StudieS in Mycology 64: 155–173. 2009.
available online at www.studiesinmycology.org
doi:10.3114/sim.2009.64.09
molecular systematics of the marine Dothideomycetes
S. Suetrong1, 2, C.L. Schoch3, J.W. Spatafora4, J. Kohlmeyer5, B. Volkmann-Kohlmeyer5, J. Sakayaroj2, S. Phongpaichit1, K. Tanaka6, K.
Hirayama6 and E.B.G. Jones2*
Department of Microbiology, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand; 2Bioresources Technology Unit, National Center for Genetic
Engineering and Biotechnology (BIOTEC), 113 Thailand Science Park, Paholyothin Road, Khlong 1, Khlong Luang, Pathum Thani, 12120, Thailand; 3National Center for
Biothechnology Information, National Library of Medicine, National Institutes of Health, 45 Center Drive, MSC 6510, Bethesda, Maryland 20892-6510, U.S.A.; 4Department of
Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, 97331, U.S.A.; 5Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City,
North Carolina 28557, U.S.A.; 6Faculty of Agriculture & Life Sciences, Hirosaki University, Bunkyo-cho 3, Hirosaki, Aomori 036-8561, Japan
1
*Correspondence: E.B. Gareth Jones, remispora@gmail.com
abstract: Phylogenetic analyses of four nuclear genes, namely the large and small subunits of the nuclear ribosomal RNA, transcription elongation factor 1-alpha and
the second largest RNA polymerase II subunit, established that the ecological group of marine bitunicate ascomycetes has representatives in the orders Capnodiales,
Hysteriales, Jahnulales, Mytilinidiales, Patellariales and Pleosporales. Most of the fungi sequenced were intertidal mangrove taxa and belong to members of 12 families
in the Pleosporales: Aigialaceae, Didymellaceae, Leptosphaeriaceae, Lenthitheciaceae, Lophiostomataceae, Massarinaceae, Montagnulaceae, Morosphaeriaceae,
Phaeosphaeriaceae, Pleosporaceae, Testudinaceae and Trematosphaeriaceae. Two new families are described: Aigialaceae and Morosphaeriaceae, and three new genera
proposed: Halomassarina, Morosphaeria and Rimora. Few marine species are reported from the Dothideomycetidae (e.g. Mycosphaerellaceae, Capnodiales), a group poorly
studied at the molecular level. New marine lineages include the Testudinaceae and Manglicola guatemalensis in the Jahnulales. Signiicantly, most marine Dothideomycetes are
intertidal tropical species with only a few from temperate regions on salt marsh plants (Spartina species and Juncus roemerianus), and rarely totally submerged (e.g. Halotthia
posidoniae and Pontoporeia biturbinata on the seagrasses Posidonia oceanica and Cymodocea nodosum). Speciic attention is given to the adaptation of the Dothideomycetes
to the marine milieu, new lineages of marine fungi and their host speciicity.
Key words: Dothideomycetes, ecology, marine fungi, multi-locus, new genera, systematics.
Taxonomic novelties: Aigialaceae Suetrong, Sakayaroj, E.B.G. Jones, Kohlm., Volkm.-Kohlm. & Schoch, fam. nov., Halomassarina Suetrong, Sakayaroj, E.B.G. Jones,
Kohlm., Volkm.-Kohlm. & Schoch, gen. nov., Halomassarina thalassiae (Kohlm. & Volkm.-Kohlm.), Suetrong, Sakayaroj, E.B.G. Jones, Kohlm., Volkm.-Kohlm. & Schoch,
comb. nov., Suetrong, Sakayaroj, E.B.G. Jones, Kohlm., Volkm.-Kohlm.,comb. nov., Clade V. Morosphaeriaceae Suetrong, Sakayaroj, E.B.G. Jones, & Schoch, fam. nov.,
Morosphaeria velataspora (K.D. Hyde & Borse) Suetrong,. Sakayaroj, E.B.G. Jones & Schoch, comb. nov., Morosphaeria ramunculicola (K.D. Hyde) Suetrong,. Sakayaroj,
E.B.G. Jones & Schoch, comb. nov., Rimora Kohlm., Volkm-Kohlm., Suetrong, Sakayaroj, E.B.G. Jones, gen. nov., Rimora mangrovei (Kohlm. & Vittal) Kohlm.,Volkm-Kohlm.,
Suetrong, Sakayaroj, E.B.G. Jones, comb. nov.
InTroDuCTIon
Most marine Dothideomycetes are intertidal, primarily from
mangrove habitats and rely on the active discharge of their
ascospores. They are frequently found as saprobes of decaying
woody materials in the marine environment. The species that
occur completely submerged in the sea are mostly parasites
or symbionts of seagrasses or marine algae. It is not clear how
ascospore discharge occurs in these species as their hosts are
often submerged for most of the time. Jones et al. (2009) list 64
genera and ca. 108 species of marine Dothideomycetes that fall into
three accepted orders (Capnodiales, Dothideales, Pleosporales),
three orders incertae sedis (Hysteriales, Patellariales, Jahnulales)
and 23 genera not assigned with conidence to any order. Most
of these higher order taxa are represented by a single genus or
species while most are members of the Pleosporales with 25
genera and 61 species (+ 13 genera, 20 species, incertae sedis).
Taxa that can not be assigned with conidence to either an order
or family include Aigialus, Halotthia, Lautospora, Manglicola,
Mauritiana, Passeriniella, Pontoporeia, and Tirisporella. A notable
feature of the marine Dothideomycetes is how few anamorphs
are known. Examples include Amarenographium metableticum,
Scolecosporiella typhae, Stemphylium triglochinicola and
Phialophora cf. olivacea and molecular data indicates that the
teleomorphs of Amorosia littoralis, Dendryphiella salina and D.
arenaria may be in the Pleosporales (Mantle et al. 2006, Jones
et al. 2008). This paucity of marine anamorphic fungi is in marked
contrast to freshwater fungi and terrestrial genera of the class (Cai
et al. 2006, Shenoy et al. 2007, Shearer et al. 2009; this volume).
Marine Dothideomycetes occur on a wide range of substrata:
mangrove wood, twigs and leaves; sea and marsh grasses
(especially Spartina spp. and Juncus roemerianus) (Kohlmeyer et
al. 1995a–c, 1996, 1997a–b). Culms and leaves of sea and marsh
grasses are ideal substrata for saprobic fungi because they may
remain standing for several years during and after senescence
(Christian et al. 1990, Kohlmeyer & Volkmann-Kohlmeyer 2001).
Other species are found on brown and red seaweeds, e.g. Lautitia
danica and Pleospora gracilariae (Schatz 1984, Simmons & Schatz
1989), on wood associated with sand e.g. Caryospora australiensis
and Decaisnella formosa (Abdel-Wahab & Jones 2003) or on
the brackish water palm Nypa fruticans, e.g. Carinispora nypae,
Herpotrichia nypicola, Tirisporella beccariana and Helicascus
nypae (Jones et al. 1996, Hyde & Alias 2000). Few marine
Dothideomycetes produce elaborate appendaged ascospores, and
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155
Suetrong et al.
most possess gelatinous sheaths that swell in water when released
from the asci (Massarina velataspora and Tremateia halophila).
Genera with appendaged ascospores, although generally
modiications of a gelatinous sheath, include: Carinispora nypae,
Decorospora gaudefroyi and Falciformispora lignatilis.
The main objective of this study is to provide information on
the taxa that are unique to the marine milieu, e.g. Aigialus spp.,
Manglicola guatemalensis, Halotthia posidoniae and Pontoporeia
biturbinata and conirm the taxonomic assignment of other marine
ascomycetes within the context of a well sampled analysis with
other related fungi.
maTerIal anD meTHoDS
Collection of fungi
Drift and attached wood, culms and leaves of marsh plants,
seagrasses and seaweeds were collected from a variety of habitats
and geographical locations, placed in clean plastic bags and
returned to the laboratory. After washing with freshwater to remove
sediments, the samples were examined for fungi. Samples were
kept moist by spraying with sterilised distilled water. Sporulating
fungi were examined, identiied, illustrated and single-spore
isolations made. Most of the fungi sequenced in this study were
obligate species, but some facultative and halotolerant terrestrial
taxa from Juncus roemerianus have also been included so as to
increase the sampling diversity.
fungal isolates and culture characteristics
A selection of specimens were isolated by cutting the top of an
ascoma with a sterilised razor blade, removing the contents of the
centrum by making a spore suspension and then streaking the
spores on antibiotic seawater agar (Kohlmeyer & Kohlmeyer 1979,
Schoch et al. 2007) and germinating spores picked up. Other single
ascospore isolations were made on cornmeal seawater agar (CMA/
SW) with added antibiotics (streptomycin sulfate 0.5g/L, penicillin
G 0.5 g/L) and allowed to germinate overnight. Germinating spores
were transferred to a fresh agar plate and incubated for 2 wk at
25 ºC and deposited in relevant culture collections (Table 1 - see
online Supplementary Information).
Dna extraction, ampliication and sequencing
Fungal genomic DNA from a selection of cultures was isolated by
iltering mycelia grown in seawater broth at 22 ºC with subsequent
lyophilisation (Spatafora et al. 1998). DNA was then extracted
using the FastDNA kit and cells were ground on the Fast-Prep
instrument from MPI Biochemicals (Irvine, CA, U.S.A.) following
manufacturer recommendations. Fungal biomass was harvested
for a different set of isolates by iltering through cheesecloth, and
washed several times with sterile distilled water. The harvested
mycelium was stored at -20 °C and ground to a ine powder with
a mortar and pestle. Fifty to 100 mg ground fungal mycelium was
placed into 400 mL lysis buffer (O’Donnell et al. 1997) and DNA
extracted as follows: the tube was incubated at 70 °C for 30 min,
and an equal volume of phenol-chloroform (PIERCE) added. The
upper liquid phase was transferred to a new microtube containing
chilled absolute ethanol and 7.5 M ammonium acetate. The mixture
was kept at -20 °C for 30 min, or until the DNA had precipitated,
and then centrifuged at 14 000 rpm, 4 °C, for 15 min. The DNA
pellet was washed twice with chilled 75 % ethanol and air dried.
156
The DNA was resuspended in 50 mL TE buffer and checked for
quantity and quality by 1 % agarose gel electrophoresis.
The following four genes were chosen for this study: small (18S)
and large subunit (28S) of the nuclear ribosomal DNA (SSU, LSU)
plus the gene fragments from the second largest subunit of RNA
polymerase (RPB2) and the translation elongation factor 1-alpha
(TEF1) gene. The rDNA was ampliied with Taq DNA polymerase
from FERMENTAS (Cat.No. MBDOEPO402) using PCR Model
MJ Research DYAD ALD ALD 1244 thermocycler (MJ Research,
Waltham, MA). Primers used for ampliication include the SSU, LSU,
RPB2 and TEF1 (White et al. 1990, Bunyard et al. 1994, Liu et al.
1999, Rehner 2001, respectively). The PCR products were puriied
using a NucleoSpin Extraction Kit (Macherey-Nagel, Germany),
following the manufacturer’s instructions. The characterisation
of PCR products was performed via agarose gel electrophoresis
on 1 % agarose gel containing ethidium bromide as the staining
agent. PCR products were directly sequenced by Macrogen Inc.,
Korea. The sequencing primers used for as the different regions
are SSU: NS1, NS3, NS4, NS6 (White et al. 1990); LSU: JS1, JS8,
LROR and LR7 (Bunyard et al. 1994); TEF1: 983F, 2218R, CEFF2
and CEFR2 (Rehner 2001); RPB2: 5F1, 5F2, 7cR and 7R (Liu
et al. 1999). Each sequence was checked for ambiguous bases
and assembled using BioEdit v. 6.0.7 (Hall 2004) and SeqMerge,
forming part of the GCG v. 10 software suite (Accelrys, San Diego,
U.S.A.).
Sequence alignment and phylogenetic analyses
A total of 51 species (90 new sequences – Table 1) from the
Dothideomycetes, representing 46 teleomorphic genera and ive
anamorphic genera were analysed along with reference fungal
sequences from fungal families that were downloaded from the
GenBank (listed in Table 1).
The consensus sequences for each DNA region were initially
aligned with ClustalW v. 1.6 (Thompson et al. 1994) and improved
in MUSCLE (Edgar 2004) (as part of Geneious Pro v. 4.7.4
(Biomatters, Auckland, N.Z.). When necessary new sequences
were added to a core set of seed sequences using MAFFT v.
6.708b (Katoh & Toh 2008) using the e-insi option. Sequence
homologies were also analysed using BLAST (Altschul et al. 1990)
to facilitate the selection of other fungal sequences to be used in
the analyses. Alignments were checked and manually optimised
along with other sequences obtained from the GenBank nucleotide
database. The dataset was reined visually in BioEdit v. 7.0.1 (Hall
2004). Incomplete data at the 5΄- and 3΄-end of partial sequences
were coded as missing. Following Wiens (2006), we included taxa
in our multi-locus matrix even if they did not have all genes present.
All absent genes were coded as missing data, forming at least 30
% of the total characters. Two members of the Arthoniomycetes,
namely Roccella fuciformis and Opegrapha dolomitica, were
chosen as outgroup sequences based on their placement as sister
to the Dothideomycetes (Schoch et al. 2009).
Phylogenetic trees based on individual SSU, individual LSU,
combined SSU and LSU and combined SSU, LSU and TEF
datasets (data not shown) were congruent with the combined SSU,
LSU, RPB2 and TEF1 data sets. However the position of the taxa
Biatriospora marina and Quintaria lignatilis (in Clades XIV and XVI,
respectively) and Saccardoella rhizophorae (unresolved taxon)
were not constant. The phylogenetic analyses of the combined
SSU, LSU, RPB2 and TEF1 data were performed using parsimony,
Bayesian and maximum likelihood algorithms.
Molecular SySteMaticS of the Marine DothiDeomycetes
(i) Maximum parsimony (MP) analyses: MP analyses were
performed using PAUP v. 4.0b10 (Swofford 2003). Gaps were
treated as missing data with 100 replicates of random stepwise
addition of sequences and tree-bisection reconnection (TBR)
branch-swapping. All characters were given equal weight. The
consistency indices (CI; Kluge & Farris 1969), retention indices (RI;
Farris 1989) and rescaled consistency indices (RC; Farris 1989)
were calculated for each tree generated. Bootstrap support values
(Felsenstein 1985) were calculated for all parsimony analyses by
1000 bootstrap replicates (full heuristic searches, 10 replicates of
random stepwise addition of sequences). Maximum parsimony
bootstrap values (MPBP) equal or greater than 50 % are given
above each node (Fig. 1).
(ii) Bayesian analyses (Larget & Simon 1999): The model
of substitution used for Bayesian analyses was chosen with
MrModeltest v. 2.2 (Nylander 2004). Independent Bayesian
phylogenetic analyses were performed in MrBayes v. 3.1.2
(Huelsenbeck & Ronquist 2001) using a uniform [GTR+I+G] model,
lset nst = 6 rates = invgamma; prset statefreqpr = dirichlet (1,1,1,1).
The Metropolis-Coupled Markov Chain Monte Carlo (MCMC)
sampling approach was used to calculate posterior probabilities
(PP). Four Markov chains were run from a random starting tree for
5 000 000 generations and trees sampled every 100 generations.
The irst 5 000 trees were discarded as burn-in prior to convergence
of the four chains. The remaining trees were used to construct a 50
% majority rule consensus tree and to calculate Bayesian Posterior
Probabilities (BYPP) with those equal or greater than 0.95 given
below each node (Fig. 1).
(iii) Maximum likelihood analyses (ML) were conducted in
RAxML v. 7.2.2 (Stamatakis 2006). The dataset was partitioned
according to each gene and separate codons (eight partitions)
as previously done in Schoch et al. (2009). A general time
reversible model (GTR) with a discrete gamma distribution
and four rate classes was applied to each partition. A tree was
obtained by simultaneously running a fast bootstrap search of
1 000 pseudoreplicates followed by a search for the most likely tree
under functional setting "a". We also did 100 successive searches
in RAxML under the GTR model with gamma rate distribution and
starting each search from a randomised tree. Maximum Likelihood
bootstrap values (MLBP) equal or greater than 50 % are given
above each node (Fig. 1).
Phylogenetic trees were drawn using Treeview v. 1.6.6 (Page
2001) and TreeDyn 198.3 (Chevenet et al. 2006). Sequences
derived in this study are deposited in GenBank, and the alignments
in TreeBASE (www.treebase.org).
reSulTS
molecular phylogenies
The BLAST search based on SSU and LSU sequences revealed
the closest matches with taxa in Dothideomycetes and SSU, LSU,
TEF1, and RPB2 sequences generated as part of this study are
listed in Table 1. These sequences were combined with previously
published data from various orders of the Dothideomycetes
(Botryosphaeriales, Capnodiales, Dothideales, Hysteriales,
Pleosporales and Myriangiales) obtained from GenBank (Table
1). The data set consisted of 199 taxa, with Opegrapha dolomitica
and Roccella fuciformis included as the outgroup taxa. The
www.studiesinmycology.org
maximum parsimony dataset consists of 4 141 total characters,
1 890 (45.6 %) characters are constant, 532 (12.8 %) characters
are parsimony informative and 1 791 (41.6 %) characters are
parsimony uninformative. The heuristic search resulted in a single
most parsimonious tree (MPT) with a length of 18 715 steps (CI
= 0.208, RI = 0.623, RC = 0.130; data not shown). One hundred
successive searches using a rapid hill-climbing algorithm from
distinct randomised starting trees in RAxML yielded a best scoring
likely tree (Fig. 1) with a log likelihood –84765.605900. The matrix
had 2 985 alignment patterns with 32 % of the characters consisting
of gaps or undetermined characters. The alignment patterns were
distributed across seven partitions as follows: LSU – 859, SSU –
217, TEF1 codon1 – 195, TEF1 codon2 – 309, TEF1 codon3 – 309,
RPB2 codon1 – 230, RPB2 codon2 – 203, RPB2 codon1 – 254.
Phylogenetic trees obtained from maximum likelihood,
Bayesian and maximum parsimony analyses yielded trees with
similar overall topology at subclass, order and family relationship
in agreement with previous work based on maximum likelihood
(Schoch et al. 2006). However, the internal node relationships
of some taxa were resolved differently between the maximum
likelihood, Bayesian and maximum parsimony trees. For example:
the taxonomic position of Biatriospora marina differed between the
maximum likelihood, Bayesian and Maximum parsimony trees In
the maximum likelihood and Bayesian tree, B. marina grouped
in a basal part of Clade XIV- Residual paraphyletic assemblage.
But in the maximum parsimony tree, B. marina grouped in a basal
clade to the Testudinaceae. This is not unexpected as divergence
in evolutionary rates and the presence of missing data affects all
these methods differently. Nevertheless, we describe new taxa
based on agreement in support for all three computational methods.
Taxonomy
This study resulted in the sampling of 51 marine dothideomycetous
species (Table 1) with most of the marine genera beloning in the
Pleosporomycetidae, and only two taxa (Mycosphaerella, Scirrhia)
referred to the Dothideomycetidae. Only clades with marine taxa (in
blue bold in the tree) are discussed in the text.
Marine Dothideomycetes show great variation in the
morphology of the ascomata, asci and ascospores as illustrated in
Figs 2–3. Many genera possess ascospores with a mucilaginous
sheath that swells in water, once released from the asci. In others
the sheaths are drawn out to form appendages (e.g. Carinispora
nypae, Decorospora gaudefroyi, Falciformispora lignatilis).
Pleosporomycetidae
1. Pleosporales, fig. 1.
Delineation of families in the Pleosporales previously relied
extensively on morphological characters which resulted in 17 to
19 families (Kirk et al. 2001, Lumbsch & Huhndorf 2007). These
were poorly resolved at the molecular level and Schoch et al.
(2006) could only ind reasonable support for seven families in
a phylogeny generated from four genes: Leptosphaeriaceae,
Lophiostomataceae,
Phaeosphaeriaceae,
Pleosporaceae,
Sporormiaceae, Testudinaceae and Trematosphaeriaceae. A major
reassessment of these taxa is needed and attempts are underway
to complete this (see Mugambi et al. 2009a, and Zhang et al.
2009; this volume). As part of this process we attempted to place
a diverse selection of marine Dothideomycetes using phylogenetic
157
Suetrong et al.
84/98 Lentithecium (Massarina) arundinaceum CBS 619.86
/54
Lentithecium (Massarina) phragmiticola CBS 110446
78/75
Keissleriella rara CBS 118429
Keissleriella cladophila CBS 104.55
Wettsteinina lacustris CBS 618.86
99/88 Helminthosporium velutinum ATCC 38969
Helminthosporium solani HSWS 04
100/ 100
1.00
Massarina eburnea CBS 473.64
100 /100
1.00
Massarina eburnea HKUCC 4054
0.97
MLBS/MPBS
BYPP
63 /
0.96
/
Bimuria novae-zelandiae CBS 107.79
100 /94
100/94 1.00
Tremateia halophila JK 5517J
1.00
100 /96
Phaeodothis winteri CBS 182.58
1.00
Clade I- Lentitheciaceae
Clade II- Massarinaceae
Clade III-Montagnulaceae
Montagnula opulenta CBS 168.34
Byssothecium circinans CBS 675.92
/
Massarina igniaria CBS 845.96
83/56
66/ Halomassarina (Massarina) thalassiae BCC 17054
1.00
Halomassarina (Massarina) thalassiae JK 5262D
/
100 100
Halomassarina (Massarina) thalassiae BCC 17055
1.00
90/88
Halomassarina (Massarina) thalassiae JK 5385B
1.00
Trematosphaeria pertusa CBS 122371
100 /100
94/90
1.00
Trematosphaeria pertusa CBS 122368
1.00
Falciformispora lignatilis BCC 21118
76 /61
100 / 100
1.00
1.00
Falciformispora lignatilis BCC 21117
93/62
Massaria platani CBS 221.37
1.00
100 /87 Morosphaeria (Massarina) ramunculicola BCC 18404
1.00 Morosphaeria (Massarina) ramunculicola BCC 18405
100/100
Morosphaeria (Massarina) ramunculicola HKUCC 7649
1.00
Morosphaeria (Massarina) ramunculicola JK 5304B
96 /95
1.00
100 /100 Morosphaeria (Massarina) velataspora BCC 17059
1.00 Morosphaeria (Massarina) velataspora BCC 17058
100/100
Helicascus nypae BCC 36752
1.00
100 / 99 Helicascus nypae BCC 36751
85/51 1.00
Helicascus nypae PP 6066
76 /65
Helicascus kanaloanus A 237
0.99
Kirschsteiniothelia elaterascus HKUCC 7769
100 / 99
1.00 Alternaria maritima CBS 126.60
74 /60
Alternaria alternata CBS 916.96
89 /80
Lewia infectoria IMI 303186
1.00
Allewia eureka DAOM 195275
60 / 66/92
0.98 Dendryphiella salina CBS 142.60
Dendryphiella arenaria CBS 181.58
98 /99 100 / 98
96/89
1.00 1.00 Pleospora herbarum CBS 541.72
/
64
65
1.00
Pleospora sedicola CBS 109843
100/84
Pyrenophora tritici-repentis OSC 100066
1.00
Pyrenophora phaeocomes DAOM 222769
85/76
1.00
Decorospora gaudefroyi CBS 322.63
/
99/97 Phaeosphaeria avenaria DAOM 226215
55/ 1.00 Phaeosphaeria eustoma CBS 576.86
95/65
75 / Loratospora aestuarii JK 5535D
1.00
1.00
Phaeosphaeria olivacea JK 5540Q
90 /93
86/80
1.00 Phaeosphaeria spartinicola JK 5177A
1.00
Phaeosphaeria albopunctata CBS 254.64
67/53
0.98 Ophiosphaerella herpotricha ATCC 12279
57/
Leptosphaeria biglobosa CBS 303.51
Leptosphaeria doliolum CBS 505.75
87/
/99
100
Leptosphaeria maculans DAOM 229267
100
1.00 /
83/57
Phoma herbarum CBS 615.75
88/76
1.00 Platychora ulmi CBS 361.52
96/82
Ascochyta pisi CBS 126.54
1.00
95/93
Leptosphaerulina australis CBS 939.69
1.00
67/
99/97 Didymella cucurbitacearum IMI 373225
1.00
Didymella fucicola JK 2932
Julella avicenniae BCC 20173
Julella avicenniae CY 2462
88/ Pleosporaceae sp. OSC 100706
100 / 100
Julella avicenniae JK 5326A
1.00
Julella avicenniae BCC 18422
83/88 Melanomma pulvis-pyrius CBS 109.77
100 / 100
Herpotrichia juniperi CBS 200.31
1.00
Herpotrichia diffusa CBS 250.62
Lophiostoma macrostomum KT 709
52/61
Lophiostoma macrostomum KT 635
/59
Lophiostoma arundinis CBS 621.86
/
/61
Lophiostoma crenatum CBS 629.86
62 /55
Lophiostoma heterosporum CBS 644.86
53/69
Lophiostoma sagittiforme HHUF 29754
100 /100
1.00
Lophiostoma (Platystomum) scabridisporum BCC 22836
53/
Lophiostoma (Platystomum) scabridisporum BCC 22835
89/57
Paraliomyces lentiferus CY 3525
94/67
Lophiostoma bipolarae
/ 1.00
100 /100 Lophiostoma fuckelii CBS 113432
1.00
Lophiostoma fuckelii CBS 101952
/
Clade IV- Trematosphaeriaceae
Clade V- Morosphaeriaceae
Clade VI- Pleosporaceae
Clade VII-Phaeosphaeriaceae
Clade VIII- Leptosphaeriaceae
Clade IX-Didymellaceae
Clade X-Julella
Clade XI- Melanommataceae
Clade XII- Lophiostomataceae
Amorosia_littoralis_NN6654
fig. 1. RAxML tree of marine Dothideomycetes with bootstrap support values for maximum likelihood and maximum parsimony above the nodes. The values below the nodes
are Bayesian posterior probalities. Relevant clades are highlighted in colour.
158
Molecular SySteMaticS of the Marine DothiDeomycetes
93
52 /
1.00
66 /
Amorosia littoralis NN 6654
100/99
98/94 1.00 Westerdykella dispersa CBS 508.75
1.00
Westerdykella angulata CBS 610.74
75/56
1.00
Westerdykella cylindrica CBS 454.72
58/
0.96
Preussia terricola DAOM 230091
100 /100 Berkleasmium nigroapicale BCC 8220
1.00 Berkleasmium micronesiacium BCC 8141
/
100/100 Floricola striata JK 5603K
100/99 1.00
Floricola striata JK 5678I
1.00
62 /
/
Clade XIII- Sporormiaceae
Preussia minima CBS 524.50
/
100/100
1.00
Melanomma radicans ATCC 42522
Decaisnella formosa BCC 25617
Decaisnella formosa BCC 25616
Halotthia posidoniae BBH 22481
87/
XIV- Residual paraphyletic
assemblage
Pontoporeia biturbinata BBH 23338
92 /
100 /100 Mauritiana rhizophorae BCC 28867
1.00 Mauritiana rhizophorae BCC 28866
/
Biatriospora marina CY 1228
Verruculina enalia BCC 18401
100/100 Verruculina enalia JK 5253A
1.00
67/ 64 / 87 Verruculina enalia BCC 18402
1.00
Ulospora bilgramii CBS 101364
Clade XV- Testudinaceae
Neotestudina rosatii CBS 690.82
Massarina ricifera JK 5535F
61/
Quintaria lignatilis BCC 17444
98 / 83
Quintaria lignatilis CBS 117700
Carinispora nypae BCC 36316
100/100 Acrocordiopsis patilii BCC 28167
/
63/83 1.00
Acrocordiopsis patilii BCC 28166
0.99
Passeriniella savoryellopsis JK 5167C
/
Salsuginea ramicola KT 2597.1
100/100
/
1.00
Salsuginea ramicola KT 2597.2
88/
Repetophragma ontariense HKUCC 10830
/
Quintaria submersa CBS 115553
Aigialus grandis BCC 20000
Aigialus grandis JK 4770
98 /90 Aigialus grandis BCC 18419
1.00 Aigialus grandis CY 2909
59/
Aigialus grandis JK 5244A
100/100Aigialus mangrovei BCC 33564
69/56 1.00 Aigialus mangrovei BCC 33563
1.00
89 /
100/100 100/ 100
Aigialus rhizophorae BCC 33572
1.00 Aigialus rhizophorae BCC 33573
Aigialus parvus BCC 18403
68/ 100/96 Aigialus parvus BCC 32558
Aigialus parvus CY 5061
/
Ascocratera manglicola BCC 9270
100 /100
100/100 Ascocratera manglicola HHUF 30032
1.00
Ascocratera manglicola JK 5262C
97/ 99
Rimora (Lophiostoma) mangrovei JK 5437B
0.96 Rimora (Lophiostoma) mangrovei JK 5246A
86 /
Delitschia winteri CBS 225.62
Gloniopsis subrugosa CBS 123346
81/98
1.00
Gloniopsis praelonga CBS 112415
69/66
1.00
100 /100 Oedohysterium insidens CBS 238.34
/
1.00
Oedohysterium sinense CBS 123345
100/100 Hysterobrevium smilacis CBS 114601
/ 1.00 Hysterobrevium mori CBS 123564
Psiloglonium simulans CBS 206.34
100/100
51/
/
1.00
Psiloglonium araucanum CBS 112412
1.00
Psiloglonium clavisporum CBS 123339
76/60
99 /98 1.00
Ostreichnion curtisii CBS 19834
1.00
100/100 Hysterium angustatum CBS 236.34
92/75 1.00 Hysterium pulicare CBS 123377
0.96
58 /
Ostreichnion sassafras CBS 322.34
81/90
Lophium mytilinum CBS 269.34
1.00
Kirschsteiniothelia maritima CBS 221.60
100 / 100
1.00
93 / 71 Mytilinidion mytilinellum CBS 303.34
70 /
1.00
Mytilinidion andinense CBS 123562
Saccardoella rhizophorae JK 5349A
Pseudorobillarda texana BCC 12535
66 / 70
100 /100 0.95
Pseudorobillarda phragmitis CBS 842.84
1.00
Pseudorobillarda siamensis CBS 842.84
62 / 56/
Farlowiella carmichaeliana CBS 206.36
100 /100 Botryosphaeria stevensii CBS 431.82
59/ 1.00
Botryosphaeria tsugae CBS 418.64
Botryosphaeria ribis CBS 115475
100/100
1.00
Botryosphaeria dothidea CBS 115476
100/100 97/
54 /
Macrophomina phaseolina CBS 277.33
1.00
1.00
Guignardia bidwellii CBS 237.48
100/100
1.00
Guigardia gaultheriae CBS 444.70
100 /100 Patellaria cf. atrata BCC 28877
1.00
100 / 100
Patellaria cf. atrata BCC 28876
1.00
Patellaria atrata CBS 95897
85 /
Hysteropatella elliptica CBS 935.97
100 / 100
1.00
Hysteropatella clavispora CBS 247.34
50/
56/
P
l
e
o
s
p
o
r
a
l
e
s
P
l
e
o
s
p
o
r
o
m
y
c
e
t
i
d
a
e
XVI-Residual paraphyletic
assemblage
Clade XVII- Aigialaceae
Clade XVIII- Hysteriaceae
Clade XIX-
Mytilinidiales,
Mytiliniadiaceae
Clade XX- Unresolved taxa
Clade XXI- Botryosphaeriales,
Botryosphaeriaceae
Clade XXII-
Patellariales,
Patellariaceae
fig. 1. (Continued).
www.studiesinmycology.org
159
Suetrong et al.
D
o
t
h
i
d
e
o
m
y
c
e
t
i
d
a
e
/
60 /
65 / 50
99 / 82
1.00
Dothidea hippophaës DAOM 231303
50 /
Stylodothis puccinioides CBS 193.58
0.98
100 /100 Dothidea insculpta CBS 189.58
89/75 1.00
Dothidea sambuci DAOM 231303
1.00
100/100
Dothiora cannabinae CBS 737.71
1.00
Sydowia
polyspora CBS 116.29
100/100
100 /100
1.00 Delphinella strobiligena CBS 735.71
1.00
100/100 Columnosphaeria fagi CBS 171.93
1.00
Aureobasidium pullans CBS 584.75
53 /
Clade XXIIIDothideales,
Dothideaceae
Elsinoë centrolobii CBS 222.50
99/92
97/77 1.00
Elsinoë phaseoli CBS 165.31
0.98
Elsinoë
veneta CBS 150.27
100/100
1.00
Myriangium hispanicum CBS 247.33
100/ 100
1.00
Myriangium duriaei CBS 260.36
Clade XXIVMyriangiales,
Myriangiaceae
C
a
p 83/72
Mycosphaerella graminicola CBS 292.38
84/89
85/86 1.00
Mycosphaerella punctiformis CBS 113265
Clade XXVn 1.00
61/ 1.00
Mycosphaerella fijiensis OSC 100622
o
Mycosphaerellaceae
70/
Scirrhia annulata JK 5546G
d
1.00
Mycosphaerella eurypotami JK 5586J
80/
i
/
Capnodium coffeae CBS 147.52
1.00
a 98/ 83 60 /
Capnodium salicinum CBS 131.34
Clade XXVI- Capnodiaceae
0.99
l
1.00
Scorias spongiosa CBS 325.33
e
Davidiella tassiana CBS 399.80
100 / 100
Clade XXVII- Davidiellaceae
1.00
Cladosporium cladosporioides CBS 170.54
s
94/67
100 / 100
1.00
Heleiosa barbatula JK 5548I
Lineolata rhizophorae CBS 641.66
Lineolata rhizophorae JK 5248A
Lineolata rhizophorae CBS 118422
Caryosporella rhizophorae JK 5386C
Clade XVIIIUnresolved taxa
fig. 1. (Continued).
reconstruction. This resulted in 11 supported clades corresponding
to families, with marine representatives (Fig. 1) (DidymellaceaeClade IX, Lentitheciaceae-Clade I, Leptosphaeriaceae-Clade
VIII, Lophiostomataceae-Clade XII, Massarinaceae-Clade
II, Montagnulaceae-Clade III, Phaeosphaeriaceae-Clade
VII, Pleosporaceae-Clade VI, Sporormiaceae-Clade XIII,
Testudinaceae-Clade XV, Trematosphaeriaceae-Clade IV) and two
new families: 1) Aigialaceae (Clade XVII) for Aigialus and related
taxa (Ascocratera manglicola and Lophiostoma mangrovei), and
2) Morosphaeriaceae (Clade V) for the species Morosphaeria
(Massarina ramunculicola, Massarina velataspora), Helicascus
nypae, H. kanaloanus and Kirschsteiniothelia elaterascus. Further
clades are also identiied, but their position remains unresolved,
e.g. the familial position of the taxa Halotthia posidoniae, Mauritiana
rhizophorae and Pontoporeia biturbinata in clade XIV.
Clade I. Lentitheciaceae
The marine Massarina species are not monophyletic which is
in agreement with observations on terrestrial and freshwater
members of the genus (Zhang et al. 2009b). Consequently a
number of taxonomic changes are proposed in this chapter. Zhang
et al. (2009a; this volume) erected the family Lentitheciaceae,
and the genus Lentithecium for Massarina that do not group in
the Massarinaceae. However the monophyly of Lentithecium is
not supported in the current study. Massarina phragmiticola was
described from the saltmarsh grass Phragmites australis (Poon
et al. 1998), and groups within this family. It grouped with M.
arundinacea with 84 % MLBP and 98 % MPBP support (Fig. 1).
However Zhang et al. (2009a; this volume) refers M. arundinacea
to the new genus Lentithecium and we place M. phragmiticola in
synonymy with Lentithecium arundinaceum.
Keissleriella (type species K. aesculi) comprises some 25 species
(Kirk et al. 2008) and two species group with Lentithecium in clade
I, with high support. Keissleriella rara was described from the salt
marsh species Juncus roemerianus, a rare halotolerant species
(Kohlmeyer et al. 1995c). Zhang et al. (2009a) also included
Keissleriella linearis in their phylogenetic analysis and transferred
it to Lentithecium.
160
Clade II. Massarinaceae
Aptroot (1998) reviewed the genus Massarina and reduced the 160
names in the literature to 43 taxa, while others (especially those
from aquatic habitats) have been transferred to Lophiostoma (Hyde
& Aptroot 1998, Hyde et al. 2002b, Liew et al. 2002). However,
subsequent studies indicate that Massarina and Lophiostoma
species are polyphyletic (Zhang et al. 2009a; this volume). These
genera and the families Lophiostomataceae / Massarinaceae are
dificult to separate and often have overlapping characters (Zhang
et al. 2009b). In our analysis the type species Massarina eburnea
forms a well supported clade (Clade II) with two Helminthosporium
species (H. velutinum, H. solani) as a sister group.
Jones et al. (2009) referred the genus Massarina to the
Lophiostomataceae based on the molecular evaluation of Hyde et
al. (2002b) and Liew et al. (2002). Lophiostoma has been reported
as a monophyletic genus (Tanaka & Harada 2003, Tanaka & Hosoya
2008) while Zhang et al. (2009b) have shown that Lophiostoma
is phylogenetically divided into two groups: Lophiostoma I which
includes the type species L. macrostomum (voucher Lundqvist
20504), and Lophiostoma II which also contains sequences of L.
macrostomum (voucher HHUF 27293 and HHUF 27290). Zhang et
al. (2009b) were unable to verify the identity of the different strains
of L. macrostomum and consequently could not determine the
taxonomic position of Lophiostoma s. str. The paraphyletic nature
of the Lophiostomataceae has previously been noted (Schoch et
al. 2006) and clade XII is likely to represent the narrow concept
of the Lophiostomataceae, although it is still too early to draw this
conclusion until type material of Lophiostoma (L. macrostomum)
is obtained (Zhang et al. 2009b). In our analysis we have selected
the accession numbers AB433273 and AB433274 from the voucher
specimens HHUF 27290 and HHUF 27293, respectively, and regard
this clade as representing the family Lophiostomataceae (Clade XII).
Clade III. Montagnulaceae
Based on morphological data, Jones et al. (2009) referred the
genus Tremateia to the Pleosporaceae, but molecular data places
it with high support in the Montagnulaceae (100 % MLBP, 94 %
MPBP, 1.00 BYPP) with Bimuria novae-zelandiae as a sister
Molecular SySteMaticS of the Marine DothiDeomycetes
taxon. Kohlmeyer et al. (1995a) described Tremateia halophila
from senescent leaves of Juncus roemerianus and regarded it as
a facultative marine ascomycete. Characteristic features include
an apical cap on the ascus, I- ocular chamber, and muriform
ascospores with a wide mucilaginous sheath, and a Phoma-like
anamorph.
Clade IV. Trematosphaeriaceae
This clade comprises four strains of Massarina thalassiae, a common
species on mangrove wood, from Aldabra, Australia, Belize, Brunei,
Florida, Galapagos, India, Malaysia, Mexico, Thailand (Kohlmeyer
& Volkmann-Kohlmeyer 1987, Hyde 1992d, 1993, Alias & Jones
2000, Jones et al. 2006), with Trematosphaeria pertusa as a sister
taxon. Falciformispora lignatilis (Fig. 2T, W) also groups in this clade
with high support (94 % MLBP, 90 % MPBP, 1.00 BYPP); a species
found on mangrove wood as well as on the fronds of the terrestrial
oil palm (U. Pinruan, pers. comm.). As Massarina thalassiae cannot
be accommodated in the genus Massarina based on molecular
evidence, a new genus Halomassarina, is described.
Halomassarina Suetrong, Sakayaroj, E.B.G. Jones,
Kohlm., Volkm.-Kohlm. & C.L. Schoch, gen. nov. MycoBank
MB515951. Fig. 2AF.
Etymology: From the Greek hals = salt, in reference to the marine
origin of the fungus.
Ascomata subglobosa ad pyriformia, immersa vel erumpentia, ostiolata, periphysata,
papillata vel epapillata, clypeata, coriacea, brunnea, singularia. Peridium cellulis
applanatis pachydermisque, texturam angularem formans. Hamathecium
pseudoparaphysibus simplicibus, rariter anastomosantibus. Asci octospori, cylindrici
ad clavati, pedunculati, pachydermi, issitunicati, camera oculare, sine apparatu
apicali, I non reagentes. Ascosporae distichae, ellipsoideae, triseptatae, hyalinae,
tunica gelatinosa tectae.
Ascomata subglobose to pyriform, immersed or erumpent,
ostiolate, periphysate, papillate or apapillate, clypeate, coriaceous,
brown, single. Peridium of lattened, thick-walled cells, forming a
textura angularis. Hamathecium of simple, rarely anastomosing
pseudoparaphyses. Asci 8-spored, cylindrical to clavate,
pedunculate, thick-walled, issitunicate, with ocular chamber but
without apical apparatus, I-negative. Ascospores distichous,
ellipsoidal, 3-septate, hyaline, surrounded by a gelatinous sheath.
Type species: Halomassarina thalassiae Kohlm. & Volkm.-Kohlm.),
Suetrong, Sakayaroj, E.B.G. Jones, Kohlm., Volkm.-Kohlm. & C.L.
Schoch.
Halomassarina thalassiae (Kohlm. & Volkm.-Kohlm.)
Suetrong, Sakayaroj, E.B.G. Jones, Kohlm., Volkm.-Kohlm.
& C.L. Schoch, comb. nov. MycoBank MB515952.
Basionym: Massarina thalassiae Kohlm. & Volkm.-Kohlm. Canad.
J. Bot. 65: 575. 1987.
This is a widely collected tropical species from intertidal and
subtidal mangrove wood or ishing crafts (Kohlmeyer & VolkmannKohlmeyer 1987).
Clade V. Morosphaeriaceae
This clade, comprising four marine species Massarina
ramunculicola, M. velataspora, Helicascus kanaloanus and
H. nypae, is well supported (100 % MLBP, 100 % MPBP,
www.studiesinmycology.org
1.00 BYPP) with the Massarinaceae, Montagnulaceae and
Trematosphaeriaceae as sister clades. As M. ramunculicola and
M. velataspora do not group with other Massarina species, a new
family and genus Morosphaeria are proposed.
Morosphaeriaceae Suetrong, Sakayaroj, E.B.G. Jones &
C.L. Schoch, fam. nov. MycoBank MB515953.
Familia Pleosporalium, Ascomycetium. Ascomata subglobosa, conica, lenticulara,
immersa ad supericialia, ostiolata, papillata, periphysata, brunnea vel nigra,
coriacea vel carbonacea, solitaria, vel gregaria, cum 3–4 loculis, ostiolo communi
ad centrum. Hamathecium pseudoparaphysibus ilamentosis, numerosis, ramosis
ad basem, ramosis anastomosantibusque supra ascos. Asci octospori, clavati vel
cylindrici pedunculati, pachydermi, issitunicati, persistentes, camera apicale et
disco apicale, IKI non-reagentes. Ascosporae biseriatae, hyalinae ad brunneae,
septatae constrictae ad leviter constrictae, tunica vel calyptra gelatinosa tectae, vel
sine tunica.
Family in the Pleosporales, Ascomycota. Ascomata subglobose,
conical, lenticular, immersed to supericial, ostiolate, papillate,
periphysate, brown to black, coriaceaous or carbonaceous, single
to gregarious, stromatic with 3–4 loculi with a common central
ostiole. Hamathecium with ilamentous pseudoparaphyses,
unbranched to branched at the base, anastomosing above the
asci, embedded in a gelatinous matrix. Asci 8-spored, clavate to
cylindrical, pedunculate, thick-walled, issitunicate, with an ocular
chamber and apical ring, non-amyloid, persistent. Ascospores
biseriate, hyaline to brown, septate, with or without a gelatinous
sheath or cap.
Type genus: Morosphaeria Suetrong, Sakayaroj, E.B.G. Jones &
C.L. Schoch.
Morosphaeria Suetrong, Sakayaroj, E.B.G. Jones & C.L.
Schoch, gen. nov. MycoBank MB515954.
Etymology: Named after Mor = sea in Welsh in reference to its
marine habitat and sphaeria in reference to the perithecial ascomata
Ascomata solitaria vel gregaria, subglobosa vel lenticularia, immersa, erumpentia,
ostiolata, papillata, coriacea, brunnea ad nigra, pseudoparaphysibus angusti,
hyalinis, simplicibus et numerosis. Asci octospori, clavati vel cylindrici, pedunculati,
bitunicati, pachydermi, issitunicati, cum camera apicale et aparatu apicale, IKI non
reagentes. Ascosporae uniseriatae vel biseriatae, fusiformes vel ellipsoidales, 1–3
septatae, constrictae ad septae, cum tunica gelatinosae.
Ascomata solitary or gregarious, subglobose to lenticular,
immersed becoming supericial, ostiolate, papillate, coriaceous,
brown to black, pseudoparaphyses ilamenatous, anastomosing,
branching, and numerous. Asci 8-spored, clavate to cylindrical,
short pedunculate, thick-walled, bitunicate, issitunicate, with an
ocular chamber and apical apparatus, persistent. Ascospores
hyaline, 1–3 septate, constricted at the septa, fusiform to ellipsoidal,
surrounded by a mucilaginous sheath.
Type species: Morosphaeria velataspora (K.D. Hyde & Borse)
Suetrong, Sakayaroj, E.B.G. Jones & C.L. Schoch.
Morosphaeria velataspora (K.D. Hyde & Borse) Suetrong,
Sakayaroj, E.B.G. Jones & C.L. Schoch, comb. nov.
MycoBank MB515955. Fig. 2 AG.
Basionym: Massarina velataspora K.D. Hyde & Borse, Mycotaxon
27: 163. 1986.
161
Suetrong et al.
Morosphaeria ramunculicola (K.D. Hyde) Suetrong,
Sakayaroj, E.B.G. Jones & C.L. Schoch, comb. nov.
MycoBank MB515956. Fig. 3A, H.
Basionym: Massarina ramunculicola K.D. Hyde, Mycologia 83:
839. 1992.
Both species are common and frequently collected on dead wood
of various mangrove trees in tropical and subtropical localities
(Hyde & Borse 1986b, Hyde 1992a, Schmit & Shearer 2003, Jones
162
& Abdel-Wahab 2005, Jones et al. 2006). Ascospores of both
species possess a well-developed sheath (Au et al. 2001, Au &
Vrijmoed 2002), while in M. ramunculicola polar appendages are
formed as outgrowth of the ibrillar material within the inner regions
of the sheath through polar discontinuities (Read et al. 1997a, b).
The taxa Helicascus kanaloanus and H. nypae form a sister
group to Morosphaeria species with high bootstrap support. Jones
et al. (2009) referred this genus to the Pleosporaceae as in previous
analyses (Tam et al. 2003) and grouped it with Kirschsteiniothelia
Molecular SySteMaticS of the Marine DothiDeomycetes
fig. 2. (p. 162) Morphological features of marine Dothideomycetes. A. Immersed lenticular ascomata beneath clypeus of Carinispora nypae. B. Apothecium of Patellaria cf. atrata
(Patellariales). C. Broadly conical ascomata of Halotthia posidoniae. D. Immersed ascomata of Helicascus nypae. E. Globose ascoma of Pontoporeia biturbinata. F. Immersed
ascomata of Quintaria lignatilis. Released asci (arrow) from ostiole. G. Mature ascomata of Manglicola guatemalensis (Jahnulales). H. Tangential section of Helicascus nypae
through stroma with several loculi. I. Longitudinal section (l.s.) of Manglicola guatemalensis ascoma with asci and pseudoparaphyses. J. Pontoporeia biturbinata, non-ostiolate
ascoma, asci originating at the periphery of a hemispherical basal pulvinus. K. Longitudinal section through ascoma of Verruculina enalia. Asci. L–U. Ascus tip of Manglicola
guatemalensis. Ascospores show the apical appendage (arrow) in ascus. M. Ascus tip of Salsuginea ramicola, consisting of a large distinctive ocular chamber and prominent
ring (arrows). N. Clavate ascus of Quintaria lignatilis with apical plate. O. Clavate ascus of Quintaria lignatilis, with biseriate ascospores, in Nomarski and Quartz. P. Ovoidal
or ellipsoidal ascospores in cylindrical asci of Acrocordiopsis patilii. Q. Clavate to long-cylindrical ascus of Carinispora nypae. R. Clavate ascus of Patellaria cf. atrata. S.
Subcylindrical asci with pseudoparaphyses of Helicascus nypae. T. Clavate asci of Falciformispora lignatilis (Trematosphaeriaceae). U. Broadly clavate ascus of Pontoporeia
biturbinata. V–AH. Ascospores of marine Dothideomycetes: V. Carinispora nypae. Cylindrical and multiseptate ascospore with keel-like mucilaginous sheath (arrows). W.
Falciformispora lignatilis. Fusiform ascospores surrounded by thin mucilaginous sheath and single scythe-like appendage (arrow) at the base. X. Salsuginea ramicola. Ovoid,
dark brown ascospore with hyaline apical germ pores. Y. Manglicola guatemalensis. Fusiform ascospore with lager, pale brown apical cell and hyaline turbinate basal cell. Z.
Halotthia posidoniae. Ellipsoidal, dark brown ascospores, darker around septum. AA. Verruculina enalia. Ellipsoidal, dark brown ascospore, 1-septate. AB. Helicascus nypae.
Obovoidal ascospore with persistent mucilaginous sheath. AC. Mauritiania rhizophorae. Fusiform ascospore, 9–13-distoseptate. AD. Patellaria cf. atrata. Clavate ascospore,
5–7-septate. AE. Julella avicenniae. Muriform ascospores with dilated sheath (arrows), straining in ink. AF. Halomassarina (Massarina) thalassiae. Ellipsoidal ascospores with
gelatinous sheath (arrows). AG. Morosphaeria (Massarina) velataspora. Fusiform to ellipsoidal ascospores, 3-septate with mucilaginous sheath (arrows). AH. Morosphaeria
(Massarina) ramunculicola. Fusiform ascospores with fully dilated mucilaginous sheath (arrows). Habitat: A, D, G, H, I, L, Q, S, V, Y, AB. On the surface of Nypa fruticans. B, F,
K, M–P, R, X, AA, AC–AD, AF–AH. On mangrove wood. C, E, J, U, Z. On rhizomes of Posidonia oceanica. T, W. On oil palm (Elaeis guineensis). AE. On Avicennia spp. Scale
bars: A–C, E–H = 500 mm; D = 1000 mm; I = 250 mm; K = 200 mm; J = 150 mm; L–Z, AB, AF–AH = 20 mm; AA, AC–AE = 10 mm.
elaterascus (Shearer 1993a). However, Kirschsteiniothelia is
polyphyletic with the marine species K. maritima grouping in our
analysis in the Mytilinidaceae (Clade XIX, Fig. 1). In addition to
this the type species of the genus, K. aethiops and its anamorph,
Dendryphiopsis atra, are placed outside of the Pleosporales as
currently deined, always in close association with an isolate of
Phaeotrichum benjaminii, originally isolated from dung (Lumbsch
& Lindemuth 2001, Kruys et al. 2006, Schoch et al. 2009b). This
continues to demonstrate the polyphyletic nature of this genus in
agreement with clear morphological differences alluded to earlier
(Shearer 1993a). There is great morphological variation in the
three genera assigned to this family, especially the ascospores,
hyaline in Morosphaeria, brown to dark-brown in K. elaterascus
and Helicascus species, respectively.
Clade VI. Pleosporaceae
Jones et al. (2009) referred ive genera with marine representatives
in this family: Decorospora, Helicascus, Falciformispora, Pleospora
and Tremateia. The current study conirms the placement of D.
gaudefroyi in this family (Inderbitzin et al. 2002), along with the
two anamorphic species, Dendryphiella arenaria and D. salina,
that form a sister group to Pleospora herbarum and Pleospora
sedicola (Jones et al. 2008). Alternaria maritima groups as a
sister taxon with Alternaria alternata and Lewia species with
moderate support (74 % MLBP, 60 % MPBP). The current study
refers Tremateia to the Montagnulaceae (Clade II) and Helicascus
to the new family Morosphaeriaceae (Clade V), respectively,
while Falciformispora groups in a sister group to Halomassarina
thalassiae and Trematosphaeria pertusa (Clade IV, Fig. 1). (Zhang
et al. 2009a; this volume). The identity of the Alternaria maritima
strain is questioned as this taxon was regarded as nomen dubium
by Kohlmeyer & Kohlmeyer (1979) since there is no type material
to verify the original description by Sutherland (1916).
Clade VII. Phaeosphaeriaceae
The families Leptosphaeriaceae and Phaeosphaeriaceae are
closely related as recent sequence data have shown (Khashnobish
& Shearer 1996, Cámara et al. 2002, Kodsueb et al. 2006, Schoch
et al. 2006). The consensus was that they should both be retained
(Câmara et al. 2002, Cannon & Kirk 2007).
Loratospora aestuarii, Phaeosphaeria albopunctata, Ph.
olivacea, and Ph. spartinicola are the only marine species
represented in the Phaeosphaeriaceae in this data set. Based on ITS2
www.studiesinmycology.org
and partial 28S nrDNA sequences Khashnobish & Shearer (1996)
conirmed the inclusion of Ph. albopunctata and Ph. typharum in the
Phaeosphaeriaceae, and suggested that Leptosphaeria orae-maris
had a closer relationship with Phaeosphaeria than Leptosphaeria.
Jones et al. (2009) tentatively referred the genera Carinispora,
Lautitia and Phaeosphaeria to this family, with Loratospora
aestuarii in the Planistromellaceae (Dothideomycetidae, family
incertae sedis), based on morphological observations. Barr (1996)
erected the Planistromellaceae for six genera in the Dothideales
based on brown-celled pseudoparenchymatous ascostroma with
one or more locules which open schizogeneously and contain
asci, which are separated and overtopped by interthecial tissues
at maturity. However molecular data suggests that species in some
currently accepted genera sensu Lumbsch & Huhndorf (2007) e.g.
Comminutispora, are unrelated (Schoch et al. 2009a; this volume).
Zhang et al. (2009a; this volume) include the following marine
species in the Phaeosphaeriaceae: Leptosphaeria albopunctata,
Ph. spartinae, Ph. spartinicola, Ph. typharum as well as
Amarenomyces ammophilae. Eriksson (1981) established the new
genus Amarenomyces for Ph. ammophilae, but molecular data
places it in Phaeosphaeria and thus the earlier name as proposed
by Kohlmeyer & Kohlmeyer (1965) and Leuchtmann (1984) should
be retained. Phaeosphaeria olivacea is a facultative marine species
collected on Juncus roemerianus throughout the year (Kohlmeyer
et al. 1997a). Of the marine taxa included in this family all occur
on salt marsh plants: L. aestuarii, Ph. olivacea on J. roemerianus,
Ph. spartinae, and Ph. spartinicola on Spartina spp., while Ph.
ammophilae occurs on a range of grasses and sedges, but primarily
on Ammophila arenaria (Kohlmeyer & Kohlmeyer 1979).
Clade VIII. Leptosphaeriaceae
Currently ive Leptosphaeria species are referred to this family
(Jones et al. 2009), but no sequences of marine Leptosphaeria are
available for any of these, and therefore their taxonomic position
cannot be veriied.
Clade IX. Didymellaceae
The family Didymellaceae was recently described for the
teleomorphic genera Didymella, Leptosphaerulina, including
several Phoma anamorphs (de Gruyter et al. 2009). Four marine
Didymella species have been described, three from brown or red
seaweeds and D. avicenniae from wood of Avicennia (Patil & Borse
1985, Jones et al. 2009). In our analyses it forms a well-supported
163
Suetrong et al.
fig. 3. Morphological features of marine Dothideomycetes in the Aigialaceae and Coronopapilla mangrovei. A. Aigialus grandis. Immersed ascomata with ascospores (arrow)
released from ostiole. B–E. Longitudinal section (l.s.) through ascomata of Aigialus grandis (A), A. parvus (B), A. mangrovis (C) and A. rhizophorae (D). F. A. parvus. Surface
wood showing ascoma with thick peridium. G. A. parvus. Sagittal section through ascoma. H. Ascocratera manglicola. Crater-like ascomata with released ascus (arrow) from
the ostiole. I. Ascocratera manglicola. l.s. of ascoma illed with gelatinous matrix. J. Coronopapilla mangrovei. Surface view of ascomata. K. Rimora (Lophiostoma) mangrovei.
Broadly oblong ascomata. L. Aigialus grandis. Asci with apical refractive ring (arrows) and ascospores. M. Coronopapilla mangrovei. Ascus tip, thick-walled with ocular chamber.
N–T. Ascospores of marine Dothideomycetes in Aigialaceae: N. Aigialus grandis. Broadly fusiform (front view), muriform ascospores with drop of mucilage from end cells.
O. Aigialus parvus. Ellipsoidal to broadly fusiform (front view), muriform ascospores with a gelatinous cap around apical and subapical cells (arrows). P. Aigialus mangrovis.
Ellipsoidal to fusiform (front view), muriform ascospores. Q. Aigialus rhizophorae. Broadly fusiform (front view), muriform ascospores. R. Ascocratera manglicola. Ellipsoidal
ascospores, initially 1-septate, later becoming 3-septate with gelatinous sheath (arrow). S. Rimora (Lophiostoma) mangrovei. Fusiform ascospore with gelatinous sheath
(arrow). T. Coronopapilla mangrovei. Ellipsoidal ascospore. Habitat A–T. On mangrove wood. Scale bars: A, D–G, J–K = 500 mm; B–C, H = 250 mm; L, N–S = 25 mm; M, T =
10 mm.
basal clade (99 % MLBP, 97 % MPBP, 1.00 BYPP) to the families
Phaeosphaeriaceae, Pleosporaceae, and Leptosphaeriaceae.
Kohlmeyer & Volkmann-Kohlmeyer (2003) questioned the
taxonomic position of Didymella magnei, a species found on the
red seaweed Palmaria palmata, because the ascospores differed
morphologically from those of other Didymella species.
164
Clade X. Julella clade
The genus Julella was previously assigned to the Pleosporales
incertae sedis and Phaeosphaeriaceae, respectively (Jones et
al. 2009). Julella avicenniae (Fig. 2 AE) was initially described
as a Pleospora species but because the ascomata develop
on woody substrata, immersed beneath a clypeus with narrow
pseudoparaphyses, Hyde (1992b) transferred it to Julella.
Molecular SySteMaticS of the Marine DothiDeomycetes
However, ascomata can be supericial on well-decayed mangrove
wood. Although regarded as an obligate marine ascomycete (Hyde
1992b), it may be implicated in the dieback of young shoots of
Avicennia marina, at Morib mangrove, Malaysia, not submerged
in seawater (Jones 2007). Julella avicenniae strains form a
monophyletic clade with an unidentiied pleosporaceous sequence
(OSC 100706). This forms a moderately supported clade separated
from other families in the Pleosporales (67 % MLBP).
Clade XII. Lophiostomataceae
In our analyses the families Lophiostomataceae and Massarinaceae
are distinct, and distantly placed within the Pleosporales. This is
conirmed elsewhere (Zhang et al. 2009a; this volume). Jones
et al. (2009) referred seven genera with marine species to this
family (Decaisnella-Clade XIV, Unresolved, Herpotrichia-Clade
XI, Melanommataceae, Lophiostoma, Massarina-Clade II,
Massarinaceae, Paraliomyces, Platystomum, Quintaria-Clade XVI
Residual assemblage). However, molecular data places some of
these in other families, as indicated in the above sentence (Fig. 1).
Of these genera, only Platystomum and Paraliomyces (Tam et al.
2003) were included in the present analysis. Currently four marine
Lophiostoma species are recognised: L. acrostichi, L. armatisporum,
L. rhizophorae and Platystomum scabridisporum; however,
Suetrong et al. (pers. obs.) propose the transfer of the latter species
to Lophiostoma based on morphological and molecular data. Other
Lophiostoma species have been transferred to Astrosphaeriella
(A. asiana, A. mangrovis) by Hyde et al. (2002b) and Liew et al.
(2002). In our analysis, based on molecular data, Lophiostoma
mangrovei is referred to the family Aigialaceae (Clade XVII, Fig. 1),
while other Massarina species are placed in the Lentitheciaceae
(Clade I) [Lentithecium (Massarina) phragmiticola], or the new
family Morosphaeriaceae (clade V) [Morosphaeria (Massarina)
ramunculicola, M. (Massarina) velataspora]. No molecular data is
available for the marine species Herpotrichia nypicola which occurs
on the palm Nypa fruticosa, while Quintaria lignatilis forms a sister
group to the Testudinaceae with low support (Schoch et al. 2006).
Clade XIV. Residual paraphyletic assemblage
Several unresolved species form part of a poorly resolved group
that includes some members of the Lophiostomataceae and it is
not clear whether missing data inluenced this result. One of these
is the marine anamorphic species Amorosia littoralis (isolated from
the littoral zone in the Bahamas) and referred to the Sporormiacaeae
based on molecular data (Mantle et al. 2006). Another anamorphic
species, Floricola striata, is a facultative marine coelomycete from
Juncus roemerianus, which grouped with Melanomma radicans
with high support (100 % MLBP, 99 % MPBP, 1.00 BYPP). The
teleomorph genera forming part of this poorly resolved group
include: Decaisnella (Lophiostomataceae), Halotthia (Fig. 2C)
(Pleosporales incertae sedis), Mauritiana (Requienellaceae) (Fig.
2AC) and Pontoporeia (Fig. 2E, J, Z) (Zopiaceae) with weak
support and previously assigned to the families listed in brackets
(Jones et al. 2009). Morphologically they differ radically with
perithecioid or cleistothecial ascomata, clavate to cylindrical asci
and ascospores that are 3-septate and thick-walled in Halotthia
posidoniae and Pontoporeia biturbinata, muriform in Decaisnella
formosa and with 9–13 distosepta in Mauritiana rhizophorae.
They also occur on different substrata: Decaisnella formosa on
wood associated with sand, Mauritiana rhizophorae on mangrove
wood, and Halotthia and Pontoporeia on submerged rhizomes of
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the seagrasses Posidonia oceanica and Cymodocea nodosa. The
latter are temperate hosts, while D. formosa and M. rhizophorae
are from the tropics.
Clade XV. Testudinaceae
Verruculina and Massarina ricifera (Fig. 2K, AA) are the only marine
genera referred to this family, poorly supported in the current
analysis, but conirming the results of a previous study (Schoch et
al. 2006). In their analysis the family formed the basal node to the
Pleosporales. Members of the Testudinaceae form a monophyletic
clade and are characterised by ascospores that are 1-septate,
brown without germ slits and with or without ornamentation (Kruys
et al. 2006). However, Verruculina enalia shares few characters
with members of the Testudinaceae, it differs especially by its
marine habitat and persistent asci. Massarina ricifera is an obligate
marine ascomycete growing on Juncus roemerianus and referred
by Kohlmeyer et al. (1995b) to the Lophiostomataceae “with
hesitation” as it did not fully agree with the type species Massarina
eburnea. Molecular data presented here clearly indicates that it
does not belong in Massarina, but further assignment must await
additional collections.
Clade XVI. Residual paraphyletic assemblage
Several unresolved species form part of a poorly resolved group that
includes the Testudinaceae and it is not clear whether missing data
played a role in this. The genera in question include: Carinispora (Fig.
2AV), Massarina ricifera, Passeriniella, Salsuginea and Quintaria
(Fig. 2F). Jones et al. (2009) referred Salsuginea ramicola (Fig.
2M, X) to the Pleosporales incertae sedis; a genus with similarities
to Helicascus (Kohlmeyer 1969, Hyde 1991) while Hyde (1991)
suggested the Dothideales incertae sedis. Both genera occur on
mangrove wood but differ in that Salsuginea lacks a stroma, the
ascomata form under a clypeus, asci have a distinctive ocular
chamber and ascospores with prominent apical pores and lacking a
mucilaginous sheath. It is a species collected from various mangrove
tree species with ascospore measurements differing, but whether
this is in response to the host remains to be evaluated (Hyde 1991).
The genera Acrocordiopsis (Fig. 3P) and Passeriniella form an
unsupported clade with both taxa known from mangrove wood in
the tropics (Hyde & Mouzouras 1988, Borse & Hyde 1989, Alias
et al. 1999) and referred previously to the Melanommataceae
and Dothideales incertae sedis, respectively (Jones et al.
2009). Morphologically they would appear to share few common
characters. Acrocordiopsis species are characterised by large
(< 2 mm) ascomata that are conical, supericial on the host and
carbonaceous with the asci formed on a thin layer of peridial tissue
on the host substratum while the ascospores are hyaline and
1-septate (Alias et al. 1999). Currently two Passeriniella species
are accepted (Jones et al. 2009), namely P. mangrovei and P.
savoryellopsis, with coriaceous, globose to subglobose, immersed
ascomata, and ascospores that are 3-septate, central cells brown,
and hyaline end cells (Hyde & Mouzouras 1988, Maria & Sridhar
2002). The taxonomic characterisation of the genus Passeriniella
is confusing and has been discussed by Hyde & Mouzouras (1988)
and Kohlmeyer & Volkmann-Kohlmeyer (1991).
Byssothecium (Passeriniella) obiones, a common species on
senescent culms of Spartina, has a checkered history, assigned
to Pleospora, Leptosphaeria, Didymosphaeria, Metasphaeria
and Passeriniella (Jones et al. 2009). Khashnobish & Shearer
(1996) showed that based on ITS sequence data, Byssothecium
165
Suetrong et al.
(Passeriniella) obiones did not belong in either Leptosphaeria
or Phaeosphaeria. Subsequently, Barr (2002) assigned it to
Byssothecium, based on the vericolourous ascospores in
the Teichosporaceae. In our original data set, it grouped with
Mycosphaerella species in the Capnodiales. As the origin of
this sequence (JK 4748) cannot be veriied, and because of the
distinctive morphology of B. obiones which has little in common with
those of Mycosphaerella and other members in the Capnodiales,
we did not present these data here.
Two sequences of Quintaria lignatilis form a sister group to
the Testudinaceae but with moderate support for all analyses. The
genus has previously been referred to the Lophiostomataceae (Cai
et al. 2006) and shares features in common with Trematosphaeria.
Quintaria differs from Trematosphaeria by having completely
immersed ascomata with rounded bases, black incrustations lining
the sides of the ostiolar canal, a non-amyloid plate in the ascus and
hyaline ascospores (Kohlmeyer & Volkmann-Kohlmeyer 1991).
Carinispora nypae is another anomalous taxon whose
taxonomic position cannot be resolved at this time. It is placed
in the paraphyletic assemblage XVI by maximum likelihood and
Bayesian derived phylogenies, but not for those obtained by
maximum parsimony. This may be due to artifacts associated
with long branch lengths and its placement will require more in
depth analysis. Carinispora nypae is found growing on the marine
palm Nypa fruticans and has raised crust-like spots covered in a
soft crust-like stroma, with lenticular ascomata under a clypeus,
cylindrical and narrow asci, and yellow to pale-brown ascospores
with a pronounced sheath drawn out on one side into a spine-like
polar appendage (Hyde 1992a). Hyde (1992a) commented that it
was close to Phaeosphaeria, but our data do not support this view.
Clade XVII. Aigialaceae Suetrong, Sakayaroj, E.B.G. Jones,
Kohlm., Volkm.-Kohlm. & C.L. Schoch, fam. nov. MycoBank
MB515957.
Etymology: Named after the type genus.
Familia Pleosporalium, Ascomycetium. Ascomata subglobosa, conica, immersa ad
supericialia, ostiolata, ostiolum rotundum vel issuriforme, epapillata, periphysata.
Hamathecium pseudoparaphysibus trabeculatis, eramosis ad basem, ramosis
anastomosantibusque supra ascos. Asci octospori, cylindrici pedunculati,
pachydermi, issitunicati, disco apicale, IKI non-reagentes. Ascosporae biseriatae
vel uniseriatae, hyalinae ad atro-brunneae, septatae vel muriformes, constrictae ad
leviter constrictae, tunica vel calyptra gelatinosa tectae.
Family in the Pleosporales, Ascomycota. Ascomata subglobose
and immersed to supericial or conical, ostiolate, ostiolum round or
cleft-like, apapillate, black, carbonaceous to coriaceous, single to
gregarious. Periphysate. Hamathecium trabeculate, unbranched at
the base, anastomosing above the asci, embedded in a gelatinous
matrix. Asci 8-spored, cylindrical, pedunculate, thick-walled,
issitunicate, with a refractive apical ring, non-amyloid. Ascospores
biseriate or monostichous, hyaline to brown, septate to muriform,
with a gelatinous sheath or cap.
Type genus: Aigialus Kohlm. & Schatz.
Aigialus Kohlm. & S. Schatz, Trans. Brit. Mycol. Soc. 85: 699. 1985.
A. grandis Kohlm. & S. Schatz, Trans. Brit. Mycol. Soc. 85: 699.
1985 (Type species). Fig. 3A–B, L, N
A. mangrovis Borse, Trans. Brit. Mycol. Soc. 88: 424. 1987. Fig.
3D, P
A. parvus S. Schatz & Kohlm., Trans. Brit. Mycol. Soc. 85: 704.
1985. Fig. 3C, F–G, O
166
A. rhizophorae Borse, Trans. Brit. Mycol. Soc. 88 : 424. 1987. Fig.
3E, Q
A. striatispora K.D. Hyde, Mycol. Res. 96: 1044. 1992.
Jones et al. (2009) accepted four species in this genus, but rejected
A. rhizophorae as it shared a number of features with A. grandis, but
only differed in the vertical septation in the subapical cell. Recent
collections made in Thailand have enabled us to sequence this
species and it is clearly distinct from A. grandis. This is a commonly
encountered genus on mangrove wood and widely reported in
the literature (Borse 1987, Schmit & Shearer 2003, Abdel-Wahab
2005, Jones et al. 2006). Aigialus striatispora was described from
Ranong mangrove, Thailand, but no further collections have been
made (Hyde et al. 1990, 1993).
Ascocratera Kohlm., Canad. J. Bot. 64: 3036. 1986.
A. manglicola Kohlm., Canad. J. Bot. 64: 3036. 1986 (Type species).
Ascocratera manglicola is characterised by carbonaceous, black,
gregarious ascomata that are conical, crater-like, supericial on
wood, on a black stroma, by trabeculate pseudoparaphyses, by asci
with a refractive apical ring, and hyaline ascospores, surrounded by
a gelatinous evanescent sheath (Kohlmeyer 1986). It is a common
species on mangrove wood in the intertidal zone, and known from
various tropical geographic locations (Schmit & Shearer 2003).
Rimora Kohlm., Volkm-Kohlm., Suetrong, Sakayaroj &
E.B.G. Jones, gen. nov. MycoBank MB515958.
Etymology: From the Latin rima = cleft, issure and os = mouth, in
reference to the cleft-like ostiole, a unique feature among marine
ascomycetes.
Ascomata erumpentia, apice plano, elongata, epapillata, ostiolo issuriforme,
periphysata, nigra, gregaria. Peridium cellulis pachydermis, texturam angularem
formans. Hamathecium pseudoparaphysibus ramosibus. Asci octospori, cylindrici,
pedunculati, pachydermi, issitunicati, sine apparatu apicali. Ascosporae distichae,
fusiformes, triseptatae, hyalinae, tunica gelatinosa tectae.
Ascomata erumpent, with lat tops, elongated, apapillate, opening
with a periphysate cleft-like ostiole, black, gregarious. Peridium
of thick-walled cells, forming a textura angularis. Hamathecium
of branched pseudoparaphyses. Asci 8-spored, cylindrical,
pedunculate, thick-walled, issitunicate, without apical apparati.
Ascospores biseriate, fusiform, 3-septate, hyaline, surrounded by
an evanescent sheath.
Type species: Rimora mangrovei (Kohlm. & Vittal) Kohlm.,VolkmKohlm., Suetrong, Sakayaroj, E.B.G. Jones.
Rimora mangrovei (Kohlm. & Vittal) Kohlm.,Volkm-Kohlm.,
Suetrong, Sakayaroj & E.B.G. Jones, comb. nov. MycoBank
MB515959. Fig. 3K, S.
Basionym: Lophiostoma mangrovei Kohlm. & Vittal, Mycologia 78:
487. 1986.
≡ Astrosphaeriella mangrovei (Kohlm. & Vittal) Aptroot & K.D. Hyde, in
K.D. Hyde, Fungi in Marine Environments. Fungal Diversity Press 7: 106.
2002.
Rimora mangrovei was described from collections of bark and wood
of mangrove trees from Belize and India (Kohlmeyer & Vittal 1986)
as Lophiostoma. It was subsequently transferred to Astrosphaeriella
(Hyde et al. 2002b) based on the trabeculate morphology of
Molecular SySteMaticS of the Marine DothiDeomycetes
the pseudoparaphyses. However, the aforementioned authors
conceded that A. mangrovis (and A. asiana) differed from other
Astrosphaeriella species by their round lattened ascomata, slit-like
ostioles and non monocotyledonous hosts.
All three genera Aigialus, Ascocratera and Rimora share
features such as carbonaceous, apapillate ascomata, trabeculate
pseudoparaphyses, cylindrical asci with an apical apparatus and
ascospores with a sheath. However, they differ in the morphology
of their ascospores: brown and muriform in Aigialus, hyaline and
1–3-septate in Ascocratera and Rimora.
2. Mytilinidiales, fig. 1
Clade XIX. Mytilinidiaceae
The common bitunicate ascomycete Kirschsteiniothelia maritima
groups with Lophium mytilinum, with Mytilinidion mytilinellum and
Hysterium andinense as a sister group. The genus Kirschsteiniothelia
has been referred to the Pleosporaceae (Eriksson & Hawksworth
1998, Kirk et al. 2001), Pleomassariaceae (Barr 1993), and
questionably the Massarinaceae (Kodsueb et al. 2006). The genus
appears to be polyphyletic, and Shearer (1993a) and Schoch et
al. (2006) are of the opinion that K. aethiops does not belong in
the Pleosporaceae. Kodsueb et al. (2006) show that K. elaterascus
(a freshwater species) clusters with Morosphaeria (Massarina)
ramunculicola in a sister clade to the Melanommataceae (see
also clade XI, Fig. 1). However, K. elaterascus differs from K.
maritima, and other Kirschsteiniothelia species in ascus structure,
its unusual endoascus with a long, coiled base that uncoils during
ascus dehiscence, ascospore measurements, the presence of an
ascospore sheath and its freshwater occurrence (Shearer 1993a).
Clade XX. unresolved taxa
Included in this clade are three coelomycete species of which
Pseudorobillarda phragmitis has been reported from pine and
yellow poplar test panels from estuarine waters (Salinity 3–16
ppt) (Jones et al. 2009). This monophyletic group formed a wellsupported clade and a sister group to the Mytilinidiales. However
in the current study they form a weakly supported clade with
Farlowiella carmichaeliana and are basal to the Mytilinidiales in all
analyses.
3. Patellariales, fig. 1
Clade XXII. Patellariaceae
Patellaria cf. atrata (Fig 2B, R, AD), a species found growing on
various mangrove wood species collected in Hong Kong and
Thailand, forms a sister group to Hysteropatella species, taxa
normally assigned to the Hysteriales, but recently removed (Boehm
et al. 2009a, b; this volume). Morphologically, little distinguishes
Gloniella clavatispora and Patellaria atrata; paraphyses in the
latter species are distinctly branched and club-shaped (Suetrong &
Jones 2006). The paraphyses illustrated by Steinke & Hyde (1997)
are simple and not branched (Suetrong & Jones 2006). Boehm et
al. (2009a; this volume) refer Gloniella to the Hysteriaceae, and
Patellaria in the Patellariaceae; further collections of the marine
taxa are required to resolve their identiication.
A number of marine species do not group within existing orders
of Dothideomycetes and this may indicate new supergeneric taxa
not yet circumscribed. The lack of suficient protein coding gene
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sequences for these in our analysis and the tendency for these
species to be associated with fast evolving branches on our trees
further complicates the development of phylogenetic hypotheses
for these taxa.
(i) Biatriospora marina (Clade XIV), in all analyses, forms a distinct
long branch and is a basal taxon to the Pleosporomycetidae without
any closely related taxa (Fig. 1). It is an unusual species described
from Sonneratia alba mangrove wood collected in the Seychelles
and India (Hyde & Borse 1986a). It has immersed subglobose to
pyriform ascomata that are black and carbonaceous, cylindrical
asci and brown, septate ascospores with hyaline, globose refractive
chamber or an appendage at each end. Septation is unusual in
that ascospores are non-septate in the center but septate at both
ends and not constricted at the septa. Additional collections have
been made from mangroves in Hong Kong, Malaysia and Thailand
(Jones et al. 2006, E.B.G. Jones unpubl. data).
(ii) Saccardoella rhizophorae Clade XIX. Saccardoella species
have been regarded as having unitunicate asci and thus classiied
in the Clypeosphaeriaceae (Barr 1994). However, Mathiassen
(1989) was of the opinion that the asci are bitunicate and this would
appear to be supported by the current study. Saccardoella species
are known from terrestrial, marine and freshwater habitats (Hyde
1992c, Tsui et al. 1998). However in all phylogenetic analyses to
date this species does not group within any known family or order,
and further studies are required to determine its phylogenetic
relationship.
4. Jahnulales
Aliquandostipitaceae (data not shown)
The family Aliquandostipitaceae was established for species in
the genus Aliquandostipite based on the phylogenetic analyses
of SSU nrDNA sequences (Inderbitzin et al. 2001). Subsequently
Pang et al. (2002) introduced the new order Jahnulales into the
Dothideomycetes, Ascomycota, based on phylogenetic analysis
of SSU nrDNA sequences of Aliquandostipite, Jahnula and
Patescospora. More recently, Campbell et al. (2007) studied the
phylogenetic relationships of taxa in the Jahnulales inferred from
SSU and LSU nrDNA sequences and recognised four groups : 1)
a basal group with Megalohypha aqua-dulces; 2) a Jahnula group
comprising the type species J. aquatica; 3) ive Aliquandostipite
species; and 4) four Jahnula species and the anamorphic genera
Brachiosphaera and Xylomyces. They emended the ordinal
description to include brown, wide hyphae (>10 µm) and greater
variation of ascospore morphology.
Three marine fungi belong in the Jahnulales, the teleomorph
Manglicola guatemalensis and the anamorphic species Xylomyces
chlamydosporus and X. rhizophorae (Suetrong et al. 2010).
Manglicola guatemalensis is a poorly known species with only
three previous collections (Kohlmeyer & Kohlmeyer 1971, Hyde
1988, Jones et al. 2009, Suetrong et al. 2010). The type strain
was collected from dead roots of Rhizophora mangle in Guatemala
(Kohlmeyer & Kohlmeyer 1971). Subsequent collections have
been made on intertidal prop roots of Rhizophora apiculata at Kpg.
Danau, Brunei (Hyde 1988) and frond bases of Nypa fruticans
(Jones et al. 2009). Common features M. guatemalensis shares with
the Jahnulales include stipitate ascomata, bitunicate asci, reticulate
pseudoparaphyses and 1-septate brown ascospores. Manglicola
guatemalensis differs from other bitunicate ascomycetes by its large
167
Suetrong et al.
ascomata, wide ostiole, large unequally 1-septate ascospores and
mangrove habitat on R. mangle and the frond bases of N. fruticans.
Huhndorf (1994) referred Manglicola to the Hypsostromataceae,
a family with no known relationship to any group in the
Dothideomycetes (Loculoascomycetes) but “probably with afinities
to the Melanommatales” (Mugambi & Huhndorf 2009; this volume).
Characteristics that unite Manglicola and the Hypsostromataceae
include supericial, large, elongate ascomata (stalked) with a softtexture, trabeculate pseudoparaphyses, stipitate asci attached in a
basal arrangement in the centrum and fusiform, septate ascospores
(Huhndorf 1994).
Dothideomycetidae
5. Capnodiales, fig. 1
Fourteen genera, such as Belizeana, Caryosporella, Coronopapilla,
Lautospora, Loratospora, Pontoporeia and Thalassoascus,
assigned to the subclass Dothideomycetidae, have only marine
species, and represent new lineages of fungi that may be
associated with the Capnodiales (Jones et al. 2009). Importantly,
few have been studied at the molecular level. Placement of the
genera Passeriniella and Pontoporeia has already been discussed
above.
Clade XXV. Mycosphaerellaceae
Mycosphaerella eurypotami, a halotolerant terrestrial species
found on Juncus roemerianus, was tentatively referred to the
genus by Kohlmeyer et al. (1997b). In the current study it is a
sister taxon to all Mycosphaerella species with moderate support.
Jones et al. (2009) list three marine Mycosphaerella species (M.
salicorniae, M. staticiola, M. suaedae-australis) found on salt
marsh plants (Armeria, Limonium, Salicornia and Suaeda), while
M. pneumatophorae is a common species on the pneumatophores
of Avicennia species in Asia and the Carribean (Kohlmeyer &
Kohlmeyer 1979, Schmit & Shearer 2003, E.B.G. Jones, pers.
comm.). However recent molecular phylogenies containing a
single culture did not support the placement of M. pneumatophorae
in Mycosphaerella (Schoch et al. 2006); instead it was found on a
poorly resolved branch within Dothideomycetes.
In our analysis, Scirrhia annulata, described from senescent
leaves of Juncus roemerianus (Kohlmeyer et al. 1996), groups with
various Mycosphaerella species with moderate support. Diagnostic
features are the linear stromata, 1–3 mm long, generally supericial,
multiloculate with ascomata in longitudinal rows, asci clavate with
apical apparatus (several rings), ascospores 3-septate, brown, with
a thin evanescent sheath, and measuring 46–60 x 9–11.5 µm.
Clade XVIII. unresolved taxa (fig. 1)
(i) The taxonomic position of Heleiosa barbatula (Fig. 1) is unresolved
as observed by its swapping position in different analyses (data not
shown) and previously referred to the Dothideales and Pleosporales
incertae sedis, respectively (Kohlmeyer et al. 1996, Jones et al.
2009). This species, collected on Juncus roemerianus, is rare
and is not obligately marine. Characteristics include immersed
ostiolate epapillate ascomata formed beneath a clypeus, with
pseudoparaphyses, asci cylindrical with short pedicel, refractive
apical apparatus and ascospores that are pale brown, ellipsoid,
1-septate with 10 or more cilia-like polar appendages at each end.
168
(ii) The genera Caryosporella, and Lineolata form a basal clade
in all analyses with weak support, genera previously assigned to
Melanommataceae and Pleosporales incertae sedis, respectively
(Jones et al. 2009). Both occur on mangrove substrata and have
been widely reported from different geographical locations (Schmit
& Shearer 2003).
Caryosporella was thought to be related to Caryospora,
with which it shares a number of common features (Kohlmeyer
1985). It is found on dead wood of intertidal roots and branches
of mangrove trees and has large ascomata and 1-septate, darkbrown ascospores that are thickened at their apices.
Lineolata was initially described as a Didymosphaeria but
transferred to this genus (Kohlmeyer & Volkmann-Kohlmeyer
1990) as it differs in the following respects: no clypeus, almost
supericial ascomata, hamathecium with a gelatinous matrix, asci
with an apical ring-like structure around the ocular chamber and
ornamented brown ascospores. It remains enigmatically placed
here, although three monophyletically placed isolates obtained
from different geographic locations heighten our conidence in the
provenance of these sequences.
DISCuSSIon
marine lineages of the Dothideomycetes
The study conirms the occurrence of several marine
Dothideomycetes with well supported sequence data. The
Pleosporales includes ten families and three unresolved clades
with marine species, while the orders Capnodiales, Jahnulales,
Mytilinidiales, and Patellariales are represented by few taxa.
This is in common with their known diversity (?) in nature
(Kohlmeyer & Kohlmeyer 1979, Jones et al. 2009). While many
terrestrial genera have marine members, e.g. Mycosphaerella,
Passeriniella, Lophiostoma, Massarina, Trematosphaeria and
Phaeosphaeria, others have no known terrestrial counterparts.
The uniqeness of these has necessitated the introduction of two
new families in the Pleosporales, Aigialaceae (all marine genera:
Aigialus, Ascocratera, Rimora) and Morosphaeriaceae (marine
genera Helicascus, Morosphaeria and the freshwater species
Kirschsteiniothelia elaterascus). The taxonomic position of other
exclusively marine genera/species remains to be resolved e.g.
the seagrass ascomycetes Halotthia posidoniae, Pontoporeia
biturbinata (CladeXIV), and Lineolata rhizophorae (Clade XVIII)
and Biatriospora marina (Clade XIV).
A number of new marine lineages have been highlighted as
result of molecular studies including Manglicola guatemalensis,
the irst member of the Jahnulales reported from marine habitats
(Suetrong et al. 2010). This is of particular interest as all other
Jahnulales members are fresh water or peat swamp species and
raises the question as to whether these marine fungi are derived
from terrestrial and freshwater taxa that have migrated to the sea.
This would support earlier phylogenetic analyses (Spatafora et al.
1998) that strongly suggest a terrestrial origin of another marine
ascomycete family in the Sordariomycetes, the Halosphaeriaceae.
A more recent data set (Schoch et al. 2009a; this volume) continues
to support this hypothesis. The marine species M. guatemalensis
occurs in estuarine mangrove habitats on the palm fronds of Nypa
fruticans and Rhizophora wood and may well form a link between
lignicolous freshwater taxa and species from estuarine to marine
environments. Another Jahnulales species of interest is the
anamorph Xylomyces rhizophorae, found on various marine and
Molecular SySteMaticS of the Marine DothiDeomycetes
mangrove substrata (Kohlmeyer & Volkmann-Kohlmeyer 1998,
S. Sivichai, pers. comm.). Campbell et al. (2007) and Prihatini
et al. (2008) have shown that Xylomyces chlamydosporus has a
teleomorph in the Jahnulales.
A second marine lineage is the Aigialaceae comprising three
genera: Aigialus, Ascocratera, and the new genus Rimora, a family
within the Pleosporales. Morphologically they show few common
characteristics but all are to be found in mangrove habitats.
Schoch et al. (2006) showed that Verruculina enalia is a
member of the Testudinaceae, and another marine lineage in the
Dothideomycetes. Previously referred to the Didymosphaeriaceae
(Kohlmeyer & Volkmann-Kohlmeyer 1990), it forms a well supported
basal clade to the Pleosporales. Continued molecular studies of
unresolved taxa may yield further lineages of marine ascomycetes.
Taxa for future phylogenetic study
Marine Dothideomycetes include a broad spectrum of genera and
a wide variety has been sequenced for the current study. However,
several remain to be investigated with DNA sequence data,
especially the genera Belizeana, Capillatospora and Thalassoascus
(Dothideales incertae sedis); Lautospora (Dothideomycetidae
incertae sedis); Bicrouania (Melanommataceae?); Lautitia
(Phaeosphaeriaceae?) and Tirisporella (Pleosporales incertae
sedis). Most are only rarely collected, have yet to be isolated,
are intertidal, or rarely totally submerged. Other more frequently
collected taxa also require further analysis: Quintaria lignatilis
(mangrove species), Decaisnella formosa (wood in association
with sand) and Byssothecium obiones (on Spartina grass).
adaptation to the marine environment
Of the 64 genera (108 species) of marine Dothideomycetes nearly
all are intertidal species found in mangrove habitats, with the
exception of those that occur on marine algae, saltmarsh plants
or seagrasses, e.g. Thalassoascus, Lautitia, Pharcidia (algae),
Bicrouania (marsh plants), Halotthia, Pontoporeia (seagrasses);
Caryospora australiensis, Decaisnella formosa and Platystomum
scabridisporum (wood associated with sand) (Abdel-Wahab
& Jones 2000, 2003). Most of them would appear to be well
adapted to intertidal estuarine habitats with active discharge of
their ascospores. Although they lack the elaborate ascospore
appendages found in the Halosphaeriaceae (Jones 1994, 1995)
many have mucilaginous sheaths, often elaborated to form polar
appendages (Yusoff et al. 1994, Read et al. 1997a, b, Alias
et al. 2001, Au et al. 1999). Ascospores within the ascus are
surrounded by a well-deined delimiting membrane which prevents
the mucilaginous sheath from expanding, thus ensuring effective
ascospore discharge (Read et al. 1994, Yusoff et al. 1994). Once
ejected from the ascus the sheaths (and appendages) take up
water, swell and help in the attachment of the spores to suitable
substrata (Jones 1995).
Some species form ascospore appendages by fragmentation
of a sheath e.g. Capronia ciliomaris (Au et al. 1999) and Tirisporella
beccariana (Jones et al. 1996). A similar mechanism of appendage
unfolding appears to occur in Heleiosa barbatula (Kohlmeyer et al.
1996). As with the ensheathed ascospores, the appendages do not
dilate until they are dispersed into water.
Few marine anamorphic fungi have been reported in comparison
to those found in freshwater habitats (Marvanová 1997, Belliveau
& Bärlocher 2005, Cai et al. 2006). Currently some 94 marine
anamorphs are known, but only a few have been linked to teleomorphs
www.studiesinmycology.org
in the Dothideomycetes: Amorosia littoralis (Mantle et al. 2006),
Dendryphiella arenaria, D. salina (Jones et al. 2008), Xylomyces
spp. (Campbell et al. 2007, Prihatini et al. 2008), Pseudorobillarda
phragmitis (Rungjindamai, pers. comm.), and Robillarda rhizophorae
(Rungjindamai, pers. comm.). A strain of Alternaria maritima groups
within the Pleosporaceae in the current study, while other marine
anamorphic species e.g. Stemphylium spp. Stagonospora spp., may
also be linked to teleomorphs in the Dothideomycetes.
Freshwater anamorphic fungi are uniquely adapted to their
habitat with branched, sigmoid and tetraradiate conidia (Jones
2006, Campbell et al. 2007); many have teleomorphs in the
Dothideomycetes (Webster & Descals 1979, Tsui & Berbee 2006,
Tsui et al. 2006). In contrast few of the marine hyphomycetes
appear to be adapted to their milieu, lacking any elaboration of their
conidia (except e.g. Varicosporina ramulosa and Dwayaangam
junci). This is particularly so for species with recorded teleomorphs
in the Dothideomycetes (Jones et al. 2008).
Speciic habitats of marine Dothideomycetes
Marine Dothideomycetes are generally intertidal ascomycetes and
more common in mangroves, with only a few documented from
temperate climates.
(i) Nypa fruticans: Currently some 100 saprophytic fungi have
been documented from Nypa fruticans, a brackish water palm that
occurs from fully saline conditions to freshwater habitats. Common
fungi on this palm include Astrosphaeriella nypae, Astrosphaeriella
striatispora, Helicascus nypae, Linocarpon appendiculatum and
Tirisporella beccariana. Many of the fungi occurring in Nypa are
not found on other mangrove or marine substrata, for example,
Linocarpon spp., Astrosphaeriella spp., Oxydothis spp. and
Fasciatispora lignicola. Therefore one could ask, are these fungi
host-speciic or is their occurrence on Nypa determined by the
salinity of the habitat? A signiicant number of fungi on Nypa are
unique to the palm, e.g. Helicascus nypae, Tirisporella beccariana
and Carinispora nypae while recently Manglicola guatemalensis
has been found to be common on this palm in Thailand.
(ii) Seagrasses: The diversity of fungi in seagrasses has been a
neglected ield (Raghukumar 2008). Generally, diverse seagrass
species support low diversity and density of saprophytic and
endophytic fungi, as conirmed by many studies (Wilson 1998, Alva
et al. 2002, Devarajan et al. 2002, Rodríguez 2008, Sakayaroj et al.
2010). The most common marine fungi associated with seagrasses
include Sordariomycetes, Corollospora maritima, Lindra thalassiae,
Lulworthia sp. and anamorphic fungi (Kohlmeyer & Kohlmeyer
1979, Newell & Fell 1980). Cuomo et al. (1982, 1985) reported
that the marine Dothideomycetes, Pontoporeia biturbinata, and
Halotthia posidoniae were commonly found on Posidonia oceanica
and Cymodocea nodosa from Mediterranean coasts (Cuomo et al.
1982, 1985) and Cyprus (Jones et al. 2009). These two obligate
marine Dothideomycetes appear to be host speciic and are
frequently found on rhizomes of seagrass (Kohlmeyer & Kohlmeyer
1979).
Many anamorphic dothideomycetous fungi have been found
predominantly as endophytes associated with living seagrass
tissues (Sakayaroj et al. 2010). They are mostly sterile mycelia and
have only been identiied by DNA sequence analysis (Sakayaroj
et al. 2010). So far the diversity of marine fungi associated with
seagrasses, compared with other substrata, is relatively low
(Kohlmeyer & Kohlmeyer 1979). This is probably due to 1) growth
169
Suetrong et al.
inhibiting substances present in seagrass, 2) possibly the frail
leaves of seagrass break up before most of the ascomycetes are
able to colonise or sporulate and inally 3) they are attacked by
other competitors such as bacteria, protozoa, lower fungi, fast
growing anamorphic and/or terrestrial fungi (Sakayaroj et al. 2010).
(iii) Saltmarsh plants: Spartina and Juncus roemerianus: The
mycota of the saltmarsh plant Juncus roemerianus, endemic to
the U.S. east coast and to the Gulf of Mexico, is unique among
herbaceous plants and can only be vaguely compared to that
of mangrove trees, which also host obligate marine as well as
terrestrial species. The terete leaves of J. roemerianus remain
standing for three years or more and the extreme conditions of the
habitat are the reason for the unique fungal diversity (117 species,
17 families; Kohlmeyer & Volkmann-Kohlmeyer 2001). Bitunicates
appear to be less abundant than other groups of fungi; they range
from obligate marine taxa at the base to terrestrial but halotolerant
species at the tip of the leaves.
Spartina species are common saltmarsh plants in temperate
climates that support a wide range of fungi. Kohlmeyer & VolkmannKohlmeyer (2002) list 39 obligate and facultative marine fungi
reported from Spartina species, of which 13 are bitunicate species.
Phaeosphaeria species appear to be the most common bitunicate
genus on this substratum.
(iv) Mangroves: Some 54 species of mangrove trees and 60
associates occur in the new and old world (Tomlinson 1986) with
senescent wood, leaves and fruits offereing a unique habitat for
fungi. It is interesting that maglicolous fungi are predominantly
bitunicate species, while unitunicate ascomycetes are more
prevalent in other marine habitats. Of the 108 described marine
Dothideomycetes, 90 sequences are currently available enabling
the taxonomic resolution of a number of genera and species; in
particular of Massarina species which are frequently found on
mangrove substrata.
future studies
Many habitats, substrata, geographical locations remain virgin territory
for studies on marine fungi. For example, a recent investigation of the
fungal diversity associated with the brown alga Fucus serratus found
several unknown phylotypes within the Dothideomycetes, including
some grouping with an anamorph species isolated from leaf litter
(Sporidesmium obclavatulum; Shenoy et al. 2006) without obvious
marine assocations (Zuccaro et al. 2008). Previously Zuccaro &
Mitchell (2005) isolated fungi from living and cast fronds of the alga,
with 33 % belonging in the Dothideomycetes. Many other niches
such as endophytes from marine animals and mangroves await
intense study (Pang et al. 2008, Schulz et al. 2008, Wang et al.
2008). Practical applications are also possible as marine endophytes
from plants and animals have already yielded a wide range of new
chemical structures (Jones 2008, Pan et al. 2008). Unknown fungi,
including those belonging to the Dothideomycetes, have even been
isolated from extreme marine environments, e.g. ocean sediments
and deep sea hydrothermal ecosystems (Burgaud et al. 2009).
Although it remains to be seen whether these fungi truly qualify as
marine fungi the increase in fungal and dothideomycete phylotypes
from these environments suggest additional sources of untapped
diversity (Le Calvez et al. 2009).
In conclusion, marine bitunicate ascomycetes, (as other
marine fungi) is a broadly deined ecological group that occupy
170
a wide range of habitats within the maritime environment. Within
this study facultative and halotolerant species from Juncus
roemerianus were also included, as well as two genera on
submerged seagrasses from European regions. The vast majority
of fungi presented are predominantly tropical/subtropical mangrove
species. When compared to the other diverse groups of marine
fungi in the Sordariomycetes the prevalence of mangrove fungi in
Dothideomycetes is even more noticeable. Does this ecological
predominance relect a radiation event of these fungi in the
Dothideomycetes? Or is our sampling still biased towards speciic
geographies and ecologies? Only a renewed focus on the niches
described above will provide us with the answer. It is our hope that
a broader scope will provide enough resolution to begin to address
ecological shifts in this fascinating group of fungi.
aCKnowleDGemenTS
This work was supported by TRF/BIOTEC Special Program for Biodiversity
Research and Training Grant BRT R251006, BRT R351004 BRT R352015, and
a TOTAL Corporate Foundation, TOTAL E & P Thailand. We thank Y. Zhang and
Dr K.D. Hyde for exchange of data and useful discussions. SS acknowledges the
Songklanagarind Scholarship for Graduate Studies from the Prince of Songkla
University. We thank Prof. M. Tanticharoen, Dr K. Kirtikara and Dr L. Eurwilaichitr for
continued support. We thank A. Klaysuban for technical assistance, and U. Pinruan,
N. Rungjindamai, R. Choeyklin, A. Loilong, S. Preedanon and O. Supaphon for
assistance with the ield work. Work performed by CLS after 2008 was supported in
part by the Intramural Research Program of the NIH, National Library of Medicine.
Part of this work was also funded by a grant from NSF (DEB-0717476) to JWS and
CLS (until 2008).
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SupplemenTary InformaTIon
Table 1. The list of species used in this study.
Taxon
Substrate
Collector
location
Source
SSu
lSu
RPB2
TEF1
Acrocordiopsis patilii
Mangrove wood
J. Sakayaroj
Thailand, Hat Khanom
Mu Ko Thale Tai
National Park
BCC 28166
Gu479736
Gu479772
Gu479811
–
Acrocordiopsis patilii
Mangrove wood
J. Sakayaroj.
Thailand, Hat Khanom
Mu Ko Thale Tai
National Park
BCC 28167
Gu479737
Gu479773
Gu479812
–
Aigialus grandis
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 18419
Gu479738
Gu479774
Gu479813
Gu479838
Aigialus grandis
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 20000
Gu479739
Gu479775
Gu479814
Gu479839
Aigialus grandis
Mangrove wood
J. Kohlmeyer
Belize, Stewart Island
JK 5244A
Gu296131
Gu301793
Gu371762
–
Aigialus grandis
Mangrove wood
J. Kohlmeyer
Bahamas, Mores
Island
JK 4770
Gu479740
–
–
–
Aigialus grandis
Mangrove wood
E.B.G Jones
Malaysia, Morib
CY 2909
AF441172
–
–
–
Aigialus mangrovei
Mangrove wood
S. Suetrong
Thailand, Kung
Krabaen Bay Royal
development Study
Center
BCC 33563
Gu479741
Gu479776
Gu479815
Gu479840
Aigialus mangrovei
Mangrove wood
S. Suetrong
Thailand, Kung
Krabaen Bay Royal
development Study
Center
BCC 33564
Gu479742
Gu479777
Gu479816
Gu479841
Aigialus parvus
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 18403
Gu479743
Gu479778
Gu479817
Gu479842
Aigialus parvus
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 32558
Gu479744
Gu479779
Gu479818
Gu479843
Aigialus parvus
Mangrove wood
E.B.G. Jones
Malaysia Morib
CY 5061
AF441173
–
–
–
Aigialus rhizophorae
Mangrove wood
S. Suetrong
Thailand, Mu Ko
Chang National Park
BCC 33572
Gu479745
Gu479780
Gu479819
Gu479844
Aigialus rhizophorae
Mangrove wood
S. Suetrong
Thailand, Mu Ko
Chang National Park
BCC 33573
Gu479746
Gu479781
Gu479820
Gu479845
DAOM 195275
DQ677994
DQ678044
DQ677938
DQ677883
CBS 916.96
DQ678031
DQ678082
DQ677980
DQ677927
–
Allewia eureka
Alternaria alternata
Alternaria maritima
Ubiquitous
Amorosia littoralis
Littoral zone
CBS 126.60
Gu456294
Gu456317
–
NN 6654
AM292056
AM292055
–
–
P.G. Mantle
Bahamas, Crooked
Island
CBS 126.54
DQ678018
DQ678070
DQ677967
DQ677913
K. Tanaka
Japan, Okinawa
HHUF 30032
Gu479748
Gu479783
Gu479822
Gu479847
E.B.G. Jones
Thailand, Ranong
Mangrove forest
BCC 09270
Gu479747
Gu479782
Gu479821
Gu479846
J. Kohlmeyer
Belize, Tobacco
Range
JK 5262C,
CBS 120023
Gu296136
Gu301799
Gu371763
–
Aureobasidium pullulans
CBS 584.75
DQ471004
DQ470956
DQ470906
DQ471075
Berkleasmium
micronescium
BCC 8141
DQ280268
DQ280272
–
–
Berkleasmium nigroapicale
BCC 8220
DQ280269
DQ280273
–
–
CY 1228
GQ925835
GQ925848
Gu479823
Gu479848
Bimuria novae-zelandiae
CBS 107.79
DQ677998
DQ678051
DQ677944
DQ767637
Botryosphaeria dothidea
CBS 115476
DQ677998
DQ678051
DQ677944
DQ767637
Botryosphaeria ribis
CBS 115475
DQ678000
DQ678053
DQ677947
DQ677893
Botryosphaeria stevensii
CBS 431.82
DQ678012
DQ678064
DQ677960
DQ677907
Botryosphaeria tsugae
CBS 418.64
AF271127
DQ767655
DQ767644
DQ677914
Ascochyta pisi
Ascocratera manglicola
Ascocratera manglicola
Mangrove wood
Ascocratera manglicola
Biatriospora marina
Mangrove wood
www.studiesinmycology.org
E.B.G. Jones
Singapore, Singapore
mangrove forest
173-S1
Molecular SySteMaticS of the Marine DothiDeomycetes
Table 1. (Continued).
Source
SSu
lSu
RPB2
TEF1
Byssothecium circinnans
CBS 675.92
AY016339
AY016357
DQ767646
-
Capnodium coffeae
CBS 147.52
DQ247808
DQ247800
DQ247788
DQ471089
CBS 131.34
Taxon
Substrate
Collector
location
DQ677997
DQ678050
–
DQ677889
Carinispora nypae
Mangrove wood
(Nypa fruticans)
A. Loilong
Thailand,Tambon
Bang Pao
BCC 36316
Gu479749
–
–
Gu479849
Caryosporella
rhizophorae
Mangrove wood
J. Kohlmeyer
Fiji, Suva
JK 5302A
Gu479750
Gu479784
–
–
Cladosporium
cladosporioides
CBS 170.54
DQ678004
DQ678057
DQ677952
DQ677898
Columnosphaeria fagi
CBS 171.93
AY016342
AY016359
DQ677966
–
Davidiella tassiana
CBS 399.80
DQ678022
DQ678074
DQ677971
DQ677918
Capnodium salicinum
Decaisnella formosa
E.B.G. Jones
Australia, The
Mornington Peninsula
National Park
BCC 25617
GQ925834
GQ925847
Gu479824
Gu479850
E.B.G. Jones
Australia, The
Mornington Peninsula
National Park
BCC 25616
GQ925833
GQ925846
Gu479825
Gu479851
CBS 322.63
AF394542
–
–
–
Delitschia winteri
CBS 225.62
DQ678026
DQ678077
DQ677975
DQ677922
Delphinella strobiligena
CBS 735.71
DQ471029
DQ470977
DQ677951
DQ471100
Decaisnella formosa
Wood, sand
Decorospora gaudefroyi
Salt marsh plants
Dendryphiella arenaria
Algae, sand
J. Nicot
France, Gironde,
Arcachon area
CBS 181.58
DQ471022
DQ470971
DQ470924
DQ677890
Dendryphiella salina
Spartina sp.
E.B.G. Jones
U.K., England;
Southampton,
Langstone Harbour
CBS 142.60
–
–
DQ435066
DQ414251
IMI 373225
AY293779
AY293792
–
–
JK 2932
–
EF177852
–
–
Dothidea hippophaes
DAOM 231303
U42475
DQ678048
DQ677942
DQ677887
Dothidea insculpta
CBS 189.58
DQ247810
DQ247802
AF107800
DQ471081
Dothidea sambuci
DAOM 231303
AY544722
AY544681
DQ522854
DQ497606
Dothiora cannabinae
CBS 737.71
DQ479933
DQ470984
DQ470936
DQ471107
Elsinoë centrolobi
CBS 222.50
DQ678041
DQ678094
–
DQ677934
Elsinoë phaseoli
CBS 165.31
DQ678042
DQ678095
–
DQ677935
Elsinoë veneta
CBS 150.27
DQ767651
DQ767658
–
DQ767641
Didymella cucurbitacearum
Didymella fucicola
Alga (Fucus
vesiculosus)
J. Kohlmeyer
U.K., West Looe
Falciformispora lignatilis
Mangrove wood
(Elaeis guineensis)
U. Pinruan
Thailand, Ban Bang
Sak
BCC 21118
Gu371835
Gu371827
–
Gu371820
Falciformispora lignatilis
Mangrove wood
(Elaeis guineensis)
U. Pinruan
Thailand, Ban Bang
Sak
BCC 21117
Gu371834
Gu371826
–
Gu371819
CBS 206.36
AY541482
AY541492
DQ677989
DQ677931
Farlowiella carmichaeliana
Floricola striata
Juncus roemerianus
(Facultative)
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5678I
Gu296149
Gu301813
Gu371758
Gu479852
Floricola striata
Juncus roemerianus
(Facultative)
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5603K
Gu479751
Gu479785
–
–
Gloniopsis praelonga
CBS 112415
FJ161134
FJ161173
FJ161113
FJ161090
Gloniopsis subrugosa
CBS 123346
FJ161170
FJ161210
FJ161131
–
Guignardia bidwellii
CBS 237.48
DQ678034
DQ678085
DQ677983
–
Guignardia gaultheriae
CBS 444.70
–
DQ678089
DQ677987
DQ677930
Halomassarina
(Massarina) thalassiae
Mangrove wood
J. Kohlmeyer
Fiji, Viti Levu, Suva
JK 5385B
–
Gu479804
–
Gu479853
Halomassarina
(Massarina) thalassiae
Mangrove wood
J. Kohlmeyer.
Belize, Tobacco
Range
JK 5262D
–
Gu301816
–
Gu349011
173-S2
Suetrong et al.
Table 1. (Continued).
Taxon
Substrate
Collector
location
Source
SSu
lSu
RPB2
TEF1
Halomassarina
(Massarina) thalassiae
Mangrove wood
E.B.G. Jones
U.S.A., Florida
BCC 17055
GQ925843
GQ925850
–
–
Halomassarina
(Massarina) thalassiae
Mangrove wood
E.B.G. Jones
U.S.A., Florida
BCC 17054
GQ925842
GQ925849
–
–
Halotthia posidoniae
Seagrasses
(Posidoniae
oceanica)
E.B.G. Jones
Cyprus
BBH 22481
Gu479752
Gu479786
–
–
Heleiosa barbatula
Juncus roemerianus
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5548I
Gu479753
Gu479787
–
–
A 237
AF053729
–
–
–
Helicascus nypae
Mangrove wood
(Nypa fruticans)
A. Loilong
Thailand, Tambon
Bang Pao
BCC 36751
Gu479754
Gu479788
Gu479826
Gu479854
Helicascus nypae
Mangrove wood
(Nypa fruticans)
A. Loilong
Thailand, Tambon
Bang Pao
BCC 36752
Gu479755
Gu479789
Gu479827
Gu479855
Helicascus nypae
Mangrove wood
(Nypa fruticans)
E.B.G. Jones
Malaysia, Kuala
Selangor
PP 6066
AF441174
–
–
–
Helminthosporium solani
HSWS 04
AF120253
–
–
–
Helminthosporium
velutinum
ATCC 38969
AF120254
–
–
–
Herpotrichia diffusa
CBS 250.62
DQ678019
DQ678071
DQ677968
DQ677915
Herpotrichia juniperi
CBS 200.31
DDQ678029
DQ678080
DQ677978
DQ677925
Hysterium andinense
CBS 123562
FJ161159
FJ161199
FJ161125
FJ161107
Hysterium angustatum
CBS 236.34
–
FJ161180
FJ161117
FJ161096
Hysterium pulicare
CBS 123377
FJ161161
FJ161201
FJ161127
FJ161109
Hysterobrevium mori
CBS 123564
FJ161158
FJ161198
–
FJ161106
Hysterobrevium smilacis
CBS 114601
FJ161135
FJ161174
FJ161114
FJ161091
Hysteropatella clavispora
CBS 247.34
DQ678006
AY541493
DQ677955
DQ677901
Hysteropatella elliptica
CBS 935.97
EF495114
DQ767657
DQ767647
DQ767640
Helicascus kanaloanus
Julella avicenniae
Mangrove wood
E.B.G. Jones
Thailand, Mu Ko
Chang National Park
BCC 18422
Gu371831
Gu371823
Gu371787
Gu371816
Julella avicenniae
Mangrove wood
E.B.G. Jones
Thailand, Mu Ko
Chang National Park
BCC 20173
Gu371830
Gu371822
Gu371786
Gu371815
Julella avicenniae
Mangrove wood
J. Kohlmeyer
JK 5326A
Gu479756
Gu479790
–
–
Julella avicenniae
Mangrove wood
E.B.G. Jones
CY 2462
AF441175
–
–
–
CBS 104.55
Gu296155
Gu301822
Gu371735
Gu349043
CBS 118429
Gu479757
Gu479791
–
–
HKUCC 7769
& A22-5A
AF053727
AY787934
–
–
Hong Kong Tingkok
Keissleriella cladophila
Keissleriella rara
Juncus roemerianus
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
Kirschsteiniothelia
elaterascus
Kirschsteiniothelia
maritima
Driftwood
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., Washington,
Friday Harbor
Laboratories
CBS 221.60
–
Gu323203
–
Gu349001
Lentithecium (Massarina)
phragmiticola
Phragmites, grass
C. Tsui
Hong KongTai, O
Lantau Island
CBS 110446
DQ813512
DQ813510
–
–
Lentithecium
arundinaceum (Massarina
arundinacea)
CBS 619.86
DQ813513
DQ813509
–
–
Leptosphaeria biglobosa
CBS 303.51
–
Gu301826
–
Gu349010
Leptosphaeria doliolum
CBS 505.75
U43447
U43474
–
–
Leptosphaeria maculans
DAOM
2229267
DQ470993
DQ470946
DQ471062
DQ471062
Leptosphaerulina australis
CBS 939.69
EU754068
EU754167
–
–
www.studiesinmycology.org
173-S3
Molecular SySteMaticS of the Marine DothiDeomycetes
Table 1. (Continued).
Taxon
Substrate
Collector
location
Lewia infectoria
Source
SSu
lSu
RPB2
TEF1
IMI 303186
U43465
U43482
–
–
Lineolata rhizophorae
Mangrove wood
J. Kohlmeyer
U.S.A., Florida
CBS 641.66
Gu479758
Gu479792
Gu479828
–
Lineolata rhizophorae
Mangrove wood
J. Kohlmeyer
Australia, Queensland
CBS 118422
–
Gu479805
–
–
Lineolata rhizophorae
Mangrove wood
J. Kohlmeyer
Belize, Blue Ground
Range
JK 5248A
–
Gu479806
–
–
Lophiostoma
(Platystomum)
scabridisporum
Wood, sand
E.B.G. Jones
Australia, The
Mornington Peninsula
National Park
BCC 22836
GQ925832
GQ925845
Gu479829
Gu479856
Lophiostoma
(Platystomum)
scabridisporum
Wood, sand
E.B.G. Jones
Australia, The
Mornington Peninsula
National Park
BCC 22835
GQ925831
GQ925844
Gu479830
Gu479857
Lophiostoma arundinis
CBS 621.86
DQ782383
DQ782384
DQ782386
DQ782387
Lophiostoma bipolarae
(Massarina bipolaris)
HKUCC 1053
AF164365
–
–
–
Lophiostoma crenatum
CBS 629.86
DQ678017
DQ678069
DQ677965
DQ677912
Lophiostoma fuckelii
CBS 113432
–
EU552139
–
–
Lophiostoma fuckelii
CBS 101952
–
DQ399531
–
–
Lophiostoma
macrostomum
KT 709
AB521732
AB433274
–
–
Lophiostoma
macrostomum
KT 635
AB521731
AB433273
–
–
Lophiostoma sagittiforme
HHUF 29754
–
AB369267
–
–
Lophium mytilinum
CBS 269.34
DQ678030
DQ678081
DQ677979
DQ677926
JK 5535D
Gu296168
Gu301838
Gu371760
Macrophomina phaseolina
CBS 277.33
DQ678037
DQ678088
DQ677986
Massaria platani
CBS 221.37
DQ678013
DQ678065
DQ677961
DQ677908
Massarina eburnea
CBS 473.64
AF164367
–
–
–
Massarina eburnea
HKUCC 4054
AF164366
–
–
–
Massarina igniaria
CBS 845.96
DQ813511
DQ810223
–
–
Loratospora aestuarii
Juncus roemerianus
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
DQ677929
Massarina ricifera
Juncus roemerianus
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5535F
Gu479759
Gu479793
–
–
Mauritiana rhizophorae
Mangrove wood
S. Suetrong
Thailand, Kung
Krabaen Bay Royal
development Study
Center
BCC 28866
Gu371832
Gu371824
Gu371796
Gu371817
Mauritiana rhizophorae
Mangrove wood
S. Suetrong
Thailand, Kung
Krabaen Bay Royal
development Study
Center
BCC 28867
Gu371833
Gu371825
Gu371797
Gu371818
Melanomma pulvis-pyrius
CBS 109.77
AF164369
DQ384095
–
–
Melanomma radicans
ATCC 42522
U43461
U43479
AY485625
–
Montagnula opulenta
CBS 168.34
AF164370
DQ678086
DQ677984
–
Morosphaeria
(Massarina)
ramunculicola
Mangrove wood
J. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5304B
Gu479760
Gu479794
Gu479831
–
Morosphaeria
(Massarina)
ramunculicola
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 18405
GQ925839
GQ925854
–
–
Morosphaeria
(Massarina)
ramunculicola
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 18404
GQ925838
GQ925853
–
–
Morosphaeria
(Massarina)
ramunculicola
Mangrove wood
HKUCC 7649
–
DQ528762
–
–
173-S4
Suetrong et al.
Table 1. (Continued).
Taxon
Substrate
Collector
location
Source
SSu
lSu
RPB2
TEF1
Morosphaeria
(Massarina) velataspora
Mangrove wood
E.B.G. Jones
U.S.A., Florida
BCC 17059
GQ925841
GQ925852
–
–
Morosphaeria
(Massarina) velataspora
Mangrove wood
E.B.G. Jones
U.S.A., Florida
BCC 17058
GQ925840
GQ925851
–
–
Mycosphaerella
eurypotami
Juncus roemerianus
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5586J
Gu479761
Gu301852
Gu371722
Gu371722
Mycosphaerella ijiensis
OSC 100622
DQ767652
DQ678098
DQ677993
–
Mycosphaerella
graminicola
CBS 292.38
DQ678033
DQ678084
DQ677982
–
Mycosphaerella
punctiformis
CBS 113265
DQ471017
DQ470968
DQ470920
–
Myrangium duriaei
CBS 260.36
AY016347
DQ678059
DQ677954
DQ677900
Myriangium hispanicum
CBS 247.33
Gu296180
Gu301854
Gu371744
Gu349055
Mytilinidimytilinellum
CBS 303.34
FJ161144
FJ161184
FJ161119
FJ161100
Neotestudina rosatii
CBS 690.82
DQ384069
DQ384107
–
–
Oedohysterium insidens
CBS 238.34
FJ161142
FJ161182
FJ161118
FJ161097
Oedohysterium sinense
EB 0333
FJ161169
FJ161209
FJ161130
–
Opegrapha dolomitica
–
DQ883706
–
DQ883714
DQ883732
Ophiosphaerella
herpotrichus
ATCC 12279
U43453
U43471
–
–
Ostreichnicurtisii
CBS 19834
FJ161137
FJ161176
–
FJ161093
Ostreichnisassafras
CBS 322.34
FJ161148
FJ161188
FJ161122
–
Paraliomyces lentiferus
Mangrove wood
E.B.G. Jones
Hong Kong, North
Lantau
CY 3525
AF441176
–
–
–
Passeriniella
savoryellopsis
Mangrove wood
J. Kohlmeyer
Belize, Tobacco
Range
JK 5167C
Gu479762
Gu479795
–
Gu479858
CBS 958.97
Gu296181
Gu301855
–
Gu349038
–
Patellaria atrata
Patellaria cf. atrata 1
Mangrove wood
S. Suetrong
Thailand, Kung
Krabaen Bay Royal
development Study
Center
BCC 28877
Gu371837
Gu371829
–
Patellaria cf. atrata 2
Mangrove wood
S. Suetrong
Thailand, Kung
Krabaen Bay Royal
development Study
Center
BCC 28876
Gu371836
Gu371828
–
-
CBS 182.58
DQ678021
DQ678073
DQ677970
DQ677917
CBS 254.64
–
Gu45631
–
–
Phaeosphaeria avenaria
DAOM 226215
AY544725
AY544684
DQ677941
DQ677885
Phaeosphaeria eustoma
CBS 576.86
DQ678011
DQ678063
DQ677959
DQ677906
Phaeodothis winteri
Phaeosphaeria
albopunctata
(Leptosphaeria
albopunctata)
Spartina alternilora
J. Kohlmeyer
U.S.A., North
Carolina, Beaufort
Phaeosphaeria olivacea
Juncus roemeriaus
J. Kohlmeyer,
B. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
JK 5540Q
–
Gu479807
–
–
Phaeosphaeria
spartinicola
Spartina sp.
J.Kohlmeyer
U.S.A., Maryland,
Solomons
JK 5177A
–
Gu479808
–
–
Phoma herbarum
CBS 615.75
EU754087
EU754186
–
–
Platychora ulmi
CBS 361.52
EF114726
EF114702
–
–
Pleospora herbarum
CBS 191.86
DQ247812
DQ247804
DQ247794
DQ471090
Pleospora sedicola
CBS 109843
–
AY849958
–
–
Pleosporaceae sp. 1
OSC 100706
–
Gu479809
–
–
Pontoporeia biturbinata
Seagrasses
Preussia minima
www.studiesinmycology.org
E.B.G. Jones
Cyprus
BBH 23338
Gu479763
Gu479796
Gu479837
–
CBS 524.50
DQ678003
DQ678056
DQ677950
DQ677897
173-S5
Molecular SySteMaticS of the Marine DothiDeomycetes
Table 1. (Continued).
Source
SSu
lSu
RPB2
TEF1
Preussia terricola
DAOM 230091
AY544726
AY544686
DQ470895
DQ471063
Pseudorobillarda
phragmitis
CBS 842.84
EU754103
EU754202
–
–
Pseudorobillarda
siamensis
BCC 12531
FJ825365
FJ825375
–
–
Pseudorobillarda texana
BCC 12535
FJ825367
FJ825377
–
–
Psiloglonium araucanum
CBS 112412
FJ161133
FJ161172
FJ161112
FJ161089
Psiloglonium clavisporum
CBS 123339
FJ161157
FJ167526
FJ161124
FJ161105
Psiloglonium simulans
CBS 206.34
FJ161139
FJ161178
FJ161116
FJ161094
Pyrenophora phaeocomes
DAOM 222769
DQ499595
DQ499596
DQ497614
DQ497607
Pyrenophora tritici-repentis
OSC 100066
AY544716
AY544672
–
DQ677882
Taxon
Substrate
Collector
location
Quintaria lignatilis
Mangrove wood
J. Kohlmeyer,
B. Kohlmeyer
French Polynesia,
Moorea
JK 5390A,
CBS 117700
Gu296188
Gu301865
Gu371761
–
Quintaria lignatilis
Mangrove wood
E.B.G. Jones
U.S.A., Florida
BCC 17444
Gu479764
Gu479797
Gu479832
Gu479859
Quintaria submersa
CBS 115553
–
Gu479810
–
–
Repetophragma
ontariense
HKUCC 10830
–
DQ408575
DQ435077
–
Rimora (Lophiostoma)
mangrovei
Mangrove wood
J. Kohlmeyer
Belize, Blue Ground
Range
JK 5246A
Gu296193
Gu301868
Gu371759
–
Rimora (Lophiostoma)
mangrovei
Mangrove wood
J. Kohlmeyer
India, Goa
JK 5437B
Gu479765
Gu479798
–-
–
DUKE 15572
AY584678
AY584654
DQ782866
–
Roccella fuciformis
Saccardoella
rhizophorae
Mangrove wood
J. Kohlmeyer,
B. Kohlmeyer
Hawaii, Oahu
JK 5456A
Gu479766
Gu479799
–
Gu479860
Salsuginea ramicola
Mangrove wood
K. Tanaka
Japan, Okinawa
KT 2597.1
Gu479767
Gu479800
Gu479833
Gu479861
K. Tanaka
Japan, Okinawa
KT 2597.2
Gu479768
Gu479801
Gu479834
Gu479862
S. Newell
U.S.A., Georgia,
Sapelo Island
JK 5546G
Gu479769
–
–
–
Scorias spongiosa
CBS 325.33
DQ678024
DQ678075
DQ677973
DQ677920
Stylodothis puccinioides
CBS 193.58
AY016353
AY004342
–
DQ677886
Sydowia polyspora
CBS 116.29
DQ678005
DQ678058
DQ677953
DQ677899
JK 5517J
Gu296201
–
Gu371721
–
Trematosphaeria
(Lophiostoma) heterospora
CBS 644.86
AY016354
AY016369
DQ497615
DQ471049
Trematosphaeria pertusa
CBS 122371
FJ201993
FJ201992
–
–
Trematosphaeria pertusa
CBS 122368
FJ201991
FJ201990
–
–
Salsuginea ramicola
Scirrhia annulata
Tremateia halophila
Juncus roemerianus
Juncus roemeriaus
J. Kohlmeyer
U.S.A., North
Carolina, Carteret
County
CBS 110020
DQ678025
DQ678076
DQ677974
DQ677921
Verruculina enalia
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 18401
Gu479770
Gu479802
Gu479835
Gu479863
Verruculina enalia
Mangrove wood
E.B.G. Jones
Malaysia, Morib
BCC 18402
Gu479771
Gu479803
Gu479836
Gu479864
Verruculina enalia
Mangrove wood
J. Kohlmeyer,
B. Kohlmeyer
Belize, Blue Ground
Range
JK 5253A
DQ678028
DQ678079
DQ677977
–
Westerdykella
(Eremodothis) angulata
CBS 610.74
DQ384067
DQ384105
–
–
Westerdykella cylindrica
CBS 454.72
AY016355
AY004343
DQ470925
DQ497610
Westerdykella dispersa
CBS 508.75
U42488
DQ468050
–
–
Wettsteinina lacustris
CBS 618.86
DQ678023
–
DQ677972
DQ677919
Ulospora bilgramii
173-S6