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Recognition of hypoxyloid and xylarioid Entonaema species and allied Xylaria species from a comparison of holomorphic morphology, HPLC profiles, and ribosomal DNA sequences

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Abstract

The genus Entonaema comprises Xylariaceae with hollow, gelatinous stromata that accumulate liquid. Some of its species, including the type species, appear related to Daldinia from a polyphasic approach, comprising morphological studies, comparisons of ribosomal DNA sequences, and high performance liquid chromatography (HPLC) profiles with diode array and mass spectrometric detection (HPLC-DAD-MS). This methodology was used to study Entonaema pallidum. Its major stromatal constituent was identified as xylaral, a secondary metabolite known from Xylaria polymorpha. This compound was detected in several Xylaria spp., including the tropical X. telfairii and morphologically similar taxa, whose stromata may also become hollow and filled with liquid. Cultures of E. pallidum resembled those of Xylaria, substantially differing from other Entonaema spp., in their morphology, 5.8S/ITS nrDNA sequences, and HPLC profiles. The type specimen of E. mesentericum was located in the spirit collection of the herbarium B and found to agree morphologically with the nomenclatorily younger E. pallidum. Traces of xylaral were even detected by HPLC-DAD-MS in the spirit in which the fungus had been preserved. Entonaema pallidum is thus regarded as a later synonym of E. mesentericum. Therefore, the latter name is transferred to Xylaria. A key to entonaemoid Xylariaceae is provided. Colour reactions (NH3, KOH) of the ectostroma were applied to a limited number of Xylaria spp., but metabolite profiles of cultures appear more promising as chemotaxonomic traits to segregate this genus. As xylaral was also found in Nemania and Stilbohypoxylon spp., while being apparently absent in Hypoxylon and allied genera, it may be a chemotaxonomic marker for Xylariaceae with Geniculosporium-like anamorphs.

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Notes

  1. These terms correspond to “subfamilies”, Hypoxyloideae and Xylarioideae, which were used in previous publications but are not valid taxa; see Bitzer et al. (2008).

  2. See http://www.bgbm.org/BGBM/research/colls/herb.

  3. A luxurious collection (TL-8380, unfortunately lost in a fire) can be viewed on http://www.mycokey.com/Ecuador.htmls.

  4. (for specimens with larger ascospores cf. E. moluccanum ss. Sánchez-Jacomé & Guzmán-Davalos 2005).

References

  • Abate D, Abraham WR, Meyer H (1997) Cytochalasins and phytotoxins from Xylaria obovata. Phytochemistry 44:1443–1448. DOI 10.1016/S0031-9422(96)00780-7

    Article  CAS  Google Scholar 

  • Adeboya MO, Edwards RL, Læssøe T, Maitland DJ (1995) Metabolites of the higher fungi. Part 28. Globoscinic acid and globoscin, a labile acid-lactone system from Xylaria globosa and Xylaria obovata. J Chem Soc Perkin I 1995:2067–2072

    Article  Google Scholar 

  • Adeboya MO, Edwards RL, Læssøe T, Maitland DJ, Whalley AJS (1996) Threo- and erythro-telfairic acid and 2,3-didehydrotelfairic acid anhydride from the fungus Xylaria telfairii. Liebigs Ann 9:1437–1441

    Google Scholar 

  • Benkert D (1993) Kotlabaea macrospora Benkert sp. nov. und einige weitere bemerkenswerte Ascomyceten aus Bulgarien. Fedd Rep 104:547–549

    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 (in press) (DOI 10.1016/j.mycres.2007.07.004)

  • 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 61:332–338

    Article  CAS  Google Scholar 

  • Callan BE, Rogers JD (1990) Teleomorph-anamorph connections and correlations in some Xylaria species. Mycotaxon 36:343–369

    Google Scholar 

  • Callan BE, Rogers JD (1993) A synoptic key to Xylaria species from continental United States and Canada based on cultural and anamorphic features. Mycotaxon 46:141–154

    Google Scholar 

  • Clements F, Shear CL (1931) The genera of fungi. Noble, New York

    Google Scholar 

  • Dennis RWG (1956) Some Xylarias of tropical America. Kew Bull 11:172–332

    Article  Google Scholar 

  • Dennis RWG (1957) Further notes on tropical American Xylariaceae. Kew Bull 12:297–332

    Article  Google Scholar 

  • Dennis RWG (1961) Xylarioideae and Thamnomycetoideae of Congo. Bull Jard Bot Bruxelles 31:109–154

    Article  Google Scholar 

  • Espada A, Rivera-Sagredo A, de la Fuente JM, Hueso-Rodríguez JA, Elson SW (1997) New cytochalasins from the fungus Xylaria hypoxylon. Tetrahedron 53:6485–6492

    Article  CAS  Google Scholar 

  • Friederichsen I (1977) The fate of the fungi collected by A. Möller in Brazil (1890–1895) and a list of specimens in the collection still existing. Mitt Inst Allg Bot Hamburg 15:99–104

    Google Scholar 

  • Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci USA 104:4979–4983

    Article  PubMed  CAS  Google Scholar 

  • Greenhalgh GN, Chesters CGC (1968) Conidiophore morphology in some British members of the Xylariaceae. Trans Brit Myc Soc 51:57–82

    Article  Google Scholar 

  • Gunawan S, Steffan B, Steglich W (1990) Xylaral, ein. Hydroxyphthalid-Derivat aus Fruchtkörpern von Xylaria polymorpha (Ascomycetes). Liebigs Ann Chem 1990:825–827

    Article  Google Scholar 

  • Guo LD, Hyde KD, Liew ECY (2000) Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 147:617–630. DOI 10.1046/j.1469-8137.2000.00716.x

    Article  CAS  Google Scholar 

  • Hellwig V, Ju Y-M, 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 Progr 4:39–54. DOI 10.1007/s11557-006-0108-6

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jong SC, Rogers JD (1972) Conidial stages of some Hypoxylon species. Washington State University College Agricultural Technical Bulletin 71:1–49

    Google Scholar 

  • Ju YM, Rogers JD (1996) A revision of the genus Hypoxylon [Mycologia Memoir no. 20]. APS Press, St. Paul, MN

    Google Scholar 

  • Læssøe T (1994) Index ascomycetum 1. Xylariaceae. Syst Ascomycetum 13:43–112

    Google Scholar 

  • Læssøe T (1997) Entonaema cinnabarina – en eksotisk kernesvamp. Svampe 36:21–22

    Google Scholar 

  • Lee JS, Kwan SK, Jung HS (2000) Phylogenetic analysis of Xylaria based on nuclear ribosomal ITS–5.8S–ITS2 sequences. FEMS Microbiol Lett 187:89–93

    Article  PubMed  CAS  Google Scholar 

  • Martin GW (1938) New or noteworthy fungi from Panama and Colombia II. Mycologia 30:431–441

    Article  Google Scholar 

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

    Google Scholar 

  • Möller A (1901) Phycomyceten und Ascomyceten, Untersuchungen aus Brasilien. Bot. Mitth. Tropen, Heft 9. Fischer, Jena

    Google Scholar 

  • Nitschke T (1867) Pyrenomycetes Germanici. Breslau

  • Petrini LE, Müller E (1986) Haupt- und Nebenfruchtformen europäischer Hypoxylon-Arten (Xylariaceae, Sphaeriales) und verwandter Pilze. Mycol Helv 1:501–627

    Google Scholar 

  • Polishook JD, Ondeyka JG, Dobrowski, AW, Peláez F, Platas G, Teran AM (2001) Biogeography and relatedness of Nodulisporium strains producing nodulisporic acid. Mycologia 93:1125–1137

    Article  CAS  Google Scholar 

  • Promputtha I, Lumyong S, Dhanasekaran V, McKenzie EH, Hyde KD, Jeewon R (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53:579–590

    Article  PubMed  Google Scholar 

  • Quang DN, Hashimoto T, Tanaka M, Stadler M, Asakawa Y (2004) Constituents of the inedible mushroom Hypoxylon rubiginosum. J Nat Prod 67:1152–1155. DOI 10.1021/np040063l CCC

    Article  PubMed  CAS  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 65:797–809. DOI 10.1016/j.phytochem.2005.02.006

    Article  CAS  Google Scholar 

  • Quang DN, Bach DD, Hashimoto T, Asakawa Y (2006) Chemical constituents of the Vietnamese inedible mushroom Xylaria intracolorata. Nat Prod Res 20:317–321

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Rogers JD (1981) Sarcoxylon and Entonaema (Xylariaceae). Mycologia 73:28–61

    Article  Google Scholar 

  • Rogers JD (1982) Entonaema liquescens: Description of the anamorph and thoughts on its systematic position. Mycotaxon 15:500–506

    Google Scholar 

  • Rogers JD (2000) Thoughts and musings about tropical Xylariaceae. Mycol Res 104:1412–1420

    Article  Google Scholar 

  • Rogers, JD, Callan BE, Rossman AY, Samuels GJ (1988) Xylaria (Sphaeriales, Xylariaceae) from Cerro de la Neblina, Venezuela. Mycotaxon 31:103–153

    Google Scholar 

  • Rogers JD, San Martín F, Ju YM (1996) Xylaria entosulphurea sp. nov. and neotypification of Entonaema globosum. Mycotaxon 58:483–487

    Google Scholar 

  • Sánchez-Jacomé M, Guzmán-Davalos L (2005) New records of ascomycetes from Jalisco, Mexico. Mycotaxon 92:177–191

    Google Scholar 

  • 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 

  • Sihanonth P, Thienhirun S, Whalley AJS (1998) Entonaema in Thailand. Mycol Res 102:458–460

    Article  Google Scholar 

  • Šrutka P, Pažoutova S, Kolařik M (2007) Daldinia decipiens and Entonaema cinnabarina as fungal symbionts of Xiphydria wood wasps. Mycol Res 111:224–231. DOI 10.1016/j.mycres.2006.10.006

    Article  PubMed  Google Scholar 

  • Stadler M, Fournier J (2006) Pigment chemistry, taxonomy and phylogeny of the Hypoxyloideae (Xylariaceae). Rev Iberoam Micol 23:160–170. (URL: http://www.reviberoammicol.com/2006-23/160170.pdf)

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

    CAS  Google Scholar 

  • Stadler M, Wollweber H, Mühlbauer A, Asakawa Y, Hashimoto T, Rogers JD, Ju YM, Wetzstein HG, Tichy HV (2001) Molecular chemotaxonomy of Daldinia and other Xylariaceae. Mycol Res 105:1190–1205

    Article  Google Scholar 

  • Stadler M, Wollweber H, Fournier J (2004a) A host-specific species of Hypoxylon from France, and notes on the chemotaxonomy of the “Hypoxylon rubiginosum complex”. Mycotaxon 90:187–211

    Google Scholar 

  • Stadler M, Ju YM, Rogers JD (2004b) Chemotaxonomy of Entonaema, Rhopalostroma and other Xylariaceae. Mycol Res 108:239–256. DOI 10.1017/S0953756204009347

    Article  PubMed  Google Scholar 

  • Stadler M, Quang DN, Tomita A, Hashimoto T, Asakawa Y (2006) Production of bioactive metabolites during stromatal ontogeny of Hypoxylon fragiforme. Mycol Res 110:811–820. DOI 10.1016/j.mycres.2006.03.013

    Article  PubMed  CAS  Google Scholar 

  • Stadler M, Mayer-Bartschmid A, Seip S, Bitzer J, Müller H, Benet-Buchholz J, Gantner F, Tichy HV, Reinemer P, Bacon KB (2007a) Cinnabaramides A-G, lactacystin and salinosporamide analogues from a terrestrial Streptomyces species. J Nat Prod 70:246–252. DOI 10.1021/np060162u

    Article  PubMed  CAS  Google Scholar 

  • Stadler M, Fournier J, Quang DN, Akulov AY (2007b) Metabolomic studies on the chemical ecology of the Xylariaceae (Ascomycota). Nat Prod Comm 2:287–304

    CAS  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 Hedw 80:25–43. DOI 10.1127/0029-5035/2005/0080-0025

    Article  Google Scholar 

  • Tulasne L, Tulasne C (1863) Selecta fungorum Carpologia. II. English translation by W. B. Grove 1931. Oxford University Press, Oxford

  • van Brummelen J (1967) A world-monograph of the genera Ascobolus and Saccobolus (Ascomycetes, Pezizales). Persoonia, supplement vol. I, Rijksherbarium, Leiden

  • Wang XN, Tan RX, Wang F, Steglich W, Liu JK (2005a) The first isolation of a phlegmacin type pigment from the ascomycete Xylaria euglossa. Z Naturforsch 60b:333–336

    Google Scholar 

  • Wang XN, Tan RX, Liu JK (2005b) Xylactam, a new nitrogen-containing compound from the fruiting bodies of ascomycete Xylaria euglossa. J Antibiot 58:268–270

    PubMed  CAS  Google Scholar 

  • Whalley AJS, Edwards RL (1995) Secondary metabolites and systematic arrangement within the Xylariaceae. Can J Bot 73(Suppl. 1):S802–S810

    Article  CAS  Google Scholar 

  • Wollweber H, Stadler M (2001) Zur Kenntnis der Gattung Daldinia in Deutschland und Europa. Z Mykol 67:3–53

    Google Scholar 

Download references

Acknowledgements

Our warmest thanks go to Burghard Hein and Harrie Sipman (B), Genevieve Lewis-Gentry (FH), Anna-Lena Anderberg (S), Begoña Aguirre-Hudson (K), Ellen Bloch (NY), Erin McCray (BPI), Laura Guzmán-Dávalos (GUAD) and all other curators of public herbaria, for kindly sending us specimens, and to Dagmar Triebel (M), also for help with international loan transactions. We acknowledge the input by Régis Courtecuisse, Lille, for facilitating collection work in the French West Indies. Furthermore, we thank Jack D. Rogers, Francoise Candoussau, Jean Louis Cheype and Ralph Mangelsdorff, for providing us with specimens, and Wolfgang Steglich (Munich, Germany) and Norbert Arnold (Leibniz Institute for Plant Biochemistry, Halle/Saale, Germany) for providing us with a standard of xylaral. Expert technical assistance by Dirk Müller (InterMed) for recording HPLC-MS spectra, and by Beata Schmieschek and Michael Benfer (dto.) for assistance in handling the cultures and performing HPLC-DAD analyses, is also gratefully acknowledged. Finally, we thank two anonymous referees for their valuable comments, which substantially improved our manuscript.

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Authors and Affiliations

  1. InterMed Discovery GmbH, Otto-Hahn-Strasse 15, 44227, Dortmund, Germany

    Marc Stadler

  2. Lehrstuhl für Pflanzensystematik, Department Mycology, University of Bayreuth, Universitätstrasse 30, NW1, 95440, Bayreuth, Germany

    Marc Stadler

  3. Las Muros, 09420, Rimont, France

    Jacques Fournier

  4. Institute of Biology, University of Copenhagen, Universitetsparken 15, DK-2100, Copenhagen Ø, Denmark

    Thomas Læssøe

  5. AscoFrance, 64 route de Chizé, 79360, Villiers-en-Bois, France

    Christian Lechat

  6. LUFA-ITL-GmbH, Dr.-Hell-Str. 6, 24107, Kiel, Germany

    Hans-Volker Tichy

  7. Institut für Ökologie, Evolution und Diversität, J.W. Goethe-Universität Frankfurt am Main, Siesmayerstr. 71-73, 60323, Frankfurt am Main, Germany

    Meike Piepenbring

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  1. Marc Stadler
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Correspondence to Marc Stadler.

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Taxonomic novelty

Xylaria mesenterica (Möller) M. Stadler, Læssøe & J. Fournier.

This paper is dedicated to the memory of our colleague Jean-F. Magni.

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Stadler, M., Fournier, J., Læssøe, T. et al. Recognition of hypoxyloid and xylarioid Entonaema species and allied Xylaria species from a comparison of holomorphic morphology, HPLC profiles, and ribosomal DNA sequences. Mycol Progress 7, 53–73 (2008). https://doi.org/10.1007/s11557-008-0553-5

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