maasoglossum, a basal genus in geoglossomycetes · huhndorf 2010). in this paper we provide an...
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Short communication
Maasoglossum, a basal genus in Geoglossomycetes
Vincent P. Hustad a,b,*, Andrew N. Miller b
a Department of Plant Biology, University of Illinois at Urbana-Champaign, 505 S. Goodwin Ave., Urbana,
IL 61801, USAb Illinois Natural History Survey, University of Illinois, 1816 S. Oak St., Champaign, IL 61820, USA
a r t i c l e i n f o
Article history:
Received 19 January 2015
Received in revised form
22 May 2015
Accepted 24 May 2015
Available online 24 June 2015
Keywords:
Ascomycota
Earth tongues
Geoglossum
Phylogenetics
Systematics
* Corresponding author. Department of PlantUSA. Tel.: þ01 618 843 0784; fax: þ01 217 265
E-mail address: [email protected] (V.Phttp://dx.doi.org/10.1016/j.myc.2015.05.0031340-3540/© 2015 The Mycological Society of
a b s t r a c t
The genus Maasoglossum is examined using morphology, ecology, and molecular system-
atics of the internal transcribed spacer region and large subunit of the nuclear ribosomal
RNA gene, all of which support the placement of Maasoglossum among the basal members
of Geoglossomycetes. The morphology of the genus extends the range of ascocarp and
ascospore development in Geoglossomycetes. The ecology and conservational significance
of the genus is discussed, a nomenclatural transfer of Geoglossum aseptatum to Maaso-
glossum is made, and an emended description of Maasoglossum is provided.
© 2015 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved.
The class Geoglossomycetes is a basal ascocarp-producing
member of the ‘Leotiomyceta’ (Schoch et al. 2009). Kirk et al.
(2008) suggest 48 species in four genera belong in the class,
while Index Fungorum lists over 200 names for these same
four genera. Recent research indicates eight genera belong in
the class: Geoglossum Pers., Glutinoglossum Hustad et al., Hem-
ileucoglossum Arauzo, Leucoglossum S. Imai, Nothomitra Maas
Geest., Sabuloglossum Hustad et al., Sarcoleotia S. Ito & S. Imai,
and Trichoglossum Boud. (Hustad et al. 2013; Arauzo and
Iglesias 2014). The prevalence of rarely collected species has
made an accurate estimation of the number of species in the
class difficult.
The rare species, Geoglossum aseptatum Hakelier ex Nitare,
is characterized by light brown, aseptatemature ascospores, a
Biology, University of Illi4678.
. Hustad).
Japan. Published by Else
character not found in any other member of the genus Geo-
glossum. Preliminary molecular analysis (data not shown)
suggested that this fungus belonged in a separate lineage from
Geoglossum and a review of the literature suggested a possible
link between G. aseptatum and the genus Maasoglossum Thind
& R. Sharma.
The genus Maasoglossum was described by Thind and
Sharma (1984) to accommodate a single species, M. verrucis-
porum, described from a collection made in 1981 from the
temperate Eastern Himalayan forest of Bhutan. The authors
noted the macroscopic similarity of the ascocarp to that of
Geoglossum, but that it differed in the hymenium of M. verru-
cisporum contained small ridges and grooves that became
more prominent upon drying, a character rarely encountered
nois at Urbana-Champaign, 505 S. Goodwin Ave., Urbana IL 61801,
vier B.V. All rights reserved.
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myc o s c i e n c e 5 6 ( 2 0 1 5 ) 5 7 2e5 7 9 573
in Geoglossum. Additionally, the one-celled, lightly-colored,
warted ascospores precluded the placement of this fungus in
Geoglossum. Since no other members of the Geoglossaceae
sensu lato contain ornamented ascospores, they were unsure
of the placement of this genus within Geoglossaceae sensu lato
or Leotiomycetes (Microglossum). The genus is currently
regarded as incertae sedis within Leotiomycetes (Lumbsch and
Huhndorf 2010). In this paper we provide an in-depth
assessment of the genus Maasoglossum based on
morphology, ecology, and molecular systematics, and test the
hypotheses that Maasoglossum is a basal member of Geo-
glossomycetes and that G. aseptatum belongs in the genus
Maasoglossum.
For this study, the type specimens of both Geoglossum
aseptatum and Maasoglossum verrucisporum were obtained and
examined. Dried ascomata were hand-sectioned and squash
mounted in 5% KOH andmicromorphological characters were
observed. Images of pertinent micromorphological characters
were captured using a QImaging QColor 3 digital camera
mounted on an Olympus BX51 compound microscope using
differential interference microscopy. Images were processed
with Adobe Photoshop v. 7.0 (Adobe Systems Inc., Mountain
View, California). A minimum of 30 measurements was made
for each micromorphological character using NIH Image v.
1.63 (National Institutes of Health, Bethesda, Maryland).
Taxonomic novelties and associated data were deposited in
MycoBank (Crous et al. 2004).
Total genomic DNA was extracted from approximately
0.5 cm2 of hymenium tissue from a single dried ascoma with
the DNeasy Plant Mini Kit (QIAGEN Inc., Valencia, California)
for recently-collected specimens (collected within 20 years).
For older specimens, DNA was extracted from approximately
0.2 cm2 of hymenium tissue using the EZNA Forensic DNA kit
(Omega Bio-Tek, Norcross, Georgia). Gene fragments were PCR
amplified following the methods outlined in Promputtha and
Miller (2010) and purified using a Wizard SV Gel and PCR
Clean-Up System (Promega Corp., Fitchburg, Wisconsin). Se-
quenceswere generated on an ABI Applied Biosystems 3730XL
high-throughput DNA capillary sequencer at the UIUC Keck
Center for Comparative and Functional Genomics. Two re-
gions of the nuclear rRNA gene were used for molecular
phylogenetic analysis: the ca. 570 bp internal transcribed
spacer (ITS) region, consisting of the ITS1, 5.8S, and ITS2 re-
gions, was amplified and sequenced using a combination of
the primers ITS5, ITS1, ITS2, ITS3, and ITS4 (White et al. 1990);
and a ca. 630 bp fragment of the 28S large subunit (LSU) region
was amplified and sequenced with the primers JS1 (Landvik
1996) and LR3 (Vilgalys and Hester 1990). Due to the age of
the material, attempts to PCR amplify single-copy protein
coding genes (i.e. RPB1, RPB2, MCM7) were unsuccessful. Out-
group species were chosen from closely related taxa based on
previous studies (Wang et al. 2006; Hustad et al. 2013).
Sequence alignments were created by eye in Sequencher
5.0.1 (Gene Codes Corp., Ann Arbor, Michigan) and optimized
if necessary using Muscle v. 3.8.31 (Edgar 2004) in SeaView v.
4.4.2 (Gouy et al. 2010). Ambiguous regions were removed
from each dataset using Gblocks 0.91b (Castresana 2000)
under the following parameters: for ITS: minimum number of
sequences for both conserved and flanking regions ¼ 15,maximum number of contiguous, nonconserved regions ¼ 2,
minimum length of a block ¼ 2, and allowed gap positions in50% of sequences; for LSU: same as ITS except minimum
number of sequences for both conserved and flanking
regions ¼ 14.The GTR þ I þ G model was determined to be the best-fit
model of evolution for both ribosomal regions using the
Akaike Information Criterion (AIC) (Posada and Buckley 2004)
in jModelTest 2.0 v. 0.1.1 (Guindon and Gascuel 2003; Darriba
et al. 2012) on the XSEDE platform of the CIPRES Science
Gateway Teragrid (Miller et al. 2010) and was used in phylo-
genetic analyses of each individual dataset. Maximum likeli-
hood (ML) analyses were performed using PhyML 3.0 (Guindon
et al. 2010) on the ATGC server (http://www.atgc-montpellier.
fr/phyml/). The best of subtree pruning and regrafting (SPR)
and nearest neighbor interchange (NNI) was implemented
during the heuristic search. Nonparametric bootstrap support
(Felsenstein 1985) (BS) was determined with 1000 replicates.
Clades with BS values of �70% were considered significant(Hillis and Bull 1993).
Bayesian inference employing aMarkov ChainMonte Carlo
(MCMC) algorithm was performed using MrBayes v. 3.2.2
(Ronquist et al. 2012) on the XSEDE platform. Four indepen-
dent chains of MCMC were run for 10 million generations.
Clades with Bayesian posterior probability (BPP) values of
�95% were considered significant (Alfaro et al. 2003). Tracer v.1.5 (Rambaut and Drummond 2009) was used to estimate
effective sample size (ESS) using the standard deviation of
split frequencies produced by Bayesian analysis.
Individual ITS and LSU datasets were examined for po-
tential conflict before concatenation into a single dataset for
total evidence analysis (Kluge 1989; Eernisse and Kluge 1993).
Individual gene phylogenies were considered to be incon-
gruent if clades with significant ML BS and BPP support were
conflicting in individual tree topologies (Wiens 1998; Alfaro
et al. 2003; Lutzoni et al. 2004). Since no incongruencies were
found among individual phylogenies, the ITS and LSU data-
sets were concatenated and final ML and Bayesian analyses
were performed on the combined dataset. Alignments and
trees are deposited in TreeBASE (http://treebase.org) under
submission ID 16591.
Ten new sequences were generated in this study, five ITS
and five LSU sequences (Table 1). These were analyzed
together with 23 ITS and 21 LSU sequences from our previous
studies (Hustad and Miller 2011; Hustad et al. 2011, 2013, 2014)
along with sequences of Geoglossomycetes from previously
published research (Pfister 1997; Zhao et al. 2001; Wang et al.
2002, 2005, 2006, 2011; Peterson 2008; Brock et al. 2009;
Ohenoja et al. 2010). Twenty-eight collections, representing a
total of 15 Geoglossomycetes species (including sequences
from type species of each genus in Geoglossomycetes except
Sarcoleotia) and eleven outgroup species, were included in the
analyses. Of the 28 collections included in the final dataset,
none lack ITS and only two lack LSU, with sequences for both
markers available for 93% of the collections (Table 1).
The final combined data matrix had an aligned length of
2712 bp, which was reduced to 1110 bp after the removal of
1602 bp of ambiguously aligned regions by Gblocks. Of the
1110 characters used in the final phylogenetic analyses, 554
were constant and 556 were variable. A burn-in of 10% was
estimated using Tracer v. 1.5 to be sufficient to remove the
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Table 1 e List of taxa, locality, collection/strain numbers of voucher specimens, fungarium accession numbers, andGenBank accession numbers for specimens used in this study.
Species Locality Voucher Fungarium no. GenBank Accession no.
ITS 28S
Aspergillus fumigatus USA, Connecticut C. Thom 118 ATCC 1022 EF669931 U28460
A. nidulans USA, Texas 97-726 GenBank AF078899 AF109338
Geoglossum difforme USA, North Carolina ASM 10498 ILLS 67349 KC222124 KC222137
G. glabrum Czech Republic J. Gaisler s.n. ILLS 72358 KP657559 KP657564
G. simile USA, New York TJB 9613 ILLS 71160 KF944381 KF944383
Glutinoglossum glutinosum Czech Republic J. Gaisler s.n. ILLS 67353 KC222128 KC222141
G. heptaseptatum Czech Republic J. Gaisler s.n. ILLS 63754 KC222130 KC222143
Graddonia coracina USA, Tennessee ANM 2018 ILLS 60491 JQ256423 JN012009
Hemileucoglossum alveolatum USA, Michigan Imshaug 3640 MICH s.n. KP657560 KP657565
H. littorale Denmark Lœssøe 32VNJ2704 C: 35673 KP657561 KP657566Leucoglossum durandii China s.n. HMAS 70090 HQ222875 N/A
Maasoglossum aseptatum Sweden J. Nitare s.n. UPS: F-118883 KP657562 KP657567
M. verrucisporum Bhutan Sharma 17725 CUP-IN-000606 KP657563 KP657568
Microglossum olivaceum Unknown FH-DSH97-103 GenBank AY789398 AY789397
M. rufum Unknown Ingo-Clark-Geo 163 GenBank DQ257360 DQ470981
Nothomitra cinnamomea France Moingeon s.n. ILLS 61042 JQ256424 JQ256439
Orbilia auricolor United Kingdom AFTOL-ID 906 CBS 547.63 DQ491512 DQ470953
O. delicatula USA, Maine DHP 108 GenBank U72595 N/A
Peziza phyllogena USA, Massachusetts WZ-Geo44-Clark GenBank AY789329 AY789328
P. varia Unknown WZ-Geo94-Clark GenBank AY789392 AY789391
Sabuloglossum arenarium The Netherlands CFR 181007 ILLS 61043 JQ256426 JQ256440
S. arenarium Finland Ohenoja s.n. OULU-F077201 GU324765 GU324764
Sarcoleotia globosa USA, Washington Trappe 26123 OSC 63633 AY789410 AY789409
S. globosa Unknown s.n. MBH 52476 AY789429 AY789428
Spathularia flavida Unknown wz95 GenBank AF433155 AF433144
Thuemenidium atropurpureum United Kingdom S. Kelly s.n. K(M): 135612 EU784253 AY789307
Trichoglossum hirsutum USA, Tennessee ANM 2233 ILLS 67355 KC222132 KC222145
T. octopartitum USA, Tennessee ANM 2227 ILLS 67356 KC222134 KC222147
Collector acronyms: ANM ¼ Andrew N. Miller, ASM ¼ Andrew Methven, CFR ¼ Kees Roobeek, DHP ¼ Donald Pfister, DSH ¼ David Hibbett,TJB¼ Timothy Baroni, WZ¼ ZhengWang. Fungarium acronyms: ATCC¼ American Type Culture Collection, C¼University of Copenhagen, CBS¼ Centraalbureau voor Schimmelcultures, CUP ¼ Cornell University, HMAS ¼ Kunming University, ILLS ¼ Illinois Natural History Survey,K(M)¼Kew (Mycology), MBH¼Marlborough College, MICH¼University ofMichigan, OSC¼Oregon State University, OULU¼University of Oulu,UPS ¼ Uppsala University. Newly generated sequences are in bold. All other sequences are from GenBank. s.n. ¼ sine numero (no voucher orfungarium number is available).
my c o s c i e n c e 5 6 ( 2 0 1 5 ) 5 7 2e5 7 9574
pre-stationary posterior probability distribution, resulting in
an ESS value of 2894.54. The standard deviation of split fre-
quencies was 0.000284 at the end of the Bayesian analysis.
Fig. 1 represents themost likely tree produced by PhyML of the
final combined dataset.
Geoglossomycetes was supported as a clade with 90% ML
BS, although with less than 0.95 BPP. Maasoglossum was
recovered as a distinct genus within Geoglossomycetes, with
the clade containing the generaMaasoglossum,Nothomitra, and
Sarcoleotia well-supported (99% ML BS, 1.0 BPP) and distinct
from the remaining members of Geoglossomycetes. Maaso-
glossum appears most closely related to Sarcoleotia, although
branch support is lacking. Geoglossum aseptatum and M. ver-
rucisporum appear as separate species in the Maasoglossum
clade, with 12% ITS and 9% LSU sequence divergence between
these two species (data not shown).
Maasoglossum K.S. Thind & R. Sharma emend. Hustad & A.N.
Mill., Kavaka 12: 37 (1984)
Mycobank no.: MB 25055.
Ascomata scattered to gregarious, black, glabrous,
becoming slightly longitudinally rugulose upon drying,
2e8 cm tall, up to 2 mm wide. Stipe terete, glabrous, textura
porrecta, with dark-colored narrow hyphae intertwining
inflated longitudinal cells. Paraphyses longer than the asci,
hyaline to light brown, straight to curved or circinate, enlarged
at the apex (up to 15 mm broad), agglutinated into an epi-
thecum by a light brown amorphous matter above. Asci
clavate to clavate-cylindric, up to 165 mm in length and 16 mm
wide, mostly 8-spored, tip Jþ in Melzer's. Ascospores lightbrown in maturity, cymbiform to ellipsoid, straight to slightly
curved, aseptate, occasionally with 1e2 oil drops. Growing in
soil, often in disturbed habitats.
The light brown, aseptate ascospores separate this genus
from other members of Geoglossomycetes. Sabuloglossum also
has aseptate ascospores, althoughmature, septate ascospores
are rarely encountered and the ascospores in that genus are
typically hyaline except for occasional yellowish to light
brown pigments in mature ascospores. Maasoglossum can be
distinguished from Hemileucoglossum in that the paraphyses,
while strongly agglutinated into an epithecum of brown
amorphousmatter, are often curved to circinate at the apex in
Maasoglossum, whereas the paraphyses are straight in Hemi-
leucoglossum. Furthermore, the agglutinating material in
Maasoglossum is a paler brown than in Hemileucoglossum.
Hemileucoglossum also has ascospores that long remain
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Geoglossum glabrum ILLS 72358Geoglossum difforme ILLS 67349
79
Geoglossum simile ILLS 7116097
Leucoglossum durandii HMAS 7009092
Sabuloglossum arenarium ILLS 61043Sabuloglossum arenarium OULU-F077201
Trichoglossum hirsutum ILLS 67355Trichoglossum octopartitum ILLS 67356
100
Glutinoglossum glutinosum ILLS 67353Glutinoglossum heptaseptatum ILLS 63754
97
Hemileucoglossum alveolatum Imshaug 3640Hemileucoglossum littorale C: 35673
100
87
Maasoglossum aseptatum UPS: F-118883Maasoglossum verrucisporum CUP-IN-000606
100
Sarcoleotia globosa OSC 63633Sarcoleotia globosa MBH 52476
91
Nothomitra cinnamomea ILLS 61042
99
90
Microglossum rufum Ingo-Clark-Geo 163Thuemenidium atropurpureum K(M): 135612
90
Microglossum olivaceum FH-DSH97-10397
Spathularia flavida wz95Graddonia coracina ILLS 60491
9297
Aspergillus fumigatus NRRL 163Aspergillus nidulans 97-726
100
90
73
Orbilia delicatula DHP 108Orbilia auricolor AFTOL-ID 906
91
Peziza phyllogena WZ-Geo44-ClarkPeziza varia ZW-Geo94-Clark
100
0.01
Geoglossomycetes
Fig. 1 e PhyMLmaximum likelihood phylogeny showing the position ofMaasoglossumwithin Geoglossomycetes based on a
combined dataset (1110 bp) of ITS and LSU nrDNA sequences ((-ln)L score¼ 9595.503). Numbers at nodes indicate significantBS values (≥70%) based on 100 replicates; thickened branches indicate significant BPP (≥95%). Numbers associated withtaxon names are fungarium accession numbers or strain numbers obtained from GenBank. Type species for genera in the
Geoglossomycetes are shown in bold.
myc o s c i e n c e 5 6 ( 2 0 1 5 ) 5 7 2e5 7 9 575
hyaline, but the ascospores rapidly develop septation and
some species (e.g. Hemileucoglossum littorale (Rostr.) Arauzo)
have pigmented mature ascospores. Sarcoleotia produces a
pileate ascocarp and ascospores that remain hyaline and
develop up to five septa at maturity.
Maasoglossum aseptatum (Hakelier ex Nitare) Hustad & A.N.
Mill. comb. nov.
Basionym ¼ Geoglossum aseptatum Hakelier ex Nitare, Wind-ahlia 14: 40 (1984) [as “asaeptatum”].
Mycobank no.: MB 811291 Fig. 2.
Type: SWEDEN, €Orebro, N€arke, Axberg, Vitmossen, on soil
in moss in the drip line of a small building, 1 Sep 1977, leg. N.
Hakelier s.n. (holotype, UPS:F-116948).
Etymology: Refers to the aseptate mature ascospores.
Ascomata black throughout, lanceolate-linear, becoming
slightly longitudinally rugulose upon drying, 3.1e8.2 cm tall,
0.1e0.5 cm wide. Stipe smooth, black, terete, not distinctly
different from fertile hymenium, up to 13 mm wide. Paraphy-
seshyaline to subhyaline, straight to curvedor circinate at tips,
often enlarged at the apex (Fig. 2C), longer than asci, the upper
portions strongly agglutinated by a light brown amorphous
matter (Fig. 2E). Asci clavate, (80e)104e131(e141) � (9.6e)10.5e13.1(e14.2) mm (average 117.12 ± 13.21 � 11.8 ± 1.23 mm,n ¼ 30), 8-spored, having zero or at most two uniseriate asco-spores below, biseriate or triseriate above (Fig. 2A), ascus tip
lightly Jþ in Melzer's (Fig. 2D). Ascospores cymbiform toobovoid or clavate, often enlarged at one end, (16.2e)
23.1e29.9(e35.0) � (4.9e)5.4e6.3(e6.9) mm (average25.47 ± 2.54 � 5.96 ± 0.48 mm, n ¼ 30), aseptate, hyaline to lightgolden brown, sometimes with one or two oil drops (Fig. 2B).
Distribution: Finland (Bonsdorff von et al. 2012), the
Netherlands (Nitare 2012; www.gbif.org), Sweden (Nitare 1982,
1984, 2012, www.gbif.org).
Specimens examined: Holotype (UPS:F-118883); SWEDEN,
V€astra G€otaland, Bohusl€an, G€oteborg; G€oteborgs Botaniska
Tr€adgård (Gothenburg Botanic Garden), in soil among moss, 1
Sep 1987, J. Nitare s.n.
Macroscopically, Maasoglossum aseptatum is hardly distin-
guishable from other species in Geoglossum. The ascocarp is
within normal size ranges of other species of Geoglossum and
is black throughout. Upon drying, the hymenium becomes
slightly longitudinally rugulose. The small, light brown,
aseptate ascospores are the most noticeable difference be-
tween this species and other Geoglossum. Additionally, the
paraphyses are slightly agglutinated with an amorphous
brown material. This combination of characters led Nitare
(1982) to suggest M. aseptatum as a potential link between
the genus Geoglossum and Thuemenidium atropurpureum
(Batsch) Kuntze, a fungus formerly considered to belong in
Geoglossaceae but which is now considered to belong in
Leotiomycetes (Ohenoja et al. 2010; Hustad et al. 2013).
Maasoglossum aseptatum was described from collections
made byNils Hakelier froma single location in central Sweden
in 1977 (Nitare 1984). To date, the fungus has only been found
in four sites: two locations in Sweden (Bohusl€an, in the
Gothenburg Botanic Garden and the type locality in N€arke),
one location in Finland (Tavastia, H€ameenlinna, Levonkallio),
and one location in the Netherlands (Gelderland, Voorst,
Gietelse Bos). Each location where ascocarps of M. aseptatum
were found fruiting in disturbed soil has a history of cultiva-
tion, gardening, forestry, or other soil disturbance. The species
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Fig. 2 e Maasoglossum aseptatum from dried holotype material (UPS:BOT:F-116948). A: Ascus; B: Ascospores; C: Paraphyses;
D: Ascus tip lightly Jþ; E: Hymenium. Bars: 10 mm.
Fig. 3 e Maasoglossum verrucisporum from dried isotype
material (CUP-IN 000606). A: Ascospores; B: Paraphyses; C:
Ascus; D: Transverse section of axial stipe hyphae. Bars:
10 mm.
my c o s c i e n c e 5 6 ( 2 0 1 5 ) 5 7 2e5 7 9576
has been reported from gardens and forests and possible as-
sociations may exist between the fungus and plants including
Rumex acetosa L., Luzula pilosa (L.) Willd., mosses including
Atrichumundulatum (Hedw.) P. Beauv. and Fissidens adianthoides
Hedw., and trees including Prunus padus L.,Ulmus glabraHuds.,
and Picea abies (L.) H. Karst. (Nitare 1984, 2012; Bonsdorff von
et al. 2012). Nitare (2012) suggested that the fungus acts as a
decomposer in these ecosystems, although he also hypothe-
sized the possibility that the fungus may form ericoid
mycorrhizae with shrubs and trees.
Although Maasoglossum aseptatum is regarded as Data
Deficient in regional red lists of Swedish Fungi (G€ardenfors
2010), this fungus should almost certainly be regarded as
Critically Endangered due to the rarity of occurrence and the
fragility of its habitat. Of the two Swedish localities for M.
aseptatum, the site at the Gothenburg Botanic Garden was
destroyed during renovations and the fungus has not been
collected there since 2005 (G€ardenfors 2010; Nitare 2012). The
site in the Netherlands was also destroyed. Of the four
known locations of M. aseptatum in the world, only the type
location in Sweden (N€arke) and the location in Finland
remain.
Maasoglossum verrucisporum K.S. Thind & R. Sharma, Kavaka
12: 37 (1984) [as “verrucosporum”].
Mycobank no.: MB 544188 Fig. 3.
Type: BHUTAN, Thimphu, Dochula, on soil among mosses
in mixed forest, 10,000 feet elev., 3 Aug 1984, R. Sharma 17725,
(holotype PAN 17725, isotype CUP-IN-000606).
Etymology: Refers to the warted ascospores.
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myc o s c i e n c e 5 6 ( 2 0 1 5 ) 5 7 2e5 7 9 577
Ascomata scattered to gregarious, black throughout,
cylindrical-clavate, distinctly rugose with longitudinal ridges
especially prominent in dried specimens, 2e6 cm tall,
0.1e0.5 cm wide. Stipe smooth, black, terete, not distinctly
different from fertile hymenium, up to 1.5 mm wide. Pa-
raphyses hyaline to subhyaline, straight to curved at tips,
somewhat enlarged at the apex (Fig. 3B), longer than asci, the
upper portions agglutinated by a light brown amorphous
matter. Asci clavate-cylindric, (112e)130e151(e165) � (10.2e)12.5e14.4(e16.0) mm (average 141.2 ± 10.1 � 13.3 ± 0.9 mm,n ¼ 30), 8-spored (occasionally 4-spored), ascospores biseriate(Fig. 3C), ascus tip Jþ in Melzer's. Ascospores cymbiform toobovoid or clavate, (23.9e)26.1e30.0(e32.0) � (5.8e)6.2e7.3(e7.9) mm (average 28.05 ± 1.95� 6.78 ± 0.52 mm, n¼ 30),aseptate, hyaline to light brown, distinctly covered with
minute, profuse warts (Fig. 3A).
Distribution: Bhutan (Thind and Sharma 1984).
Specimen examined: Isotype, CUP-IN-000606.
Maasoglossum verrucisporum is known only from the type
collection found in Bhutan. The continuous, light brown,
warted ascospores distinguish this species from all other
members of Geoglossomycetes. The fungus is not named in
the 2009 Biodiversity Action Plan for Bhutan (NBSAP 2009),
although it should certainly be regarded as Critically Endan-
gered due to the extreme rarity of occurrence.
Our results suggest that Maasoglossum belongs in Geo-
glossomycetes and is likely most closely related to Nothomitra
and Sarcoleotia, although the long-branch connecting Maaso-
glossum to these genera suggests that Maasoglossum has long
been evolving independently of Nothomitra and Sarcoleotia.
These three genera have ecological and morphological simi-
larities. Each of these genera is characterized by mature as-
cospores that are hyaline or lightly colored and are aseptate,
although they can become 1- to 3-septate when overmature in
Nothomitra and 3- to 5-septate when overmature in Sarcoleotia.
The derived members of Geoglossomycetes are characterized
by ascospores that are more consistently darkly pigmented
and generally multiseptate when mature. These species may
also be ecologically linked by fruiting in response to soil
disturbance.
Production of fruiting bodies following soil disturbance is
common in several fungi (Sagara 1992). Many discomycetous
fungi are known to fruit following soil disturbance (e.g. Geo-
pyxis (Pers.) Sacc., Octospora Hedw., Peziza Dill. ex Fries, and
Trichophaea Cooke & W. Phillips) (Petersen 1970; Dix and
Webster 1995). Production of fruiting bodies in response to
disturbance appears to be a basal character in Geo-
glossomycetes, with Sarcoleotia globosa (Sommerf.: Fr) Korf
being most commonly encountered on recently disturbed soil
(Schumacher and Sivertsen 1987; Jumpponen et al. 1997).
Petch (1922) described the genus Phaeoglossum Petch in
Geoglossaceae to accommodate the species Phaeoglossum
zeylanicum Petch from Sri Lanka. While we have not seen
material of this species, we concur with Nitare (1984) that this
genus name does not apply to Maasoglossum based on differ-
ences in morphology and habitat between the two genera.
Petch's Phaeoglossum was described as a black club-shapedfungus with white internal hyphae not known to be present
in Geoglossomycetes. It is also described as growing on
decaying Loranthus L. fruits, a habitat not found in other
members of Geoglossomycetes. Lastly, the name Phaeoglossum
Petch is illegitimate pursuant to Article 53.1 of the ICN
(McNeill 2012) as it is a later homonym of Phaeoglossum
Skottsb., a brown alga described by Skottsberg (1907).
Maasoglossum has previously been misidentified as Thue-
menidium (Geoglossum) atropurpureum (Nitare 2012) and more
collections of it may exist under that misnomer in fungaria in
Northern Europe. Both species of Maasoglossum and T. atro-
purpureum possess hyaline paraphyses that are agglutinated
into an epithecum, although in T. atropurpureum the epi-
thecum is a vinous-brown compared to a light brown in both
species ofMaasoglossum. The ascomata of T. atropurpureum are
distinctly purplish-brown when fresh, and the fertile portion
is often irregular to spathulate and distinct from the sterile
stipe. Maasoglossum and T. atropurpureum are also easily
separated based on ascospore morphology: ascospores in T.
atropurpureum are initially continuous but become multi-
guttulate and finally septate when overmature and remain
hyaline throughout development, whereas in both species of
Maasoglossum the ascospores are continuous and light brown
with distinct warts present in M. verrucisporum.
The hyphae at the apex of the stipe in Maasoglossum
contain inflated, hyaline, longitudinal elements and an
anastomosing network of brown, narrow hyphae intertwining
them (Fig. 3D). The more derived members of Geo-
glossomycetes also contain anastomosing hyphae in the stipe,
but the longitudinal cells are not as strongly inflated. The
inflated longitudinal cells and narrower binding hyphae in the
axial stipe of Maasoglossum are similar to those found in
Thuemenidium atropurpureum, but different from Microglossum
(Maas Geesteranus 1964). In Microglossum, the axial stipe hy-
phae are comprised primarily of agglutinated, narrower lon-
gitudinal elements, with binding hyphae very rarely observed.
Nothomitra and Sarcoleotia also contain a densely interwoven
internal stipe hyphal system, although the longitudinal ele-
ments are not inflated as they are in Maasoglossum.
In summary, our study supported the inclusion of Maa-
soglossum as a basal member of Geoglossomycetes. Our
findings suggest that genera with hyaline- to lightly-pig-
mented and aseptate ascospores form the base of the Geo-
glossomycetes clade, with the more derived members of the
clade exhibiting darkly-pigmented and multiseptate asco-
spores (e.g. Geoglossum and Trichoglossum). The ascocarp of
Maasoglossum is morphologically similar to the more derived
members of Geoglossomycetes, with the fertile hymenium
intergrading entirely with the sterile stipe. The morphology
of the ascospores and internal stipe hyphae of Maasoglossum
hints at the common ancestry between Geoglossomycetes
and stalked earth tongues in Leotiomycetes, such as
Thuemenidium.
Acknowledgments
We wish to thank the following for graciously providing
specimens for study: T Baroni, T Læssøe, P Lizon, AS Methven,
J-M Moingeon, CF Roobeek, and the fungaria at CUP, MICH,
SAV, and WTU. The authors wish to acknowledge the
following sources of funding to VPH: American Society of
http://dx.doi.org/10.1016/j.myc.2015.05.003http://dx.doi.org/10.1016/j.myc.2015.05.003
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my c o s c i e n c e 5 6 ( 2 0 1 5 ) 5 7 2e5 7 9578
Plant Taxonomists, Discover Life in America, the Graduate
College at the University of Illinois at Urbana-Champaign,
Mycological Society of America, and the North American
Mycological Association.
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Maasoglossum, a basal genus in GeoglossomycetesAcknowledgmentsReferences