Mycosphere Doi 10.5943/mycosphere/2/6/5/
Inclusion of Nothomitra in Geoglossomycetes
Hustad VP1,2*, Miller AN2, Moingeon J-M3 and Priou J-P4
1
Department of Plant Biology, University of Illinois at Urbana-Champaign, 505 S. Goodwin Ave., Urbana, IL 61801
Illinois Natural History Survey, University of Illinois, 1816 S. Oak St., Champaign, IL 61820
3
28 Grande Rue, 25520 Goux-les-Usiers, France
4
7 Rue De Picardie, F- 56200 La Gacilly, France
2
Hustad VP, Miller AN, Moingeon J-M, Priou J-P 2011 – Inclusion of Nothomitra in
Geoglossomycetes. Mycosphere 2(6), 646-654, Doi 10.5943/mycosphere/2/6/5/
Nothomitra is a small genus of earth tongues consisting of three species. Historically placed within
the Geoglossaceae sensu lato, the genus is currently considered incertae sedis within the Helotiales.
We reviewed the morphology and analyzed the phylogenetic relationships of Nothomitra using a
combined dataset of ITS, LSU and Mcm7 DNA sequences representing 22 species. The placement
of Nothomitra was strongly supported within the Geoglossomycetes clade, forming part of the
ancestral base of the class with Sarcoleotia globosa and Thuemenidium arenarium. The inclusion of
Nothomitra within the Geoglossomycetes is confirmed.
Key words – Ascomycota – earth tongues – Geoglossaceae – Leotiomycetes – phylogeny
Article Information
Received 1 December 2011
Accepted 5 December 2011
Published online 29 December 2011
*Corresponding author: Vincent Hustad – e-mail – vhustad@illinois.edu
Introduction
Earth tongues are among the most
widely distributed groups of fungi on earth and
have been a subject of mycological inquiry
since Persoon first described Geoglossum in
the late 18th century. Genera typically referred
to as earth tongues include Geoglossum,
Trichoglossum, Microglossum, Leotia, and
Spathularia. During the last 200 years, numerous genera and species have been included and
removed from this group based primarily on
morphological data. Recent molecular studies
(Pfister and Kimbrough 2001, Wang et al.
2006a and b, Schoch et al. 2009, Ohenoja et al.
2010) have suggested earth tongues are not a
monophyletic group and this resulted in the
introduction of the class Geoglossomycetes
(Schoch et al. 2009), which contains four
genera and approximately 50 species. Currently
included within the Geoglossomycetes are
Geoglossum (22 species), Sarcoleotia (4
species), Thuemenidium (5 species), and
646
Trichoglossum (19 species) (Kirk et al. 2008).
However, several genera formerly included
within the Geoglossaceae sensu lato are
currently considered incertae sedis and the
placement of these taxa within the Pezizomycotina is unknown.
The monotypic genus Nothomitra was
introduced by Maas Geesteranus (1964) to
accommodate N. cinnamomea Maas Geest.,
which was described from specimens collected
in Upper Austria during the autumn of 1962.
Three species are accepted in the current
concept of the genus following the additions of
Nothomitra kovalii Raitviir (1971) from
Kunashir in the Kuril Islands and Nothomitra
sinensis Zhuang and Wang (1997) from China.
At present, Nothomitra is only known to occur
in Europe and Asia, though extensive distribution data is lacking. All species in
Nothomitra are terrestrial with N. cinnamomea
reported growing amongst Sphagnum, N.
kovalii reported from rocky soil, and N.
Mycosphere Doi 10.5943/mycosphere/2/6/5/
sinensis reported from mossy soil in coniferous
forests. Nothomitra is found across a wide
range of altitudes. N. cinnamomea is recorded
from the European Alps from 670 to 1100 m
elevation, Nothomitra kovalii is found between
400-800 m elevation on Mt. Mendeleyeva in
the Kuril Islands, whereas N. sinensis is described from the Qilian Mountains in Northern
China at 2850 m elevation.
Nothomitra is characterized by the
distinct free edge of the hymenium at the
junction of the stipe, unlike Microglossum in
which the hymenium intergrades with the stipe
on the flattened sides (see Fig 1C). Nothomitra
is also differentiated from Microglossum in that
the fertile head of the ascocarp is not flattened
as in Microglossum, and the internal stipe
hyphae of Nothomitra are parallel and easily
separable versus the interwoven and
agglutinated hyphae found in Microglossum.
These morphological differences were cited by
Maas Geesteranus (1964) as evidence that
Nothomitra is not congeneric with Microglossum. However, Moingeon and Moingeon
(2004) argued that these characters were not
sufficient to support Nothomitra as a separate
genus and advocated the placement of N.
cinnamomea into Microglossum, thereby rendering the genus Nothomitra a synonym.
Since the importance of the morphological differences between Nothomitra and
Microglossum are disputed as is the taxonomic
placement of Nothomitra, it is necessary to
evaluate molecular characters in order to determine the phylogenetic relationships of this
genus. As such, the purpose of this study is to
include Nothomitra in a modern phylogenetic
analysis for the first time to determine its
placement within the Pezizomycotina and to
provide detailed insight into the systematics of
the Geoglossomycetes using a multi-gene phylogeny.
Methods
Generation of Molecular Data
Total genomic DNA was extracted from
dried ascomata using a QIAGEN DNeasy Plant
Mini Kit (QIAGEN Inc., Valencia, California)
and gene fragments were PCR amplified and
sequenced following the meth-ods outlined in
Promputtha and Miller (2010) and Raja et al.
(2011). Gene fragments were amplified using
the following sets of primers: ITS1 and ITS4
(White et al. 1990) for the internal transcribed
spacer (ITS) region of nrDNA; JS1 (Landvik
1996) and LR6 (Vilgal-ys and Hester 1990) for
the partial 28S nuclear ribosomal large subunit
(LSU) of nrDNA; 709F and 1348R (Schmitt et
al. 2009) for the DNA replication licensing
factor MS456 (Mcm7).
These genes were chosen because: a)
they provide appropriate resolution at various
taxonomic levels (i.e. species to class), b)
fungal and ascomycete–specific primers have
been developed for these genes, c) a large
number of available sequences are available
from GenBank because previous researchers
(e.g. Wang et al. 2006a and b, Schoch et al.
2009, Ohenoja et al. 2010, Hustad and Miller
2011) have used the nuclear ribosomal genes to
effectively reconstruct phylogenies within Geoglossomycetes and neighboring groups, d)
based on our preliminary data (Raja et al.
2011), Mcm7 shows promise for reconstruction
of accurate species-level to class-level phylogenies, and, e) incorporating both ribosomal and
protein–coding genes allows for higher
certainty in assessing phylogenetic relationships.
Sequence Alignment and Phylogenetic
Analyses
Each generated ITS and LSU sequence
fragment was subjected to an individual blast
search to verify its identity. Mcm7 sequences
were only used from specimens which provided reliable ITS and/or LSU sequences. Sequences were assembled using Sequencher 4.9
(Gene Codes Corp., Ann Arbor, Michigan),
optimized by eye and manually corrected when
necessary. Alignments of individual genes
were created manually by eye in Sequencher
4.9 or using Muscle 3.7 (Edgar 2004) in
Seaview 4.2 (Galtier et al. 1996). Individual
gene datasets were then analyzed using Gblocks 0.91b (Castresana 2000) to identify and
remove ambiguous regions from the alignment.
The Akaike Information Criterion
(AIC) (Posada and Buckley 2004) as implemented in jModelTest 0.1.1 (Posada 2008)
determined GTR+I+G as the best fit model of
evolution for both maximum likelihood and
Bayesian inference. Maximum likelihood
analyses were performed using PhyML
647
Mycosphere Doi 10.5943/mycosphere/2/6/5/
(Guindon and Gascuel 2003) under the GTR
substitution model with six rate classes and
invariable sites optimized. A BioNJ starting
tree was constructed and the best of nearest
neighbor interchange (NNI) and subtree
pruning and regrafting (SPR) tree improvement
was
implemented.
Bootstrap
support
(Felsenstein 1985) (BS) was determined with
100 bootstrap replicates. Clades with >70% BS
were considered significant and highly
supported (Hillis and Bull 1993).
Bayesian inference employing a
Markov Chain Monte Carlo (MCMC)
algorithm was performed using MrBayes 3.1.2
(Huelsenbeck and Ronquist 2001) as an additional means of assessing branch support. The
GTR+I+G model with six rate classes was
employed. Four independent chains of MCMC
were run for 10 million generations to insure
that trees were not trapped in local optima.
Clades with Bayesian posterior probability
(BPP) >95% were considered significant and
highly supported (Alfaro et al. 2003).
The individual ITS, LSU, and Mcm7
datasets were examined for potential conflict
before concatenation into a single dataset for
total evidence analysis (Kluge 1989, Eernisse
and Kluge 1993). The individual gene phylogenies were considered incongruent if clades
with significant ML bootstrap and Bayesian
posterior probability (>70% BS or >95% BPP)
were conflicting in the individual tree
topologies (Wiens 1998, Alfaro et al. 2003,
Lutzoni et al. 2004). As no incongruencies
were found among the three individual data
sets, they were concatenated using Seaview 4.2
and subjected to phylogenetic analyses as
above.
Results
Morphology
Nothomitra cinnamomea Maas Geest.,
Persoonia 3(1): 92, 1964.
= Microglossum cinnamomeum S.
Moingeon
&
J.M.
Moingeon,
Miscellannea Mycologica 80–81:
31, 2004.
Type: Austria, Attergau, Fehra Moos, SW of
St. Georgen, 29 September 1969, J.T. Palmer
11391. L 962.271-144.
648
Ascomata scattered to gregarious occurring in
soil, 1–3.3 cm high, hymenium borne on variously-shaped fertile heads, head glabrous, spathulate to obovoid or subglobose with concolorous wavy lobes, pale cinnamon to olivaceous,
darkening with age, 3–9 mm broad (Fig 1A,
B), hymenium distinctly separated from stipe
(Fig 1C), stipe straight or flexuous, terete,
tapering towards base, ochraceous above
becoming paler toward base, squamulose
above, becoming glabrous at base, 0.7–2.4 cm
high. Hyphae at center of stipe easily separated,
often swollen at the septa, thin–walled and
often branched. Hyphae near the periphery of
the stipe thin-walled and tightly bundled.
Paraphyses filiform, upper cells hyaline, with
brownish guttules in lower cells, septate,
sometimes branched at apex or base, curved at
the apex, slightly longer than asci, 1–1.5 m
wide, expanding to 2–3 m wide at apex. Asci
cylindrical–clavate, with crosiers, inoperculate,
apical ring euamyloid, deep blue in IKI, small,
not occupying entire apex, 150–180 × 9.5–
12.5m (Fig 1B), 8–spored, biseriate. Ascospores fusiform to narrowly obclavate, rounded
at apex, acute at base, hyaline, smooth, multiguttulate, single–celled in ascus, becoming up
to 5–septate when mature or old, 35–47 (–55) ×
3.5–5.5 (–6) m (Fig 1D).
Habitat: Growing among Sphagnum and
Aulocomnium palustre (Hedw.) Schwägr.,
often accompanying Geoglossum sphagnophilum Ehrenb. September–October.
Distribution: Known from Austria and France.
Anamorph: Unknown.
Material examined – France, Jura, Bellefontaine, September 2001, 1100 m, leg. J.M.
Moingeon s.n., ILLS Acc. ANM463; ILLS
Acc. ANM538; ILLS Acc. ANM540; October
2001, leg. J.M. Moingeon s.n., ILLS Acc.
ANM549.
Phylogenetic analyses
Twenty–two taxa were included in the
final analyses (Table 1). Mcm7 data for Microglossum olivaceum and Sarcoleotia globosa
were not available. The final data matrix had an
aligned length of 2720 base pairs, which was
reduced to 2091 after the removal of 629
ambiguous characters by Gblocks. Of the 2091
characters used in the final analyses, 76 were
Mycosphere Doi 10.5943/mycosphere/2/6/5/
Figs 1 (A-D) – Nothomitra cinnamomea. A In situ photograph of ascomata. B Ascus, total
magnification = 400X. C Close up of fertile tip, arrow denotes separation of head and stipe. D
Ascospores illustrating variable septation, total magnification = 800X.
constant, 819 were parsimony–uninformative,
and 1196 were parsimony informative. The
maximum likelihood tree produced from the
combined ITS, LSU, and Mcm7 dataset is presented in Fig 2. The topology of Geoglossomycetes is congruent with those produced from
similar analyses including Geoglossomycetes
taxa (Schoch et al. 2009, Ohenoja et al. 2010,
Wang et al. 2011). Two major clades are present and strongly supported in our analyses: the
Leotiomycetes clade (BP=100%, PP=1.0) and
the Geoglossomycetes clade (BP=100%,
PP=1.0). Nothomitra cinnamomea was placed
within Geoglossomycetes as a sister taxon to
Sarcoleotia globosa with moderate support
(BS=78%). Geoglossum occurred as a strongly
supported monophyletic group (BP=100%,
PP=1.0), whereas Trichoglossum was paraphyletic.
of Geoglossomycetes, closely aligned with
Sarcoleotia globosa as the most basal members
of the class. Morphologically, S. globosa is
rather similar to N. cinnamomea (Fig 3). Both
species possess a distinct capitate hymenium
that is clearly separated from the stipe when
mature, but the margin of the hymenium is
completely free in N. cinnamomea and completely inrolled in S. globosa. Both species also
possess hyaline ascospores that develop 3-5
septa upon maturation. Lastly, both species are
terrestrial and collection data suggests that an
association with mosses exists in both species
(Maas Geesteranus 1964, Schumacher and
Silvertsen 1987). These morphological and
ecological similarities support the close phylogenetic relationship of N. cinnamomea and S.
globosa revealed by the molecular phylogeny
(Fig 2).
Discussion
Our analyses confirm Nothomitra
cinnamonmea as a strongly supported member
Another morphological feature that links N.
cinnamomea within Geoglossomycetes is that
the hyphae at the axis of the stipe are not
649
Mycosphere Doi 10.5943/mycosphere/2/6/5/
Table 1 List of taxa, GenBank and herbarium accession numbers, collections numbers, and locality
for specimens used in this study.
Name
Bisporella citrine
Collection
Number
Herbarium
#
ILLS61033
VPH s.n.
Locality
ITS
LSU
Mcm7
JQ256414
JQ256432
JN672971
JQ256415
JQ256416
JN012006
JQ256433
JN672988
JQ256444
JQ256417
JQ256434
JQ256445
JQ256418
JN673044
JN672990
JQ256419
JQ256435
JQ256446
JQ256420
JQ256436
JQ256447
JQ256421
JQ256437
JQ256448
JQ256422
JQ256438
JQ256449
JQ256423
JQ268558
AY789398
JN198494
JN012009
JN673046
AY789397
AF286411
JN672993
JN672997
N/A
XM958785
JQ256424
JQ256439
JQ256450
JQ256425
AY789300
JN012015
AY789299
JQ256451
N/A
JQ256426
JQ256440
JQ256452
JQ256427
JQ256441
JQ256453
JQ256428
JQ256442
JQ256454
JQ256429
JQ256443
JQ256455
JQ256430
JN673053
JN673022
JQ256431
JN012017
JN673023
ILLS60488
Cudoniella clavus
Geoglossum barlae
Geoglossum cookeanum
ANM2087
Moingeon s.n.
ILLS61034
ILLS61035
ANM2257
ILLS61036
Geoglossum difforme
ANM2169
ILLS61037
Geoglossum fallax
J. Gaisler s.n.
ILLS61038
Geoglossum glabrum
ANM2267
ILLS61039
Geoglossum simile
ANM2171
ILLS61040
Geoglossum umbratile
CFR251108
ILLS60491
Graddonia coracina
Hymenoscyphus fructigenus
Microglossum olivaceum
Neurospora crassa
Nothomitra cinnamomea
ANM2018
ASM10619
GenBank
GenBank
ILLS61041
N/A
N/A
ILLS61042
Moingeon s.n.
ILLS60497
Propolis versicolor
Sarcoleotia globosa
ANM2050
GenBank
Thuemenidium arenarium
CFR181007
N/A
ILLS61043
ILLS61044
Thuemenidium
atropurpureum
ASM4931
ILLS61045
Trichoglossum hirsutum
J. Gaisler s.n.
ILLS61046
Trichoglossum octopartitum
JPP10191
ILLS61047
Trichoglossum walteri
Vibrissia filisporia f.
filisporia
ANM2203
ILLS60499
ANM2064
agglutinated and easily separable, a character
commonly seen in Geoglossomycetes. Maas
Geesteranus (1964) cited this character in his
original proposal to separate Nothomitra from
Microglossum, and this character appears to be
one of the few conserved characters throughout
the class. As in previous molecular based
phylogenies (Wang et al. 2006a and b, Schoch
et al. 2009, Ohenoja et al. 2010), Microglossum
olivaceum and Thuemenidium atropurpureum
were shown to occur in the Leotiomycetes.
650
Champaign
County, Illinois
GSMNP,
Tennessee
France
GSMNP, North
Carolina
Cades Cove,
GSMNP,
Tennessee
Hamrstejn,
Czech Republic
GSMNP,
Tennessee
GSMNP,
Tennessee
Kennemerland,
Netherlands
GSMNP,
Tennessee
Samara, Russia
N/A
N/A
Bellefontaine,
Jura, France
GSMNP, North
Carolina
N/A
Kennemerland,
Netherlands
Cortland
County, New
York
Hamrstejn,
Czech Republic
Senavelle,
France
GSMNP, North
Carolina
GSMNP, North
Carolina
Both Microglossum and Thuemenidium possess
hyaline ascospores but this character is not
sufficient to exclude these genera from
Geoglossomycetes since several Geoglossum
species
possess
hyaline
ascospores.
Microglossum can be delineated from
Geoglossomycetes based on its ascomata that
range from brightly colored to brown.
Thuemenidium is a polyphyletic genus
composed of at least two disparate species, T.
arenarium, which belongs in Geoglosso
Mycosphere Doi 10.5943/mycosphere/2/6/5/
Fig 2 – Maximum likelihood phylogeny of Geoglossomycetes based on a combined dataset (2091
bp) of ITS, LSU, and Mcm7 DNA sequences representing 22 taxa using PhyML ((-ln)L score =
13700). Thickened branches indicate significant Bayesian posterior probabilities (>95%); numbers
refer to PhyML bootstrap support values >70% based on 1000 replicates. Neurospora crassa and
the Leotiomycetes were used as outgroup taxa.
Fig 3 – Sarcoleotia globosa. Arrow indicates distinct separation of fertile head and stipe.
651
Mycosphere Doi 10.5943/mycosphere/2/6/5/
mycetes, and T. atropurpureum, shown by
this study and Ohenoja et al. (2010) to
belong in Leotiomycetes. Thuemenidium
atropurpureum produces ascomata ranging
from brown to purplish black, whereas T.
arenarium does not possess any purplish
coloration.
The Geoglossomycetes are an earlydiverging lineage appearing on a long
branch within the Ascomycota and further
molecular research is needed in the group to
construct a comprehensive phylogeny of the
class. Several genera have historically been
associated within this group which are now
considered incertae sedis (e.g. Hemiglossum
Pat., Leucoglossum Imai, and Maasoglossum Thind and Sharma), and representatives
from these genera need to be examined
using molecular phylogenies to fully
understand their place within the
Pezizomycotina. Moreover, several species
complexes are likely present within the
group and Australasian lineages appear to
have origins entirely separate from Northern
Hemisphere counterparts (Wang et al.
2011). Further molecular data are also
needed to provide accurate reference
sequences for environmental sampling as
ongoing efforts in this field may shed some
light on the enigmatic host associations
within Geoglossomycetes.
Acknowledgements
This project was funded in part by an
American Society of Plant Taxonomists
Graduate Student Research Grant to VPH.
The authors wish to thank Bohumil
Dolensky, Jan Gaisler, Andrew Methven,
and Kees Roobeek for kindly providing
specimens used in this study.
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