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Mycological Progress

, Volume 18, Issue 1–2, pp 175–185 | Cite as

Daldinia sacchari (Hypoxylaceae) from India produces the new cytochalasins Saccalasins A and B and belongs to the D. eschscholtzii species complex

  • Abolfazl Narmani
  • Sridhar Pichai
  • Perumal Palani
  • Mahdi Arzanlou
  • Frank Surup
  • Marc StadlerEmail author
Original Article

Abstract

Stromata of a Daldinia species were collected from half-burnt sugarcane stalks in South India. Based on a combination of morphological and chemotaxonomic evidence, the species was identified as the first recent record of Daldinia sacchari. While it was impossible to obtain cultures from the ascospores, the stromata were subjected to DNA extraction and DNA sequencing and secondary metabolites were analyzed by high-performance liquid chromatography coupled with diode array and mass spectrometric detection (HPLC-DAD/MS). The fruiting body extract was subjected to preparative HPLC for the isolation of secondary metabolites. Two new cytochalasins, for which we propose the trivial names saccalasins A and B, were elucidated besides two known cytochalasins and binaphthalene tetrol (BNT) by NMR spectroscopy and mass spectrometry. Whereas sequencing of housekeeping genes from the stromatal DNA unfortunately failed, an ITS DNA sequence was obtained from this species for the first time and compared to those of related Hypoxylaceae in a phylogenetic tree. The results indicate a close relationship of D. sacchari to the D. eschscholtzii complex, from which cytochalasins are also known as predominant stromatal metabolites. Phylogenetic analyses based on the ITS-rDNA barcode (which can only discriminate the Hypoxylaceae and other Sordariomycetes into species groups, rather than serve as a means of genus or species discrimination) confirmed that D. sacchari belongs to the D. eschscholtzii species complex. However, as with the majority of tropical Hypoxylaceae species, the availability of cultures that can be used to generate DNA sequence data that are more conclusive than ITS will be imperative to further narrow down the phylogenetic affinities of these fungi.

Keywords

Polyphasic taxonomy Secondary metabolites Sugarcane Xylariales 

Notes

Acknowledgements

Expert technical assistance by Cäcilia Bergmann is gratefully acknowledged. The Ministry of Science, Research and Technology (MSRT) of Iran is also gratefully acknowledged for the financial support. Furthermore, we are grateful to various colleagues at the HZI: Kathrin I. Mohr and Wera Collisi for conducting the bioassays and Christel Kakoschke for recording NMR spectra.

Supplementary material

11557_2018_1413_MOESM1_ESM.pdf (686 kb)
ESM 1 (PDF 685 kb)

References

  1. 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 112:251–270CrossRefGoogle Scholar
  2. Buchanan MS, Hashimoto T, Asakawa Y (1996) Cytochalasins from a Daldinia sp. of fungus. Phytochemistry 41(3):821–828CrossRefGoogle Scholar
  3. Chepkirui C, Matasyoh JC, Decock C, Stadler M (2017) Two cytotoxic triterpenes from cultures of a Kenyan Laetiporus sp. (Basidiomycota). Phytochem Lett 20:106–110CrossRefGoogle Scholar
  4. Child M (1932) The genus Daldinia. Ann Mo Bot Gard 19:429–496CrossRefGoogle Scholar
  5. Daranagama DA, Hyde KD, Sir EB, Thambugala KM, Tian Q, Samarakoon MC, McKenzie EHC, Jayasiri SC, Tibpromma S, Bhat JD, Liu X, Stadler M (2018) Towards a natural classification and backbone tree for Graphostromataceae, Hypoxylaceae, Lopadostomataceae and Xylariaceae. Fungal Divers 88:1–165CrossRefGoogle Scholar
  6. Davey ML (2010) Annellosporium nemorosum gen. et sp. nov., an annellidic anamorph with phylogenetic affinities to the genus Daldinia (Xylariales). Karstenia 50:1–10CrossRefGoogle Scholar
  7. Helaly SE, Thongbai B, Stadler M (2018) Diversity of biologically active secondary metabolites from endophytic and saprotrophic fungi of the ascomycete order Xylariales. Nat Prod Rep, in press ( https://doi.org/10.1039/c8np00010g)
  8. Hsieh HM, Ju YM, Rogers JD (2005) Molecular phylogeny of Hypoxylon and closely related genera. Mycologia 97:844–865CrossRefGoogle Scholar
  9. Johannesson H, Laessøe T, Stenlid J (2000) Molecular and morphological investigation of the genus Daldinia in Northern Europe. Mycol Res 104:275–280CrossRefGoogle Scholar
  10. Ju YM, Rogers JD, San Martín F (1997) A revision of the genus Daldinia. Mycotaxon 61:243–293Google Scholar
  11. Kuhnert E, Sir EB, Lambert C, Hyde KD, Hladki AI, Romero AI, Rohde M, Stadler M (2017) Phylogenetic and chemotaxonomic resolution of the genus Annulohypoxylon (Xylariaceae) including four new species. Fungal Divers 85(1):–43Google Scholar
  12. Nylander, J.A.A (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  13. 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 60:107–123CrossRefGoogle Scholar
  14. Rayner RW (1970) A mycological colour chart. Commonwealth Mycological Institute Kew and British Mycological SocietyGoogle Scholar
  15. Richter C, Helaly SE, Thongbai B, Hyde KD, Stadler M (2016) Pyristriatins A and B: Pyridino-cyathane antibiotics from the basidiomycete Cyathus cf. striatus. J Nat Prod 79:1684–1688CrossRefGoogle Scholar
  16. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  17. Sandargo B, Thongbai B, Stadler M, Surup F (2018) Cysteine-derived pleurotin congeners from the nematode-trapping basidiomycete Hohenbuehelia grisea. J Nat Prod 81:286–291CrossRefGoogle Scholar
  18. Skellam E (2017) The biosynthesis of cytochalasans. Nat Prod Rep 34(11):1252–1263CrossRefGoogle Scholar
  19. Sir EB, Lambert C, Wendt L, Hladki A, Romero A, Stadler M (2017) A new species of Daldinia (Xylariaceae) from the argentine subtropical montane forest. Mycosphere 7(9):1378–1388CrossRefGoogle Scholar
  20. Sir EB, Kuhnert E, Lambert C, Hladki AI, Romero AI, Stadler M (2016) New species and reports of Hypoxylon from Argentina recognized by a polyphasic approach. Mycol Prog 15:42CrossRefGoogle Scholar
  21. Stadler M, Wollweber H, Mühlbauer 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 77:379–429Google Scholar
  22. Stadler M, Hellwig V (2005) Chemotaxonomy of the Xylariaceae and remarkable bioactive compounds from Xylariales and their associated asexual stages. Recent Res Dev Phytochem 9:1–53Google Scholar
  23. Stadler M, Quang DN, Tomita A, Hashimoto T, Asakawa Y (2006) Production of bioactive metabolites during stromatal ontogeny of Hypoxylon fragiforme. Mycol Res 110:811–820CrossRefGoogle Scholar
  24. Stadler M, Fournier J, Læssøe T, Lechat C, Tichy HV, Piepenbring M (2008) Recognition of hypoxyloid and xylarioid Entonaema species from a comparison of holomorphic morphology, HPLC profiles, and ribosomal DNA sequences. Mycol Prog 7:53–73CrossRefGoogle Scholar
  25. Stadler M, Læssøe T, Fournier J, Decock C, Schmieschek B, Tichy HV, Peršoh D (2014) A polyphasic taxonomy of Daldinia (Xylariaceae). Stud Mycol 77:1–143CrossRefGoogle Scholar
  26. Triebel D, Peršoh D, Wollweber H, Stadler M (2005) Phylogenetic relationships among Daldinia, Entonaema and Hypoxylon as inferred from ITS nrDNA sequences. Nova Hedw 80:25–43CrossRefGoogle Scholar
  27. Vasilyeva L, Stadler M (2008) Pyrenomycetes of the Russian Far East 3. Three new Daldinia species (Xylariaceae). Mycotaxon 104:284–296Google Scholar
  28. Van der Gucht K (1994) The Xylariaceae of Papua New Guinea. Ph.D. dissertation. Univ. GentGoogle Scholar
  29. Wang J, Wang Z, Ju Z, Wan J, Liao S, Lin X, Liu Y (2015) Cytotoxic cytochalasins from marine-derived fungus Arthrinium arundinis. Planta Med 81:160–166CrossRefGoogle Scholar
  30. Wendt L, Sir EB, Kuhnert E, Heitkämper S, Lambert C, Hladki AI, Romero AI, Luangsa-ard JJ, Srikitikulchai P, Peršoh D, Stadler M (2018) Resurrection and emendation of the Hypoxylaceae, recognised from a multi-gene genealogy of the Xylariales. Mycol Prog 17:115–154CrossRefGoogle Scholar
  31. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: A guide to methods and applications. Academic Press, Inc, New York, pp 315–322Google Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Plant Protection Department, Agriculture FacultyUniversity of TabrizTabrizIran
  2. 2.Department of Microbial DrugsHelmholtz-Zentrum für Infektionsforschung GmbHBraunschweigGermany
  3. 3.Centre for Advanced Studies in BotanyUniversity of MadrasChennaiIndia
  4. 4.Mikrobielle WirkstoffeHelmholtz-Zentrum für InfektionsforschungBraunschweigGermany

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