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Fungal Diversity

Thailandiomyces bisetulosus gen. et sp. nov. (, , ) and its anamorph Craspedodidymum, is described based on nuclear SSU and LSU rDNA sequences

Pinruan, U.1,2, Sakayaroj, J.2, Hyde, K.D.3,4 and Jones, E.B.G.2*

1Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand 50200 2National Center for Genetic Engineering and Biotechnology, 113 Thailand Science Park, Paholyothin Road, Khlong 1, Khlong Luang, Pathum Thani, Thailand 12120 3International Fungal Research & Development Centre, The Research Institute of Resource Insects, Chinese Academy of Forestry, Balonssi, Kunming 650224, PR China 4School of Science, Mae Fah Luang University, Tasud, Chiang Rai 57100, Thailand

Pinruan, U., Sakayaroj, J., Hyde, K.D., and Jones, E.B.G. (2008). Thailandiomyces bisetulosus gen. et sp. nov. (Diaporthales, Sordariomycetidae, Sordariomycetes) and its anamorph Craspedodidymum, is described based on nuclear SSU and LSU rDNA sequences. Fungal Diversity 29: 89-98.

Thailandiomyces gen. nov. (Diaporthales) is described from senescent trunks of a palm (Licuala longicalycata) in a peat swamp. Phylogenetic analysis of Thailandiomyces was undertaken, with partial SSU and LSU rDNA sequences. Our morphological and molecular results show that this is well placed in the Diaporthales. However, it is not related to the genus it most closely resembles morphologically. It differs from Diaporthe species in number of characters: partially immersed to superficial ascomata, ascospore measurements, bipolar appendages, not surrounded by a mucilaginous sheath, and with Craspedodidymum licualae Pinruan as its anamorph. This is the first report of a teleomorph for the genus Craspedodidymum.

Key words: Craspedodidymum anamorph, freshwater ascomycete, molecular phylogeny, palm, peat swamp, rDNA

Article Information Received 15 May 2007 Accepted 20 November 2007 Published online 31 March 2008 *Corresponding author: E.B.G. Jones; e-mail: [email protected]

Introduction dae, Sordariomycetes), Flammispora bioteca (Sordariomycetes incertae sedis) and an Between May 2002-October 2004 a unusual Diaporthe-like ascomycete with cylin- detailed survey of the fungi associated with drical bipolar appendaged ascospores and with palms in Sirindhorn Peat Swamp Forest, Craspedodidymum licualae as its anamorph. Narathiwat Province, southern Thailand, was undertaken (Pinnoi et al., 2006; Pinruan et al., Material and methods 2007). Species diversity on the selected palms was high with the discovery of 53 new taxa, 17 Fungal isolation and 15 on Licuala longicalycata and Eleiodoxa Senescent trunks of palm material were conferta, respectively (Hyde et al., 2002; collected from Sirindhorn Peat Swamp Forest, McKenzie et al., 2002; Pinruan et al., 2002; Narathiwat, southern Thailand during May Pinnoi et al., 2003a,b; 2004; Pinruan et al., 2001. Palm samples were placed in plastic 2004a,b,c,d). New ascomycetes on senescent bags, returned to the laboratory, incubated in parts of the palm Licuala longicalycata plastic boxes with moist tissue to allow fungal included Jahnula appendiculata (Jahnulales, fruiting bodies to develop and examined within incertae sedis), Phruensis four weeks (Pinnoi et al., 2006; Pinruan et al., brunneispora (Diaporthales, Sordariomyceti- 2002, 2007). Type material has been deposited

89 in the BIOTEC Bangkok Herbarium (BBH) families and complexes in the Diaporthales and cultures in the BIOTEC Culture Collection (the , , - (BCC). Single ascospore isolations were made ceae, , , on corn meal agar (CMA) with added anti- , complex and biotics to suppress bacterial growth. All obser- Harknessia complex) were chosen for the vations, including photographic document- analysis, and the served as tation, and measurements were of material the outgroup. mounted in water, and examined in a differ- Phylogenetic trees for both datasets were ential interference microscope. generated using equally weighted maximum parsimony (heuristic searches with a stepwise Growth of fungi, DNA extraction, amplifi- starting tree, a random stepwise addition of 10 cation and sequencing replicates and tree-bisection-reconnection Stock cultures of the were (TBR) branch-swapping algorithm, with gaps maintained on potato dextrose agar (PDA) at treated as missing data). Bootstrap analysis 25°C. The fungus was grown in potato dextrose (Felsenstein, 1985) based on equally weighted broth (PDB) on a rotary shaker at 200 rpm at maximum parsimony was performed with full 25°C. Fungal biomass was harvested by heuristic searches on 1,000 replicates, 10 vacuum filtration and washed with sterile replicates of random stepwise addition of taxa, distilled water. The biomass was frozen in TBR branch-swapping algorithm. Kishino- liquid nitrogen and ground with a mortar and Hasegawa (K-H) maximum likelihood test pestle. DNA was extracted using a (Kishino and Hasegawa, 1989) was performed NucleoSpinR DNA extraction kit (MAC- in to obtain the best phylogenetic HEREY-NAGEL, Catalogue No. 740 590. 50). hypothesis for the dataset. Nuclear SSU and LSU rDNA were amplified, Bayesian phylogenetic inference of SSU using FINNZYMES, DyNAzymeTM II DNA and LSU sequences was calculated using Polymerase Kit (MACHEREY-NAGEL, MrBayes 3.0b4 with general time reversible Product code F-551S), in a Perkin Elmer (GTR) model of DNA substitution and a thermal cycler. The primer pairs and gamma distribution rate variation across sites amplification cycles were performed following (Huelsenbeck and Ronquist, 2001). Four White et al. (1990), Bunyard et al. (1994), and Markov chains were run from random starting Landvik (1996). The PCR products were trees for 2,000,000 generations and sampled purified using a NucleoSpinR Plant DNA every 100 generations. The first 100,000 purification kit (MACHEREY-NAGEL, Cata- generations were discarded as burn-in of the logue No. 740 570. 50), then sequenced chain. A majority rule consensus tree of all automatically by Macrogen Inc. (Korea) using remaining trees, as well as the posterior primers NS1, NS3, NS4, NS5, NS6, LROR, probabilities, was calculated. The alignments JS5 and LR7 (White et al., 1990; Bunyard et were deposited in TreeBase: matrix accession al., 1994; Landvik, 1996). numbers = SN 3396, SN 3397. Accession numbers for taxa obtained from GenBank are Phylogenetic analyses indicated next to each taxon name in the trees. Two strains of Thailandiomyces bisetu- losus (BCC00018, BCC00200) were sequenced Results to confirm their monophyly (Table 1). SSU and LSU rDNA sequences were aligned indivi- SSU phylogeny dually using BioEdit version 7.0.5 (Hall, 2005). The SSU dataset consists of 1,769 The alignments were entered into PAUP* characters of which 1,500 are constant, 188 are 4.0b10 (Swofford, 2002). SSU dataset com- parsimony informative and 81 are parsimony prised 28 taxa within the subclass Sordario- uninformative. This alignment consists of 402 mycetidae (the Diaporthales, Magnaportha- and 14 inserted bases at the same position in ceae, and ) with two strains of Thailandiomyces bisetulosus the as the outgroup. Sequences of BCC00018 and BCC00200, respectively. The LSU rDNA comprised 42 taxa from selected maximum parsimony analysis resulted in eight 90 Fungal Diversity

Table 1 Fungal isolates sequenced for this only differ in the minor swapping position study. within the Diaporthaceae and Togniniaceae. One of the 24 MPTs inferred with the best Species name GenBankaccession topology from K-H test is shown in Fig. 20. number The LSU data showed that the branches SSU LSU Thailandiomyces bisetulosus EF622229 EF622230 leading to the major families in the Diapor- (BCC00018) thales are reasonably stable, although with Thailandiomyces bisetulosus EF622228 EF622231 weak support in some of the terminal taxa. The (BCC00200) two Th. bisetulosus strains are monophyletic and form a clade to the Diaporthaceae most parsimonious trees (MPTs) 469 steps long and Diaporthales incertae sedis with 100% (CI = 0.673, RI = 0.776, RC = 0.523). The bootstrap and 100% posterior probabilities, major branches are stable, and differ only in the with the Togniniaceae as a sister clade (Fig. position of Lollipopaia minuta AF301534 and 20). Phruensis brunneispora AY581944 within the Diaporthales. The K-H test resulted in the best phylogenetic hypothesis for the dataset as Thailandiomyces Pinruan, Sakayaroj, Hyde & shown in Fig. 19. Jones, gen. nov. The two Th. bisetulosus isolates are MycoBank: 511583 monophyletic and positioned as a basal clade of Etymology: Thailand, in reference to the name of the Diaporthales with species as a the host country. sister clade (50% bootstrap, 100% posterior Ascomata semi-immersa vel superficialia, globo- probabilities). All taxa sampled in this analysis sa, nigra, coriacea, ostiolata, scattered. Cello longis cylindrical. Peridium cella crassitunicatum et textura are well positioned in the Diaporthales, angularis. Paraphyses. Asci cylindrica vel clavate, apedi- although with low bootstrap and posterior cellati, J-, apparatus subapicale praediti. Ascosporae probabilities at node * (Fig. 19). Thailan- rectae vel curvatae fusiformes, hyalinae, 1-septatae, diomyces bisetulosus forms an unsupported guttulatae, appendiculae bipolaris. clade with Lollipopaia minuta AF301534 and Ascomata partially immersed to super- is distantly placed to ficial, globose, black, coriaceous, ostiolate, AY779278 and D. eres DQ471015 (the only scattered to gregarious, with long cylindrical two SSU sequences of Diaporthe available for necks, periphysate with short hyaline cells. the analysis in the GenBank), but without Peridium composed of one stratum of com- bootstrap and posterior probabilities support pressed cells, (textura angularis), black to the (Fig. 19). outside, brown inwardly. Paraphyses present but deliquescent, irregular in width, rarely LSU phylogeny septate, tapering towards the apices, embedded Further taxa from the Diaporthales, in a mucilaginous matrix. Asci cylindrical to based on recent data by Gryzenhout et al. clavate, unitunicate, apedicellate, free-floating, (2006) were added to the LSU analyses. The apically truncate, with a J- subapical ring. LSU dataset consists of 1,667 total characters Ascospores overlapping 2-seriate, fusoid, of which 305 positions were excluded, due to straight or curved, hyaline, 1-septate, smooth- the presence of an intron in the Crypto- walled, with bipolar appendages. diaporthe corni AF408343 sequence. Therefore Anamorph: Craspedodidymum Hol.-Jech. 1,302 total characters, of which 1,020 were Type species: Thailandiomyces bisetu- constant characters, 244 parsimony informative losus Pinruan. characters and 38 parsimony uninformative characters were included in the analyses. Thailandiomyces bisetulosus Pinruan, Maximum parsimony resulted in 24 MPTs with Sakayaroj, Hyde & Jones, sp. nov. (Figs 1-13) tree length, CI, RI and RC of 649 steps, 0.550, MycoBank: 511589 0.803 and 0.442, respectively. The overall Etymology: from bisetulosus, in reference to the topology for all 24 MPTs are the same, and bipolar ascospore appendages. 91

Figs 1-13. Light micrographs of Thailiomyces setulis sp. nov. (from holotype). 1. Ascoma on substratum. 2. Periphyses. 3-4, 7. Asci. 8. Peridium. 5-6, 9-13. Ascospores. Bars: 1 = 400 µm; 2-13 = 10 µm.

Ascomata 275-325 µm diam, semi-immersa vel compressed cells, of textura angularis, black to superficialia, globosa, nigra, coriacea, ostiolata, scat- the outside, brown inwardly (Fig. 8). Para- tered. Neck ad 1 mm longa, 100 µm diam, cylindrica. Peridium ad 45 µm crassum, cella crassitunicatum et physes present but deliquescent, irregular in textura angularis. Paraphyses. Asci 65-75 × 6-7.5 µm, width, up to 5-6.5 µm wide, rarely septate, cylindrica vel clavate, apedicellati, sup-apicale J- tapering towards apices, embedded in a praediti, 2 × 2 µm. Ascosporae 20-25 × 3.5-5 µm, rectae mucilaginous matrix. Asci 65-75 × 6-7.5 µm vel curvatae fusiformes, hyalinae, 1-septatae, guttulatae, ( x = 67.5 × 6.8 µm, n = 20), 8-spored, appendiculae bipolaris. cylindrical to clavate, unitunicate, apedicellate, Ascomata 275-325 µm diameter, partially free-floating, apically truncate, with a J- immersed to superficial, globose, black, coria- subapical ring, 2 × 2 µm (Figs 3-4, 7). ceous, ostiolate, scattered to gregarious (Fig. Ascospores 20-25 × 3.5-5 µm ( x = 22.9 × 4 1). Neck up to 1 mm long, 100 µm diam., µm, n = 30), overlapping 2-seriate, fusoid, periphyses with short hyaline cells, central, straight or curved, hyaline, 1-septate, smooth- cylindrical, black (Fig. 2). Peridium up to 45 walled, with 4-5 large guttules, with bipolar µm thick, composed of one stratum of 92 Fungal Diversity

Figs 14-18. Light micrographs of Craspedodidymum licualae anamorph in culture. 14-15. Single ascospore germination (arrowed). 16-18. Conidiophores and conidia. Bars: 14-18 = 10 µm. spine-like appendages, usually bent laterally, 5- broadly rounded at both ends, brown, papillate 7.5 µm long, 1-1.5 µm diam (Figs 5-6, 9-13). at the basal end, O-septate. Anamorph: Craspedodidymum licualae Holotype: THAILAND, Narathiwat, Sirindhorn Pinruan (Figs 14-18). Peat Swamp Forest, on submerged trunk of Licuala Colonies on natural substratum effuse, longicalycata, 12 May 2001, U. Pinruan (Wah 110) in BBH. black. Mycelium superficial. Conidiophores Cultural characteristics: Colonies on macronematous, mononemataus, erect, brown, PDA (BCC00018 and BCC00200 used for the paler toward the apex, straight or flexuous, molecular study) cottony, reaching 1 cm diam smooth, but rough at the apex. Conidiogenous in 3 days at room temperature (22-24ºC), with cells integrated, terminal, 20-27.5 × 6.2-7.5 dark grey mycelium, hyphae smooth-walled. µm, enteroblastic and monophialidic. Conidia Anamorph and teleomorph sporulate on the 13.7-17.5 × 7.5-10 µm, obovoid or ellipsoid, same plate in culture, developing after 2 weeks,

93

79 Diaporthe phaseolorum AY779278 - DQ471015 93 100 padicola AF277112 90 aceriferum AF277111 * 100 70 carpinea AF277110 78 - - gyrosa U78540

Cryphonectria havanensis L42440 * 99 cubensis L42439 -

orthales 94 AF277120 p 50 100 persoonii M83259

Dia 100 Phruensis brunneispora AY581944

92 Lollipopaia minuta AF301534 100 100 Thailandiomyces bisetulosus BCC00200 100 Thailandiomyces bisetulosus BCC00018 89 Togninia fraxinopennsylvanica AY761070 - - Togninia novaezealandiae AY179958

97 99 salvinii U78546 100 graminis AF050488 Magnaporthaceae 87 - leptosporum AF050474 97 Pseudohalonectria lignicola AF050478 100 100 100 100 europhioides AB007667 100 100 Ophiostoma piliferum AJ243295 Ophiostomatales 100 M83261 99 Chaetomium globosum U20379 100 99 M83257 Sordariales 100 Sordaria fimicola X69851 Xylaria carpophila Z49785 Xylariales Xylaria sp. AB014042 10 changes

Fig. 19. One of eight MPTs resulted from maximum parsimony analysis from partial SSU rDNA sequences. Bootstrap values from maximum parsimony higher than 50% and Bayesian posterior probabilities greater than 95% are given above and below each branch. Scale bar indicates 10 character state changes. Low supported clades are indicated by an asterisk (*). and 3-4 weeks, respectively. Initially the 2007). However Th. bisetulosus can not be anamorph was isolated from conidia as assigned to any family at this time. Characters reported in Pinruan et al. (2004d). In this study, Th. bisetulosus shares with members of the single ascospore were isolated which gave rise Diaporthales include its saprobic habitat on

to the anamorph and the teleomorph. decaying plant material, partially-immersed ascomata, long periphysate necks, unbranched Discussion paraphyses that deliquesce early in develop- ment, unitunicate asci that float free within the Phylogenetic analyses of SSU and LSU centrum and asci with a refractive, apical J- rDNA sequences showed that Thailandiomyces ring (Barr, 1991; Samuels and Blackwell, bisetulosus is well positioned in the order 2001). Diaporthales (Sordariomycetes, Sordariomy- The Diaporthales comprise phylogenetic cetidae) (Zhang et al., 2006; Hibbett et al., groups based on morphological and molecular 94 Fungal Diversity

70 musaiaensis AF408337 - Schizoparme straminea AF362569 100 Schizoparme complex 100 Pilidiella castaneicola AF408378 Pilidiella granati AF408379 gyrosa AY194108

90 Rostraureum tropicale AY194092 - gyrosa AF362555 Chryphonectriaceae corni AF408343 58 Chrysoporthe cubensis AF408338 - 60 98 errabunda AF408334 99 99 99 AF408362 Gnomoniaceae 100 100 hypodermia AF408347 100 stilbostoma AF362567 100 Melanconidaceae 62 99 Melanconis marginalis AF408373 - 79 Harknessia eucalypti AF408363 orthales orthales - Harknessia complex p molokaiensis AF408390

Dia 100 adhaerens AF408388 100 100 AF408387 100 Valsa ambiens AF362564 90 99 Diaporthe medusaea AF362560 Diaporthe pardalota AF408355 51 Diaporthe fibrosa AF408351 - Diaporthe eres AF362565 Diaporthaceae 95 - Diaporthe arctii AF362562

97 Diaporthe angelicae AY196780 100 Diaporthe perjuncta AF408356 61 Diaporthe padi AF408354 - 100 Melanconis desmazierii AF408372 100 100 tiliae AF408365 100 100 Apoharknessia insueta AY720814 100 Apoharknessia insueta AY720813

86 100 Thailandiomyces bisetulosus BCC00018 100 100 Thailandiomyces bisetulosus BCC00200 Togninia fraxinopennsylvanica AY761083 100 Togninia minima AY761082 100 Togniniaceae 100 Togninia novaezealandiae AY761081 100 aleophilum AY249088

100 fraterna AY346285 100 Jobellisia luteola AY346286 100 AB026819 100 grisea AF362554 Magnaporthaceae Gaeumannomyces graminis AF362557 10 changes

Fig. 20. One of 24 MPTs resulted from maximum parsimony analysis from partial LSU rDNA sequences. Bootstrap values from maximum parsimony higher than 50% and Bayesian posterior probabilities greater than 95% are given above and below each branch. Scale bar indicates 10 character state changes.

95 data: Gnomoniaceae, Melanconidaceae, Valsa- distinct conidiophores. The conidia of Ch. ceae, Diaporthaceae, Togniniaceae and a new ellisii, Ch. raciborskii and Ch. rubicunda are family Cryphonectriaceae (Castlebury et al., globose, while in C. licualae they are cylin- 2002; Gryzenhout et al., 2006). However, drical or obovoid. The conidial forms of Ch. recent sequence data highlights a number of rubicunda and one collection of Ch. racibo- lineages that can not be referred to these rskii, also differ in having elongate hyaline families: Schizoparme and Harknessia com- appendages. The three Craspedodidymum plexes (Castlebury et al., 2002; Gryzenhout et species isolated from peat swamp palm al., 2006), Apoharknessia insueta, Hercospora material (Pinruan et al., 2004d) do not resem- tiliae, Melanconis desmazierii, Jobellisia ble those illustrated by Huhndorf and species and Th. bistulosus (Fig. 20). Fernández (2005). All Diaporthe species included in the Morphologically Th. bisetulosus shares SSU/LSU analyses formed a well-supported few characters in common with Lollipopaia clade (Figs 19-20). However, morphological minuta. In L. minuta, ascomata are born on a and molecular results show that Th. bisetulosus stroma, asci are cylindrical, ascospores are is not closely related to Diaporthe species filiform, lacking a sheath or appendages. While (Diaporthaceae), the genus it morphologically Th. bisetulosus is not stromatic, asci are most resembles. Diaporthe comprises circa 780 cylindrical to clavate, ascospores fusoid with species (Index Fungorum, http://www.index- apical appendages. fun gorum. org/ Names/Names.asp) and a Exploration of new habitats and geogra- number of these have appendaged ascospores: phical locations has yielded a number of new D. dakotensis, D. decedens, D. laschii, D. and interesting taxa. In Thailand, three genera oxyspora, D. pruni and D. salsuginosa from freshwater habitats have been discovered (Wehmeyer, 1933; Vrijmoed et al., 1994; with affinities with the Diaporthales: Lollipo- Wong and Hyde, 2001). Ascospores of Th. paia minuta on submerged wood with hyaline, bisetulosus are distinct from these species in septate ascospores; Phruensis brunneispora spore measurements, lacking a mucilaginous with versicoloured, septate ascospores, and Th. sheath but with bipolar appendages. Ascomata bisetulosus with hyaline 1-septate spores, both of Th. bisetulosus are partially immersed in the on palm material from a peat swamp substratum to superficial, while in Diaporthe (Inderbitizin and Berbee, 2001; Pinruan et al., species they are generally stromatic. A further 2004a; present study). However, their familial difference between Th. bisetulosus and Diapor- position remains unresolved. Phruensis brun- the spp. is in their anamorphs, the former with neispora and L. minuta grouped within the Craspedodidymum licualae as its anamorph, Valsaceae, Diaporthales (Pinruan et al., 2001). while Diaporthe species universally have a The current analysis does not support this with anamorph. L. minuta and Th. bisetulosus forming a Craspedodidymum has 12 species but no subclade to the Diaporthaceae along with other teleomorph has been linked to any of these, genera and families of uncertain affinities (e.g. prior to this study. Pinruan et al. (2004d) Apoharknessia, Jobellisia and Togninia). described three new Craspedodidymum species Further collections and sequences from a wider from the same locality as Th. bisetulosus one of range of genes are required to resolve their which is its anamorph, C. licualae. Subsequen- taxonomic position. tly, Huhndorf and Fernández (2005) described five Chaetosphaeria species with Craspedo- Acknowledgements didymum-like anamorphs, but did not identify any of them to species. Craspedodidymum This work was supported by the TRF/BIOTEC licualae differs from these Craspedodidymum- Special Program for Biodiversity Research and Training grants BRT R_148008 and R_248002 and Thailand like species in the morphology of the conidia Graduate Institute of Science and Technology grants and conidiogenous cells. Craspedodidymum- TG-22-10-49-019D. We are grateful to Profs. Saisamorn like anamorphs of Chaetosphaeria ellisii, Ch. Lumyong, Morakot Tanticharoen and Dr. Kanyawim raciborskii and Ch. rubicunda, have phialides Kirtikara for continued support, to Mr. Manetr formed directly on the hyphae without forming Boonyanant and his staff for research facilities at the 96 Fungal Diversity

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