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Phylogenetic classification and generic delineation of Calyptosphaeria gen. nov., Lentomitella , Spadicoides and Torrentispora ( Sordariomycetes )

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The genus Ceratostomella has a long history of taxonomic confusion. While species with evanescent asci have been transferred to the Microascales and Ophiostomatales, the taxonomic status of species with persistent asci has not been completely resolved. In previous studies using DNA sequence data, cultures and morphology, several Ceratostomella spp. were allocated in 13 genera in the Eurotiomycetes and Sordariomycetes. In our study, the systematics of the remaining Ceratostomella spp. with persistent asci is revisited with new collection data, cultures and phylogeny based on novel DNA sequences from six nuclear loci. Bayesian inference and Maximum Likelihood analyses support the monophyly of several wood-inhabiting species formerly classified in Ceratostomella and other unknown morphologically similar taxa and their division into four genera, i.e. Lentomitella, Spadicoides, Torrentispora and the newly described Calyptosphaeria. This robust clade represents the order Xenospadicoidales in the Sordariomycetidae. Comparative analysis of the ITS2 secondary structure revealed a genetic variation among Lentomitella isolates; 11 species were recognised, of which five are newly introduced and two are new combinations. Other taxonomic novelties include four new species and eight new combinations in Calyptosphaeria, Spadicoides, and Torrentispora. Molecular data suggest that Spadicoides is polyphyletic. The core of the genus is positioned in the Xenospadicoidales; Spadicoides s. str. is experimentally linked with sexual morphs for the first time. Based on DNA sequence data, the monotypic genera Xenospadicoides and Pseudodiplococcium are reduced to synonymy under Spadicoides, while Fusoidispora and Pseudoannulatascus are synonymised with Torrentispora. Members of the Xenospadicoidales inhabit decaying wood in terrestrial and freshwater environments and share a few morphological characters such as the absence of stromatic tissue, ascomata with a cylindrical or rostrate neck, similar anatomies of the ascomatal walls, thin-walled unitunicate asci with a non-amyloid apical annulus, disintegrating paraphyses, usually ellipsoidal to fusiform ascospores and holoblastic-denticulate or tretic conidiogenesis. Revised Ceratostomella spp. with persistent asci are listed and the taxonomic status of each species is re-evaluated based on revision of the holotype and other representative material, published details and available phylogenetic data.
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Phylogenetic classication and generic delineation of
Calyptosphaeria gen. nov., Lentomitella,Spadicoides and
Torrentispora (Sordariomycetes)
M. R
eblov
a
1*
, A.N. Miller
2
,K.R
eblov
a
3
, and V.
St
ep
anek
4
1
Institute of Botany of the Czech Academy of Sciences, Průhonice 252 43, Czech Republic;
2
Illinois Natural History Survey, University of Illinois, Champaign, IL 61820,
USA;
3
Central European Institute of Technology, Masaryk University, Brno 625 00, Czech Republic;
4
Institute of Microbiology of the Czech Academy of Sciences, Prague
142 20, Czech Republic
*Correspondence:M.R
eblov
a,
martina.reblova@ibot.cas.cz
Abstract: The genus Ceratostomella has a long history of taxonomic confusion. While species with evanescent asci have been transferred to the Microascales and
Ophiostomatales, the taxonomic status of species with persistent asci has not been completely resolved. In previous studies using DNA sequence data, cultures and
morphology, several Ceratostomella spp. were allocated in 13 genera in the Eurotiomycetes and Sordariomycetes. In our study, the systematics of the remaining
Ceratostomella spp. with persistent asci is revisited with new collection data, cultures and phylogeny based on novel DNA sequences from six nuclear loci. Bayesian
inference and Maximum Likelihood analyses support the monophyly of several wood-inhabiting species formerly classied in Ceratostomella and other unknown
morphologically similar taxa and their division into four genera, i.e. Lentomitella,Spadicoides,Torrentispora and the newly described Calyptosphaeria. This robust clade
represents the order Xenospadicoidales in the Sordariomycetidae. Comparative analysis of the ITS2 secondary structure revealed a genetic variation among Lentomitella
isolates; 11 species were recognised, of which ve are newly introduced and two are new combinations. Other taxonomic novelties include four new species and eight
new combinations in Calyptosphaeria,Spadicoides, and Torrentispora. Molecular data suggest that Spadicoides is polyphyletic. The core of the genus is positioned in the
Xenospadicoidales;Spadicoides s. str. is experimentally linked with sexual morphs for the rst time. Based on DNA sequence data, the monotypic genera
Xenospadicoides and Pseudodiplococcium are reduced to synonymy under Spadicoides, while Fusoidispora and Pseudoannulatascus are synonymised with
Torrentispora. Members of the Xenospadicoidales inhabit decaying wood in terrestrial and freshwater environments and share a few morphological characters such as
the absence of stromatic tissue, ascomata with a cylindrical or rostrate neck, similar anatomies of the ascomatal walls, thin-walled unitunicate asci with a non-amyloid
apical annulus, disintegrating paraphyses, usually ellipsoidal to fusiform ascospores and holoblastic-denticulate or tretic conidiogenesis. Revised Ceratostomella spp. with
persistent asci are listed and the taxonomic status of each species is re-evaluated based on revision of the holotype and other representative material, published details
and available phylogenetic data.
Key words: Ceratostomella, Conidiogenesis, Holoblastic-denticulate, Molecular systematics, New taxa, Phaeoisaria-like, Selenosporella-like, Tretic, Taxonomy,
Xenospadicoidales.
Taxonomic novelties: New genus: Calyptosphaeria R
eblov
a & A.N. Mill; New species: Calyptosphaeria collapsa R
eblov
a & A.N. Mill., C. tenebrosa R
eblov
a & A.N.
Mill., Lentomitella magna R
eblov
a, L. obscura R
eblov
a, L. striatella R
eblov
a, L. sulcata R
eblov
a, L. tenuirostris R
eblov
a, Torrentispora calembola R
eblov
a & A.N. Mill.,
T. novae-zelandiae R
eblov
a & A.N. Mill; New combinations: Calyptosphaeria subdenudata (Peck) R
eblov
a & A.N. Mill., C. tropica (Huhndorf et al.)R
eblov
a & A.N. Mill.,
Lentomitella conoidea (Feltg.) R
eblov
a, L. investita (Schw.) R
eblov
a, Spadicoides fuscolutea (Rehm) R
eblov
a, S. hyalostoma (Munk) R
eblov
a, Spadicoides iberica (Hern.-
Restr. et al.)R
eblov
a & A.N. Mill., Torrentispora aquatica (Vijaykr. et al.)R
eblov
a & A.N. Mill., T. biatriispora (K.D. Hyde) R
eblov
a & A.N. Mill., T. dubia (Sacc.) R
eblov
a&
A.N. Mill.
Available online 6 December 2017; https://doi.org/10.1016/j.simyco.2017.11.004.
INTRODUCTION
The perithecial ascomycete genus Ceratostomella (Saccardo
1878a) has a long history of taxonomic debate. Although the
simple generic diagnosis comprised only hyaline, aseptate as-
cospores, asci and perithecia, which are similar to those of
Ceratostoma (Fries 1818), Ceratostomella soon became a large,
heterogeneous assemblage of fungi for which Index Fungorum
lists 110 epithets. Although widely distributed throughout the
Northern Hemisphere, members of Ceratostomella are incon-
spicuous and difcult to nd due to their small immersed to
supercial, long-necked ascomata. The asci are persistent or
evanescent containing septate or aseptate, hyaline or brown
ascospores, and most of the species are difcult to culture.
The homogeneity of Ceratostomella was soon challenged by
Kuntze (1898), who transferred 29 species with persistent asci
and mostly hyaline ascospores to Amphitrichum (Nees & Nees
1818). Amphitrichum was emended by Corda (1837) based on
A. olivaceum (= ? Cladosporium sp. de Hughes 1958), but later it
was determined to be a nomen dubium de Hughes (1958),asno
type specimen was given. Kuntze (1898) clearly misinterpreted
the generic concept of Amphitrichum, which is likely a dematia-
ceous hyphomycete. Another step towards clarication of the
concept of Ceratostomella was made by Höhnel (1906a).Len-
tomitella, originally described as a monotypic genus for Cera-
tostomella vestita, was introduced in order to segregate taxa with
ellipsoidal, 1-septate, hyaline, longitudinally striate ascospores
from species with similar ascospores containing more than one
septum and 24 large drops. Höhnel (1906a) suggested that
such taxa should belong to Ceratosphaeria and Lentomita.
However, von Arx (1952) did not accept Höhnel's narrow concept
and designated Ceratostomella as the correct generic name.
The broadly perceived Ceratostomella was redened by
R
eblov
a (2006) based on the lectotype species, C. rostrata
Peer review under responsibility of Westerdijk Fungal Biodiversity Institute.
© 2017 Westerdijk Fungal Biodiversity Institute. Production and hosting by ELSEVIER B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 89: 162 (2018).
1
(Clements & Shear 1931), and three other accepted species.
Using comparative morphology, Ceratostomella was conned to
taxa with non-stromatic ascomata with a cylindrical neck, asco-
matal wall up to 100 μm thick, persistent clavate asci arising from
supporting ascogenous cells, broad-celled paraphyses and
brown, aseptate, ellipsoidal to reniform ascospores. Based on
DNA sequence data of two representative species, C. cuspidata
and C. pyrenaica, the genus was classied as Sordariomycetidae
incertae sedis. Species with evanescent asci and dark perithecia
with liform necks were recombined and placed in Ceratocystis,
Huntiella and Thielaviopsis of the Microascales,orLep-
tographium,Ophiostoma and Pesotum of the Ophiostomatales
(Höhnel 1918, Elliott 1925, Moreau 1952, Hunt 1956, de Beer
et al. 2013a, b, 2014). Based on multigene phylogenetic ana-
lyses, the placement of the remaining Ceratostomella spp. with
persistent asci was partially resolved resulting in the recovery of
three robust phylogenetic lineages centred around the Amplis-
tromatales,Calosphaeriales and Ophiostomatales. The genus
Wallrothiella (Saccardo 1882)(Amplistromatales)basedon
W. congregata [= Ceratostomella sphaerosperma] was redened
with the aid of DNA sequence data, recently collected material
and an acrodontium-like asexual morph (R
eblov
a & Seifert 2004,
Huhndorf et al. 2009). Several other Ceratostomella species were
reclassied in Jattaea and Togniniella (Calosphaeriales) and
Phaeoacremonium (Togniniales) based on the revision of type
material, evidence from molecular data and phialophora- or
acremonium-like asexual morphs producing phialidic conidia
in vitro (R
eblov
aet al. 2004, 2015a, R
eblov
a 2011, Gramaje et al.
2015). The ophiostomataceouslineage comprised Ceratosto-
mella s. str. and also Barbatosphaeria,Lentomitella,Natantiella,
and Xylomelasma (Höhnel 1906a, R
eblov
a 2006, 2007, Huhndorf
et al. 2008, Marincowitz et al. 2008, R
eblov
a&
St
ep
anek 2009).
The asexual morphs linked with genera of this lineage are
dematiaceous hyphomycetes with holoblastic conidia produced
on a sympodially extending rachis or on a terminal cluster of
denticles. They are part of the life cycle of Barbatosphaeria as
ramichloridium- and sporothrix-like (Samuels & Candoussau
1996, R
eblov
a 2007, R
eblov
aet al. 2015b) and Lentomitella as
phaeoisaria-like (R
eblov
a2006) asexual morphs. Other Cera-
tostomella spp. were dispersed to Ceratosphaeria (Magnapor-
thales)(Niessl 1876, Huhndorf et al. 2008), Chaetosphaeria
(Chaetosphaeriales)(Booth 1957, Huhndorf & Fern
andez 2005),
Daruvedia (Pyrenulales)(Dennis 1988) and Pseudorhynchia
(Hypocreales)(Samuels & Barr 1997).
The ongoing taxonomic revision of species of Ceratostomella
s. lat. with persistent asci revealed for many of them striking
morphological similarities with Lentomitella. Based on nucLSU
and nucSSU rDNA sequence data, comparative morphology and
cultures, Lentomitella was reinstated in the Sordariomycetidae
and shown to be distantly related to Ceratostomella (R
eblov
a
2006). The generic concept of Lentomitella was expanded to
include species with 13-septate, longitudinally striate, hyaline
ascospores, and also aseptate, smooth-walled, hyaline (R
eblov
a
2006) and brown ascospores (Huhndorf et al. 2008). Members of
Lentomitella bear a certain resemblance to Torrentispora (Hyde
et al. 2000) and Pseudoannulatascus (Luo et al. 2015) charac-
terised by ascomata with a long-neck, cylindrical asci and fusi-
form, hyaline, smooth- and thick-walled, usually aseptate
ascospores, rarely with delayed formation of septa (Hyde et al.
2000, Fryar & Hyde 2004, Barbosa et al. 2013). A monotypic
family, the Lentomitellaceae, was introduced by Zhang et al.
(2017).
In this study, several species historically treated in Ceratos-
tomella were recollected and isolated in axenic culture. Together
with other unknown, morphologically similar taxa resembling
Lentomitella and Torrentispora were subjected to phylogenetic
analyses. Fungi of this assemblage occur on decaying wood or
in bark in terrestrial habitats or on wood submerged in water.
They share a simple inconspicuous morphology of non-stromatic
ascomata with a cylindrical or rostrate neck, hyaline or brown,
aseptate or septate, ornamented or smooth-walled ascospores,
persistent asci with a non-amyloid apical annulus and partially
disintegrating paraphyses. Little is known about their asexual
morphs, which so far include only phaeoisaria-like morphs linked
with Lentomitella. However, the majority of these fungi are dif-
cult to culture or they produce only sterile mycelium in vitro.
Recently, we found Ceratostomella fuscolutea (Rehm 1908),
Ceratostomella hyalostoma (Untereiner 1993), and an unknown
lentomitella-like species to produce Spadicoides asexual morphs
in vitro. This dematiaceous hyphomycete is characterised by
polytretic conidiogenous cells, unbranched conidiophores and
dark brown septate or aseptate conidia borne singly or in short
chains (Hughes 1958, Ellis 1963) and has not yet been linked
with any sexually reproducing ascomycetes as a part of their life
cycle. DNA sequence data suggest that Spadicoides is poly-
phyletic (Shenoy et al. 2010); S. atra was shown closely related
to Lentomitella.Hern
andez-Restrepo et al. (2017) conrmed the
placement of S. bina, the type species, in the Cordanales and
segregated S. atra from Spadicoides into a monotypic genus
Xenospadicoides in the Xenospadicoidales.
In order to unravel this part of the fungal tree of life, determine
the placement of Ceratostomella spp. listed above and other
similar taxa in monophyletic genera and resolve their familial and
ordinal relationships, we employed a polyphasic approach in this
study. We generated a multigene-based phylogeny of six nuclear
ribosomal and protein-coding loci of the new isolates and inten-
sively examined morphological characters of specimens and
isolates in pure culture. We also investigated intraspecicre-
lationships among members of Lentomitella using the Compen-
satory Base Change (CBC) criterion in the ITS2 secondary (2D)
structure in two most conserved helices II and III (Mai & Coleman
1997, Coleman 2009) and also in helix I (Müller et al. 2007). The
ITS2 is a fast-evolving part of the nuclear-coded rRNA operon,
which has proven useful for formulating molecular taxonomic
concepts, and its 2D structure has a potential to predict sexual
incompatibility among closely related organisms. The CBC hy-
pothesis is based on occurrence of compensatory base changes,
i.e. co-evolution of nucleotides involved in the double-sided
substitution in helices of the ITS2 molecule (Coleman 2000,
Müller et al. 2007). We performed in-depth comparative ana-
lyses of ITS2 2D structures of Lentomitella spp. and mapped all
existing substitutions among co-evolving nucleotides onto the
predicted 2D model of ITS2 of the type species L. vestita.
MATERIAL AND METHODS
Herbarium material and fungal strains
Herbarium material was rehydrated with water and examined
with an Olympus SZX12 dissecting microscope; hand-sectioned
ascomata, centrum material (including asci, ascospores and
paraphyses), conidiophores and conidia from living cultures were
R
EBLOV
AET AL.
2
mounted in 90 % lactic acid, Melzer's reagent or Lugol's iodine.
All measurements were made in Melzer's reagent.
Means ± standard deviation (SD) based on 2025 measure-
ments are given for dimensions of asci, ascospores, con-
idiogenous cells and conidia. Microscopic structures were
examined using an Olympus BX51 compound microscope
(Olympus America, Inc., Melville, USA) with differential interfer-
ence contrast (DIC) and phase contrast (PC) illumination. Im-
ages of microscopic structures were captured with an Olympus
DP70 camera operated by Imaging Software Cell^D (Olympus).
Macroscopic images of colonies were documented using an
Olympus C-3030 digital camera with daylight spectrum 5600K
16W LED lights. All images were processed with Adobe Pho-
toshop CS6 (Adobe Systems, San Jose, USA).
Cultures were maintained on Modied Leonian's agar (MLA)
(Malloch 1981). For comparative purposes, strains were grown
on MLA and potato-carrot agar (PCA) (Gams et al. 1998). De-
scriptions of colonies are based on 28-d-old cultures. Ex-type
and other cultures are maintained at the Westerdijk Fungal
Biodiversity Institute (CBS), Utrecht, the Netherlands and the
International Collection of Microorganisms from Plants (ICMP),
Auckland, New Zealand. Type and other herbarium material are
deposited in the Herbarium of the Institute of Botany (PRA),
Průhonice, Czech Republic, the New Zealand Fungarium (PDD),
Auckland, New Zealand, and the Illinois Natural History Survey
Fungarium (ILLS), Champaign, Illinois, USA.
DNA extraction, amplication and sequencing
Total genomic DNA was extracted from either mycelium removed
from 14-d-old cultures grown on MLA or mature ascomata from
herbarium material using the UltraClean Microbial DNA Kit
(MoBio Laboratories Inc., Carlsbad, USA). For DNA extracted
from herbarium material, an alternative lysis method was incor-
porated: the gelatinous centrum of 1015 ascomata was satu-
rated with distilled water, carefully removed with a needle and
placed in a 1.9 mL MicroBead tube provided by the manufac-
turer. After the fungal material was dissolved in 300 μLof
MicroBead Solution and 50 μL of Solution MD1, the preparations
were heated to 65 ºC for 10 min. The remaining steps for DNA
extraction from cultures and herbarium material followed the
manufacturer's protocol for lamentous fungi. All amplications
were carried out in 0.5 mL thin-walled PCR tubes (Eppendorf
AG, Hamburg, Germany) using a PTC-200 thermal cycler (MJ
Research Inc., Watertown, USA). PCR reactions and primers
used for the amplication and sequencing of the internal tran-
scribed spacer (ITS) of the nuclear rRNA cistron, portions of the
nuclear ribosomal large subunit (nucLSU) and small subunit
(nucSSU) RNA gene, and segments 57 of the second largest
subunit of RNA polymerase II (rpb2) were carried out according
to the methods of R
eblov
aet al. (2017).
Primers used for the amplication and sequencing of other
genes included: 1) ACT-512F and ACT-783R (Carbone & Kohn
1999) for alpha-actin (act1) gene and 2) T1 and Bt2a in combi-
nation with Bt2b (Glass & Donaldson 1995, ODonnell & Cigelnik
1997) for exons 26 of beta-tubulin (tub2) gene. PCR reactions
containing 4 mM MgSO
4
were performed using Platinum
®
Taq
DNA polymerase High Fidelity (Invitrogen, Carlsbad, USA) in
25 μL volume reactions. PCR conditions were (act1) 2 min at
94 °C, 4548 cycles of 30 s at 94 °C, 30 s at 5455 °C and 30 s at
68 °C; (tub2) 2 min at 94 °C, 4048 cycles of 30 s at 94 °C, 30 s at
5456 °C and 4560 s at 68 °C, with a nal extension of 10 min at
68 °C for all amplications. Amplicons were either puried directly
from PCR solution after amplication or isolated from agarose gel
using the High Pure PCR Product Purication Kit (Roche Applied
Science, Mannheim, Germany) following the manufacturer'sdi-
rections. Automated sequencing was carried out by GATC
Sequencing Service (Cologne, Germany). Raw sequence data
were assembled, examined and edited using Sequencher v. 5.4.1
software (Gene Codes Corp., Ann Arbor, USA).
GenBank accession numbers for act1, ITS, nucLSU,
nucSSU, rpb2 and tub2 sequences generated during this study
and homologous sequences of representatives of the Sordar-
iomycetes and Leotiomycetes retrieved from GenBank are listed
in Table 1. Retrievable sequences have been published in
various studies, e.g. Suh & Blackwell (1999), Huhndorf et al.
(2004), Miller & Huhndorf (2004a, 2005), R
eblov
a & Seifert
(2004), R
eblov
a (2006, 2013), Arzanlou et al. (2007),
Spatafora et al. (2007), Damm et al. (2008), Schoch et al.
(2009), Shenoy et al. (2010), R
eblov
aet al. (2011, 2015b,
2016), Jaklitsch et al. (2013) Untereiner et al. (2013),
Hern
andez-Restrepo et al. (2014), Su et al. (2016).
Sequence alignment
ITS, nucLSU, nucSSU and rpb2 sequences were manually
aligned in BioEdit v. 7.1.8 (Hall 1999). Alignments of act1 and
tub2 sequences were generated in MAFFT v. 7 (Katoh &
Standley 2013) and manually corrected where necessary.
Consensus 2D structure models for the ITS1 and ITS2 were
obtained for all members of the Xenospadicoidales and used to
determine positions of homologous nucleotides in the ITS
alignment. Introns occurring in nucLSU and nucSSU were
delimited manually and excluded from the alignment; in addition,
438 nucleotides (nt) of nucLSU at the 3
0
-end and 127 nt of
nucSSU at the 5
0
-end were excluded from the alignment
because of the incompleteness in the majority of sequences.
The single-locus data sets were examined for topological
incongruence among loci for members of the Xenospadicoidales
(act1: 35 sequences/338 characters including gaps, ITS: 37/757,
nucLSU: 39/1 842, nucSSU: 34/1 668, rpb2: 29/1 127, tub2: 28/
966), and members of the Sordariomycetidae (nucLSU: 104/
1 973, nucSSU: 71/1 787, rpb2: 65/1 189). Congruence among
the loci was tested using the 70 % reciprocal bootstrap criterion
(Mason-Gamer & Kellogg 1996). For each individual partition,
1 000 bootstrap replicates were generated with RAxML-HPC v.
7.0.3 (Stamatakis 2006) and PAUP v. 4.0b10 (Swofford 2002)
and compared visually for topological conict among supported
clades in phylogenetic trees. The conict-free alignments were
concatenated into a multi-locus alignment that was subjected to
subsequent phylogenetic analyses. The multiple sequence
alignment is deposited in TreeBASE (S21034).
Phylogenetic analyses
In order to explore monophyly and infrageneric relationships
within Lentomitella,Spadicoides,Torrentispora and other
morphologically similar taxa, and to resolve their phylogenetic
relationships in a broader context we performed analyses of
combined act1, ITS, nucLSU, nucSSU, rpb2 and tub2 sequences
on two datasets: a reduced dataset consisting of members of
these genera and a full dataset consisting of these taxa along
SORDARIOMYCETES
www.studiesinmycology.org 3
Table 1. List of fungi, isolate information and new sequences determined for this study and those retrieved from GenBank. The asterisk (*) denotes ex-type strains of members of the
Xenospadicoidales. GenBank accession numbers in bold were generated for this study.
Classication Taxon Source GenBank accession numbers
nucLSU nucSSU rpb2 ITS act1 tub2 References
Annulatascales Annulatascus velatisporus A 70-18 AY316354 – ––––Raja et al. (2003)
Annulusmagnus triseptatus CBS 131483 GQ996540 JQ429242 JQ429258 –––R
eblov
aet al. (2010, 2012)
Ascitendus austriacus CBS 131685 GQ996539 GQ996542 JQ429257 –––R
eblov
aet al. (2010, 2012)
Atractosporales Atractospora decumbens CBS 139032 KT991658 KT991640 KT991647 –––R
eblov
aet al. (2016)
A. ellipsoidea A 411-3 AY316356 – ––––Raja et al. (2003)
A. reticulata CBS 127884 KT991660 KT991649 –––R
eblov
aet al. (2016)
A. verruculosa CBS 132040 KT991659 KT991641 KT991648 –––R
eblov
aet al. (2016)
Rubellisphaeria abscondita CBS 132078 KT991666 KT991646 KT991657 –––R
eblov
aet al. (2016)
Barbatosphaeriaceae Barbatosphaeria barbirostris CBS 121149 EF577059 KM492851 KM492903 –––R
eblov
aet al. (2015b)
B. dryina CBS 127691 KM492864 KM492852 KM492904 –––R
eblov
aet al. (2015b)
Boliniales Camarops microspora CBS 649.92 AY083821 DQ471036 DQ470937 –––Smith et al. (2003), Spatafora et al. (2007)
Apiorhynchostoma curreyi UAMH 11088 JX460989 KY931894 KY931926 –––Untereiner et al. (2013), this study
Endoxyla operculata UAMH 11085 JX460992 KY931895 KY931927 –––Untereiner et al. (2013), this study
Calosphaeriales Calosphaeria pulchella CBS 115999 AY761075 AY761071 GU180661 –––R
eblov
aet al. (2004, 2011)
Jattaea algeriensis CBS 120871 EU367457 EU367462 HQ878603 –––Damm et al. (2008), R
eblov
a (2011)
Togniniella acerosa CBS 113648 AY761076 AY761073 GU180660 –––R
eblov
aet al. (2004), R
eblov
a (2011)
Chaetosphaeriales Chaetosphaeria ciliata ICMP 18253 GU180637 GU180614 GU180659 –––R
eblov
aet al. (2011)
C. curvispora ICMP 18255 GU180636 AY502933 GU180655 –––R
eblov
aet al. (2011)
Melanochaeta hemipsila S.M.H. 2125 AY346292 AY780184 –––Huhndorf et al. (2004), Miller & Huhndorf (2005)
Coniochaetales Barrina polyspora AWR 9560A AY346261 – – –––Huhndorf et al. (2004)
Coniochaeta discoidea SANK 12878 AY346297 AJ875179 AY780191 –––Huhndorf et al. (2004), García et al. (2006)
C. ostrea CBS 507.70 DQ470959 DQ471007 DQ470909 –––Spatafora et al. (2007)
Cordanales Cordana terrestris ICMP 15117 EF063573 – ––––R
eblov
a & Seifert (2007)
C. pauciseptata M.R. 1150 AF178563 – – –––R
eblov
a & Winka (2000)
C. pauciseptata CBS 113708 EF204507 EF204490 –––Shenoy et al. (2010)
C. pauciseptata IMI 102120 HE672158 – – –––Hern
andez-Restrepo et al. (2014)
C. ellipsoidea IMI 229746 HE672156 – ––––Hern
andez-Restrepo et al. (2014)
C. inaequalis CBS 508.83 HE672157 – – –––Hern
andez-Restrepo et al. (2014)
Diaporthales Diaporthe phaseolorum FAU 458, NRRL 13736 U47830 L36985 AY641036 –––Spatafora & Blackwell (1993), Reeb et al. (2004)
Gnomonia gnomon CBS 199.53 AF408361 DQ471019 DQ470922 –––Castlebury et al. (2002), Spatafora et al. (2007)
Valsa ambiens AR 3516 AF362564 DQ862056 DQ862025 –––Zhang et al. (2007)
Distoseptisporaceae Distoseptispora uminicola MFLUCC 15-0417 KU376270 – – –––Su et al. (2016)
D. aquatica MFLUCC 15-0374 KU376268 – – –––Su et al. (2016)
D. adscendens HKUCC 10820 DQ408561 DQ435092 –––Shenoy et al. (2006)
D. leonensis HKUCC 10822 DQ408566 DQ435089 –––Shenoy et al. (2006)
Jobellisiales Jobellisia fraterna S.M.H. 2863 AY346285 – – –––Huhndorf et al. (2004)
J. luteola S.M.H. 2753 AY346286 – – –––Huhndorf et al. (2004)
Magnaporthales Gaeumannomyces graminis AR 3401, M 57 AF362557 JF414874 ––––Farr et al. (2001), Zhang et al. (2011)
Macgarvieomyces borealis CBS 461.65 DQ341511 DQ341489 KM485070 –––Thongkantha et al. (2009), Klabauf et al. (2014)
R
EBLOV
AET AL.
4
Table 1. (Continued).
Classication Taxon Source GenBank accession numbers
nucLSU nucSSU rpb2 ITS act1 tub2 References
Magnaporthe grisea Ina168, 70-15 AB026819 DQ493955 ––––Sone et al. (2000), Rehmeyer et al. (2006)
Myrmecridiales Myrmecridium exuosum CBS 398.76 EU041825 ––EU041768 ––Arzanlou et al. (2007)
M. montsegurinum PRM 934684 KT991664 KT991645 KT991654 KT991674 ––R
eblov
aet al. (2016)
M. schulzeri CBS 100.54 EU041826 ––EU041769 ––Arzanlou et al. (2007)
Ophiostomatales Ceratocystiopsis minuta UM 1533, WIN(M)1537 EU913657 HQ634854 ––––Plattner et al. (2009), Hafez et al. (2012)
Fragosphaeria purpurea CBS 133.34 AF096191 AF096176 ––––Suh & Blackwell (1999)
Ophiostoma piliferum CBS 158.74 DQ470955 DQ471003 DQ470905 –––Spatafora et al. (2007)
Raffaelea ambrosiae CBS 185.64 EU984297 AY497518 –––Gebhardt et al. (2004), Massoumi Alamouti et al. (2009)
Papulosaceae Brunneosporella aquatica HKUCC 3708 AF132326 – – –––Ranghoo et al. (1999)
Fluminicola coronata HKUCC 3717 AF132332 – ––––Ranghoo et al. (1999)
Papulosa amerospora J.K. 5547F DQ470950 DQ470998 DQ470901 –––Spatafora et al. (2007)
Phomatosporales Lanspora coronata J.K. 4839A U46889 DQ470996 DQ470899 –––Spatafora et al. (1998, 2007)
Phomatospora bellaminuta J.K. 5543N FJ176857 FJ176803 FJ238345 –––Schoch et al. (2009)
Sordariales Gelasinospora tetrasperma CBS 178.33 DQ470980 DQ471032 DQ470932 –––Spatafora et al. (2007)
Lasiosphaeria ovina S.M.H. 1538, CBS 958.72 AF064643 AY083799 AY600292 –––Fern
andez et al. (1999), Smith et al. (2003),
Miller & Huhndorf (2004a)
Sordaria micola S.M.H. 4106, MUCL 937, CBS 723.96 AY780079 X69851 DQ368647 –––Miller & Huhndorf (2005), Tang et al. (2007)
Sporidesmiaceae Sporidesmium parvum HKUCC 10836 DQ408558 – ––––Shenoy et al. (2006)
S. minigelatinosa NN 47497 DQ408567 DQ435090 –––Shenoy et al. (2006)
S. bambusicola HKUCC 3578 DQ408562 – ––––Shenoy et al. (2006)
S. uminicola MFLUCC 15-0346 KU376271 – – –––Su et al. (2016)
S. aquaticum MFLUCC 15-0420 KU376273 – – –––Su et al. (2016)
S. submersum MFLUCC 15-0421 KU376272 – – –––Su et al. (2016)
Togniniales Phaeoacremonium minimum CBS 213.31, CBS 111015 AY761082 AY761068 HQ878610 –––R
eblov
aet al. (2004), R
eblov
a (2011)
P. fraxinopennsylvanicum CBS 128920 HQ878595 HQ878600 HQ878609 –––R
eblov
a (2011)
Woswasiaceae Woswasia atropurpurea CBS 133167 JX233658 JX233658 JX233659 –––Jaklitsch et al. (2013)
Xylochrysis lucida CBS 135996 KF539911 KF539912 KF539913 –––R
eblov
aet al. (2014)
Xenospadicoidales Calyptosphaeria collapsa PRA-12743* KY931834 KY931892 KY931861 KY931808 KY931771 KY931924 This study
C. subdenudata S.M.H. 3877* EU527994 ––
KY931774 KY931739 Huhndorf et al. (2008), this study
C. subdenudata S.M.H. 2534 EU527993 ––KY931775 KY931740 Huhndorf et al. (2008), this study
C. tenebrosa PRA-12742 –––KY931776 KY931741 This study
C. tenebrosa PRA-12741 KY931809 KY931864 KY931836 KY931777 KY931742 KY931898 This study
C. tenebrosa PRA-12740* KY931810 KY931865 KY931837 KY931778 KY931743 KY931899 This study
C. tropica S.M.H. 1797* EU527992 KY931866 KY931779 KY931744 Huhndorf et al. (2008), this study
C. tropica S.M.H. 3225 EU527999 – ––––Huhndorf et al. (2008), this study
Lentomitella cirrhosa ICMP 15131* AY761085 AY761089 KM492911 KY931780 KY931745 KY931900 R
eblov
a (2006), R
eblov
aet al. (2015b), this study
L. crinigera CBS 138678 KY931811 KY931867 KY931781 KY931746 KY931901 This study
L. conoidea CBS 131481 KT991663 KT991644 KT991653 KY931782 KY931747 R
eblov
aet al. (2016), this study
L. conoidea CBS 131660 KY931812 KY931868 KY931840 KY931783 KY931748 KY931902 This study
L. conoidea CBS 141370 KY931813 KY931869 KY931841 KY931784 KY931749 KY931903 This study
(continued on next page)
SORDARIOMYCETES
www.studiesinmycology.org 5
Table 1. (Continued).
Classication Taxon Source GenBank accession numbers
nucLSU nucSSU rpb2 ITS act1 tub2 References
L. conoidea M.R. 3135 KY931814 KY931870 KY931842 KY931785 KY931750 KY931904 This study
L. magna ICMP 18371* KY931815 KY931871 KY931843 KY931786 KY931751 This study
L. obscura CBS 137799 KY931816 KY931872 KY931844 KY931787 KY931752 KY931905 This study
L. obscura CBS 138735 KY931817 KY931873 KY931788 KY931753 KY931906 This study
L. obscura CBS 138736* KY931818 KY931874 KY931845 KY931789 KY931754 KY931907 This study
L. striatella ICMP 18369* KY931819 KY931875 KY931846 KY931790 KY931755 KY931908 This study
L. sulcata ICMP 15124* AY761086 KY931876 KY931847 KY931791 KY931756 KY931909 This study
L. tenuirostris CBS 138734* KY931821 KY931877 KY931849 KY931792 KY931758 KY931910 This study
L. tenuirostris CBS 141371 KY931822 KY931878 KY931850 KY931793 KY931759 KY931911 This study
L. vestita PRA-12739 KY931820 KY931879 KY931848 KY931794 KY931757 This study
Lentomitella sp. M.R. 2953 KY931823 KY931880 KY931795 KY931912 This study
Spadicoides atra CBS 489.77 EF204506 EF204521 EF204489 –––Shenoy et al. (2010)
S. bina CBS 137794 KY931824 KY931881 KY931851 KY931796 KY931760 KY931913 This study
S. fuscolutea CBS 141262 KY931825 KY931882 KY931852 KY931797 KY931761 KY931914 This study
S. fuscolutea CBS 141263 KY931826 KY931883 KY931853 KY931798 KY931762 KY931915 This study
S. hyalostoma CBS 131268 KY931827 KY931884