Content uploaded by Chun-Lin Yang
Author content
All content in this area was uploaded by Chun-Lin Yang on Apr 17, 2020
Content may be subject to copyright.
1 23
Mycological Progress
ISSN 1617-416X
Volume 18
Number 6
Mycol Progress (2019) 18:833-845
DOI 10.1007/s11557-019-01492-4
Parakarstenia phyllostachydis, a new
genus and species of non-lichenized
Odontotremataceae (Ostropales,
Ascomycota)
Chunlin Yang, Hans-Otto Baral, Xiulan
Xu & Yinggao Liu
1 23
Your article is protected by copyright and
all rights are held exclusively by German
Mycological Society and Springer-Verlag
GmbH Germany, part of Springer Nature. This
e-offprint is for personal use only and shall not
be self-archived in electronic repositories. If
you wish to self-archive your article, please
use the accepted manuscript version for
posting on your own website. You may
further deposit the accepted manuscript
version in any repository, provided it is only
made publicly available 12 months after
official publication or later and provided
acknowledgement is given to the original
source of publication and a link is inserted
to the published article on Springer's
website. The link must be accompanied by
the following text: "The final publication is
available at link.springer.com”.
ORIGINAL ARTICLE
Parakarstenia phyllostachydis, a new genus and species
of non-lichenized Odontotremataceae (Ostropales, Ascomycota)
Chunlin Yang
1
&Hans-Otto Baral
2
&Xiulan Xu
1,3
&Yinggao Liu
1
Received: 19 December 2018 / Revised: 31 March 2019 / Accepted: 4 April 2019
#German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
The new species Parakarstenia phyllostachydis was discovered on stems of Phyllostachys heteroclada in Sichuan Province of
China and is placed in a new genus within Odontotremataceae in this paper. A multigene analysis of a combined nuclear ITS and
LSU rDNA and mtSSU sequence dataset and comparable morphologies suggests the taxonomic affinity of the new taxon in this
family. Maximum likelihood and Bayesian inference phylogenetic analyses provide evidence that the fungus is best placed in a
distinct genus within this family. The new genus is compared with similar genera of Ostropales and a comprehensive description
and illustration are offered. Parakarstenia is characterized by its distinct suite of features, such as initially immersed, intracortical,
later erumpent and seemingly superficial, sessile and usually gregarious apothecia with a flat to slightly convex, greyish white or
pale brown disc; a hairless, buff to yellow receptacle; a non-protruding margin, absent periphysoids and crystals, cylindrical to
clavate asci with conical apex and a hemiamyloid (type RR) outer wall; and narrowly cylindrical-clavate to fusoid, vermiform,
straight to medium curved, initially non-septate, at maturity transversely multiseptate ascospores. An updated phylogram for
Ostropales with selected, predominantly non-lichenized members based on multigene analysis is provided.
Keywords New genus and species .Bambusicolous fungi .Karstenia .Phylogeny .Taxo nomy
Introduction
The class Lecanoromycetes O.E. Erikss. & Winka, formally
erectedbyErikssonandWinka(1997), constitutes one of the
largest classes of Ascomycota with more than 14,200 species
(Wedin et al. 2005a; Miadlikowska et al. 2014; Gueidan et al.
2015; Lücking et al. 2017;Kraichaketal.2018) and currently
includes four subclasses, namely Acarosporomycetidae,
Lecanoromycetidae, Ostropomycetidae and
Umbilicariomycetidae (Voglmayr et al. 2019). This class com-
prises the largest number of lichen-forming ascomycetes, of
which the majority (over 95%) are lichenized species
(Eriksson et al. 2004; Lumbsch and Huhndorf 2007,2010;
Kirk et al. 2008; Miadlikowska et al. 2014; Gueidan et al.
2015;Kraichaketal.2018; Wijayawardene et al. 2018).
However, several genera comprising non-lichenized species
are incorporated within this lineage (Sherwood 1977;
Mayrhofer and Poelt 1985; Sherwood-Pike 1987; Holm and
Holm 1993; Kohlmeyer and Volkmann-Kohlmeyer 1996;
Döbbeler 2003,2006; Wedin et al. 2005b; Evans et al. 2010;
Barreto et al. 2012; Flakus and Kukwa 2012;Balochetal.
2013; Miadlikowska et al. 2014; Gueidan et al. 2015; van
Nieuwenhuijzen et al. 2016; Ohmura and Mayrhofer 2016;
Koukol et al. 2017;Jahnetal.2017; Fernández-Brime et al.
2017), namely Deltopyxis,Malvinia and Spirographa (incertae
sedis); Claviradulomyces,Coccomycetella,Odontotrema,
Odontura,Potriphila,Rogellia and Stromatothecia
(Odontotremataceae); Mycowinteria and Protothelenella
(Protothelenellaceae); and Acarosporina,Cryptodiscus,
Cyanodermella,Dendroseptoria,Karstenia,Lillicoa,Ostropa,
Propoliopsis,Robergea,Schizoxylon,Sphaeropezia,Stictis,
Stictophacidium,Thelopsis and Glomerobolus (Stictidaceae).
Most non-lichenized genera with more than 130 species are
nested within the order Ostropales of the Ostropomycetidae
(Lumbsch et al. 2007;Balochetal.2010; Gueidan et al.
2015; Diederich et al. 2018). They grow as saprophytes or
Section Editor: Gerhard Rambold
*Yinggao Liu
lyg927@263.net
1
College of Forestry, Sichuan Agricultural University, Huiming Road
211, Wenjiang, Chengdu 611130, China
2
Blaihofstraße 42, D-72074, Tübingen, Germany
3
Forestry Research Institute, Chengdu Academy of Agricultural and
Forestry Sciences, Nongke Road 200, Chengdu 611130, China
Mycological Progress (2019) 18:833–845
https://doi.org/10.1007/s11557-019-01492-4
Author's personal copy
sometimes parasites on leaves, herbaceous stems, bark and
wood of branches and trunks, mosses and ferns and lichens.
Sometimes species include several life strategies (lichenized
and saprotrophic) (Wedin et al. 2004,2006). Most species occur
on plants, but no bamboos are recorded in the known literature
(Sherwood 1977; Eriksson 1981; Sherwood-Pike 1987;
Wilberforce 1999; Döbbeler 2003,2006;Balochetal.2010,
2013; Miadlikowska et al. 2014; Gueidan et al. 2015;Liand
Hou 2016; Koukol et al. 2017; Fernández-Brime et al. 2017).
The order Ostropales was established by Nannfeldt (1932)
and was for a long time the largest order in Ostropomycetidae
(Baloch et al. 2010;Miadlikowskaetal.2014; Gueidan et al.
2015). Now only two families are recognized with over 180
species (Kraichak et al. 2018; Index Fungorum 2019), viz.
Odontotremataceae and Stictidaceae, while other families
were transferred to Baeomycetales, Graphidales and
Gyalectales. In the new circumscription, a majority of mem-
bers of Ostropales are characterized by a special type of
hemiangiocarpous ascoma ontogeny and the hymenia and asci
being hemiamyloid, i.e. the entire ascus wall reacts red in
Lugol’s solution (IKI), while no reaction is obtained in
Melzer’s reagent (MLZ) and a blue reaction in either reagent
when KOH-pretreated (Baral 2009; Lumbsch et al. 2007;
Baloch et al. 2010; Gueidan et al. 2015). Due to the huge
diversity in phenotypic characters and large-scale phylogeny,
the circumscription of Ostropales has frequently changed over
time (Table 1). It is worth mentioning that Kraichak et al.
(2018) recently addressed the circumscription of families
and orders within Ostropomycetidae using the temporal
banding approach, which is an effective method to appraise
the phylogenetic placement of taxa above familial level, and
accepted eight orders and 32 families in Ostropomycetidae. In
this study, this delimitation is followed.
The family Odontotremataceae was introduced by
Hawksworth and Sherwood (1982) who initially accepted
eight genera, with Odontotrema as the type genus.
Sherwood-Pike (1987) subsequently presented a monograph
of Odontotremataceae and reappraised the circumscription in
which Spilomela was excluded and two genera
(Coccomycetella and Pleospilis)were included. Since that
time, five genera were introduced to the family (Döbbeler
1996,1999;Magnes1997; Calatayud et al. 2001;Lumbsch
and Huhndorf 2007; Evans et al. 2010) and nine transitional
genera were transferred to other groups or determined as syn-
onymous (Holien and Triebel 1996; Diederich et al. 2002,
2018;Balochetal.2009,2013; Zhurbenko and
Yakovchenko 2014; Suija et al. 2015; Wijayawardene et al.
2018), namely Bryodiscus (a synonym of Sphaeropezia in
Table 1 The circumscription of the order Ostropales as it changed during the past decade
Lumbsch and
Huhndorf (2007)
Lumbsch and
Huhndorf (2010)
Miadlikowska et al. (2014);
Gueidan et al. (2015)
Lücking et al.
(2017)
Wijayawardene
et al. (2018)
Zhurbenko and Etayo (2013);
Diederich (2014,2018);
Kraichak et al. (2018); This study
Families
Coenogoniaceae Coenogoniaceae Coenogoniaceae Coenogoniaceae Coenogoniaceae Odontotremataceae
Gomphillaceae Gomphillaceae Graphidaceae Gomphillaceae Gomphillaceae Stictidaceae
Graphidaceae Graphidaceae Gyalectaceae Graphidaceae Graphidaceae
Gyalectaceae Gyalectaceae Myeloconidaceae Gyalectaceae Gyalectaceae
Myeloconidaceae Myeloconidaceae Odontotremataceae Phlyctidaceae Odontotremataceae
Odontotremataceae Odontotremataceae Phaneromycetaceae Porinaceae Phaneromycetaceae
Phaneromycetaceae Phaneromycetaceae Phlyctidaceae Protothelenellaceae Phlyctidaceae
Phlyctidaceae Phlyctidaceae Porinaceae Sagiolechiaceae Porinaceae
Porinaceae Porinaceae Sagiolechiaceae Stictidaceae Protothelenellaceae
Stictidaceae Stictidaceae Stictidaceae Thelenellaceae Sagiolechiaceae
Thelotremataceae Thrombiaceae Stictidaceae
Thelenellaceae
Thrombiaceae
Genera incertae sedis
Amphorothecium Amphorothecium Amphorothecium Amphorothecium Aabaarnia
?Leucogymnospora ?Leucogymnospora Anzina Anzina Amphorothecium
Malvinia Malvinia Corticifraga Biazrovia
?Phaeographopsis ?Phaeographopsis Malvinia Malvinia
Platygramme Platygraphopsis Normanogalla
Platygraphopsis ?Xyloschistes Paralethariicola
?Xyloschistes
834 Mycol Progress (2019) 18:833–845
Author's personal copy
Stictidaceae), Geltingia (a genus of Helicogoniaceae in
Phacidiales), Lethariicola (a synonym of Sphaeropezia in
Stictidaceae), Paschelkiella (a synonym of Cryptodiscus in
Stictidaceae), Pleospilis (a synonym of Spirographa in
Ostropomycetidae), Rhymbocarpus and Skyttea (two genera
of Cordieritidaceae in Helotiales) and Sphaeropezia (a genus
of Stictidaceae). Spirographa is a pendulous genus which was
transferred to Ostropomycetidae or Ostropales incertae sedis
(Diederich et al. 2018; Wijayawardene et al. 2018). Currently,
nine genera are recognized in Odontotremataceae (Diederich
et al. 2018; Wijayawardene et al. 2018; This study), i.e.
Claviradulomyces,Coccomycetella,Odontotrema,
Table 2 Molecular data used in this study and GenBank accession numbers. The newly generated sequences are highlighted in bold and red
Species Specimen voucher Family Order LSU mtSSU ITS
Absconditella sphagnorum 17 Feb 02 Palice (HB Palice) Stictidaceae Ostropales AY300824 AY300872 –
Absconditella sphagnorum M24 Stictidaceae Ostropales EU940095 EU940247 EU940172
Acarosporina microspora CBS 338.39 Stictidaceae Ostropales AY584643 AY584612 DQ782834
Carestiella socia GG2437a Stictidaceae Ostropales AY661682 AY661678 AY661682
Carestiella socia GG2410 Stictidaceae Ostropales AY661687 AY661677 AY661687
Claviradulomyces dabeicola IMI 393994 Odontotremataceae Ostropales GQ337897 GQ337898 GQ337899
Claviradulomyces xylopiae CBS 133260 Odontotremataceae Ostropales JX843525 –JX843524
Coccomycetella richardsonii EB74 Odontotremataceae Ostropales HM244761 HM244737 –
Cryptodiscus muriformis UPS F-647154 Stictidaceae Ostropales MG281962 MG281972 MG281962
Cryptodiscus muriformis H.B. 6773 Stictidaceae Ostropales MG281963 MG281973 MG281963
Cryptodiscus pallidus EB152 Stictidaceae Ostropales FJ904679 FJ904701 FJ904679
Cryptodiscus pallidus EB173 Stictidaceae Ostropales FJ904680 FJ904702 FJ904680
Cryptodiscus tabularum EB169 Stictidaceae Ostropales FJ904689 FJ904711 FJ904689
Cryptodiscus tabularum CO205 Stictidaceae Ostropales FJ904690 FJ904712 FJ904690
Cyanodermella asteris 03HOR06-2-4 Stictidaceae Ostropales KT758843 –KT758843
Cyanodermella banksiae CPC 32105 Stictidaceae Ostropales MH327850 –MH327814
Dendroseptoria mucilaginosa PRC3990 Stictidaceae Ostropales LT934543 –LT934540
Geisleria sychnogonoides Caceres & Aptroot 13560 (ABL) Stictidaceae Ostropales KC689752 KC689751 –
Geisleria sychnogonoides GESY7510 Stictidaceae Ostropales KF220304 KF220306 –
Glomerobolus gelineus OSC 100192 Stictidaceae Ostropales DQ247803 DQ247783 DQ247782
Ingvariella bispora BCNLich 17183 Stictidaceae Ostropales HQ659185 HQ659174 –
Ingvariella bispora MALich 15288 Stictidaceae Ostropales HQ659184 HQ659173 –
Karstenia macer H.B. 10084a Odontotremataceae Ostropales ––UDB035013
Karstenia macer H.B. 9770 Odontotremataceae Ostropales ––UDB034357
Karstenia rhopaloides EB100 Odontotremataceae Ostropales FJ904685 FJ904707 FJ904685
Odontotrema phacidiellum EB54 Odontotremataceae Ostropales HM244769 HM244748 –
Odontotrema phacidioides EB168 Odontotremataceae Ostropales HM244770 HM244749 –
Ostropa barbara EB85 Stictidaceae Ostropales HM244773 HM244752 HM244773
Ostropa barbara S F302817 Stictidaceae Ostropales MG281965 –MG281965
Parakarstenia phyllostachydis SICAU 16-0002 Odontotremataceae Ostropales MK296470 –MK305901
Placopsis cribellans KS167 Trapeliaceae Baeomycetales KU844626 KU844570 KU844762
Placopsis perrugosa KS168 Trapeliaceae Baeomycetales KU844627 KU844571 KU844763
Robergea cubicularis G.M. 2013-05-09.1 Stictidaceae Ostropales KY611899 –KY611899
Schizoxylon albescens GG2443a Stictidaceae Ostropales AY661690 AY661681 AY661690
Schizoxylon albescens GG2365 Stictidaceae Ostropales AY661689 AY661680 AY661689
Sphaeropezia capreae GG2560 Stictidaceae Ostropales AY661684 AY661674 –
Sphaeropezia lyckselensis EB 2012a Stictidaceae Ostropales JX266158 JX266156 –
Stictis radiata MW6493 Stictidaceae Ostropales AY527309 AY527338 AY527309
Stictis radiata GG2449a Stictidaceae Ostropales AY527308 AY340532 AY527308
Trapelia coarctata KS46 Trapeliaceae Baeomycetales KR017170 KR017353 KR017072
Xyloschistes platytropa H:Bjork 05-242 Stictidaceae Ostropales KJ766680 KJ766517 –
The newly generated sequences are highlighted in bold
Mycol Progress (2019) 18:833–845 835
Author's personal copy
Fig. 1 Phylogram generated from maximum likelihood analysis (RAxML)
based on a combined LSU, mtSSU and ITS sequenced data of taxa from the
order Ostropales. The tree is rooted to Placopsis cribellans (KS167),
P. perrugosa (KS168) and Trapelia coarctata (KS46). Bootstrap support
values (left) and Bayesian posterior probabilities (right) are given at the nodes.
The newly introduced taxon is highlighted in bold and red
836 Mycol Progress (2019) 18:833–845
Author's personal copy
Odontura,Potriphila,Rogellia,Stromatothecia,Tryb lis and
Xerotrema. The family is morphologically close to
Stictidaceae, and its delimitation could be based on the ab-
sence of both a crystalline ascoma margin and filiform asco-
spores (Sherwood 1977,1981; Sherwood-Pike 1987).
However, these morphological characters do not have high
phylogenetic significance to permit differentiation and the ne-
cessity of using multigene sequence data to separate them
needs to be emphasized.
The present study is part of our work on fungi associated
with bamboo in Sichuan Province of China, which is the
hometown of the giant panda which eats bamboo species
(Wang et al. 2010,2017). This study resulted in the introduc-
tion of a new genus and species in Odontotremataceae which
was discovered on stems of Phyllostachys heteroclada Oliv. in
Ya’an City of Sichuan Province. Combined three gene (ITS,
LSU, mtSSU) analyses were performed to confirm its taxo-
nomic placement in Ostropales. Detailed description and illus-
tration are provided and a comparison with similar genera is
carried out.
Materials and methods
Morphological studies
The holotype was collected in Sichuan Province, China and
deposited in the Herbarium of Sichuan Agricultural
University (SICAU). External shape, size and colour of
apothecia were observed and photographed in fresh state
using a dissecting microscope (Shanghai Advanced
Photoelectric Technology Co., Ltd., NVT-GG, China). The
material was dried and 2 weeks later rehydrated for micro-
scopic examination. Mature apothecia were selected for mor-
phological observation. Their anatomical details were obtain-
ed using a Nikon ECLIPSE Nicompound microscope fitted to
a Canon 600D digital camera or an OPTEC BK-DM320 mi-
croscope matched to a VS-800C microdigital camera
(Shenzhen Weishen Times Technology Co., Ltd., China).
Median sections were performed freehand with a razor blade.
Mounting media were sterilized water and different lethal me-
dia. Symbols were used for the living (*) and dead state (†)of
the observed cells according to Baral (1992). Iodine reactions
of the ascus wall were tested in Lugol’s solution (IKI, ca. 1%
I
2
concentration) and Melzer’s reagent (MLZ) without or with
3% potassium hydroxide (KOH) pretreatment. The type RR
means a red reaction at both low and high iodine concentration
(without KOH pretreatment), while type RB means a blue
reaction at low concentration and dirty red at high concentra-
tion (Baral 2009). Measurements were taken from median
sections and from squash mounts in lactophenol cotton blue
or Congo red solution. The gelatinous sheath was observed in
Black Indian ink. The minimum and maximum measurements
of ascospores and other anatomical features were based on the
examination of 20–30 different apothecia.
DNA extraction, PCR and sequencing
Genomic DNA was extracted directly from apothecial tissue,
following the protocol of Zheng and Zhuang (2013). LR0R
Table 3 Morphological comparison of Parakarstenia and similar genera
Genera Apothecia Periphysoids Asci Ascospores References
Coccomycetella Broadly immersed in
substrate. Margin dark,
protruding, ± dentate
Present, reaching down
to hymenial base
4–8-spored,
hemiamylo-
id
Narrowly cylindrical,
helicoid, transversely
1–3-septate
von Höhnel (1917),
Sherwood-Pike (1987),
Holien and Diederich
(2012), Personal obs.
Cryptodiscus Broadly immersed in
substrate. Margin pale,
protruding, ± even
Present but only above
hymenium
8-spored,
hemiamylo-
id (type
RB/RR)
Narrowly
cylindric-ellipsoid to
ellipsoid or
ellipsoid-fusoid,
transversely 1–7-septate
Sherwood (1977),
Fernández-Brime et al.
(2018); Personal obs.
Karstenia Broadly immersed in
substrate. Marginal pale to
dark, protruding, ± dentate
Present, reaching down
to hymenial base
8-spored,
hemiamylo-
id (type RB,
rarely RR)
Cylindrical to clavate,
transversely
3–15-septate
Sherwood (1977),
Wilberforce (1999);
Personal obs.
Odontotrema Broadly immersed in
substrate. Margin dark,
protruding, ± dentate
Present, reaching down
to hymenial base, in
a few species
indistinct
8-spored,
hemiamylo-
id (type
RB/RR)
Ellipsoid or cylindrical
suballantoid,
transversely 1–7-septate,
rarely submuriform
Sherwood-Pike (1987),
Diederich et al. (2002),
Baloch et al. (2013);
Personal obs.
Parakarstenia Only narrow stipe-like base
immersed in substrate.
Margin pale, not
protruding, ± even
Absent 8-spored,
hemiamylo-
id (type RR)
Narrowly cylindric-clavate
to fusoid, transversely 3-
-septate
This study
Mycol Progress (2019) 18:833–845 837
Author's personal copy
838 Mycol Progress (2019) 18:833–845
Author's personal copy
Phylogenetic analysis
Phylogenetic analyses were performed based on a combined
LSU, mtSSU and ITS molecular dataset. We cited all represen-
tative sequences within the order Ostropales through BLAST
searches against GenBank using newly generated sequences
and recent studies (Baloch et al. 2009,2010; Fernández-Brime
et al. 2011,2018). Placopsis cribellans (KS167), P. perrugosa
(KS168) and Trapelia coarctata (KS46) were regarded as
outgroupings. Single-gene sequence was aligned using
MAFFT v.7.110 online version (Katoh and Standley 2013)
and manually adjusted with BioEdit v. 7.0 (Hall 2004). The
congruence of overall topology was affirmed after a single-
gene sequence data compared, and consensus sequences were
allied by Mesquite v. 3.11 (build 766) (Maddison and Maddison
1997–2016). The evolutionary model was determined indepen-
dently for each gene using MrModeltest 2.2 under the Akaike
Information Criterion (AIC) (Nylander 2004). The best-fit mod-
el (GTR + I + G) was selected finally in the analysis.
Maximum likelihood analysis was run by applying the
CIPRES Science Gateway Web Server (Miller et al. 2010)with
default parameters in RAxML-HPC2 on XSEDE (8.2.10)
(Stamatakis 2014). Maximum likelihood bootstrap values
(MLBP) equal or greater than 50% were provided (Fig. 1).
Bayesian analysis was performed by using MrBayes v. 3.2.2
(Ronquist and Huelsenbeck 2003). The Bayesian inference of
the phylogeny was carried out by a Markov chain Monte Carlo
with Metropolis coupling (MCMCMC). Six simultaneous
Markov chains were run for 8,000,000 generations and trees
were sampled every 100th generation, and the program was
automatically terminated when the average standard deviation
of split frequencies reached below 0.01 (Maharachchikumbura
et al. 2015). Bayesian Posterior Probabilities (BYPP) equal or
greater than 0.95 were given (Fig. 1).
The phylograms were visualized in FigTree v. 1.4.3
(Rambaut and Drummond 2008), and additionally, layouts
were compiled with Adoble Illustrator CS6 v. 16.0.0.
Alignments were submitted to TreeBase (http://www.
treebase.org, ID number 23698).
Results
Phylogenetic analyses
The DNA matrix contains 41 taxa (Table 2) with 4460 characters
including gaps (2262 characters for LSU, 969 for mtSSU and
1229 for ITS). Single-gene datasets of LSU, mtSSU and ITS were
initially analysed and checked for topological congruence, but
these were not significantly different (data not shown). The phy-
logenetic trees were carried out from ML analyses which are the
best scoring trees (Fig. 1) and basically similar to recent studies
(Baloch et al. 2013;Fernández-Brimeetal.2018).
The alignment had 2371 distinct alignment patterns, and
the final optimization likelihood value was −30,870.705671.
Estimated base frequencies were as follows: A = 0.275588,
C = 0.215112, G = 0.262566 and T = 0.246735, with substitu-
tion rates AC = 0.995809, AG = 1.703836, AT = 1.823362,
CG = 0.827656, CT = 4.343897 and GT = 1.000000. The
gamma distribution shape parameter α= 0.406018 and the
tree length= 3.598570. Bayesian posterior probabilities were
determined by MCMCMC, and the final average standard
deviation of split frequencies was 0.009397.
Parakarstenia phyllostachydis clusters within the family
Odontotremataceae with moderate support (78% MLBP/0.99
BYPP). The multigene analyses show that our new genus is
phylogenetically close to the genus Karstenia Fr. with moder-
ately supported value in maximum likelihood analysis (80%
MLBP) and appears to be sister to the genus Coccomycetella
and Odontotrema (61% MLBP/0.98 BYPP).
Taxonomy
Parakarstenia C.L. Yang, H.O. Baral & X.L. Xu, gen. nov.
MycoBank number: MB 829065
Etymology: name reflects a relationship and partial mor-
phological similarity with the genus Karstenia.
Type species: Parakarstenia phyllostachydis C.L. Yang,
H.O. Baral & X.L. Xu.
Parasitic on living to nearly dead stems. Sexual morph:
Apothecia initially immersed, intracortical, raising the sub-
strate and rupturing it to form sessile fruiting bodies, scattered
to gregarious, usually confluent, becoming erumpent,
obrotund to irregular shape, flat to slightly convex, white to
pale brown, turning concave, brown to fuscous when dry,
periphysoids lacking, without any crystals. Receptacle hair-
less, pale yellowish-cream. Ectal excipulum of vertically
Mycol Progress (2019) 18:833–845 839
and LR5 (Vilgalys and Hester 1990), NS1 and NS4, ITS1 and
ITS4 (White et al. 1990) and EF1-983F and EF1-2218R
(Rehner 2001) primers were used for the amplification of large
subunit rDNA (28S, LSU), small subunit rDNA (18S, SSU),
internal transcribed spacers (5.8S, ITS) and translation elon-
gation factor 1-αgene region (TEF1-α) respectively. The
PCR procedure in 25-μl reactions was carried out as outlined
by Dai et al. (2016). The PCR products were purified and
sequenced by TsingKe Biological Technology Co., Ltd.
(Chengdu, China). The newly generated sequences were sub-
mitted to GenBank and the others included in this study were
retrieved from GenBank or UNITE (https://unite.ut.ee/search.
php#fndtn-panel2)(Table2).
Fig. 2 Parakarstenia phyllostachydis (SICAU 16-0002, holotype). a–c
Gross morphology of apothecia on natural substrate (fresh state). d
Apothecium in median section. eBasal part with medullary excipulum.
fEctal excipulum at flanks. g,hMargin at flanks. All in sterilized water.
Scale bars: a,b2 mm, c500 μm, d,e50 μm, f–h20 μm
Author's personal copy
840 Mycol Progress (2019) 18:833–845
Author's personal copy
oriented textura prismatica or irregularly oriented textura
globosa-angularis, hyaline to pale greyish to greyish-brown-
ish, inner cells more thick-walled and larger than thin-walled
outer cells. Medullary excipulum of small-celled textura
angularis, hyaline to pale brown. Hymenium hyaline, pale
brown above, gelatinized. Asci cylindrical to clavate, 8-
spored, stipitate, apex strongly conical, with or without apical
wall thickening, entire ascus wall hemiamyloid. Ascospores
narrowly cylindrical-clavate to fusoid (vermiform), straight to
medium curved, hyaline, without gelatinous sheath, trans-
versely multiseptate. Paraphyses densely arranged, filiform,
hyaline, septate, branched, curved above, with more or less
thick gelatinous sheath. Asexual morph: Unknown.
Notes: Phylogenetic analyses based on a combined ITS, LSU
and mtSSU sequence dataset (Fig. 1)showthatParakarstenia is
closely related to Karstenia and both form a sister clade to
Coccomycetella and Odontotrema within Odontotremataceae.
These evolutionary relationships are comparatively poorly sup-
ported with the dataset analysed, besides the fact that molecular
data of very few taxa of Odontotremataceae are currently avail-
able. When comparing the DNA sequence data of the men-
tioned taxa, the base pair discrepancies are above 7.5% for
LSU and above 20% for ITS.
Morphologically, Karstenia shares some characters with
Parakarstenia, but it also shows several significant differences
(Karsten 1885; Sherwood 1977,1980; Graddon 1986;
Wilberforce 1999; Personal observations by second author), such
as apothecia immersed with their broad base in the substrate by
lifting large lobes of host tissue; with an irregularly dentate,
strongly protruding margin, with periphysoids reaching down to
hymenial base; with ascospores often above 5-septate. The mor-
phological delimitation among these similar genera is summa-
rized in Table 3. Other gene regions gained from
P. phyllostachydis include SSU (MG214899) and TEF 1-α
(MG214900) and are available for further analyses. Based on
comprehensive analyses of phenotypic and nucleotide differ-
ences combined with multigene phylogenies, a new non-
lichenized genus Parakarstenia is introduced within
Odontotremataceae to accommodate the new species
P. phyllostachydis,as recommended by Jeewon and Hyde (2016).
Parakarstenia phyllostachydis C.L. Yang, H.O. Baral &
X.L. Xu, sp. nov.
Mycobank number: MB 829066, Figs. 2,3and 4.
Etymology: phyllostachydis, referring to the host plant on
which the new species was collected.
Holotype: SICAU 16-0002.
Parasitic on living to nearly dead stems of Phyllostachys
heteroclada (Poaceae). Sexual morph: Apothecia sessile,
gregarious or scattered, without subiculum, usually confluent,
margin often with a white rim, subsequently inconspicuous,
not protruding. Receptacle lower part covered to varying ex-
tent by host epidermis, usually also at margin with some small
adherent host residues. Ectal excipulum 40–160 μmthickat
flanks, cells at flanks and margin †5–11.5(–14) × (2.5–)3.5–
6(–7) μm, 30–80 μm thick at margin, marginal cortical cells
†3.5–6×3–4.5 μm, oriented at high angle. Medullary
excipulum 130–240 μm thick in center, 20–90 μmthickat
margin, cells †(2–)2.2–3.9(–5.4) μm. Hymenium (94–)119–
186(–210) μmthick.Subhymenium (6–)9.5–15(–16) μm
thick. Asci †(95.5–)122–139(–145) × (8.5–)13.7–
18.3(−23.2) μm(
x=130.7×16 μm, n= 30), stipitate, stipe
12–23 μm long, apex thin-walled or sometimes with a 1–
2.5-μm-thick apical wall thickening, entire outer wall and api-
cal thickening deep red in IKI (I+ hemiamyloid, type RR),
KOH/IKI deep blue (difficult to observe individually due to
gelatinized hymenium). Ascospores †(40–)42–51(–
61.3) × (3–)3.3–4.1(–4.7) μm(
x= 46.5 × 3.8 μm, n=30),fi-
nally (2–)3(–4)-septate, rarely multiseptate (5–11-septate),
parallel or intertwined in the upper part of the dead asci, con-
taining a medium amount of lipid, multiguttulate. Paraphyses
sporadically branched below apex, occasionally anastomos-
ing, 1.4–2.0(–2.4) μm wide from base to tip, twisted into coils
or spirals at the apex, forming a (7–)8.5–14.5(–18) μm thick
pale brownish epithecium.
Material examined: CHINA, Sichuan Province, Ya’an
City, Yucheng District, Yanchang Township, alt. 951 m, 29°
43′33.95″N103°4′44.4″E, on living to nearly dead stems of
Phyllostachys heteroclada, 8 April 2016, C.L. Yang & X.L.
Xu, YCL201604001 (SICAU 16-0002, holotype).
Discussion
Parakarstenia has distinct characters that can separate it from
other genera in Odontotremataceae in having a non-
periphysoid apothecium, absence of crystals and a conical
ascus apex. It is the first report of a member of Ostropales that
parasitizes on living stems of bamboo, and the remaining gen-
era in this family are mostly saprophytes on ligneous plants or
mosses (Nylander 1857;Rehm1881; Shaw and Hawksworth
1971;Döbbeler1996,1999,2003,2006; Evans et al. 2010;
Barreto et al. 2012; Holien and Diederich 2012). The discov-
ery of Parakarstenia broadens the familial concept of
Odontotremataceae. Most odontotremataceous genera were
erected merely based on morphology, and for most species,
the phylogenetic status remains unclear due to the lack of
molecular data. Most genera only include 1–2 described spe-
cies, Potriphila 3speciesandonlyaround15–28 valid species
are recorded at present in this family (Sherwood-Pike 1987;
Mycol Progress (2019) 18:833–845 841
Fig. 3 Parakarstenia phyllostachydis (SICAU 16-0002, holotype). a,b
Paraphyses. c,dTwisted and intertwined paraphyses at the apex (cin
water, din MLZ). e–hAsci (ein water, f–hin Congo red). i–vAscospores
(i–oin water, p–vin MLZ). Scale bars: a–h20 μm, i–v10 μm. Living
state (at least partly) in a–b,i–j,l–n
Author's personal copy
842 Mycol Progress (2019) 18:833–845
Author's personal copy
Jaklitsch et al. 2016; Diederich et al. 2018; Index Fungorum
2019). Therefore, extensive sampling of genera and species
lacking molecular data is needed and more gene regions
should be extracted in future study.
The genus Karstenia Fr. (non Karstenia Britzelm., nom.
illegit.) was incipiently introduced by Fries (in Karsten 1885),
and its taxonomic placement has always been unclear
(Sherwood 1977,1980,1981; Graddon 1986; Wilberforce
1999). Some mycologists provisionally placed it in
Rhytismatales (Lumbsch and Huhndorf 2007,2010), and subse-
quently,it was transferred to Stictidaceae in Ostropales only based
on morphology (Wijayawardene et al. 2018). Until now, 10–11
species are recognized in this genus (Wilberforce 1999; Jaklitsch
et al. 2016; Wijayawardene et al. 2017; Index Fungorum 2019).
Most species of Karstenia lack gene sequence data, and the
phylogenetic placement of the genus is still ambiguous.
Available rDNA sequences in official repositories (GenBank,
UNITE)arethoseofK. rhopaloides (Sacc.) Baral (≡
Cryptodiscus rhopaloides Sacc.) and K. macer (P. Karst.)
Sherwood (see Table 2). Whether the type of Karstenia,
K. sorbina (P. Karst.) P. Karst., belongs in the current concept
of the genus requires a thorough restudy of the holotype. This
restudy should include clarification of ascus amyloidity, which
Sherwood (1977) reported as absent perhaps because of using
MLZ without KOH-pretreatment. We here follow the current
concept of Karstenia and propose a new genus for the here
described, morphologically distinct species.
Based on our three gene phylogenetic analyses (Fig. 1), we
here transfer Karstenia to the family Odontotremataceae. Its
morphological characteristics are basically consistent with
other members of Odontotremataceae, such as a non-
crystalline apothecial margin, pronounced periphysoids and
vermiform, cylindrical to clavate ascospores (Sherwood
1977; Wilberforce 1999).
Acknowledgements Chun-Lin Yang warmly thanks Xue Wang, Ming
Liu, Li-Juan Liu, and Ren-Hua Chen for their help of laboratory work.
Funding information Xiu-Lan Xu received support from the Resources
Investigation of Entomopathogenic Fungi in Sichuan Province and its
Controlling Benefits to Forest Pests (Grant number: 510100-
201700290-2017-00363).
References
Baloch E, Gilenstam G, Wedin M (2009) Phylogenyand classification of
Cryptodiscus, with a taxonomic synopsis of the Swedish species.
Fungal Divers 38:51–68
Baloch E, Lücking R, Lumbsch HT, Wedin M (2010) Major clades and
phylogenetic relationships between lichenized and non-lichenized
lineages in Ostropales (Ascomycota: Lecanoromycetes). Taxon 59:
1483–1494
Baloch E, Gilenstam G, Wedin M (2013) The relationships of
Odontotrema (Odontotremataceae) and the resurrected
Sphaeropezia (Stictidaceae) - new combinations and three new
Sphaeropezia species. Mycologia 105:384–397
Baral H-O (1992) Vital versus herbarium taxonomy: morphological dif-
ferences between living and dead cells of ascomycetes, and their
taxonomic implications. Mycotaxon 44:333–390
Baral H-O (2009) Iodine reaction in Ascomycetes: why is Lugol’ssolu-
tion superior to Melzer’s reagent? Available from: http://www.gbif-
mycology.de/HostedSites/Baral/IodineReaction.htm. Accessed 18
March 2011
Barreto RW, Johnston PR, Crous PW, Evans HC (2012) A new species of
the lenticel fungus genus Claviradulomyces (Ostropales) from the
Brazilian Atlantic forest tree Xylopia sericea (Annonaceae). IMA
Fungus 3:135–141
Calatayud V, Etayo J, Diederich P (2001) Paralethariicola aspiciliae
(Ostropales, Odontotremataceae), a new genus and species of
lichenicolous fungi. Lichenologist 33:477–482
Dai D-Q, Phookamsak R, Wijayawardene NN, Li W-J, Bhat DJ, Xu J-C,
Taylor JE, Hyde KD, Chukeatirote E (2016) Bambusicolous fungi.
Fungal Divers 82:1–105
Diederich P (2014) Aabaarnia and Normanogalla, two new lichenicolous
genera of Ostropales, Ascomycota. Bulletin de la Société des
Naturalistes Luxembourgeois 115:141–149
Diederich P, Zhurbenko M, Etayo J (2002) The lichenicolous species of
Odontotrema (syn. Lethariicola) (Ascomycota, Ostropales).
Lichenologist 34:479–501
Diederich P, Lawrey JD, Ertz D (2018) The 2018 classification and
checklistof lichenicolous fungi, with 2000 non-lichenized, obligate-
ly lichenicolous taxa. Bryologist 121:340–425
Döbbeler P (1996) Potriphila navicularis gen. et sp. nov. (Ostropales,
Ascomycetes), ein bipolar verbreiteter Parasit von Polytrichum
alpinum. Nova Hedwigia 62:61–77
Döbbeler P (1999) Polytrichadelphus magellanicus - a mycological
Eldorado: five new ascomycetes on a single collection from Tierra
del Fuego. Haussknechtia 9:79–96
Döbbeler P (2003) Ascomycetes on Dendroligotrichum (Musci). Nova
Hedwigia 76:1–44
Döbbeler P (2006) Two new polytrichicolous Ascomycetes from
Ecuador. Nova Hedwigia 82:257–264
Eriksson O (1981) The families of bitunicate ascomycetes. Opera
Botanica 60:1–210
Eriksson OE, Winka K (1997) Supraordinal taxa of Ascomycota.
Myconet 1:1–16
Eriksson OE, Baral H-O, Currah RS, Hansen K, Kurtzman CP, Rambold
G, Læssøe T (2004) Outline of Ascomycota –2004. Myconet 10:1–
99
Evans HC, Johnston PR, Park D, Barreto RW, Soares DR (2010)
Claviradulomyces, a new genus of the Ostropales from West
African rainforest. Fungal Biol 114:41–48
Fernández-Brime S, Llimona X, Molnar K, Stenroos S, Högnabba F,
Björk C, Lutzoni F, Gaya E (2011) Expansion of the Stictidaceae
by the addition of the saxicolous lichen-forming genus Ingvariella.
Mycologia 103:755–763
Fernández-Brime S, Olariaga I, Baral H-O, Friebes G, Jaklitsch W, Senn-
Irlet B, Wedin M (2017, [2018]) Cryptodiscus muriformis and
Schizoxylon gilenstamii, two new species of Stictidaceae
(Ascomycota). Mycol Prog 17:295–305
Flakus A, Kukwa M (2012) New species of lichenicolous fungi from
Bolivia. Lichenologist 44:469–477
Graddon WD (1986) Some new discomycete species: 7. Trans Br Mycol
Soc 87:328–333
Mycol Progress (2019) 18:833–845 843
Fig. 4 Parakarstenia phyllostachydis (SICAU 16-0002, holotype). a
Median section of apothecium in IKI. bdo., in IKI after KOH. cdo., in
MLZ. ddo., in MLZ after KOH. e–gAsci in IKI. h–jAsci in IKI after
KOH. k,lAsci in MLZ. Scale bars: a–d=200 μm, e–l=10 μm
Author's personal copy
Gueidan C, Hill DJ, Miadlikowska J, Lutzoni F (2015) 4 Pezizomycotina:
Lecanoromycetes. In: McLaughlin D, Spatafora J (eds) Systematics
and evolution. The Mycota (A comprehensive treatise on fungi as
experimental systems for basic and applied research), vol 7B.
Springer, Berlin
Hall T (2004) BioEdit, Ibis Therapeutics, Carlsbad http://www.mbio.
ncsu.edu/BioEdit/bioedit.html. Accessed 18 Mar 2005
Hawksworth DL, Sherwood MA (1982) Two new families in the
Ascomycotina. Mycotaxon 16:262–264
Holien H, Diederich P (2012) Coccomycetella richardsonii
(Odontotremataceae, Ostropales), an ascomycete new to Norway.
Agarica 35:3–5
Holien H, Triebel D (1996) Spirographa vinosa, a new odontotremoid
fungus on Ochrolechia and Pertusaria. Lichenologist 28:307–313
Holm L, Holm K (1993) Two new northern pyrenomycetes. Blyttia 51:
121–123
Index Fungorum (2019) http://www.indexfungorum.org/Names/Names.
asp, retrieval in April 2019
Jahn L, Schafhauser T, Pan S, Weber T, Wohlleben W, Fewer D,Sivonen
K, Flor L, van Pée K-H, Caradec T, Jacques P, Huijbers MME, van
Berkel WJH, Ludwig-Müller J (2017) Cyanodermella asteris sp.
nov. (Ostropales) from the inflorescence axis of Aster tataricus.
Mycotaxon 132:107–123
Jaklitsch W, Baral HO, Lücking R, Lumbsch HT, Frey W (2016) Syllabus
of plant families, 13th ed. Part 1/2, Borntraeger, Stuttgart, 322 pp
Jeewon R, Hyde KD (2016) Establishing species boundaries and new
taxa among fungi: recommendations to resolve taxonomic ambigu-
ities. Mycosphere 7:1669–1677
Karsten PA (1885) Revisio monographica atque synopsis
Ascomycetorum in Fennia hucusque detectorum. Acta Societatis
pro Fauna et Flora Fennica 2:1–176
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment
software version 7: improvements in performance and usability.
MolBiolEvol30:772–780
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth &
Bisby’s dictionary of the fungi, 10th edn. CABI, Wallingford, Oxon
Kohlmeyer J, Volkmann-Kohlmeyer B (1996) Fungi on Juncus
roemerianus.6.Glomerobolus gen. nov., the first ballistic member
of Agonomycetales. Mycologia 88:328–337
Koukol O, Hofmann TA, Piepenbring M (2017) Dendroseptoria
mucilaginosa: a new anamorphic fungus with stauroconidia and
phylogenetic placement of Dendroseptoria. Mycol Prog 16:1065–
1070
Kraichak E, Huang J-P, Nelsen M, Leavitt SD, Lumbsch HT (2018) A
revised classification of orders and families in the two major sub-
classes of Lecanoromycetes (Ascomycota) based on a temporal ap-
proach. Bot J Linn Soc 188:233–249
Li Z-J, Hou CL (2016) A new Stictis species from China based on mor-
phological and molecular data. Phytotaxa 286:186–192
Lücking R, Hodkinson BP, Leavitt SD (2017) The 2016 classification of
lichenized fungi in the Ascomycota and Basidiomycota - ap-
proaching one thousand genera. Bryologist 119:361–416
Lumbsch HT, Huhndorf SM (2007) Outline of Ascomycota - 2007.
Myconet 13:1–58
Lumbsch HT, Huhndorf SM (2010) Outline of Ascomycota - 2009.
Myconet 14:1–64
Lumbsch HT, Schmitt I, Lücking R, Wiklund E, Wedin M (2007) The
phylogenetic placement of Ostropales within Lecanoromycetes
(Ascomycota) revisited. Mycol Res 111:257–267
Maddison W, Maddison D (1997–2016) Mesquite, version 3.11 (build
766) Copyright (c)
Magnes M (1997) Weltmonographie der Triblidiaceae. Bibl Mycol 165:
1–177
Maharachchikumbura SS, Hyde KD, Jones EBG, McKenzie EHC,
Huang S-K, Abdel-Wahab MA, Daranagama DA, Dayarathne M,
D’souza MJ, Goonasekara ID, Hongsanan S, Jayawardena RS, Kirk
PM, Konta S, Liu J-K, Liu Z-Y, Norphanphoun C, Pang K-L, Perera
RH, Senanayake IC, Shang Q-J, Shenoy BD, Xiao Y-P, Bahkali AH,
Kang J-C, Somrothipol S, Suetrong S, Wen T-C, Xu J-C (2015)
Towards a natural classification and backbone tree for
Sordariomycetes. Fungal Divers 72:199–301
Mayrhofer H, Poelt J (1985) Die Flechtengattung Microglaena sensu
Zahlbruckner in Europa. Herzogia 7:13–79
Miadlikowska J, Kauff F, Högnabba F, Oliver JC, Molnár K, Fraker E,
Gaya E, Hafellner J, Hofstetter V, Gueidan C, Otálora MAG,
Hodkinson B, Kukwa M, Lücking R, Björk C, Sipman HJM,
Burgaz AR, Thell A, Passo A, Myllys L, Goward T, Fernández-
Brime S, Hestmark G, Lendemer J, Lumbsch HT, Schmull M,
Schoch C, Sérusiaux E, Maddison DR, Arnold AE, Lutzoni F,
Stenroos S (2014) A multigene phylogenetic synthesis for the class
Lecanoromycetes (Ascomycota): 1307 fungi representing 1139
infrageneric taxa, 317 genera and 66 families. Mol Phylogenet
Evol 0:132–168
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science
Gateway for inference of large phylogenetic trees. In: Proceedings
of the Gateway Computing Environments Workshop (GCE), 14
Nov. 2010, New Orleans, LA, pp 1–8
Nannfeldt JA (1932) Studien über die Morphologie und Systematik der
nichtlichenisierten inoperculaten Discomyceten. Nova Acta Regiae
Societatis Scientiarum Upsaliensis 8(2):1–368
Nylander W (1857) Enumération générale de lichens, avec l’indication
sommaire de leur distribution géographique. Mémoires de la Société
Impériale des Sciences Naturelles de Cherbourg 5:85–146
Nylander JAA (2004) MrModeltest 2.0. Program distributed by the au-
thor. Evolutionary Biology Centre, Uppsala University.
Ohmura Y, Mayrhofer H (2016) Protothelenella
sphinctrinoides (Protothelenellaceae) new to Japan and new chem-
ical features for several species in the genus. Herzogia 29:137–142
Rambaut A, Drummond A (2008) FigTree: Tree figure drawing tool,
version 1.2.2. Institute of Evolutionary Biology, University of
Edinburgh.
Rehm H (1881) Ascomyceten in getrockneten Exemplaren
herausgegeben. Berichte des Naturhistorischen Vereins Augsburg
26:1–132
Rehner S (2001) Primers for elongation factor 1-α(EF1-α). http://ocid.
NACSE.ORG/research/deephyphae/EF1primer.pdf
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic
inference under mixed models. Bioinformatics 19:1572–1574
Shaw DE, Hawksworth DL (1971) Stromatothecia nothofagi,anewge-
nus and species of scolecospored Ascomycetes from Nothofagus in
New Guinea. Proc Papua New Guinea Sci Soc 22:21–25
Sherwood MA (1977) The ostropalean fungi. Mycotaxon 5:1–277
Sherwood MA (1980) Taxonomic studies in the Phacidiales. The genus
Coccomyces (Rhystismatales). Occas Pap Farlow Herbarium 15:1–
120
Sherwood MA (1981) Convergent evolution in discomycetes from bark
and wood. Bot J Linn Soc 82:15–34
Sherwood-Pike MA (1987) The Ostropalean fungi III: the
Odontotremataceae. Mycotaxon 28:137–177
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis
and post-analysis of large phylogenies. Bioinformatics 30:1312–
1313
Suija A, Ertz D, Lawrey JD, Diederich P (2015) Multiple origin of the
lichenicolous life habit in Helotiales, based on nuclear ribosomal
sequences. Fungal Divers 70:55–72
van Nieuwenhuijzen EJ, Miadlikowska JM, Houbraken JAMP, Adan
OCG, Lutzoni FM, Samson RA (2016) Wood staining fungi re-
vealed taxonomic novelties in Pezizomycotina: new order
Superstratomycetales and new species Cyanodermella oleoligni.
Stud Mycol 85:107–124
844 Mycol Progress (2019) 18:833–845
Author's personal copy
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of
enzymatically amplified ribosomal DNA from several Cryptococcus
species. J Bacteriol 172:4238–4246
Voglmayr H, Fournier J, Jaklitsch WM (2019) Two new classes of
Ascomycota: Xylobotryomycetes and Candelariomycetes.
Persoonia 42:36–49
von Höhnel FXR (1917) System der Phacidiales. Ber Deut Bot Ges 35:
416–422
Wang X-H, Huang Y, Guo Q-R, Zhou Z-J (2010) Regeneration of
Phyllostachys heteroclada and its relations with rhizome carbon
and nitrogen metabolism. Chin J Appl Ecol 21:1953–1958
Wang H-R, Zhong H-J, Hou R, Ayala J, Liu G-M, Yuan S-B, Yan Z,
Zhang W-P, Liu Y-L, Cai K-L, Cai Z-G, Huang H, Zhang Z-H, Wu
D (2017) A diet diverse in bamboo parts is important forgiant panda
(Ailuropoda melanoleuca) metabolism and health. Sci Rep 7:3377
Wedin M, Döring H, Gilenstam G (2004) Saprotrophy and lichenization
as options for the same fungal species on different substrata: envi-
ronmental plasticity and fungal lifestyles in the Stictis–Conotrema
complex. New Phytol 164:459–465
Wedin M, Wiklund E, Crewe A, Döring H, Ekman S, Nyberg Å, Schmitt
I, Lumbsch HT (2005a) Phylogenetic relationships of
Lecanoromycetes (Ascomycota) as revealed by analyses of mtSSU
and nLSU rDNA sequence data. Mycol Res 109:159–172
Wedin M, Döring H, Könberg K, Gilenstam G (2005b) Generic
delimitations in the family Stictidaceae (Ostropales, Ascomycota):
the Stictis-Conotrema problem. Lichenologist 37:67–75
Wedin M, Döring H, Gilenstam G (2006) Stictis s. Lat. (Ostropales,
Ascomycota) in northern Scandinavia, with a key and notes on mor-
phological variation in relation to lifestyle. Mycol Res 110:773–789
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct
sequencing of fungal ribosomal RNA genes for phylogenetics. In:
Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a
guide to methods and applications. Academic, San Diego, pp 315–
322
Wijayawardene NN, Hyde KD, Rajeshkumar KC, Hawksworth DL,
Madrid H, Kirk PM, Braun U, Singh RV, Crous PW, Kukwa M,
Lücking R, Kurtzman CP, Yurkov A, Haelewaters D, Aptroot A,
Lumbsch HT, Timdal E, Ertz D, Etayo J, Phillips AJL,
Groenewald JZ, Papizadeh M, Selbmann L, Dayarathne MC,
Weerakoon G, Jones EBG, Suetrong S, Tian Q, Castañeda-Ruiz
RF, Bahkali AH, Pang K-L, Tanaka K, Dai D-Q, Sakayaroj J,
Hujslová M, Lombard L, Shenoy BD, Suija A,
Maharachchikumbura SSN, Thambugala KM, Wanasinghe DN,
Sharma BO, Gaikwad S, Pandit G, Zucconi L, Onofri S, Egidi E,
Raja HA, Kodsueb R, Cáceres MES, Pérez-Ortega S, Fiuza PO,
Monteiro JS, Vasilyeva LN, Shivas RG, Prieto M, Wedin M,
Olariaga I, Lateef AA, Agrawal Y, Fazeli SAS, Amoozegar MA,
Zhao G-Z, Pfliegler WP, Sharma G, Oset M, Abdel-Wahab MA,
Takamatsu S, Bensch K, de Silva NI, Kesel AD, Karunarathna A,
Boonmee S, Pfister DH, Lu Y-Z, Luo Z-L, Boonyuen N,
Daranagama DA, Senanayake IC, Jayasiri SC, Samarakoon MC,
Zeng X-Y, Doilom M, Quijada L, Rampadarath S, Heredia G,
Dissanayake AJ, Jayawardana RS, Perera RH, Tang L-Z,
Phukhamsakda C, Hernández-Restrepo M, Ma X-Y, Tibpromma
S, Gusmao LFP, Weerahewa D, Karunarathna SC (2017) Notes for
genera: Ascomycota. Fungal Divers 86:1–594
Wijayawardene NN, Hyde KD, Lumbsch HT, Liu J-K,
Maharachchikumbura SSN, Ekanayaka AH, Tian Q, Phookamsak
R (2018) Outline of Ascomycota: 2017. Fungal Divers 88:167–263
Wilberforce PW (1999) A new species of Karstenia on Deschampsia
caespitosa from North Argyll, Scotland. Mycologist 13:149–150
Zheng H-D, Zhuang W-Y (2013) A new species of Roseodiscus
(Ascomycota, Fungi) from tropical China. Phytotaxa 105:51–57
Zhurbenko MP, Etayo J (2013) Biazrovia, a new genus of lichenicolous
ascomycetes from Asia. Mycobiota 1:51–56
Zhurbenko MP, Yakovchenko LS (2014) A new species, Sagediopsis
vasilyevae, and other lichenicolous fungi from Zabaikal’skii
Territory of Russia, southern Siberia. Folia Cryptogamica Estonica
51:121–130
Publisher’snoteSpringer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Mycol Progress (2019) 18:833–845 845
Author's personal copy
