Macedo
Universidade Federal de Viçosa Departamento de Fitopatologia: Universidade Federal de Vicosa Departamento de Fitopatologia
Robert Barreto ( rbarreto@ufv.br )
Universidade Federal de Viçosa Departamento de Fitopatologia: Universidade Federal de Vicosa Departamento de Fitopatologia
https://orcid.org/0000-0001-8920-4760
Research Article
Keywords: Multi-gene phylogeny, New taxa, Phaeosphaeriaceae, Pyrenochaetopsidaceae, Reappraisal, Taxonomy; three new genera; Nine new
combinations
Posted Date: August 4th, 2023
DOI: https://doi.org/10.21203/rs.3.rs-2851628/v1
License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License
Page 2/32
Abstract
Perisporiopsidaceae
includes species with supercial ascomata seated on a subiculum, and ellipsoidal oblong, one or more septate, hyaline
ascospores. Taxonomy of species in this family has been based, mainly, on morphological characters and host/substrate associations. There is
limited information about the taxonomic placement of
Perisporiopsidaceae
within the
Dothideomycetes
. Here, an assessment of the phylogenetic
position of the
Perisporiopsidaceae
was conducted based on a multilocus phylogenetic analysis of sequence data obtained from fresh material
of the type species of
Periosporiopsis
–
Perisporiopsis struthanthi
. An epitype is designated here. In addition, novel specimens and pure cultures
of
Perisporiopsis lantanae
were also obtained, inclusive from the type locality and subjected to molecular analysis. Additionally the status of
Perisporiopsis lateritia
was investigated.
Perisporiopsis struthanthi
and
P. lantanae
were found to belong to a clade within the
Phaeosphaeriaceae
.
Perisporiopsis struthanthi
grouped with
Setophoma
spp. and
P. lantanae
isolates formed a separate clade within
Phaeosphaeriaceae
. There was, nevertheless, no morphology-based indication of a connection between
Perisporiopsis
and
Setophoma.
The
members of
Setophoma
spp. that are closer to
Perisporiopsis struthanthi
(
Setophoma sacchari, S. pseudosacchari, S. vernoniae, S. chromolaenae,
S. antiqua
, and
S. endophytica
) are combined herein into
Perisporiopsis
as,
P. antiqua, P. chromolaenae, P. endophytica, P. pseudosacchari, P.
sacchari
, and
P. vernoniae
,). Additionally,
Setophoma
is splited into three genera:
Setophoma stricto
sensus (including the type species
Setophoma terrestris, S. brachypodii
, and
S. poaceicola
),
Pseudosetophoma
(type
Pseudosetophoma yunnanensis
, and with
P. yingyisheniae)
, and
Troglophoma
(type
Troglophoma caverna
, and with
T. longinqua
).
Perisporiopsis lateritia
grouped in the family
Pyrenochaetopsidaceae
,
Perisporiopsidaceae
is merged into
Phaeosphaeriaceae
, a family having nomenclatural priority over
Perisporiopsidaceae
. A new genus and
combination are proposed to accommodate
P. lantanae
, namely
Sputnikia
and
Sputnikia lantanae
whereas
P. lateritia
is combined to
Pyrenochaetopsis lateritia
. Other species and genera in
Perisporiopsidaceae
should be regarded as
Incertae sedis
, until specimens are recollected
and epitypes designated, or DNA sequences obtained from the type specimens and a molecular phylogenetic study claries their taxonomic
position.
Introduction
The family
Parodiopsidaceae
was invalidly introduced by Arnaud (1920) to accommodate the genera
Parodiopsis
,
Perisporiopsis
, and
Perisporina
, based mainly on their morphological similarity and equivalent habit, namely occurrence on leaf surfaces forming supercial
ascomata over a subiculum.
Parodiopsis
, then accepted as the type genus of Parodiopsidaceae, was considered a late synonym of
Perisporiopsis
(Arnaud, 1915). Therefore,
Perisporiopsis
became the type genus of the family (Hennings 1904). The name
Perisporiopsidaceae
was invalidly
introduced by Müller and von Arx (1962) who proposed to merge the families
Parodiellinaceae
and
Parodiopsidaceae
. Much later,
Perisporiopsidaceae
was validated and received a Latin diagnosis with
Parodiopsidaceae
interpreted as its synonym. Although
Parodiopsidaceae
was an earlier name,
Perisporiopsidaceae
was prioritized, since the type of
Parodiopsidaceae
belongs to
Perisporiopsis
(Kirschner et al., 2010)
Perisporiopsidaceae
includes species forming colonies on living leaves, having globose-pigmented ascomata developed over a subiculum and
producing ellipsoidal oblong, hyaline ascospores with one or more septa (Hyde et al., 2013). Several genera were included in this family, including
appressorial (hyphal hyphopodia)-forming fungi such as
Alina
,
Balladyna
, and
Balladynopsis
. (Barr, 1997; Sivanesan, 1981, 1984; Lumbsch and
Huhndorf, 2010; Hyde, 2013). However, later publications only accept ve genera as belonging to
Perisporiopsidaceae
, namely:
Asteronia,
Byssocallis, Chevalieropsis, Parodiellina
, and
Perisporiopsis
(Boonmee et al., 2017; Wijayawardene et al., 2018; Pem et al., 2019; Hongsanan et al.,
2020).
The asexual state of most genera in
Perisporiopsidaceae
are “
Septoidium
-like” hyphomycetes producing simple conidiophores, with monoblastic,
annellidic, or sympodial conidiogenous cells, producing pigmented and septate conidia (Sivanesan, 1984; Kirschner et al., 2010). An exception is
Perisporiopsis lantanae
, which was described as having a pycnidial asexual state (Barreto et al., 1995). The placement of the fungus found on the
weedy
Verbenaceae Lantana camara
in
Perisporiopsis
was regarded as an inadequate and provisional by RWB, who expected for an opportunity
to recollect and re-examine this fungus with modern tools, which were unavailable at the time of its discovery.
Since the early introduction of the family under the name
Parodiopsidaceae
by Arnaud (1920), it has been compared with several families and
orders (Arnaud, 1921; Hansford, 1946; Luttrell, 1951, 1955; von Arx and Müller, 1975; Barr, 1976, 1979, 1987; Sivanesan, 1984; Chaverri and Gazis,
2011; Hyde et al., 2013; Boonmee et al., 2017). Hyde et al. (2013) conjectured that
Perisporiopsidaceae
might be polyphyletic based on the
morphology of its genera. Sivanesan (1984) considered that
Perisporiopsis
might be taxonomically related to the
Leptosphaeriaceae
. To date, no
phylogenetic study has been performed to elucidate the taxonomic position of the
Perisporiopsidaceae
. This is not surprising. Fungi in
Perisporiopsidaceae
are mostly poorly known taxa which have been collected, often only once, and described from the tropics in the late 19th and
early 20th Centuries. Molecular data is available only for putative strains of an endophytic
Perisporiopsis
(Chaverri and Gazis, 2011). Sequences
from the type species of
Perisporiopsis
, were not available until the present work.
Here, we provide the results of the analysis of two species placed in
Perisporiopsis
which were recollected from their type localities in Brazil. The
information, provided here, allows for the initiation of a reappraisal of the
Perisporiopsidaceae
.
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Materials and methods
Sample collection processing and observation of fungus morphology
Samples of leaves of
Struthanthus
sp. – Loranthaceae (local name in Brazil ‘erva-de-passarinho’) and
Lantana camara
– Verbenaceae (local
name in Brazil ‘cambará’), bearing dark epiphyllous fungal colonies, were collected in the state of Rio de Janeiro, Brazil. These were screened
under a stereomicroscope and selected leaves bearing sporulating colonies of the fungi were dried in a plant press. Fungal structures were
scraped from the leaf surfaces with a scalpel and mounted in lactophenol and lactofuchsin. Observations were made with an Olympus BX53
tted with differential contrast illumination and equipped with a digital capture system Olympus Q-Color 3 (Olympus, Tokyo, Japan.
Representative specimens were deposited in the local herbarium (Herbarium Universidade Federal de Viçosa, VIC). Samples of dried material
containing fungal structures were mounted on stubs with double-sided adhesive tape, dried for four days in desiccator, and gold coated using a
Balzer’s FDU 010 sputter coater. A LEO VP 1430 (Carl-Zeiss, Oberkochen, Germany) scanning electron microscope (SEM) was used to analyze the
samples and generate images.
Leaf fragments bearing ascomata were glued to the underside of Petri plate lids, over a layer of tap water-agar. The plates were kept at 25°C, with
the ascomata facing the culture medium. Twelve hours later, single ascospores ejected onto the culture medium were transferred with a sterile
ne-pointed needle to other Petri dishes containing either potato dextrose-agar (PDA) or potato carrot-agar (PCA), and maintained at 25°C under a
12 hours daily / light regime (light provided by two white and one near-UV lamps placed 35 cm above the plates). Cultures of the fungus from
L.
camara
were obtained and described based on the observation of 30-day-old colonies. The color terminology followed Rayner (1970). No colonies
were obtained from the
Struthanthus
sp. samples.
Pure cultures of
P. lantanae
were deposited in the culture collection of the Universidade Federal de Viçosa – Coleção Octávio de Almeida Drumond
(COAD).
DNA extraction and PCR amplication
DNA extraction from
P. struthanthi
was performed according to Guatimosim et. al. (2015). In order to obtain representative DNA of the fungus,
inated/fertile fresh perithecia were examined under a stereomicroscope to check for possible colonization by fungicolous fungi. Fifty clean
perithecia were removed from the leaf surface with the aid of a ne needle and placed into a microcentrifuge tube (1.5 ml) containing 5 µl of
double distilled water and stored at -20°C for later use. For
P. lantanae
, the fungus was grown in PDA under a 12 h daily light regime for two
weeks. Approximately 50 mg of mycelium was scraped from the surface of the colonized medium and placed inside sterile plastic tubes
containing zirconium spheres and placed in a grinder (L-Beader-3, Loccus Biotecnologia, Cotia, Brazil). After 30 s grinding, the resulting
suspension was drained into a sterile plastic tube and used for DNA extraction. Genomic DNA was extracted for both fungi by using Wizard
Genomic DNA Purication Kit (Promega Corporation, WI, USA) following the manufacturer’s instructions and the additional steps described by
Pinho et al. (2012).
The large subunit of the nc 28S rDNA (LSU), the nc 18S rDNA (SSU), the and internal transcribed spacer (ITS) regions from each fungus included
in the study were amplied and sequenced with the primers LSU1Fd (Crous et al., 2009) and LR5 (Vilgalys and Hester, 1990), NS1/NS4 (Vilgalys
et al., 1990) and ITS1/ITS4 (White et al., 1990), respectively. The primer pairs EF1-983F/EF1-2218R (Rehner, 2001), fRPB2-5F/fRPB2-7cR (Liu et
al., 1999), and Btub2Fd/Btub4Rd (Woudenberg et al., 2009) were used in the attempt to amplify the coding regions of translation elongation
factor 1-alpha (
EF1
), the DNA-dependent RNA Polymerase second largest subunit (
RPB2
), and β-tubulin (
TUB
), respectively.
PCR amplications were performed in a total volume of 12.5 µL containing 10–20 ng of template DNA, 1× PCR buffer, 0.63 µL DMSO (99.9%), 1.5
mM MgCl2, 0.5 µM of each primer, 0.25 mM of each dNTP, 1.0 U BioTaq DNA polymerase (Bioline GmbH, Luckenwalde, Germany). Conditions for
PCR amplication of LSU, SSU,
EF1, RPB2
, and
TUB
consisted of an initial denaturation step of 5 min at 94 ºC followed by 35 cycles of 30 s at 94
ºC, 30 s at the appropriate annealing temperature (48 ºC for LSU, 52ºC for SSU, 55 ºC for
EF1, RPB2
, and
TUB
) and 90 s at 72 ºC. The PCR
conditions to amplify the ITS followed 40 cycles of 30 s at 94 ºC, 30 s at 58 ºC and 45 s at 72 ºC for ITS. The amplicons were analyzed on 0.8%
agarose electrophoresis gels stained with GelRed (Biotium, San Francisco, USA) in a 1× TAE buffer and visualized under UV light to check for
amplication size and purity. Each sample of PCR products were treated with 2 µL of ExoSAP-IT (Applied Biosystems by ThermoFisher Scientic,
Foster City, USA) according to the manufacturer’s instructions and sequenced by Macrogen (Seoul, South Korea).
Phylogenetic analysis
The DNA sequences generated in this study were aligned, assembled, and edited using DNA Dragon software (Sequentix, Germany). Sequences
obtained from GenBank (www.ncbi.nlm.nih.gov) and the novel consensus sequences were imported into MEGA v. 6 (Tamura et al., 2013) for
initial alignment and the construction of sequence datasets (Table1).
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Table 1
Taxa used in the phylogenetic analysis and GenBank accession numbers.
Species Culture
accession
number
GenBank accession numbers References
LSU ITS
TUB RPB2 EF1
Acericola italica
MFLUCC
13–0609* MF167429 MF167428 – – – Phookamsak et al. (2017)
Allocucurbitaria
botulispora
CBS
142452* LN907416 LT592932 LT593001 LT593070 – Valenzuela-Lopez et al.
(2018)
Allophaeosphaeria
muriformia
MFLUCC
13–0349* KP765681 KP765680 – – – Liu et al. (2015)
Allophaeosphaeria
subcylindrospora
MFLUCC
13–0380 KT314183 KT314184 – – – Liu et al. (2015)
Amarenomyces
ammophilae
CBS
114595* GU301859 KF766146 – – – Slippers et al. (2013)
Ampelomyces
quisqualis
CBS 129.79* EU754128 HQ108038 – – – De Gruyter et al. (2009)
Bhatiellae rosae
MFLUCC
17–0664* MG828989 MG828873 – – – Wanasinghe et al. (2018)
Camarosporioides
phragmitis
MFLUCC
13–0365* KX572345 KX572340 – – – Phookamsak et al. (2017)
Chaetosphaeronema
achilleae
MFLUCC
16–0476 KX765266 KX765265 – – – Hyde et al. (2016)
Chaetosphaeronema
hispidulum
CBS 216.75* KF251652 KF251148 – – – Quaedvlieg et al. (2013)
Coniothyrium carteri
CBS 105.91 KF251712 KF251209 – – – Quaedvlieg et al. (2013)
Cucurbitaria berberidis
MFLUCC
11–0387 KC506796 – – – – Valenzuela-Lopez et al.
(2018)
CBS
130007* KC506793 LT717673 LT717676 LT854936 – Valenzuela-Lopez et al.
(2018)
Dactylidina dactylidis
MFLUCC
14–0966* MG829002 MG828886 – – – Wanasinghe et al. (2018)
Dematiopleospora
mariae
MFLUCC
13–0612* KJ749653 KJ749654 – – – Wanasinghe et al. (2014)
Dematiopleospora
rosicola
MFLU 16–
0232 MG829006 MG828888 – – – Wanasinghe et al. (2018)
Dematiopleospora
salsolae
MFLUCC
17–0828 MG829007 MG828889 – – – Wanasinghe et al. (2018)
Didymocyrtis
consimilis
Gardiennet
12041* KT383796 KT383813 – – – Ertz et al. (2015)
Didymocyrtis
ramalinae
Ertz 16399 KT383802 KT383838 – – – Ertz et al. (2015)
Didymocyrtis
xanthomendozae
CBS 129666 JQ238634 KP170651 – – – Lawrey et al.
(2012);Trakunyingcharoen
et al. (2014)
Embarria clematidis
MFLUCC
14–0976* MG828987 MG828871 – – – Wanasinghe et al. (2018)
Equiseticola fusispora
MFLUCC
14–0522* KU987669 KU987668 – – – Abd-Elsalam et al. (2016)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 5/32
Species Culture
accession
number
GenBank accession numbers References
Galiicola
pseudophaeosphaeria
MFLUCC
14–0524* KT326693 KT326692 – – – Ariyawansa et al. (2015)
Hawksworthiana
alliariae
MFLUCC
13–0070* KX494877 KX494876 – – – Wanasinghe et al. (2018)
Hawksworthiana
clematidicola
MFLUCC
14–0910 MG829011 MG828901 – – – Wanasinghe et al. (2018)
Italica achilleae
MFLUCC
14–0959 MG829013 MG828903 – – – Wanasinghe et al. (2018)
Juncaceicola achilleae
MFLUCC
13–0606 KX449526 KX449525 – – – Tennakoon et al. (2016)
Juncaceicola luzulae
MFLUCC
16–0780* KX449530 KX449529 – – – Tennakoon et al. (2016)
Juncaceicola
typharum
CBS 296.54 KF251695 KF251192 – – – Quaedvlieg et al. (2013)
Leptospora galii
KUMCC 15–
0521 KX599548 KX599547 – – – Phookamsak et al. (2017)
Leptospora rubella
CPC 11006* DQ195792 DQ195780 – – – Crous et al. (2006)
Loratospora aestuarii
JK 5535B* GU301838 – – – – Schoch et al. (2009)
Melnikia anthoxanthii
MFLUCC 14-
1010* KU848204 – – – – Wijayawardene et al.
(2016)
Muriphaeosphaeria
galatellae
MFLUCC
14–0614* KT438329 KT438333 – – – Phukhamsakda et al.
(2015)
Neocamarosporium
betae
CBS 109410 EU754178 KY940790 – GU371774 – Valenzuela-Lopez et al.
(2018)
CBS 523.66 EU754179 FJ426981 KT389842 KT389670 – Valenzuela-Lopez et al.
(2018)
Neocamarosporium
calvescens
CBS 246.79 EU754131 KY940774 – KC584500 – Valenzuela-Lopez et al.
(2018)
Neocamarosporium
goegapense
CBS
138008* KJ869220 KJ869163 – – – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria
aquatica
CBS 297.74* EU754177 LT623221 LT623238 LT623278 – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria cava
CBS 115979 EU754198 AY853248 LT623234 LT623273 – Valenzuela-Lopez et al.
(2018)
CBS 257.68* EU754199 JF740260 KT389844 LT717681 – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria
hakeae
CBS
142109* KY173526 KY173436 KY173613 KY173593 – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria
irregularis
CBS
142791* LN907372 LT592916 LT592985 LT593054 – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria
keratinophila
CBS
121759* LT623215 EU885415 LT623236 LT623275 – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria
quercina
CBS
115095* GQ387619 LT623220 LT623237 LT623277 – Valenzuela-Lopez et al.
(2018)
Neocucurbitaria
unguis-hominis
UTHSC:DI16-
213; FMR
13703
LN907356 LT592910 LT592979 LT593048 – Valenzuela-Lopez et al.
(2018)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 6/32
Species Culture
accession
number
GenBank accession numbers References
CBS 111112 GQ387623 LT623222 LT623239 LT623279 – Valenzuela-Lopez et al.
(2018)
CBS 112.79 GQ387622 LT717672 LT717675 LT717682 – Valenzuela-Lopez et al.
(2018)
Neopyrenochaeta
acicola
CBS 812.95* GQ387602 LT623218 LT623232 LT623271 – Valenzuela-Lopez et al.
(2018)
N. fragariae
CBS
101634* GQ387603 LT623217 LT623231 LT623270 – Valenzuela-Lopez et al.
(2018)
N. inorescentiae
CBS
119222* EU552153 EU552153 LT623233 LT623272 – Valenzuela-Lopez et al.
(2018)
N. telephoni
CBS
139022* KM516290 KM516291 LT717678 LT717685 – Valenzuela-Lopez et al.
(2018)
Neopyrenochaetopsis
hominis
CBS
143033* LN907381 LT592923 LT592992 LT593061 – Valenzuela-Lopez et al.
(2018)
Neosetophoma
samarorum
CBS 138.96* KF251664 KF251160 – – – Quaedvlieg et al. (2013)
Neostagonospora
caricis
CBS
135092* KF251667 KF251163 – – – Quaedvlieg et al. (2013)
Neostagonospora
elegiae
CBS 135101 KF251668 KF251164 – – – Quaedvlieg et al. (2013)
Neostagonospora
spinicis
FU30120 KP676046 KP676045 – – – Yang et al. (2016)
Neosulcatispora
agaves
CPC 26407* KT950867 KT950853 – – – Crous et al. (2015)
Nodulosphaeria hirta
MFLUCC
13–0867* KU708845 KU708849 – – – Mapook et al. (2016)
Nodulosphaeria
scabiosae
MFLUCC 14-
1111 KU708846 KU708850 – – – Mapook et al. (2016)
Ophiobolopsis italica
MFLUCC 17-
1791* MG520959 MG520939 – – – Phookamsak et al. (2017)
Ophiobolus artemisiae
MFLUCC 14-
1156 KT315509 KT315508 – – – Ariyawansa et al. (2015)
Ophiobolus
disseminans
MFLUCC 17-
1787* MG520961 MG520941 – – – Phookamsak et al. (2017)
Ophiobolus senecionis
MFLUCC
13–0575 KT728366 KT728365 – – – Tibpromma et al. (2015)
Ophiosimulans
tanaceti
MFLUCC
14–0525* KU738891 KU738890 – – – Tibpromma et al. (2016)
Ophiosphaerella
aquaticus
MFLUCC
14–0033 KX767089 KX767088 – – – Ariyawansa et al. (2015)
Paracucurbitaria
italica
CBS 234.92* EU754176 LT623219 LT623235 LT623274 – Valenzuela-Lopez et al.
(2018)
Paracucurbitaria corni
CBS 248.79 GQ387608 LT903672 LT900365 LT903673 – Valenzuela-Lopez et al.
(2018)
Paraophiobolus
arundinis
MFLUCC 17-
1789* MG520965 MG520945 – – – Phookamsak et al. (2017)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 7/32
Species Culture
accession
number
GenBank accession numbers References
Paraophiobolus
plantaginis
MFLUCC
17–0245 KY815010 KY797641 – – – Phookamsak et al. (2017)
Paraphoma
chlamydocopiosa
UMPc01 – KU999072 – – – Moslemi et al. (2018)
Paraphoma
chrysanthemicola
CBS 172.70 KF251669 KF251165 – – – Quaedvlieg et al. (2013)
Paraphoma pye
UMPp02 – KU999073 – – – Moslemi et al. (2018)
Paraphoma radicina
CBS
102875* KF251677 KF251173 – – – Quaedvlieg et al. (2013)
Paraphoma
rhaphiolepidis
CBS 142524 KY979813 KY979758 – – – Crous et al. (2017)
Paraphoma vinacea
UMPV001 KU176888 KU176884 – – – Moslemi et al. (2018)
Parastagonospora
allouniseptata
MFLUCC
13–0386 KU058721 KU058711 – – – Li et al. (2015)
Parastagonospora
caricis
CBS 135671 KF251680 KF251176 – – – Quaedvlieg et al. (2013)
Parastagonospora
dactylidis
MFLUCC
13–0375 KU058722 KU058712 – – – Li et al. (2015)
Parastagonospora
italica
MFLUCC
13–0377 KU058724 KU058714 – – – Li et al. (2015)
Parastagonospora
minima
MFLUCC
13–0376 KU058723 KU058713 – – – Li et al. (2015)
Parastagonospora
nodorum
CBS
110109* KF251681 KF251177 – – – Quaedvlieg et al. (2013)
Parastagonospora
poagena
CBS 136776 KJ869174 KJ869116 – – – Crous et al. (2014)
Parastagonospora
uniseptata
MFLUCC
13–0387 KU058725 KU058715 – – – Li et al. (2015)
Parastagonosporella
fallopiae
CBS
135981* MH460545 MH460543 – – – Thambugala et al. (2017)
Parastagonosporella
fallopiae
CCTU
1151.1 MH460546 MH460544 – – – Quaedvlieg et al. (2013)
Perisporiopsis
struthanthi VIC47339 OQ191781 OQ191785 – – – this study
VIC47340 OQ191782 OQ191786 – – – this study
Phaeopoacea
festucae
MFLUCC
17–0056* KY824767 KY824766 – – – Quaedvlieg et al. (2013)
Phaeosphaeria oryzae
CBS
110110* KF251689 KF251186 – – – Quaedvlieg et al. (2013)
Phaeosphaeria
papayae
CBS 135416 KF251690 KF251187 – – – Li et al. (2015)
Phaeosphaeriopsis
glaucopunctata
CBS 653.86* KF251702 KF251199 – – – Thambugala et al. (2017)
Poaceicola arundinis
MFLUCC
15–0702* KU058726 KU058716 – – – Ariyawansa et al. (2015)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 8/32
Species Culture
accession
number
GenBank accession numbers References
Poaceicola italica
MFLUCC
13–0267 KX910094 KX926421 – – – Phookamsak et al. (2017)
Populocrescentia
forlicesenensis
MFLUCC
15–0651* KT306952 KT306948 – – – Phookamsak et al. (2017)
Pseudoophiobolus
achilleae
MFLU 17–
0925 MG520966 MG520946 – – – Hyde et al. (2016)
Pseudoophiobolus
mathieui
MFLUCC 17-
1784* MG520969 MG520949 – – – Crous et al. (2012)
Pseudophaeosphaeria
rubi
MFLUCC
14–0259* KX765299 KX765298 – – – Wanasinghe et al. (2018)
Pseudopyrenochaeta
lycopersici
CBS 306.65* EU754205 NR_103581 LT717674 LT717680 – Valenzuela-Lopez et al.
(2018)
Pseudopyrenochaeta
terretris
CBS 282.72* LT623216 LT623228 LT623246 LT623287 – Valenzuela-Lopez et al.
(2018)
Pyrenochaeta nobilis
CBS 407.76* EU754206 EU930011 KT389845 LT623276 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
americana
UTHSC:DI16-
225; FMR
13715
LN907368 LT592912 LT592981 LT593050 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
botulispora
UTHSC:DI16-
289; FMR
13781
LN907432 LT592941 LT593010 LT593080 – Valenzuela-Lopez et al.
(2018)
UTHSC:DI16-
297; FMR
13790
LN907440 LT592945 LT593014 LT593084 – Valenzuela-Lopez et al.
(2018)
CBS
142458* LN907441 LT592946 LT593015 LT593085 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
conuens
CBS
142459* LN907446 LT592950 LT593019 LT593089 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
decipiens
CBS 343.85* GQ387624 LT623223 LT623240 LT623280 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
globosa
CBS
143034* LN907418 LT592934 LT593003 LT593072 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
indica
CBS
124454* GQ387626 LT623224 LT623241 LT623281 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
leptospora
CBS
101635* GQ387627 JF740262 LT623242 LT623282 – Valenzuela-Lopez et al.
(2018)
CBS 122787 EU754151 LT623225 LT623243 LT623283 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
microspora
UTHSC:DI16-
198; FMR
13688
LN907341 LT592899 LT592968 LT593037 – Valenzuela-Lopez et al.
(2018)
CBS
102876* GQ387631 LT623226 LT623244 LT623284 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
paucisetosa
CBS
142460* LN907336 LT592897 LT592966 LT593035 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
poae
CBS
136769* KJ869175 KJ869117 KJ869243 LT623286 – Valenzuela-Lopez et al.
(2018)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 9/32
Species Culture
accession
number
GenBank accession numbers References
Pyrenochaetopsis
setosissima
CBS
119739* GQ387632 LT623227 LT623245 LT623285 – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
tabarestanensis
CBS
139506* KF803343 KF730241 KX789523 – – Valenzuela-Lopez et al.
(2018)
Pyrenochaetopsis
uberiformis
CBS
142461* LN907420 LT592935 LT593004 LT593074 – Valenzuela-Lopez et al.
(2018)
Sclerostagonospora
opuntiae
CBS 118224 JX517293 JX517284 – – – Wijayawardene et al.
(2013)
Sclerostagonospora
rosicola
MFLUCC
15–0129 MG829068 MG828957 – – – Li et al. (2015)
Scolicosporium
minkeviciusii
MFLUCC
12–0089 KF366382 – – – – Crous et al. (2015)
Septoriella allojunci
MFLUCC
15–0701 KU058728 KU058718 – – –
Septoriella phragmitis
CPC 24118* KR873279 KR873251 – – –
Setomelanomma
holmii
CBS
110217* GU301871 KT389542 – – – Schoch et al. (2009); Chen
et al. (2015)
Didymella pinodella
CBS 531.66 GU238017 FJ427052 FJ427162 – MK525067 Liu et al. (2019)
Setophoma antiqua
LC6594 MK511947 MK511909 MK524999 – MK525070 Liu et al. (2019)
LC6595 MK511948 MK511910 MK525000 – MK525071 Liu et al. (2019)
CGMCC
3.19525 =
LC6596*
– MK511911 MK525001 – MK525072 Liu et al. (2019)
Setophoma
brachypodii
CBS
145418* – MK539968 – – MK540161 Marin-Felix et al. (2019)
Setophoma caverna
LC12481 – MK511927 MK525016 – MK525088 Liu et al. (2019)
LC12842 – MK511928 MK525017 – MK525089 Liu et al. (2019)
CGMCC
3.19526 =
LC7511
MK511965 MK511944 MK525032 – MK525105 Liu et al. (2019)
Setophoma
chromolaenae
CBS
135105* KF251747 KF251244 KF252728 – KF253195 Quaedvlieg et al. (2013)
Setophoma
endophytica
LC13538 – MK511923 MK525012 – MK525084 Liu et al. (2019)
LF2067 – MK511924 MK525013 – MK525085 Liu et al. (2019)
CGMCC
3.19528 =
LC3163*
MK511956 MK511931 MK525020 – MK525092 Liu et al. (2019)
LC3164 MK511957 MK511932 MK525021 – MK525093 Liu et al. (2019)
LC3165 – MK511933 MK525022 – MK525094 Liu et al. (2019)
LC3216 MK511959 MK511938 MK525026 – MK525099 Liu et al. (2019)
LC3297 MK511962 MK511941 MK525029 – MK525102 Liu et al. (2019)
Setophoma longinqua
CGMCC
3.19524 =
LC6593*
MK511946 MK511908 MK524998 – MK525069 Liu et al. (2019)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 10/32
Species Culture
accession
number
GenBank accession numbers References
LC13481 – MK511925 MK525014 – MK525086 Liu et al. (2019)
LC13482 – MK511926 MK525015 – MK525087 Liu et al. (2019)
Setophoma
pseudosacchari
CBS
145373* – MK539969 MK540176 – – Marin-Felix et al. (2019)
Setophoma sacchari
CBS 333.39* – KF251245 – – – Quaedvlieg et al. (2013)
LC12842 – MK511928 MK525017 – MK525089 Liu et al. (2019)
Setophoma terrestris
CBS
135470* KF251739 KF251236 – Quaedvlieg et al. (2013)
CBS 335.29
= MUCL
9892 =
LC6449*
KF251749 KF251246 KF252729 – KF253196 Quaedvlieg et al. (2013)
CBS 335.87 KF251750 KF251247 KF252730 – KF253197 Liu et al. (2019)
CBS 377.52 KF251751 KF251248 KF252731 – KF253198 Liu et al. (2019)
Setophoma vervoniae
CBS
137988* – KJ869141 MK540177 – MK540162 Crous et al. (2014)
Setophoma
yingyisheniae
LC6739 – MK511912 MK525002 – MK525073 Liu et al. (2019)
LC12696 MK511950 MK511914 – – MK525075 Liu et al. (2019)
LC12699 MK511951 MK511915 MK525004 – MK525076 Liu et al. (2019)
LC13477 MK511952 MK511916 MK525005 – MK525077 Liu et al. (2019)
LC13478 – MK511917 MK525006 – MK525078 Liu et al. (2019)
CGMCC
3.19527 =
LC13479*
– MK511918 MK525007 – MK525079 Liu et al. (2019)
Setophoma
yunnanensis
LC6532 MK511945 MK511907 MK524997 – MK525068 Liu et al. (2019)
CGMCC
3.19529 =
LC6753*
MK511949 MK511913 MK525003 – MK525074 Liu et al. (2019)
Sputnikia lantanae,
comb. nov VIC 49395
COAD 3538
OQ191783 OQ191787 – – – this study
VIC 49396
COAD 3541
OQ191784 OQ191788 – – – this study
Sulcispora
pleurospora
MFLUCC
14–0995* KP271444 KP271443 – – – Tibpromma et al. (2015)
Tintelnotia
destructans
CBS 127737 KY090664 KY090652 – – – Ahmed et al. (2017)
Tintelnotia opuntiae
CBS 376.91* GU238123 KY090651 – – – Ahmed et al. (2017)
Vagicola
chlamydospora
MFLUCC
15–0177 KU163654 KU163658 – – – Jayasiri et al. (2015)
Vagicola vagans
CBS 604.86* KF251696 KF251193 – – – Quaedvlieg et al. (2013)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
Page 11/32
Species Culture
accession
number
GenBank accession numbers References
Vrystaatia aloeicola
CBS
135107* KF251781 KF251278 – – – Quaedvlieg et al. (2013)
Wojnowicia lonicerae
MFLUCC
13–0737 KP684151 KP744471 – – – Liu et al. (2015)
Wojnowicia rosicola
MFLUCC
15–0128 MG829091 MG828979 – – – Wanasinghe et al. (2018)
Wojnowicia spartii
MFLUCC
13–0402 KU058729 KU058719 – – – Li et al. (2015)
Wojnowiciella
eucalypti
CPC 25024* KR476774 KR476741 – – – Crous et al. (2015)
Wojnowiciella viburni
MFLUCC
12–0733 KC594287 KC594286 – – – Wijayawardene et al.
(2013)
Xenoseptoria
neosaccardoi
CBS 120.43 KF251783 KF251280 – – – Quaedvlieg et al. (2013)
Xenoseptoria
neosaccardoi
CBS
128665* KF251784 KF251281 – – – Quaedvlieg et al. (2013)
Xenopyrenochaetopsis
pratorum
CBS 445.81* GU238136 JF740263 KT389846 KT389671 – Valenzuela-Lopez et al.
(2018)
Yunnanensis
phragmitis
MFLUCC 17-
1361* MF684865 MF684869 – – – Karunarathna et al. (2017)
Ex-type strains are indicated with “*” after the collection number. ITS = internal transcribed spacer, LSU = large subunit of the nrDNA,
RPB2
=
polymerase II second largest subunit,
TUB
= β-tubulin,
EF1
= translation elongation factor 1-α
Ex-type strains are indicated with “*” after collection number. ITS = internal transcribed spacer, nc LSU rDNA = large subunit of the nrDNA,
RPB2 = polymerase II second largest subunit, TUB2 = β-tubulin, EF11 = translation elongation factor 1-α
The Bayesian inference analyses were conducted and the best-t evolutionary model was determined by comparing different evolutionary models
via the Akaike information criterion using PAUP v 4.0b10 (Sinauer Associates) and MrModeltest 2.2 (Nylander, 2004). Posterior probabilities were
determined by Markov Chain Monte Carlo sampling (MCMC) in MrBayes v. 3.2.1 (Ronquist et al., 2012). Six simultaneous Markov chains were run
for 10,000,000 generations and trees were sampled every 100th generation, resulting in 10,000 trees. The rst 2,000 trees, representing the burn-in
phase were discarded, whereas the remaining 8,000 trees were used for calculating posterior probabilities. Bayesian posterior probabilities are
presented at the left of each node. The analysis was hosted by CIPRES science gateway portal at San Diego supercomputer center (Miller et al.,
2011). Phylogenetic trees were visualized with the program FigTree v1.3.1 (Rambaut, 2009).
Maximum likelihood (ML) tree was generated with the Nearest-Neighbor-Interchange (NNI) ML heuristic method and the Tamura-Nei Substitution
model as tree inference options in MEGA. The branch stabilities of the phylogenetic tree were assessed by using the bootstrap re-sampling
strategy with 1,000 bootstrap test replicates. The resulting tree topologies using the three methods (ML and BI) were then compared and the
phylogram was edited using Inkscape v 1.2.2 (www.inkscape.org).
Results
Phylogeny
The ITS and LSU amplicons were obtained for two isolates of
P. struthanthi
and two isolates of
P. lantanae
, generating sequences of
approximately 540 and 820 to 920 bp, for ITS and LSU, respectively. The SSU and
EF1
amplicons were obtained only for two isolates of
P.
lantanae
, resulting in consensus sequences of 1040 to 1050 (LSU) and 950 to 960 bp (
EF1
). Consecutive attempts to amplify the coding regions
of
RPB2
and
TUB
were unsuccessful.
Four nal phylogenetic trees were generated in this study. The rst tree revealed the relationship of
P. struthanthi
and
P. lantanae
with other
species and genera in the
Phaeosphaeriaceae
(Fig.1). The alignment for the construction of this tree comprised 96 operational taxonomic units
(OTU’s) as ingroup and one outgroup. The combined matrix consisted of 1,653 characters including alignment gaps (ITS: 708 and LSU: 944). The
number of conserved sites was 1,189 (ITS: 245 and LSU: 944). The number of variable and parsimony uninformative sites was 679 (ITS: 449 and
LSU: 230) and 545 sites were variable and parsimony informative (ITS: 380 and LSU: 165).
Page 12/32
In this analysis,
Perisporiopsis
was found to be polyphyletic, with
Perisporiopsis struthanthi
nested in
Setophoma
with high support (96%/1.00 to
ML and BI, respectively).
Perisporiopsis lantanae
, formed a monophyletic clade distant phylogenetically from
P. struthanthi
and
Setophoma
, near
to
Parastagonosporella fallopiae
. Thus,
P. lantanae
is now found to belong to a genus distinct from
Perisporiopsis
for which a new name is
proposed below, in the taxonomy section.
A second tree was built to study the taxonomic position of
P. struthanthi
, within the
Setophoma
clade (Fig.2). The alignment included sequences
of 35 specimens (Table1), representing many of the known
Setophoma
species, and one outgroup taxon (
Didymella pinodella
). Four gene regions
were used for the study (ITS, LSU,
EF1
, and
TUB
), although only ITS and LSU sequences were obtained for
P. struthanthi
. The combined matrix
consisted of 2,992 characters including alignment gaps (ITS: 612, LSU: 927,
EF1
: 899,
TUB
: 554). The number of conserved sites was 1,923 (ITS:
401, LSU: 848,
EF1
: 320,
TUB
: 354). The number of variable and parsimony uninformative sites was 821 (ITS: 201, LSU: 58,
EF1
: 370,
TUB
: 192)
and 593 sites were variable and parsimony informative (ITS: 158, LSU: 28,
EF1
: 264,
TUB
: 143). The tree containing isolates of various species in
Setophoma
, showed that the two isolates of
P. struthanthi
grouped in a clade together with
Setophoma antiqua
and S.
endophytica
, (0.69 BI and
77% ML). The topology of the tree indicates that the two isolates belong to a species which is phylogenetically distinct from the other species
described in
Setophoma
.
Setophoma terrestis
, the type species of the genus, form a separated lineage from the clade in which
P. struthanthi
belongs.
A third phylogenetic reconstruction was built to explore the relationship of
P. lantanae
with other genera within
Phaeosphaeriaceae
, comprising
the closest 100 species to
P. lantanae
based on previous Blastn searches of each of
P. lantanae
sequences, limited to sequences from RefSeq
database and sequences from types ou ex-types (Supplementary Table1). The concatenated dataset comprises 122 OTUs. The combined matrix
consisted of 3,975 characters including alignment gaps (LSU: 907; ITS: 705; SSU: 1,433;
EF1
: 930). The number of conserved sites was 1,923
(LSU: 720; ITS: 280; SSU: 1,139;
EF1
: 608). The number of variable sites was 821 (LSU: 183; ITS: 410; SSU: 278;
EF1
: 318) and 593 sites were
variable and parsimony informative (LSU: 119; ITS: 326; SSU: 125;
EF1
: 224). The topology of this tree indicates that the two isolates are a
species which are phylogenetically distinct from the other species, and nested within a clade formed by
Megacoelomyces sanchezii, Paraphoma
chrysanthemicola, P. rhaphiolepidis, P. radicina, P. melnikiae, P. salicis, P. meti and Pseudophaeosphaeria rubi
(Fig.3).
Besides
P. struthanthi
and
P. lantanae
, which DNA sequences were rst obtained in the present study, a sequence of ITS from the type of
P. lateritia
was retrieved from GenBank nucleotide database and included in the phylogenetic analyses. BLASTn search using this sequence denoted high
similarity with species belonging in
Pyrenochaetopsidaceae
.Thus, a fourth tree was built to investigate the phylogenetic position of
P. lateritia
(Fig.4). Although there is only one ITS sequence available in GenBank for the type of
P. lateritia
, a multilocus phylogenetic analysis was built with
ITS, LSU,
TUB
, and
RPB2
. The study included isolates in
Pyrenochaetopsidaceae
,
Neopyrenochaetaceae
,
Pseudopyrenochaetaceae
,
Cucurbitariaceae
, and two isolates of
Neocamarosporiaceae
as outgroup. The combined matrix consisted of 3,405 characters including
alignment gaps (ITS: 650; LSU: 1,367;
TUB
: 398;
RPB2
: 990). The number of conserved sites was 2,365 (ITS: 396; LSU: 1,245;
TUB
: 198;
RPB2
:
526). The number of variable and parsimony uninformative sites was 1003 (ITS: 244; LSU: 107;
TUB
: 191;
RPB2
: 461) and 806 sites were variable
and parsimony informative (ITS: 161; LSU: 81;
TUB
: 153;
RPB2
: 411). In this phylogenetic reconstruction,
P. lateritia
belongs to the
Pyrenochaetopsidaceae
, within a group comprising species of
Pyrenochaetopsis
, namely
Py. americana
,
Py. setosissima
,
Py. uberiformis
,
Py.
globosa
, and
Py. Microspora;
therefore, a new combination of
P. lateritia
into
Pyrenochaetopsis
became necessary.
Taxonomy
Phaeosphaeriaceae M.E. Barr, Mycologia 71: 948 (1979)
Mycobank: 81637
≡ Syn. nov.
Perisporiopsidaceae
E. Müll. & Arx ex R. Kirschner & T.A. Hofm.: 238 (2012)
Note
The type genus of
Perisporiopsidaceae
,
Perisporiopsis
, and its type species,
Perisporiopsis struthantii
, were proven here to belong to
Phaeosphaeriaceae
. Other genera currently allocated in
Perisporiopsidaceae
, namely,
Asteronia
(Sacc.) Henn. (1895),
Byssocallis
Syd. (1927),
Chevalieropsis
G. Arnaud (1923), and
Parodiellina
Henn. ex G. Arnaud (1918 [1917]), should be refered as
Dothideomycetes Incertae sedis
until
proper studies including DNA sequences are carried out.
Perisporiopsis Henn., Hedwigia 43: 83 (1904)
Mycobank: 3827
=
Chaetyllis
Clem., in Clements and Shear, Gen. fung., Edn 2 (Minneapolis): 253 (1931)
=
Chrysomyces
Theiss. and Syd., Annls mycol. 15(1/2): 139 (1917)
Page 13/32
=
Cicinnobella
Henn., Hedwigia 43(6): 386 (1904)
=
Diblastospermella
Speg., Boln Acad. nac. Cienc. Córdoba 23(3–4): 579 (1918)
=
Dichothrix
Theiss., Beih. bot. Zbl., Abt. 2 29: 60 (1912)
=
Epiploca
Kleb., Haupt- und Nebenfruchtformen der Ascomyzeten (Leipzig) 1: 167 (1918)
=
Hypoplegma
Theiss. & Syd., Annls mycol. 15(1/2): 135 (1917)
=
Lasiostemma
Theiss., Syd. & P. Syd., in Sydow & Sydow, Annls mycol. 15(3/4): 218 (1917)
=
Lasiostemmella
Petr., Sydowia 4(1–6): 376 (1950)
=
Meliolidium
Speg., Boln Acad. nac. Cienc. Córdoba 26(2–4): 336 (1921)
=
Neodimerium
Petr., Sydowia 4(1–6): 341 (1950)
=
Parodiopsis
Maubl., in Arnaud, Bull. Soc. mycol. Fr. 31(1): 22 (1915)
=
Perisporina
Henn., Hedwigia 43(6): 357 (1904)
=
Piline
Theiss., Annls mycol. 14(6): 409 (1917) [1916]
=
Pseudoperis
Clem. and Shear, Gen. fung., Edn 2 (Minneapolis): 272 (1931)
=
Pseudoperisporium
Toro, Scient. Surv. P. Rico 8(1): 41 (1926)
=
Schistodes
Theiss., in Theissen & Sydow, Annls mycol. 15(6): 456 (1918) [1917]
Parasitic or epiphytic on living leaves. Sexual morph: Ascomata supercial, solitary to gregarious, seated on a subiculum, globose to subglobose
to obovoid, brown, with an apical ostiole. Peridium relatively thick-walled, comprising of dark brown cells of textura angularis. Sterile laments
branched, septate, anastomosed, hyaline, pseudoparaphyses. Asci 8-spored, bitunicate, ssitunicate, broadly ellipsoid, with short pedicel, apically
thickened, with an ocular chamber. Ascospores 2–3-seriate, ellipsoidal-oblong or fusiform, slightly curved and tapering toward the ends, 1-septate,
hyaline, sometimes pale-yellow brown, with granulate cells, smooth-walled. Asexual morph:
Septoidium
sp. (obsolete) (Kirk et al., 2008; Seifert et
al., 2011; Boonmee et al., 2017).
Type species:
Perisporiopsis struthanthi
Henn.
Note
Perisporiopsis
is characterized by supercial dark ascomata, lacking hyphal appressoria (formerly hyphopodia), indistinct pseudoparaphyses,
broadly clavate asci and ellipsoidal oblong, septate, hyaline ascospores. Currently, the Index Fungorum (2021) lists 20 epithets under
Perisporiopsis
. The asexual morph,
Septoidium
, was attributed by Arnaud (1921), but has not been mentioned in the original description of
P.
struthanthi
by Hennings (1904) nor observed during the reexam of the type specimen by Boonmee et al. (2017). Nevertheless in the epitype
material, designated here, a sub-sporodochial asexual morph was found occurring sparsely in the colonies of
P. struthanthi
which ts the
morphology described for
Septoidium.
Therefore, the name
Septoidium struthanthi
is herein formally treated as a synonym of
P. struthanthi
in
accordance to the principle of “one fungus - one name” of the International Code of Nomenclature for algae, fungi, and plants (May et al., 2019)
Perisporiopsis struthanthi
was found to belong in a clade together with
Setophoma
spp. The genus
Setophoma
was proposed by de Gruytere et
al. (2010) to accommodate two species previously placed in
Pyrenochaeta
–
Pyrenochaeta sacchari
and
Pyrenochaeta terrestris
.
Setophoma
is
characterized by having pycnidial conidiomata ornated with setae, phialidic conidiogenous cells, and hyaline, ellipsoidal to subcylindrical,
aseptate, guttulate conidia (de Gruyter et al., 2010, Quaedvlieg et al., 2013).
Position in classication:
Phaeosphaeriaceae
,
Pleosporales
,
Pleosporomycetidae
,
Dothideomycetes
,
Pezizomycotina
,
Ascomycota
,
Fungi
.
Perisporiopsis struthanthi Henn., Hedwigia 43: 83 (1904) (Fig.5).
Mycobank: 216818
≡
Parodiopsis struthanthi
(Henn.) G. Arnaud, Annls Épiphyt. 7: 54 (1921)
≡
Perisporina struthanthi
(Henn.) Hansf., Proc. Linn. Soc. London 157: 144 (1946)
Page 14/32
≡ Septoidium struthanthi
G. Arnaud 1921, Annls Épiphyt. 7: 106 (1921)
Colonies forming a sooty coating on leaves. Internal mycelium absent. External mycelium 5–10 µm diam., branched, septate, brown, smooth-
walled. Appressoria globose to subglobose, 10–25 × 10–22 µm, brown. Sexual morph: Ascomata pseudothecioid, supercial, solitary to
gregarious, seated on a subiculum, globose to subglobose to obovoid, 150–250 × 185–275 µm, walls of dark brown
textura angularis
, 40–45 µm
thick; ostiolate (ostiole single central). Pseudoparaphyses liform, branched, septate, anastomosed, 4–5 µm diam., hyaline. Asci bitunicate,
fasciculate, ssitunicate, broadly ellipsoid, 102–163 × 25–45 µm, short-pedicelate, apically thickened, with an ocular chamber, eight-spored.
Ascospores bisseriate, ellipsoidal-oblong or fusiform, 62.5–80 × 12.5–15 µm, slightly curved and tapering toward the rounded ends, 0–1-septate,
hyaline, becoming pale-yellowish brown, granulate-celled, smooth.
Asexual morph: Sub-sporodochial – fasciculate but somewhat compact at the base, 200–250 × 75–100 µm, dark brown. Conidiophores
cylindrical, 212–250 × 8.75–10 µm, erect, mononematous, macronematous, thick-walled, unbranched, 8–9 septate, pale to dark brown, smooth-
walled. Conidiogenous cells annellidic (holoblastic with percurrent proliferations), with conspicuous annellations, 27.5–30 × 5 µm, hyaline to pale
brown. Conidia ovoid to fusiform to cymbiform, 70–92.5 × 17.5–20 µm, base truncate apex rounded, 3-septate, smooth, pale brown or tinged in
pale grayish rose.
Type: BRAZIL: Rio de Janeiro, Rio de Janeiro, Serra dos Órgãos, on
Struthanthus
sp., August 1899, E. Ule 2631, Herbarium Brasiliense. Ex Herb.
Sydow (S-Fungi:F9814 – holotype).
Material examined: Brazil: Rio de Janeiro, Nova Friburgo, Debossan, on
Struthanthus
sp. parasitizing an hibiscus garden fence, 30th Jul 2019, R.
W. Barreto (VIC 47339 – epitype designated here); Nova Friburgo, Janela das Andorinhas, on
Struthanthus
sp. parasitizing an avocado tree, 11th
Apr 2019, R. W. Barreto (VIC 47340). Genbank Accession numbers of the reference sequences generated in this study: VIC 47339 LSU =
OQ191781; ITS = OQ191785; VIC 47340 = LSU = OQ191782; ITS = OQ191786.
Note
Repeated attempts to obtain a pure culture of
P. struthanthi
were unsuccessful. It is likely that this species is an obligate biotroph. Both specimens
(VIC 47339 and VIC 47340) had a morphology which was similar to the original description of Hennings (1904) and that of Boonmee et al. (2017)
for
P. struthanthi
. Nevertheless, the ascomata of our specimens were smaller than those described by Hennings (1904) and Boonmee et al. (2017)
– 150–250 µm vs. 250–300 µm and 263.5–272 µm, respectively. Ascospores in the newly collected specimens were longer than those described
in Hennings (1904) and Boonmee et al. (2017), 62.5–80 µm vs. 60–65 µm and 52.5–62 µm, respectively. Our specimens had ascospores which
were 0–1 septate whereas Hennings (1904) reported the occurrence of ascospores with up to 7 septa. In Boonmee et al. (2017) ascospores were
described as 1-septate. The asexual morph found in the epitype presented here was not observed in the reexamination of the type by Boonme et
al. (2017). A brief description and illustration of the conidia was provided by Arnaud (1921) and later illustrated by Ellis (1971), both in
accordance with the description presented here. The phylogenetic placement of VIC 47339 and VIC 47340 was within the
Setophoma
clade. This
is a genus described as having setose pycnidia. However, the only asexual morph observed for
P. struthanthi
in our study was the “
Septoidium
”
sub-sporodochial anellidic stage described above. The genus
Setophoma
was originally proposed without the description of a sexual morph.
Later, Phookamsak et al. (2014) described the sexual form of
Setophoma sacchari
as having immersed or semi-immersed ascomata, bitunicate
asci and cylindrical to cylindrical-clavate, hyaline ascospores. Ascospores of
S. sacchari
were described as 3-septate, usually having a broader
subapical cell. The morphological discrepancies between
P. struthanthi
and
S. sacchari
are evident.
Perisporiopsis antiqua (F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto comb. nov.
Mycobank: [XXXXXX]
≡
Setophoma antiqua
F. Liu & L. Cai, in Liu, Wang, Li, Wang & Cai, Fungal Systematics and Evolution 4: 50 (2019)
Description: see Crous et al. (2019).
Type: CHINA, Yunnan Province, Xishuangbanna, Mengla County, on old/arboreal Camellia sinensis, 18 Apr. 2015, F. Liu (holotype HMAS 248083,
culture ex-type CGMCC 3.19525 = LC6596 = LF1239).
Note
Based on the multi-locus phylogeny (Fig.2),
P. antiqua
is phylogenetically related to
P. endophytica
and share high sequence identity in LSU
(100%) and ITS (99%). There is no morphological differences that allow the distinction between these species. In the study of Crous et al. (2019),
P. antiqua
and
P. endophytica
were separated based on nucleotide differences of the
TUB2
and
EF1
sequences. Also, they differ in the habitat of
their common host:
P. antiqua
was isolated from a diseased tea plant (
C. sinensis
) bearing leaf spots at an unmanaged mountain forest in
Yunnan Province, whereas
P. endophytica
was isolated from healthy leaves of a tea plant from a forestry park in Jiangxi Province.
Page 15/32
Perisporiopsis chromolaenae (Quaedvl., Verkley, R.W. Barreto & Crous) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXXX]
≡
Setophoma chromolaenae
Quaedvl., Verkley, R.W. Barreto & Crous, Stud. Mycol. 75: 373 (2013)
Description: see Quaedvlieg et al. (2013)
Type: BRAZIL, Rio de Janeiro, Fazenda Santa Rosa, Ponte das Laranjeiras, on leaves of
Chromolaena odorata
(Asteraceae), 6 Apr. 2010, R.W.
Barreto (holotype CBS H-21314, culture ex-type CBS 135105 = CPC 18553).
Note
Perisporiopsis chromolaenae
was described based on asexual fungus in leaves of
Chromolaena odorata
. In the phylogenetic reconstruction
presented here,
P. chromolaenae
groups with
P. vernoniae
(BI = 1.00 and ML = 100%) forming a clade sister to the group of
P. struthanthi
,
P. antiqua
and
P. endophytica.
As with
P. vernoniae
, its sexual form is still unknown.
Perisporiopsis endophytica (F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXX]
≡
Setophoma endophytica
F. Liu & L. Cai, in Liu, Wang, Li, Wang & Cai, Fungal Systematics and Evolution 4: 51 (2019).
Description and illustration: see Liu et al. (2019) (doi.org/10.3114/fuse.2019.04.05)
Type: CHINA, Jiangxi Province, Ganzhou, Yangling NationalForest Park, on healthy leaves of Camellia sinensis, 24 Apr. 2013,F. Liu, YLBE3
(holotype HMAS 248081, culture ex-type CGMCC3.19528 = LC3163 = LF372).
Notes: See note for
S. antigua.
The status of the relation between
S. endophytica
and its tea plant host (pathogenic or symbiotic) remains
uncertain.
Perisporiopsis pseudosacchari (Crous & Y. Marín) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXXXX]
≡
Setophoma pseudosacchari
Crous & Y. Marín, in Marin-Felix, Hernández-Restrepo, Iturrieta-González, García, Gené, Groenewald, Cai, Chen,
Quaedvlieg, Schumacher, Taylor, Ambers, Bonthond, Edwards, Krueger-Hadeld, Luangsa-ard, Morton & Moslemi, Stud. Mycol. 94: 112 (2019)
Description and illustration: see Crous et al. (2019).
Type:FRANCE, La Reunion Island, leaf spots on
Saccharum ocinarum
(Poaceae), May 2015, P.W. Crous, HPC 296 (holotype CBS H-23876, CBS
145373 = CPC 26421)
Note
As
Perisporiopsis sacchari, P. pseudosacchari
, was described causing leaf spots on sugarcane. Both species share high similarities in ITS
sequence and differ in ascomata, asci, and ascospores sizes (Marin-Felix et al., 2019). These species formed a basal clade inside the clade
including
P. struthanthi, P. endophytica, P. antiqua, P. veroniae, and P. chromolaenae.
Perisporiopsis sacchari (Bitanc.) D.C. Guterres, Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXX]
Basionym:
Pyrenochaeta sacchari
Bitancourt, Arquivos Inst. Biol., Sao Paulo 9:301. 1938.
≡
Pyrenochaeta sacchari
Bitanc., Archos Inst. biol., S. Paulo 9(no. 27): 301 (1938)
≡
Setophoma sachari
(Bitanc.) Gruyter, Aveskamp & Verkley, Mycologia 102(5): 1077 (2010)
=
Pyrenochaeta setariae
H.C. Greene, Trans. Wis. Acad. Sci. Arts Lett. 53:211. 1964.
=
Pyrenochaeta penniseti
J. Kranz, Sydowia 22:360. 1968.1078
=
Phoma setariae
(H.C. Greene) Gruyter & Boerema, Persoonia 17: 559. 2002 [‘2001’].
Page 16/32
Description and illustration: for a complete description see Bitancourt (1938). De Gruyter et al. (2010) designated and epitype and provided high
quality pictures of the microscopic structures.
Type: BRAZIL, Cantareira, Sao Paulo. On leaves of
Saccharum ocinarum
, 11–13 Oct 1937, nr. 2769, IBI, coll. A.A. Bitancourt (holotype). On
leaves of
Saccharum ocinarum
var. EK28, Jul 1939, nr 3064, A.A. Bitancourt (epitype CBS H-20312 (Designated by de Gruyter et al. (2010)).
Notes: The species was originally described as
Pyrenochaeta sacchari
causing a leaf spot disease on sugarcane in Brazil (Bitancourt, 1938) and
later transferred to
Setophoma
(Gruyter et al., 2010) as
S. sacchari.
In the phylogenetic reconstruction presented here, it grouped with
P.
pseudosacchari
with high support in both analyses (BI = 1.00 and ML = 100%).
Perisporiopsis vernoniae (Crous & Alfenas) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXXX]
≡
Setophoma vernoniae
Crous & Alfenas, in Crous et al., Persoonia 32: 235 (2014)
Description and illustration: see Crous et al. (2014)
Type: BRAZIL, Minas Gerais, Viçosa, Minas Gerais, on leaves of
Vernonia polyanthes
(Compositae), May 2013, A.C. Alfenas (holotype CBS H-
21701, culture ex-type CPC 23123 = CBS 137988; ITS sequence GenBank KJ869141, LSU sequence GenBank KJ869198, MycoBank MB808920).
Notes:
Perisporiopsis vernoniae
grouped with
P. chromolaenae
forming a sister lineage to the clade including
P. struthanthi, P. endophytica, P.
antiqua, P. veroniae, and P. chromolaenae.
Unresolved species originally included in Perisporiopsis
Besides the species reexamined in the present study,
P. struthanthi, P. lantanae
, and
P. lateritia
, Index Fungorum (2023) lists 17 epithets under
Perisporiopsis
, namely:
Perisporiopsis brachystegiae
(Henn.) Arx 1962,
P. brasiliensis
(Bat. & Nascim.) Arx 1962,
P. cecropiae
(R.E.D. Baker) Arx
1962,
P. cecropiae
var.
cecropiae
(R.E.D. Baker) Arx 1962,
P. clusiae
(R.E.D. Baker) Arx 1962,
P. escharoides
(Syd.) Arx 1962,
P. fusispora
(Pat.) Arx
1962, P. hurae (G. Arnaud) Arx 1962,
P. kwangensis
(Henn.) Arx 1962,
P. lophirae
(Deighton) Arx 1962,
P. megalospora
(Sacc. & Berl.) Arx 1962,
P.
megalospora
var.
megalospora
(Sacc. & Berl.) Arx 1962,
P. melioloides
(Berk. & M.A. Curtis) Arx 1962,
P. portoricensis
(F. Stevens & Higley) Arx
1962,
P. sydowii
(Petr.) Arx 1962, and
P. torrendii
(Bat. & H. Maia) Arx 1962. These are all obscure taxa for which there is no molecular information
available. All of these require recollection and molecular analysis to allow a verication of their taxonomic placement. This is not feasible under
the context of the present work.
Pseudosetophoma D.C. Guterres, B.W. Ferreira & R.W. Barreto, gen. nov.
Mycobank: [XXXXXXX]
Similar to
Setophoma
but with conidiomata either bearing or lacking setae, sterile on cultural media, distant phylogenetically from the clade of
S.
terrestris
.
Type species: Pseudosetophoma yunnanensis
(F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto comb. nov.
Note
In a multilocus phylogeny, forming a well delimited clade (BI = 1.00, ML = 100%) apart from the
S. terrestris
clade and close to the clades formed
by
Perisporiopsis
and
Troglophoma
. The two species belonging to
Pseudosetophoma
are asexual fungi which are sterile in culture.
Pseudosetophoma yunnanensis (F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXXX]
≡
Setophoma yunnanensis
F. Liu & L. Cai, in Liu, Wang, Li, Wang & Cai, Fungal Systematics and Evolution 4: 54 (2019)
Description and illustrations: see Liu et al. (2019).
Type: CHINA, Yunnan Province, Xishuangbanna, Mengla County, Laomansa, on
Camellia sinensis
, 19 Apr. 2015, F. Liu, LMS001P (holotype HMAS
248084, culture ex-type CGMCC 3.19529 = LC6753 = LF1434)
Note
Page 17/32
Pseudosetophoma yunnanensis
was originally isolated from leaf spots leaves of arboreal tea plants (
Cammelia sinensis
). It grouped with
Ps
.
yingyisheniae
with strong support in both analyses (BI = 1.00 and ML = 100%). The main differences between
Ps. yingisheniae
and
Ps.
yunnanensis
are mentioned under the notes of
Ps. yingisheniae.
Pseudosetophoma yingyisheniae (F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [XXXXX]
≡
Setophoma yingyisheniae
F. Liu & L. Cai, in Liu, Wang, Li, Wang & Cai, Fungal Systematics and Evolution 4: 54 (2019)
Description and illustrations: see Liu et al. (2019)
Type: China, Guangxi Province, Guilin, Longsheng County, altitude 1 200 m, on
Camellia sinensis
, 21 Sep. 2016, Y.Y. Shen, GXGL01a (holotype
HMAS 248086, culture ex-type CGMCC 3.19527 = LC13479 = LF1986).
Note
Pseudosetophoma yingyisheniae
was originally isolated from both symptomatic and asymptomatic leaves of tea plants (
C. sinensis
). Together
with
Ps. yunnanensis
it forms a clade that is strongly supported (BI = 1.00 and ML = 100%). The main differences between
Ps. yingisheniae
and
Ps. yunnanensis
are the habit of the host (arboreal in
Ps. yingyisheniae
vs. herbaceous in
Ps. yunnanensis
) and the conidiogenesis. The
conidiophores of
Ps. yunnanensis
are simple and often reduced to single and ampulliform or globose conidiogenous cells, whereas conidiofores
are branched in
Ps. yingyisheniae
and bear oblong conidiogenous cells. In addition,
Ps. yingyisheniae
produces setae in culture, a character not
seen in
Ps. yunnanensis
.
Setophoma Gruyter, Aveskamp & Verkley
Mycobank: MB514658
Description: see Marin-Felix et al. (2019).
Type species:
Setophoma terrestris
(H.N. Hansen) Gruyter, Aveskamp & Verkley
Note
The original description of
Setophoma
given by De Gruyter et al. (2010) was consecutively emended as new species were added to the genus. The
most recent emendation of
Setophoma
description by Liu et al. (2019) were made to include new species that lack ascomatal setae. Here, the
species included by Liu et al. (2019) in
Setophoma
were separated into distinct genera,
Pseudosetophoma
,
Perisporiopsis
, and
Troglophoma
.
Therefore, the emendation given by Liu et al. (2019) became superuous. Here we consider the full description given by Marin-Felix et al. (2019)
the most adequate. In the present study, only three species are included in the genus
Setophoma
:
S. terrestris
,
S. brachypodii
, and
S. poaceicola
(Table2).
Page 18/32
Table 2
Current names, substrate and distribution of Perisporiopsis, Pseudosetophoma, Setophoma, and Troglophoma spp. (family Phaeosphaeriaceae)
and of Pyrenochaetopsis lateritia (Pyrenochaetopsidaceae)
Genus (Family) Current name Previous name Substrate Distribution References
Perisporiopsis
(
Phaeosphaeriaceae
)
Perisporiopsis
antiqua Setophoma
antiqua Camellia
sinensis
China Liu et al. (2019)
P. chromolaenae S.
chromolaenae Chromolaena
odorata
Brazil Quaedvlieg et al. (2013)
P. endophytica S. endophytica Camellia
sinensis
China Liu et al. (2019)
P. pseudosacchari S.
pseudosacchari Saccharum
ocinarum
France Marin-Felix et al. (2019)
P. sacchari S. sacchari Saccharum
ocinarum
Brazil de Gruyter et al. (2010)
P. struthanthi -- Struthanthus
sp. Brazil Hennings (1904), Barreto
et al. (1995)
P. vernoniae S. vernoniae Vernonia
polyanthes
Brazil Crous et al. (2014)
Pseudosetophoma
(Phaeosphaeriaceae) Pseudosetophoma
yingyisheniae S.
yingyisheniae Camellia
sinensis
China Liu et al. (2019)
Ps.yunnanensis S. yunnanensis Camellia
sinensis
China Liu et al. (2019)
Setophoma
(Phaeosphaeriaceae) Setophoma
brachypodii S. brachypodii Brachypodium
sylvaticum
Belgium Marin-Felix et al. (2019)
S. poaceicola S. poaceicola Grass
Thailand Thambugala et al.
(2017)
S. terrestris S. terrestris Allium cepa
North America,
Senegal de Gruyter et al. (2010)
Allium sativum
United States de Gruyter et al. (2010)
Brassica sp.
Canada,
Alberta Yang et al. (2017)
Cucurbita
maxima
USA, Oregon Rivedal et al. (2018)
Cucurbita
moschata
Japan Ikeda et al. (2012)
Solanum
lycopersicum
Canada,
Ontario Johnston-Monje et al.
(2017)
Troglophoma
(Phaeosphaeriaceae) Troglophoma caverna S. caverna
Carbonatite in
karst cave China Crous et al. (2019)
Troglophoma
longinqua S. longinqua Camellia
sinensis
China Liu et al. (2019)
Pyrenochaetopsis
(Pyrenochaetopsidaceae) Pyrenocaetopsis
lateritia Perisporiopsis
lateritia Hevea
brasiliensis
Peru Chaverri and Gazis
(2010)
Position in classication:
Phaeosphaeriaceae, Pleosporales, Pleosporomycetidae, Dothideomycetes, Pezizomycotina, Ascomycota, Fungi.
Setophoma terrestris (H.N. Hansen) Gruyter, Aveskamp & Verkley
MycoBank MB514659
Basionym:
Phoma terrestris
H.N. Hansen, Phytopathology 19:699. 1929.
≡
Pyrenochaeta terrestris
(H.N. Hansen) Gorenz, J.C. Walker & Larson, Phytopathology 38:838. 1948; not
Phoma terrestris
R.K. Saksena, Nand &
A.K. Sarbhoy, Mycopath. Mycol. Appl. 29:86. 1966 (syn.
Phoma multirostrata
Boerema).
Note
Page 19/32
In the presented phylogenetic reconstruction,
S. terrestris
formed a strongly supported clade together with
S. brachypodii
and
S. poaceicola
,
distant from species formerly accommodated in the genus
Setophoma
, herein separated in the older genus
Perisporiopsis
and the new genera
Pseudosetophoma
and
Troglophoma
here described.
Setophoma brachypodii Crous, R.K. Schumach. & & Y. Marín
Mycobank: 829669
Description: see Marin-Felix et al. (2019).
Type: BELGIUM, Dinant, 173 m a.s.l., on border of calcareous meadow, on a dead and attached leaf of
Brachypodium sylvaticum
(Poaceae), 2
Nov. 2016, L. Bailly & R.K. Schumacher, HPC 1503, RKS 1 (holotype CBS H-23905, culture ex-type CBS 145418 = CPC 32492)
Note
Setophoma brachypodii
isolated from
Brachypodium sylvaticum
and remained sterile on all media tested by its authors, and the original
specimen was depleted. Thus, there is no morphological description of this fungus, except for the description of the colony on MEA, PDA, and OA.
The differences from other
Setophoma
species are based on the alleles in two loci sequences (LSU and ITS). In our phylogenetic reconstruction,
S.
brachypodii
clustered with strong support in both analysis (BI = 0.99 and ML = 96%) within
S. terrestris
clade, as a basal lineage.
Setophoma poaceicola Goonas., Thambug. & K.D. Hyde
Mycobank: 552993
Description and illustration: see Thambugalae et al. (2017)
Type: THAILAND, Chiang Mai Province, Mae Taeng, Mushroom Research Center, on culm of dead grass (Poaceae), 9 March 2016, Ishani D.
Goonasekara IGm 05 (MFLU 16–2850, holotype); ibid. (HKAS 97386, isotype), ex-type living culture MFLUCC 16–0880, KUMCC 17–0021.
Note
Setophoma poaceicola
was described based only in the sexual morph and allocated in the genus
Setophoma
based on phylogenetic studies.
Here, it grouped with
S. terrestris
with strong support in both analysis (BI = 1.00 and ML = 100%).
Sputnikia B.W. Ferreira & R.W. Barreto, gen. nov.
Mycobank: [to be determined after manuscript acceptance]
Etimology: in honor of the the Earth's rst articial satellite, Sputnik-1, launched into Earth orbit in 1957.
Diagnosis: Colonies forming a sooty and broad mat adaxially on leaves but without producing any evident damage to individual leaves or host
plants. Internal mycelium not observed. External mycelium branched, septate, brown, smooth-walled. Ascomata pseudothecioid, amphigenous,
supercial, abundant, subspherical, composed of dark brown textura angularis, ornamented with abundant brown septate setae, often with a
group of shorter setae arranged as a crown surrounding the ostiole. Dehiscence ostiolate, one ostiole in the centre of each pseudothecium,
circular, papillate. Interthecial laments pseudoparaphyses, thin, branched, hyaline. Asci bitunicate, fasciculate, subclavate, 8spored. Asexual
morph: Conidiomata pycnidial, amphigenous, supercial, abundant, intermixed with ascomata, indistinguishable from ascomata in external
appearance, wall thickness, composition and colour. Dehiscence as for teleomorph. Conidiophores absent. Conidiogenous cells arising from lower
half of pycnidial wall, subcylindrical, hyaline. Conidia holoblastic, cylindrical, straight to slightly curved, apex round, base truncate, 4–6 septate,
guttulate, greyish, smooth-walled.
Position in classication:
Phaeosphaeriaceae, Pleosporales, Pleosporomycetidae, Dothideomycetes, Pezizomycotina, Ascomycota, Fungi.
Type:
Sputnikia lantanae
(F. Stevens) B.W. Ferreira & R.W. Barreto, comb. nov.
Sputnikia lantanae (F. Stevens) B.W. Ferreira & R.W. Barreto, comb. nov. (Fig.6)
Mycobank: [XXXXXX]
Basyonym:
Perisporina lantanae
F. Stevens, Transactions of the Illinois Academy of Science 10: 170 (1917).
≡Perisporiopsis lantanae
(F. Stevens) R.W. Barreto, Mycological Research 99 (7): 774 (1995)
≡Perisporina lantanae
F. Stevens, Transactions of the Illinois Academy of Science 10: 170 (1917).
Page 20/32
Description and illustration: see Steven (1917) for description of the sexual morph. Barreto et al. (1995) provided a full description with
illustrations of the sexual and asexual morphs.
Type: USA-PUERTO RICO, Lares, on leaves of
Lantana camara
, 22 Nov. 1913, F. L. Stevens 4924 (ILL 5979, Accession Number 6589, holotype);
BRAZIL, Rio de Janeiro, Rio de Janeiro, Cachoeiras de Macacu, on
Lantana camara
, 21 Nov 2019, R. W. Barreto (VIC 49395 – epitype designated
here) ex-epitype culture (COAD 3538); Genbank Accession numbers of the reference sequences generated in this study: LSU = OQ191783; ITS =
OQ191787; SSU = OQ831623; EF1 = OQ835623.
Other material examined: BRAZIL, Rio de Janeiro, Nova Friburgo, Janela das Andorinhas, on
Lantana camara
, 13 Dec 2019, R. W. Barreto (VIC
49396 – paratype), culture (COAD 3541). Genbank Accession numbers of the reference sequences generated in this study: LSU = OQ191784; ITS
= OQ191788; SSU = OQ831622; EF1 = OQ835624.
Note
Note: Stevens (1917) erected the species
Perisporina lantanae
based on material from Puerto Rico. Muller & Arx (1962) when they synonymized
Perisporina
under
Perisporiopsis
, did not propose a new combination for
Perisporina lantanae
. This was done later, by Barreto et al. (1995), who
also provided illustrations and a more detailed description for
Perisporiopsis lantanae
based on materials collected in Rio de Janeiro-Brazil. The
epitype designated here for
P. lantanae
differs slightly from the descriptions by Stevens (1917) and Barreto et al. (1995). Asci were larger in COAD
3538 and COAD 3541 than those described by Stevens (1917) and Barreto et al. (1995), 72.5–77.5 × 17.5–22.5 µm vs. 61–68 × 17–20 µm and
66–98 × 17–22 µm, respectively. Ascospores were shorter in RWB 2296 and RWB 2298 (25–37.5 µm) than those described by Barreto et al.
(1995) (35–49 µm). The asexual form was not observed in the newly collected samples. The phylogenetic analysis performed here, showed that
P. lantanae
is only distantly related to
P. struthanthi
. The isolates COAD 3538 and COAD 3541 clustered close to the genera
Paraphoma
, the mono-
specic genus
Megacoelomyces
, and the species
Pseudophaeosphaeria rubi
.
Paraphoma
is characterized by setose pycnidia, monophialidic
conidiogenous cells, and conidia enteroblastic, ellipsoid, aseptate, hyaline.
Megacoelomyces sanchezii
is an asexual ascomycete with large,
supercial, scarcely setose pycnidial conidiomata seated on loose, trichome-associated subiculum.
Pseudophaeosphaeria rubi
is a sexual
ascomycete saprobic on
Rubus idaeus
, with ascomata scattered, immersed to slightly erumpent through host tissue and asexual morph
undetermined. Sexual morphs of
Paraphoma
and
Megacoelomyces
are not known.
Troglophoma D.C. Guterres, B.W. Ferreira & R.W. Barreto, gen. nov.
Mycobank: [to be determined after manuscript acceptance]
Etimology: from the greek “Trōglē” (“hole” or “cave”) as an indicative of the origin of the type, which was obtained from carbonatite from a Karst
cave.
Type species:
Troglophoma caverna
(F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Troglophoma caverna (F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [to be determined after manuscript acceptance]
≡
Setophoma caverna
F. Liu & L. Cai, in Crous et al., Persoonia 43: 401 (2019)
Description and illustrations: see Crous et al. (2019).
Type: CHINA, Guizhou Province, Suiyang, Shuanghe Cave National Geopark, unnamed Karst cave, from carbonatite, 8 May 2015, Z.F. Zhang
(holotype HMAS 248085, ex-type culture CGMCC 3.19526 = LC7511 = R150, LSU, ITS,
TUB2
,
EF1
, and
GAPDH
sequences GenBank MK511965,
MK511944, MK525032, MK525105 and MK525066, MycoBank MB829901).
Note
Troglophoma caverna
was originally isolated from carbonatite from a Karst cave. In the phylogenetic reconstruction presente here, it clustered
with
T. longinqua
with strong support in both analyses (BI = 1.00 and ML = 88%). Morphologically,
T. caverna
differs from
T. longinqua
by the
conidial shape and dimensions (globose or ellipsoid, 3–16.5 × 2.5–10.5 µm in T.
caverna
vs. cylindrical or subcylindrical, 4–5.5 × 1.5–2 µm in
T.
longinqua
). Together, they form a lineage sister to
Perisporiopsis
clade.
Troglophoma longinqua (F. Liu & L. Cai) D.C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
Mycobank: [to be determined after manuscript acceptance]
≡ Setophoma longinqua
F. Liu & L. Cai, in Liu, Wang, Li, Wang & Cai, Fungal Systematics and Evolution 4: 53 (2019)
Page 21/32
Description and illustration: see Liu et al. (2019).
Type: CHINA, Yunnan Province, Xishuangbanna, Mengla County,on
Camellia sinensis
, 18 Apr. 2015, F. Liu, GFZCWS001P (holotypeHMAS 248082,
culture ex-type CGMCC 3.19524 = LC6593 = LF1236).
Notes:
Troglophoma longinqua
was originally isolated from the same symptomatic leaf as
P. antiqua
, however the author decided to describe
these as separated species due to phylogenetic distance between these isolates. Here,
T. longinqua
grouped with
T. caverna
in a separated clade
from
P. antiqua
and distant related to
S. terrestris.
Note
Troglophoma longinqua
was originally isolated from the same symptomatic leaf as
P. antiqua
, however the authors decided to describe them as
separated species due to phylogenetic distance between the isolates. Here,
T. longinqua
grouped with
T. caverna
in a separated clade from
P.
antiqua
and distant related to
S. terrestris.
Pyrenochaetopsidaceae Valenz.-Lopez, Crous, Cano, Guarro & Stchigel 2017
Pyrenochaetopsis Gruyter, Aveskamp & Verkley 2010
Type:
Pyrenochaetopsis leptospora
(Sacc. & Briard) Gruyter, Aveskamp & Verkley 2010
Pyrenochaetopsis lateritia (P. Chaverri & Gazis) D. C. Guterres, B.W. Ferreira & R.W. Barreto, comb. nov.
≡ Perisporiopsis lateritia P. Chaverri & Gazis, Mycotaxon 113: 164 (2010)
Description and illustration: see Chaverri and Gazis (2010).
Type: PERU, 17 June 2007, coll. R. Gazis, H.C. Evans, P. Chaverri; (Holotype BPI 880185, P.C. 811) on underside of decaying leaves of
Hevea
brasiliensis
, Picaor Research Station, near Tambopata River, Prov. Tambopata: Dept. Madre de Dios, Peru. GenBank accession number FJ884129
[ITS].
Note
The ITS sequence of the type of
Perisporiopsis lateritia
grouped with species of
Pyrenochaetopsis
, in the family
Pyrenochaetopsidaceae.
Pyrenochaetopsidaceae
was spun off from
Cucurbitareaceae
by Valenzuela-Lopez et al. (2018) and comprises fungi with pycnidial conidiomata,
pale brown to brown, solitary or conuent; pycnidial wall of textura angularis, glabrous or setose, subglobose to ovoid, with a non-papillate or
papillate ostiolar neck. Conidiogenous cells phialidic, hyaline, discrete or integrated in septate, acropleurogenous conidiophores. Conidia aseptate,
hyaline, smooth- and thin-walled, ovoid, cylindrical to allantoid, guttulate. An anamorphic picnidial phase was not described by Chaverri and Gazis
(2010) for
Py. lateritia
, in addition the authors deposited only sequences from the ITS region for the type.
Pyrenochaetopsis
spp. have been
commonly reported as saprobes (de Gruyter et al. 2010). Some species have also been reported in samples of water, plants, soil, manure, air and
as endophytes in grasses (de Gruyter et al., 2010, 2013; Crous et al., 2014; Farr and Rossman, 2021). Here, we chose to adopt a new combination
for
Py. lateritia
, differentiating it from the other species in the genus, considering that only
Py. lateritia
has its sexual morph described and an
hyphomycetous asexual morph with macro and microconidia.
Discussion
The features traditionally used to identify and separate genera and species of
Perisporiopsidaceae
, such as ascospore and conidial shape, size
and septation, allied with host identity, were shown here to be insucient to reect their phylogenetic relationships. According to the results
presented here, the connection of
Perisporiopsis with Leptosphaeriaceae
and
Phaeosphaeriaceae
as conjectured by Chaverri and Gazis (2011)
was further explored here. Our phylogenetic study has shown that the specimens of
P. struthanthi
, the type species of
Perisporiopsis
, which is the
type genus of the
Perisporiopsidaceae
, groups with
Setophoma
, in the family
Phaeosphaeriaceae
. Although the name
Perisporiopsidacea
e was
proposed earlier than
Phaeosphaeriacea
e Müller and von Arx 1962 vs. Barr 1979) it lacked priority because the authors failed to follow the
nomenclature rules at the time and the name
Perisporiopsidaceae
was considered invalid. Only much later Kirschner et al. (2010) validated the
family name. Therefore, the earliest valid name for this fungus assemblage is
Phaeosphaeriaceae
, which should now be used.
Perisporiopsidaceae
is, therefore, a synonym of
Phaeosphaeriaceae
.
Fungi in the
Phaeosphaeriaceae
represent an assemblage of taxa which is ecologically very plastic and occupying a vast range of niches and
habitats. It includes fungi that exist as endophytes, epiphytes, lichen-forming species, plant pathogens, saprobes and even some reported as
human pathogens (Phookamsak et al., 2014). The family was introduced by Barr (1979) and typied by
Phaeosphaeria
with
Phaeosphaeria
oryzae
(Miyake, 1909) as its type. The taxonomic boundaries of the
Phaeosphaeriaceae
have undergone signicant changes in recent years. New
Page 22/32
genera were introduced, whereas others were transferred to other families (Zhang et al., 2012; Hyde et al., 2013; Quaedvlieg et al., 2013;
Phookamsak et al., 2014; Trakunyingcharoen et al., 2014; Crous et al., 2015; Ertz et al., 2015; Phukhamsakda et al., 2015; Senanayake et al., 2015;
Tennakoon et al., 2016; Tibpromma et al., 2016; Ahmed et al., 2017; Wanasinghe et al., 2018). Currently, more than 50 genera including species
known either in their sexual, asexual form or both, are accepted in the family (Bakhshi et al., 2019).
The genus
Setophoma
was included in the family, to accommodate
Phoma terrestris
and
Pyrenochaeta sacchari
(de Gruyter et al., 2010). Species
of
Setophoma
are characterized as having setose pycnidia, phialidic conidiogenous cells and hyaline, ellipsoidal to subcylindrical, aseptate
conidia (de Gruyter et al., 2010; Quaedvlieg et al., 2013). According to the Index Fungorum and MycoBank, the genus currently has 14 species. All,
except
S. terrestris
, are reported to occur on single host plants (Table2). Since
P. struthanthi
, type of
Perisporiopsis
grouped in
Setophoma
, the two
genera might be treated as synonyms, with
Perisporiopsis
having nomenclatural priority over
Setophoma
. However, we decided that it would be
premature to propose the synonymization of
Setophoma
with
Perisporiopsis
here since there is no morphological evidence for justifying such a
proposal. A study involving a broader range of taxa within the two genera may justify this move in the future.
Perisporiopsis lantanae
was unique among
Perisporiopsis
spp. in having a pycnidial instead of
Septoidium
-like macro- and microconidial asexual
morph. Based on this and on the morphological characteristics of the ascospores, that resembles those of
Leptosphaeria
, Chaverri and Gazis
(2011) conjectured that
P. lantanae
could be related with
Leptosphaeria
and that it might not belong into
Perisporiopsis
. In fact, our phylogenetic
analyzes showed that
P. lantanae
is distant from
P. struthanthi
, but it also belongs to the family
Phaeosphaeriaceae
. It is not a member of the
Leptosphaeriaceae
, as suggested by Chaverri and Gazis (2011).
Perisporiopsis lantanae
formed a well-supported clade, separated from other
genera in
Phaeosphaeriaceae
. Thus, a new genus,
Sputnikia
, was proposed herein to accommodate the fungus described on
L. camara
.
Phylogenetic analysis showed that
P. lateritia
belongs to the
Pyrenochaetopsidaceae
. The isolates grouped with species in
Pyrenochaetopsis
. A
more precise clarication of the relationship of
P. lateritia
within
Pyrenochaetopsis
could not be achieved due to the lack of resolution of the ITS
region for rm phylogenetic conclusions. The morphological comparison was also not possible, since only the asexual pycnidial morph was
described for the members of the genus, and the only description for the asexual form of
P. lateritia
, is of an hyphomycetous
Septoidium
-like
asexual morph.
Septoidium
(syn.
Diplodium
) was instroduced by Arnaud (1921) based on
Sep. clusiaceae
, to accommodate the conidial form of
Parodiopsis
, family
Parodiopsidaceae.
in the group of the dematiaceous phragmosporae aiming to preserve the stability of the Saccardo’s
system. Currently, there are 16 epithets listed in Index Fungorum (2023), including
Septoidium struthanthi
, reduced here to a synonym of
P.
struthanthi
.
Most members formerly placed in the
Perisporiopsidaceae
are obscure taxa which have been described from the tropics in the early XX century
and need to be recollected. There are no DNA sequences available for most genera and species and even morphological description are
incomplete and illustrations are often lacking. Many of the materials designated as type are old, scarce or have been lost, or deteriorated, or were
inaccessible to us, making it impossible to include them in this study. The epitipication of these taxa, followed by molecular phylogenetic
analysis, may resolve their taxonomic position and produce a more natural classication for all of these taxa up to the family level.
Declarations
Acknowledgements
The authors would like to thank Dr. João P. M. Araújo for providing us with some “dicult references”. Electron microscopy studies were
performed at the Núcelo de Microscopia e Microanálise da Universidade Federal de Viçosa (NMM-UFV).
Funding
Financial support allowing this work to be performed was provided by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais
(FAPEMIG), Conselho Nacional do Desenvolvimento Cientíco e Tecnológico (CNPq) and the Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior (CAPES).
Data availability
The data generated during this study and utilized/described herein have been thoroughly referenced. Any supplementary data can be made
available on request through the corresponding author.
Contributions Conceived the study: BWF and RWB. Collected the samples: RWB. Processed the samples: BWF, DMM and DCG. Analysed the data:
BWF, DMM, DCG and RWB. Wrote original draft: BWF, DMM, and RWB. Reviewed and edited the original draft: RWB and DCG.
Ethics approval Not applicable.
Consent to participate Not applicable
Page 23/32
Consent for publication All authors have agreed to publish this manuscript.
Competing interests The authors declare no conicts of interest.
Open access Not applicable.
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Figures
Page 27/32
Figure 1
Bayesian tree inferred from combined dataset of nc LSU rDNA and ITS of 96 strains of Phaeosphaeriaceae. The phylogenetic tree shows the
relationship of
Perisporiopsis struthanthi
and
Perisporiopsis lantanae
with other genera in the family. Bootstrap support values ≥70% for
maximum likelihood (ML), and Bayesian posterior probabilities (PP) ≥0.90 are given above or below each branch respectively (– indicates lack of
support). Thickened branches denote support values higher than 0.95 in BI and 0.80 in ML. The tree was rooted to
Querciphoma carteri
(CBS
105.91). Isolates from this study are indicated by bold text
Page 28/32
Figure 2
RAxML tree inferred from combined dataset of nc LSU rDNA, ITS,
EF1
, and
TUB
showing the relationship of
Perisporiopsis struthanthi
with other
closely related
Setophoma
spp. Bootstrap support values (ML and BI) or Bayesian posterior probabilities higher than 70 % or 0.90 are indicated
above or below branches (– indicates lack of support). Thickened branches denote support values higher than 0.95 in BI and 0.80 in ML. Isolates
from this study are indicated by bold text
Page 29/32
Figure 3
Bayesian tree inferred from combined dataset of nc LSU rDNA, SSU, ITS and
EF1
of 123 strains of Phaeosphaeriaceae. The phylogenetic tree
shows the relationship of
Perisporiopsis struthanthi
and
Perisporiopsis lantanae
with other genera in the family. Bootstrap support values ≥70%
for maximum likelihood (ML), and Bayesian posterior probabilities (PP) ≥0.90 are given above or below each branch respectively (– indicates
lack of support). Thickened branches denote support values higher than 0.95 in BI and 0.80 in ML.The tree was rooted to
Querciphoma carteri
(CBS 105.91). Isolates from this study are indicated by bold text
Page 30/32
Figure 4
RAxML tree based on combined nc LSU rDNA, ITS,
RPB2
and
TUB
showing the relationship of
Perisporiopsis lateritia
with other closely related
family in
Dothideomycetes.
Bootstrap support values (MP and ML) or Bayesian posterior probabilities higher than 70 % or 0.90 are indicated
above or below branches (– indicates lack of support). Thickened branches denote support values higher than 0.95 in BI and 0.80 in ML
Page 31/32
Figure 5
Perisporiopsis struthanthi
(VIC 44410). A-C SEM image showing ascomata on leaf surface of
Struthanthus
sp. D Collapsed ascomata releasing
Asci. E Mature and imature asci. F Detail of bitunicate asci. G-J Ascospores. K Conidiophores. L Close up of conidiophores and conidia. M-N
Conidia. Scale bars: A-B = 100 μm, C = 30 μm, D and K = 50 μm, E-J and L-N = 20 μm
Page 32/32
Figure 6
Sputnikia lantanae
(VIC 44409). A-C SEM image of ascomata on leaf surface of
Lantana camara
. D Ascomata releasing Asci. EDetail of
bitunicate asci. F-I Ascospores. J-K Colony on PCA and PDA after 15 days (incubation at 25 °C in 12 h light/dark cycle). Scale bars: A = 100 μm, B
= 30 μm, C-D = 20 μm, E-I = 10 μm
