Global diversity and taxonomy of the Auricularia auricula-judae complex (Auriculariales, Basidiomycota)

Abstract

Auricularia auricula-judae was previously considered a single species, but was recently demonstrated to be a species complex. The economically important, cultivated Auricularia mushrooms are included in the complex. Two species are cultivated, but have been treated as a single species: A. auricula-judae. Fifty samples of so-called A. auricula-judae from Asia, Europe, and North America were analyzed using morphology and molecular phylogeny. Phylogenetic analyses were carried out by ITS sequence and combined ITS, LSU, and rpb2 sequence, and 16 ITS, 16 LSU, and 16 rpb2 sequences were newly generated. Seven species in the complex were delineated, including three species new to science: Auricularia angiospermarum, A. minutissima, and A. tibetica. Illustrated description of the three new species and discussions in relation to other species are introduced in this paper. Auricularia heimuer is the most extensively cultivated species of Auricularia. Auricularia villosula is also cultivated, but has been named by the mushroom production industry A. heimuer. The size of basidiospores and presence or absence of medulla are important characters for differentiating the species within the complex, and ITS sequence data is a sensitive marker to discriminate species. A synoptic table of comparison of species in the complex is provided including the most important characters of the seven species.

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References

  1. Bandara AR, Chen J, Karunarathna S, Hyde KD, Kakumyan P (2015) Auricularia thailandica sp. nov. (Auriculariaceae, Auriculariales) a widely distributed species from southeastern Asia. Phytotaxa 208:147–156. doi:10.11646/phytotaxa.208.2.3

    Article  Google Scholar 

  2. Boulet B (2003) Les Champignons des Arbres de l'Est de l'Amérique du Nord. Publications du Québec, Québec, p 744

    Google Scholar 

  3. Büttner E, Ullrich R, Strittmatter E, Piontek K, Plattner DA, Hofrichter M, Liers C (2015) Oxidation and nitration of mononitrophenols by a DyP-type peroxidase. Arch Biochem Biophys 574:86–92

    Article  PubMed  Google Scholar 

  4. Dai YC, Yang ZL (2008) A revised checklist of medicinal fungi in China. Mycosystema 27:801–824

    Google Scholar 

  5. Dai YC, Yang ZL, Cui BK, Yu CJ, Zhou LW (2009) Species diversity and utilization of medicinal mushrooms and fungi in China (Review). Int J Med Mushrooms 11:287–302. doi:10.1615/IntJMedMushr.v11.i3.80

    Article  Google Scholar 

  6. Duncan EG, Macdonald JA (1967) Micro-evolution in Auricularia auricula. Mycologia 59:803–818

    CAS  Article  PubMed  Google Scholar 

  7. Felsenstein J (1985) Confidence intervals on phylogenetics: an approach using bootstrap. Evolution 39:783–791. doi:10.2307/2408678

    Article  Google Scholar 

  8. Govorova OK (1997) Heterobasidioid fungi of Russian Far East Reserves. Mikol Fitopatol 31:10–13 (In Russian)

    Google Scholar 

  9. Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  10. Huang NL, Lin ZB, Chen GL (2010) The Chinese medicinal and edible fungi. Science Press, Shanghai, p 1834

    Google Scholar 

  11. Jayasiri SC, Ariyawansa HA, Liu JK, Jones EBG, Hyde KD (2015). The faces of fungi database: fungal names linked with morphology, molecular and human attributes. Fungal Div (in press)

  12. Kalchbrenner K, Thümen FV (1881) Fungorum in itinere Mongolico a clar. G.N. Potanin et in China boreali a cl. Dr. Bretschneider lectorum enumeratio et descriptio. Mél Biol Acad Sci St Pétersb 11:57–67

    Google Scholar 

  13. Kobayasi Y (1942) On the genus Auricularia from Eastern Asia. Bull Cent Natl Mus Manchoukuo 4:19–35

    Google Scholar 

  14. Kobayasi Y (1981) The genus Auricularia. Bull Natl Sci Mus 7:41–67

    Google Scholar 

  15. Liers C, Bobeth C, Pecyna M, Ullrich R, Hofrichter M (2010) DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes. Appl Microbiol Biotechnol 85:1869–1879

    CAS  Article  PubMed  Google Scholar 

  16. Liers C, Arnstadt T, Ullrich R, Hofrichter M (2011) Patterns of lignin degradation and oxidative enzyme secretion by different wood- and litter-colonizing basidiomycetes and ascomycetes grown on beech-wood. FEMS Microbiol Ecol 78:91–102. doi:10.1111/j.1574-6941.2011.01144.x

    CAS  Article  PubMed  Google Scholar 

  17. Looney B, Birkebak J, Matheny PB (2013) Systematics of the genus Auricularia with an emphasis on species from the southeastern United States. N Am Fungi 8:1–25. doi:10.2509/naf2013.008.006

    Google Scholar 

  18. Lowy B (1951) A morphological basis for classifying the species of Auricularia. Mycologia 43:351–358. doi:10.2307/3755598

    Article  Google Scholar 

  19. Lowy B (1952) The genus Auricularia. Mycologia 44:656–692

    Google Scholar 

  20. Lyubarsky LV, Vasilyeva LN (1975) Derevorazrushayushchie griby Dal’nego Vostoka. Nauka, Novosibirsk, p 163, plates 53

    Google Scholar 

  21. Malysheva VF (2010) Rare and interesting species of heterobasidiomycetes from Russia. Fungi non delineati. Pars LIII. Edizioni Candusso I. Alassio - (SV). pp 92

  22. Malysheva VF, Bulakh EM (2014) Contribution to the study of the genus Auricularia (Auriculariales, Basidiomycota) in Russia. Novosti Sistematiki Nizshikh Rastenii 48:164–180

    Google Scholar 

  23. Mao XL (1998) Economic fungi of China. Science Press, Beijing, p 762

    Google Scholar 

  24. Matheny PB (2005) Improving phylogenetic inference of mushrooms using RPB1 and RPB2 sequences (Inocybe, Agaricales). Mol Phylogenet Evol 35:1–20. doi:10.1016/j.ympev.2004.11.014

    CAS  Article  PubMed  Google Scholar 

  25. Montoya-Alvarez AF, Hayakawa H, Minamya Y, Fukuda T (2011) Phylogenetic relationships and review of the species of Auricularia (Fungi: Basidiomycetes) in Colombia. Caldasia 33:55–66

    Google Scholar 

  26. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  27. Parmasto E, Parmasto I (1987) Variation of basidiospores in the Hymenomycetes and its significance to their taxonomy. Bibl Mycol 115:1–168

    Google Scholar 

  28. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A (2010) How many bootstrap replicates are necessary? J Comput Biol 17:337–354. doi:10.1089/cmb.2009.0179

    CAS  Article  PubMed  Google Scholar 

  29. Petersen JH (1996) Farvekort. The Danish Mycological Society’s colour-chart. Foreningen til Svampekundskabens Fremme, Greve, p 6

    Google Scholar 

  30. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:10.1093/bioinformatics/14.9.817

    CAS  Article  PubMed  Google Scholar 

  31. Raitviir A (1967) Keys to the Heterobasidiomycetes of the USSR. Leningrad, pp 115 (In Russian)

  32. Reza MA, Jo WS, Park SC (2012) Comparative antitumor activity of jelly ear culinary-medicinal mushroom, Auricularia auricula-judae (Bull.) J. Schrot. (Higher Basidiomycetes) extracts against tumor cells in vitro. Int J Med Mushrooms 14:403–409. doi:10.1615/IntJMedMushr.v14.i4.80

    Article  PubMed  Google Scholar 

  33. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  Article  PubMed  Google Scholar 

  34. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. doi:10.1007/s13127-011-0056-0

    Article  Google Scholar 

  35. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446

    CAS  Article  PubMed  Google Scholar 

  36. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Massachusetts

    Google Scholar 

  37. Tai FL (1979) Sylloge Fungorum Sinicorum. Science Press, Beijing, p 1527

    Google Scholar 

  38. Teng SC (1939) A contribution to our knowledge of the higher fungi of China. National Institute of Zoology and Botany, Academia Sinica, Nanking, p 614

    Google Scholar 

  39. Teng SC (1963) Fungi of China. Science Press, Beijing, p 808

    Google Scholar 

  40. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  41. White TJ, Bruns T, Lee S, Taylor J (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, San Diego, pp 315–322

    Google Scholar 

  42. Wu F, Yuan Y, Malysheva VF, Du P, Dai YC (2014) Species clarification of the most important and cultivated Auricularia mushroom “Heimuer”: evidence from morphological and molecular data. Phytotaxa 186:241–253. doi:10.11646/phytotaxa.186.5.1

    Article  Google Scholar 

  43. Wu F, Yuan Y, Rivoire B, Dai YC (2015) Phylogeny and diversity of the Auricularia mesenterica (Auriculariales, Basidiomycota) complex. Mycol Prog 14:42. doi:10.1007/s11557-015-1065-8

    Article  Google Scholar 

  44. Zeng WC, Zhang Z, Gao H, Jia LR, Chen WY (2012) Characterization of antioxidant polysaccharides from Auricularia auricula using microwave-assisted extraction. Carbohydr Polym 89:694–700

    CAS  Article  PubMed  Google Scholar 

  45. Zhang JX, Chen Q (2015) History, current situation and trend of edible fungi industry development. Mycosystema 34:524–540

Download references

Acknowledgments

The authors are grateful to Drs. Beatriz Ortiz-Santana (Madison, WI, USA), Tsuyoshi Hosoya (TNS, Japan), Michal Tomsovsky (Brno, Czech Republic), Pertii Salo (Helsinki, Finland), Wanda Daley (Auckland, New Zealand), Arne Anderberg (Stockholm, Sweden), Bernard Rivoire (Orlienas, France), J.E. Taylor (UK), and Tie-Zheng Wei (Beijing, China) for loan or donations of specimens. The research was financed by the National Natural Science Foundation of China (Project No. 31372115). The Thailand Research Fund grant for taxonomy, phylogeny and biochemistry of Thai basidiomycetes (BRG 5580009) is thanked for partly supporting this study.

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Correspondence to Yu-Cheng Dai.

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Section Editor: Franz Oberwinkler

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Wu, F., Yuan, Y., He, SH. et al. Global diversity and taxonomy of the Auricularia auricula-judae complex (Auriculariales, Basidiomycota). Mycol Progress 14, 95 (2015). https://doi.org/10.1007/s11557-015-1113-4

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Keywords

  • Auriculariaceae
  • Edible mushroom
  • Multi-marker analysis
  • Taxonomy