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New Hypoxylon species from Martinique and new evidence on the molecular phylogeny of Hypoxylon based on ITS rDNA and β-tubulin data

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Abstract

Three new species of Hypoxylon (Xylariaceae) collected from Martinique in the French Caribbean are recognised by new combinations of morphological characters. Their status as undescribed taxa was supported by secondary metabolite profiling based on High performance liquid chromatography with diode array and mass spectrometric detection (HPLC/DAD-MS) as well as by comparison of ITS and partial ß-tubulin DNA sequences with related taxa. In the course of this study, the teleomorph of Nodulisporium griseobrunneum was found, and this species could be transferred to Hypoxylon. Moreover, several names in Hypoxylon are epitypified by selecting recently collected specimens from the same geographic areas as the holotypes came from. Despite the fact that our study used the hitherto most extensive taxon sampling, the phylogenetic analyses inferred from ITS and ß-tubulin sequences remain contradictory to each other, and neither genealogy was found fully in agreement with phenotype-derived traits. We conclude that the right gene (or multi-gene genealogies) to reflect the phylogeny and evolution of Hypoxylon still remains to be found. For the time being, we recommend that the application of polyphasic taxonomic concepts should be continued in taxonomic studies of Hypoxylon.

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References

  • Bell AA, Wheeler MH (1986) Biosynthesis and functions of fungal melanins. Ann Rev Phytopathol 24:411–451

    Google Scholar 

  • Bills GF, González-Menéndez V, Martín J, Platas G, Fournier J, Peršoh D, Stadler M (2012) Hypoxylon pulicicidum sp. nov. (Ascomycota, Xylariales), a pantropical insecticide-producing endophyte. PLoS ONE 7:e46687. doi:10.1371/journal.pone.0046687

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bitzer J, Köpcke B, Stadler M, Hellwig V, Ju YM, Seip S, Henkel T (2007) Accelerated dereplication of natural products, supported by reference libraries. Chimia 51:332–338

    Article  Google Scholar 

  • Bitzer J, Læssøe T, Fournier J, Kummer V, Decock C, Tichy HV, Piepenbring M, Peršoh D, Stadler M (2008) Affinities of Phylacia and the daldinoid Xylariaceae, inferred from chemotypes of cultures and ribosomal DNA sequences. Mycol Res 112:251–270

    Article  CAS  PubMed  Google Scholar 

  • Bodo B, Tih RG, Davoust D, Jacquemin H (1983) Hypoxylone, a naphthyl naphthoquinone pigment from the fungus Hypoxylon sclerophaeum. Phytochemistry 22:2579–2581

    Google Scholar 

  • Courtecuisse R (2006) Liste préliminaire des Fungi recensés dans les Îles françaises des Petites Antilles: Martinique, Guadeloupe et dépendances. 1. Basidiomycètes lamellés et affines (Agaricomycetideae). Doc Mycol 133–134:81–140

    Google Scholar 

  • Felsenstein J (1989) PHYLIP - phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Fournier J, Köpcke B, Stadler M (2010) New species of Hypoxylon from western Europe and Ethiopia. Mycotaxon 113:209–235

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto T, Tahara S, Takaoka S, Tori M, Asakawa Y (1994) Structures of daldinins A C, three novel azaphilone derivatives from ascomyceteous fungus Daldinia concentrica. Chem Pharm Bull 42:2397–2399

    Article  CAS  Google Scholar 

  • Hellwig V, Ju YM, Rogers JD, Fournier J, Stadler M (2005) Hypomiltin, a novel azaphilone from Hypoxylon hypomiltum, and chemotypes in Hypoxylon sect. Hypoxylon as inferred from analytical HPLC profiling. Mycol Prog 4:39–54

    Article  Google Scholar 

  • Hsieh HM, Ju YM, Rogers JD (2005) Molecular phylogeny of Hypoxylon and closely related genera. Mycologia 97:844–865

    Article  CAS  PubMed  Google Scholar 

  • Hsieh HM, Lin CR, Fang MJ, Rogers JD, Fournier J, Lechat C, Ju YM (2010) Phylogenetic status of Xylaria subgenus Pseudoxylaria among taxa of the subfamily Xylarioideae (Xylariaceae) and phylogeny of the taxa involved in the subfamily. Mol Phylogenet Evol 54:957–969

    Article  CAS  PubMed  Google Scholar 

  • Ju Y-M, Rogers JD (1996) A revision of the genus Hypoxylon. Mycologia Memoir no. 20. APS Press, St. Paul, 365 pp

    Google Scholar 

  • Læssøe T, Srikitikulchai P, Fournier J, Köpcke B, Stadler M (2010) Lepraric acid derivatives as chemotaxonomic markers in Hypoxylon aeruginosum, Chlorostroma subcubisporum and C. cyaninum, sp.nov. Fungal Biol 114:481–489

    Article  PubMed  Google Scholar 

  • Læssøe T, Srikitikulchai P, Luangsa-ard JJD, Stadler M (2013) Theissenia reconsidered, including molecular phylogeny of the type species T. pyrenocrata and a new genus Durotheca (Xylariaceae, Ascomycota). IMA Fungus 4:57–69

    Article  PubMed Central  PubMed  Google Scholar 

  • Lloyd CG (1917) Mycological notes 50. Mycol Writ 5(50):701–716

    Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lumbsch HT, Huhndorf SM (2010) Outline of Ascomycota–2009; notes on ascomycete systematics. Nos. 4751–5113. Myconet 14:1–69

    Google Scholar 

  • Mehrotra RS (1965) A new species of Nodulisporium. Curr Sci 34:353

    Google Scholar 

  • Miller JH (1933) Some new species of Hypoxylon. Mycologia 25:321–329

    Article  Google Scholar 

  • Miller JH (1961) A monograph of the world species of Hypoxylon. Univ. Georgia Press, Athens, 158 p

    Google Scholar 

  • Mühlbauer A, Triebel D, Peršoh D, Wollweber H, Seip S, Stadler M (2002) Macrocarpones, novel metabolites from stromata of Hypoxylon macrocarpum and new evidence on the chemotaxonomy of Hypoxylon. Mycol Prog 1:235–248

    Article  Google Scholar 

  • O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116

    Article  PubMed  Google Scholar 

  • Okane I, Srikitikulchai P, Toyama K, Læssøe T, Sivichai S, Hywel-Jones N, Nakagiri A, Potacharoen W, Suzuki K (2008) Study of endophytic Xylariaceae in Thailand: diversity and taxonomy inferred from rDNA sequence analyses with saprobes forming fruit bodies in the field. Mycoscience 49:359–372

    Article  CAS  Google Scholar 

  • Pažoutová S, Follert S, Bitzer J, Keck M, Surup F, Šrůtka P, Holuša J, Stadler M (2013) A new endophytic insect-associated Daldinia species, recognised from a comparison of secondary metabolite profiles and molecular phylogeny. Fungal Divers 60:107–123

    Article  Google Scholar 

  • Peláez F, González V, Platas G, Sánchez-Ballesteros J, Rubio V (2008) Molecular phylogenetic studies within the family Xylariaceae based on ribosomal DNA sequences. Fungal Divers 31:111–134

    Google Scholar 

  • Peršoh D, Rambold G (2002) Phacopsis - a lichenicolous genus of the family Parmeliaceae. Mycol Prog 1:43–56

    Article  Google Scholar 

  • Pouzar Z (1972) Hypoxylon fraxinophilum spec. nov. and H. moravicum spec. nov., two interesting species found on Fraxinus angustifolia. Ceská Mykol 26:129–137

    Google Scholar 

  • Quang DN, Hashimoto T, Tanaka M, Baumgartner M, Stadler M, Asakawa Y (2002) Chemical constituents of the ascomycete Daldinia concentrica. J Nat Prod 65:1869–1874

    Article  CAS  PubMed  Google Scholar 

  • Quang DN, Hashimoto T, Tanaka M, Stadler M, Asakawa Y (2004) Cyclic azaphilones daldinins E and F from the ascomycete fungus Hypoxylon fuscum (Xylariaceae). Phytochemistry 65:469–473

    Article  CAS  PubMed  Google Scholar 

  • Quang DN, Hashimoto T, Nomura Y, Wollweber H, Hellwig V, Fournier J, Stadler M, Asakawa Y (2005) Cohaerins A and B, azaphilones from the fungus Hypoxylon cohaerens, and comparison of HPLC-based metabolite profiles in Hypoxylon sect. Annulata. Phytochemistry 66:797–809

    Article  CAS  PubMed  Google Scholar 

  • Quang DN, Stadler M, Fournier J, Asakawa Y (2006) Carneic acids A and B, two chemotaxonomically significant antimicrobial agents from the xylariaceous ascomycete, Hypoxylon carneum. J Nat Prod 69:1198–1202

    Article  CAS  PubMed  Google Scholar 

  • Rayner RW (1970) A mycological colour chart. Commonwealth Mycological Institute, Kew and British Mycological Society

  • Sánchez-Ballesteros J, González V, Salazar O, Acero J, Portal MA, Julián M, Rubio V (2000) Phylogenetic study of Hypoxylon and related genera based on ribosomal ITS sequences. Mycologia 92:964–977

    Article  Google Scholar 

  • Spatafora J (2011) 1000 fungal genomes to be sequenced. IMA Fungus 2(2):41

    Google Scholar 

  • Staden R, Kathryn FB, James KB (2000) The staden package, 1998. Comput Methods Mol Biol 132:115–130

    CAS  Google Scholar 

  • Stadler M, Fournier J (2006) Pigment chemistry, taxonomy and phylogeny of the Hypoxyloideae (Xylariaceae). Rev Iberoam Micol 23:160–170

    Article  PubMed  Google Scholar 

  • Stadler M, Hellwig V (2005) Chemotaxonomy of the Xylariaceae and remarkable bioactive compounds from Xylariales and their associated asexual stages. Recent Res Dev Phytochem 9:41–93

    CAS  Google Scholar 

  • Stadler M, Wollweber H, Mühllbauer A, Henkel T, Asakawa Y, Hashimoto T, Rogers JD, Ju YM, Wetzstein HG, Tichy HV (2001) Secondary metabolite profiles, genetic fingerprints and taxonomy of Daldinia and allies. Mycotaxon 77:379–429

    Google Scholar 

  • Stadler M, Tichy HV, Katsiou E, Hellwig V (2003) Chemotaxonomy of Pochonia and other conidial fungi with Verticillium-like anamorphs. Mycol Prog 2:95–122

    Article  Google Scholar 

  • Stadler M, Fournier J, Granmo A, Beltrán-Tejera E (2008) The “red Hypoxylons” of the temperate and subtropical Northern Hemisphere. N Am Fungi 3:73–125

    Google Scholar 

  • Stadler M, Fournier J, Læssøe T, Chlebicki A, Lechat C, Flessa F, Rambold G, Peršoh D (2010) Chemotaxonomic and phylogenetic studies of Thamnomyces (Xylariaceae). Mycoscience 51:189–207

    Article  Google Scholar 

  • Stadler M, Kuhnert E, Peršoh D, Fournier J (2013a) The xylariaceae as model example for a unified nomenclature following the “One fungus-one name” (1F1N) concept. Mycol Int J Fungal Biol 4:5–21

    CAS  Google Scholar 

  • Stadler M, Læssøe T, Fournier J, Decock C, Schmieschek B, Tichy HV, Peršoh D. (2013b) A polyphasic taxonomy of Daldinia (Xylariaceae). Stud Mycol. doi:10.3114/sim0016

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Steglich W, Klaar M, Furtner W (1974) Mitorubrin derivatives from Hypoxylon fragiforme. Phytochemistry 13:2874–2875

    Article  CAS  Google Scholar 

  • Surup F, Mohr KI, Jansen R, Stadler M (2013) Cohaerins G - K, azaphilone pigments from Annulohypoxylon cohaerens and absolute stereochemistry of cohaerins C – K. Phytochemistry, in press.

  • Suwannasai N, Rodtong S, Thienhirun S, Whalley AJS (2005) New species and phylogenetic relationships of Hypoxylon species found in Thailand inferred from the internal transcribed spacer regions of ribosomal DNA sequences. Mycotaxon 94:303–324

    Google Scholar 

  • Suwannasai N, Martín MP, Phosri C, Sihanonth P, Whalley AJS, Spouge JL (2013) Fungi in Thailand: a case study of the efficacy of an ITS barcode for automatically identifying species within the Annulohypoxylon and Hypoxylon genera. PLoS ONE 8(2):e54529. doi:10.1371/journal.pone.0054529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang AMC, Jeewon R, Hyde KD (2009) A re-evaluation of the evolutionary relationships within the Xylariaceae based on ribosomal and protein-coding gene sequences. Fungal Divers 34:127–155

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Triebel D, Peršoh D, Wollweber H, Stadler M (2005) Phylogenetic relationships among Daldinia, Entonaema and Hypoxylon as inferred from ITS nrDNA sequences. Nova Hedwigia 80:25–43

    Article  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

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Acknowledgments

We gratefully acknowledge support from the curators of various international culture collections and herbaria, above all BPI, CBS, GAM, K, LIP, MUCL, NY and WSP, who provided important specimens for the present study. We also thank Markus Scholler (KR) for mediating international loan transactions, and Régis Courtecuisse for facilitating field work in the French Caribbean. Christian Lechat and Thomas Læssøe are thanked for their continuous support in finding important specimens during the field trips in the Neotropics and elsewhere, and all other co-authors of the cited publications by D. P., J. F., and M.S. are thanked for their help. The field sampling in French Guiana has also benefited from “Investissements d’Avenir” grants of the ANR (CEBA ANR-10-LABX-0025, CNRS Cayenne and Toulouse) to J.F. and co-workers. Gerhard Rambold (Univ. Bayreuth) is gratefully acknowledged for his support of our studies during supervision of the MSc thesis of E. K. Last but not least, Beata Schmieschek, Christina Leistner and Philine Wotsch are thanked for expert technical assistance, and the excellent performance of Simone Heitkämper during her student project is gratefully acknowledged.

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Authors and Affiliations

  1. Department of Microbial Drugs, Helmholtz-Zentrum für Infektionsforschung GmbH, Inhoffenstrasse 7, 38124, Braunschweig, Germany

    Eric Kuhnert & Marc Stadler

  2. Las Muros, 09420, Rimont, France

    Jacques Fournier

  3. Department of Mycology, University of Bayreuth, Universitätsstraße 30, 95540, Bayreuth, Germany

    Derek Peršoh

  4. National Center for Genetic Engineering and Biotechnology (BIOTEC), 113 Thailand Science Park, Phaholyothin Road, Klong Luang, Pathumthani, 12120, Thailand

    Janet Jennifer Divinagracia Luangsa-ard

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  1. Eric Kuhnert
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  2. Jacques Fournier
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  3. Derek Peršoh
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  4. Janet Jennifer Divinagracia Luangsa-ard
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  5. Marc Stadler
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Correspondence to Marc Stadler.

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Taxonomic Novelties: Hypoxylon griseobrunneum (B.S. Mehrotra) J. Fourn., Kuhnert & M. Stadler, comb. nov.; Hypoxylon isabellinum J. Fourn., Kuhnert & M. Stadler sp. nov.; Hypoxylon laminosum J. Fourn., Kuhnert & M. Stadler, sp. nov.; Hypoxylon lateripigmentum J. Fourn., Kuhnert & M. Stadler, sp. nov.

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Kuhnert, E., Fournier, J., Peršoh, D. et al. New Hypoxylon species from Martinique and new evidence on the molecular phylogeny of Hypoxylon based on ITS rDNA and β-tubulin data. Fungal Diversity 64, 181–203 (2014). https://doi.org/10.1007/s13225-013-0264-3

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