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Progress on the phylogeny of the Omphalotaceae: Gymnopus s. str., Marasmiellus s. str., Paragymnopus gen. nov. and Pusillomyces gen. nov.

Abstract

Omphalotaceae is the family of widely distributed and morphologically diverse marasmioid and gymnopoid agaric genera. Phylogenetic studies have included the family in Agaricales, grouping many traditionally and recently described genera of saprotrophic or parasitic mushroom-producing fungi. However, some genera in Omphalotaceae have not reached a stable concept that reflects monophyletic groups with identifiable morphological circumscription. This is the case of Gymnopus and Marasmiellus, which have been the target of two opposing views: (1) a more inclusive Gymnopus encompassing Marasmiellus, or (2) a more restricted Gymnopus (s. str.) while Marasmiellus remains a distict genus; both genera still await a more conclusive phylogenetic hypothesis coupled with morphological recognition. Furthermore, some new genera or undefined clades need more study. In the present paper, a phylogenetic study was conducted based on nrITS and nrLSU in single and multilocus analyses including members of the Omphalotaceae, more specifically of the genera belonging to the /letinuloid clade. The resulting trees support the view of a more restricted Gymnopus and a distinct Marasmiellus based on monophyletic and strongly supported clades on which their morphological circumscriptions and taxonomic treatments are proposed herein. The results also provide evidence for the description of two new genera: Paragymnopus and Pusillomyces. Pusillomyces manuripioides sp. nov. (type species of the genus) is described with morphological description, taxonomic and ecological remarks, and illustrations.

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References

  1. Antonín V, Noordeloos ME (1997) A monograph of Marasmius, Collybia and related genera in Europe. Part 2: Collybia, Gymnopus, Rhodocollybia, Crinipellis, Chaetocalathus, and additions to Marasmiellus. Libri Botanici 17:1–256

    Google Scholar 

  2. Antonín V, Noordeloos ME (2010) A monograph of marasmioid and collybioid fungi in Europe. IHW-Verlag, Eching

    Google Scholar 

  3. Antonín V, Halling RE, Noordeloos ME (1997) Generic concepts within the groups of Marasmius and Collybia sensu lato. Mycotaxon 63:359–368

    Google Scholar 

  4. Antonín V, Ryoo R, Ka K-H (2014) Marasmioid and gymnopoid fungi of the Republic of Korea. 7. Gymnopus sect. Androsacei. Mycol Prog 13:703–718. https://doi.org/10.1007/s11557-013-0953-z

    Article  Google Scholar 

  5. Berkeley MJ (1856) Decades of fungi. Decades LI - LIV. Rio Negro fungi. Hooker's J Bot Kew Gard Misc 8:129–144

    Google Scholar 

  6. Binder M, Hibbett DS (2002) Higher-level phylogenetic relationships of Homobasidiomycetes (mushroom-forming fungi) inferred from four rDNA regions. Mol Phylogenet Evol 22:76–90. https://doi.org/10.1006/mpev.2001.1043

    Article  CAS  PubMed  Google Scholar 

  7. César E, Bandala VM, Montoya L, Ramos A (2018) A new Gymnopus species with rhizomorphs and its record as nesting material by birds (Tyrannideae) in the subtropical cloud forest from eastern Mexico. MycoKeys 42:21–34. https://doi.org/10.3897/mycokeys.42.28894

    Article  Google Scholar 

  8. Coimbra VRM, Pinheiro FGB, Wartchow F, Gibertoni TB (2015) Studies on Gymnopus sect. Impudicae (Omphalotaceae, Agaricales) from Northern Brazil: two new species and notes on G. montagnei. Mycol Prog 14:110. https://doi.org/10.1007/s11557-015-1131-2

    Article  Google Scholar 

  9. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dennis RWG (1961) Fungi venezuelani: IV, Agaricales. Kew Bull 15:67–156

    Article  Google Scholar 

  11. Dentinger BTM, Gaya E, O’Brien H, Suz LM, Lachlan R, Díaz-Valderrama JR, Koch RA, Aime MC (2016) Tales from the crypt: genome mining from fungarium specimens improves resolution of the mushroom tree of life. Biol J Linn Soc 117:11–32. https://doi.org/10.1111/bij.12553

    Article  Google Scholar 

  12. Desjardin DE, Gordon SA, Petersen RH (1993) Observations on two rhizomorph-forming species of Marasmiellus. Mycol Res 97:111–122. https://doi.org/10.1016/S0953-7562(09)81147-7

    Article  Google Scholar 

  13. Dutta AK, Wilson AW, Antonín V, Acharya K (2015) Taxonomic and phylogenetic study on gymnopoid fungi from Eastern India. I. Mycol Prog 14:1–18. https://doi.org/10.1007/s11557-015-1094-3

    Article  Google Scholar 

  14. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113. https://doi.org/10.1186/1471-2105-5-113

    Article  CAS  Google Scholar 

  15. Halling RE (1983) The genus Collybia (Agaricales) in the northeastern United States and adjacent Canada. Mycol Mem 8:1–148

    Google Scholar 

  16. Halling RE (1996) Notes on Collybia. V. Gymnopus section Levipedes in tropical South America with comments on Collybia. Brittonia 48:487–494. https://doi.org/10.2307/2807862

    Article  Google Scholar 

  17. Hughes KW, Mather DA, Petersen RH (2010) A new genus to accommodate Gymnopus acervatus (Agaricales). Mycologia 102:1463–1478. https://doi.org/10.3852/09-318

    Article  PubMed  Google Scholar 

  18. Kämmerer A, Besl H, Bresinsky A (1985) Omphalotaceae fam. nov. und Paxillaceae, ein chemotaxonomischer Vergleich zweier Pilzfamilien der Boletales. Plant Syst Evol 150:101–118. https://doi.org/10.1007/BF00985571

    Article  Google Scholar 

  19. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kühner R (1933) Etudes sur le genre Marasmius. Botaniste 25:57–116

  21. Kühner R (1980) Les hyménomycetes agaricoides (Agaricales, Tricholomatales, Pluteales, Russulales). Bull Soc Linn Lyon 49:1–1027

    Google Scholar 

  22. Küppers H (2002) Atlas de los colores. Editorial Blume, Barcelona

    Google Scholar 

  23. Mata JL, Petersen RH, Hughes KW (2001) The genus Lentinula in the Americas. Mycologia 93:1102–1112. https://doi.org/10.2307/3761671

    Article  Google Scholar 

  24. Mata JL, Hughes KW, Petersen RH (2004a) Phylogenetic placement of Marasmiellus juniperinus. Mycoscience 45:214–221. https://doi.org/10.1007/S10267-004-0170-3

    Article  CAS  Google Scholar 

  25. Mata JL, Halling RE, Hughes KW, Petersen RH (2004b) Rhodocollybia in neotropical montane forests. Mycol Prog 3:337–352. https://doi.org/10.1007/s11557-006-0104-x

    Article  Google Scholar 

  26. Mata JL, Hughes KW, Petersen RH (2006) An investigation of /omphalotaceae (Fungi: Euagarics) with emphasis on the genus Gymnopus. Sydowia 58:191–189

    Google Scholar 

  27. Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo J-M, Ge ZW, Yang ZL, Slot JC, Ammirati JF, Baroni TJ, Bougher NL, Hughes KW, Lodge DJ, Kerrigan RW, Seidl MT, Aanen DK, DeNitis M, Daniele GM, Desjardin DE, Kropp BR, Norvell LL, Parker A, Vellinga EC, Vilgalys R, Hibbett DS (2006) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98:984–997. https://doi.org/10.1080/15572536.2006.11832627

    Article  Google Scholar 

  28. Moncalvo J-M, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R (2000) Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Syst Biol 49:278–305. https://doi.org/10.1093/sysbio/49.2.278

    Article  CAS  PubMed  Google Scholar 

  29. Moncalvo J-M, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clémençon H, Miller OK Jr (2002) One hundred and seventeen clades of euagarics. Mol Phyl Evol 23:357–400. https://doi.org/10.1016/S1055-7903(02)00027-1

    Article  CAS  Google Scholar 

  30. Murrill WA (1916) Agaricaceae Tribe Agariceae. N Am Flora 9:297–374

    Google Scholar 

  31. Nylander JAA (2004) Mr. Modeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

  32. Pegler DN (1983) The genus Lentinula (Tricholomataceae tribe Collybieae). Sydowia 36:227–239

    Google Scholar 

  33. Petersen RH, Hughes KW (2016) Micromphale sect. Perforantia (Agaricales, Basidiomycetes); expansion and phylogenetic placement. MycoKeys 18:1–122. https://doi.org/10.3897/mycokeys.18.10007

    Article  Google Scholar 

  34. Petersen RH, Hughes KW (2017) An investigation on Mycetinis (Euagarics, Basidiomycota). MycoKeys 24:1–138. https://doi.org/10.3897/mycokeys.24.12846

    Article  Google Scholar 

  35. Petersen RH, Hughes KW (2019) Two additional species of Gymnopus (Euagarics, Basidiomycotina). MycoKeys 45:1–24. https://doi.org/10.3897/mycokeys.45.29350

    Article  Google Scholar 

  36. Retnowati A (2018) The species of Marasmiellus (Agaricales: Omphalotaceae) from Java and Bali. Gard Bull (Singapore) 70:191–258

    Article  Google Scholar 

  37. Robert V, Vu D, Amor ABH, van de Wiele N, Brouwer C, Jabas B, Szoke S, Dridi A, Triki M, ben Daoud S, Chouchen O, Vaas L, de Cock A, Stalpers JA, Stalpers D, Verkley GJM, Groenewald M, dos Santos FB, Stegehuis G, Li W, Wu L, Zhang R, Ma J, Zhou M, Gorjón SP, Eurwilaichitr L, Ingsriswang S, Hansen K, Schoch C, Robbertse B, Irinyi L, Meyer W, Cardinali G, Hawksworth DL, Taylor JW, Crous PW (2013) MycoBank gearing up for new horizons. IMA Fungus 4:371–379. https://doi.org/10.5598/imafungus.2013.04.02.16

    Article  PubMed  PubMed Central  Google Scholar 

  38. Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  39. Sandoval-Leiva PA, McDonald JV, Thorn RG (2016) Gymnopanella nothofagi, a new genus and species of gymnopoid fungi (Omphalotaceae) from Chilean Nothofagus forests. Mycologia 108:820–827. https://doi.org/10.3852/15-303

    Article  CAS  PubMed  Google Scholar 

  40. Singer R (1939) Phylogenie und Taxonomie der Agaricales. Schweiz Z Pilzk 17:71–73

    Google Scholar 

  41. Singer R (1960) Monographs of South American Basidiomycetes, especially those of the east slope of the Andes and Brazil. 3. Reduced marasmioid genera in South America. Sydowia 14:258–280

    Google Scholar 

  42. Singer R (1976) Marasmieae (Basidiomycetes – Tricholomataceae). Flora Neotrop Monogr 17:1–347

    Google Scholar 

  43. Singer R (1986) The Agaricales in modern taxonomy, 4th edn. Koeltz Scientific Books, Koenigstein

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  45. Vellinga EC, Kuyper TW, Ammirati J, Desjardin DE, Halling RE, Justo A, Læssøe T, Lebel T, Lodge DJ, Matheny BP, Methven AS, Moreau PA, Mueller GM, Noordeloos ME, Nuytinck J, Ovrebo CL, Verbeken A (2015) Six simple guidelines for introducing new genera of fungi. IMA Fungus 6:65–68

    Article  Google Scholar 

  46. White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Sninsky DH, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc, New York, pp 315–322

    Google Scholar 

  47. Wilson AW, Desjardin E (2003) A phylogenetic analysis of the Gymnopus/ Marasmiellus complex using nLSU sequence data. Abstracts, Mycological Society of America 99

  48. Wilson AW, Desjardin DE (2005) Phylogenetic relationships in the gymnopoid and marasmioid fungi (Basidiomycetes, euagarics clade). Mycologia 97:667–679. https://doi.org/10.1080/15572536.2006.11832797

    Article  CAS  PubMed  Google Scholar 

  49. Wilson AW, Desjardin DE, Horak E (2004) Agaricales of Indonesia. 5. The genus Gymnopus from Java and Bali. Sydowia 56:137–210

    Google Scholar 

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Acknowledgments

The authors thank the INPA Herbarium for contributing to this publication, R.H.S.F. Cruz for doing the illustrations, Dr. Tarciso de Sousa Filgueiras for reviewing the names in Latin, Dr. Genevieve Gates (Honorary Associate in Mycology and Forest Ecology, Tasmanian Institute of Agriculture) for reviewing the English writing and the anonymous reviewers for relevant contribution to this paper. The authors also thank the financial and logistical support from the Fundação de Amparo à Pesquisa do Estado do Amazonas – FAPEAM, the Centro de Estudos Integrados da Biodiversidade Amazônica (INCT-CENBAM), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Biodiversity Research Program (PPBio), and the Japan Science and Technology Agency /Japan International Cooperation Agency - Science and Technology Research Partnership for Sustainable Development (JST/JICA-SATREPS). Study registered in SISGen (Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado) number A44535D.

Funding

This study was supported by “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES” with a scholarship from “Programa Nacional de Pós-doutorado – PNPD” granted to J.J.S. de Oliveira, post-doctoral fellow of DIBOT, and other to T.S. Cabral, post-doctoral fellow of DIGEN, INPA. For R. Vargas-Isla, a scholarship from “Ação Orçamentária – MCTIC/PT 19.571.2021.20VD.0001 (C, T & I para Pesquisa, Desenvolvimento, Conservação, Valoração e Sustentabilidade dos Recursos Naturais Brasileiros).

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Correspondence to Jadson J. S. Oliveira.

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Oliveira, J.J.S., Vargas-Isla, R., Cabral, T.S. et al. Progress on the phylogeny of the Omphalotaceae: Gymnopus s. str., Marasmiellus s. str., Paragymnopus gen. nov. and Pusillomyces gen. nov.. Mycol Progress 18, 713–739 (2019). https://doi.org/10.1007/s11557-019-01483-5

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Keywords

  • Agaricales
  • Amazon forest
  • Marasmioid
  • Gymnopoid
  • Plant pathogen
  • Taxonomy