Modern views on existing trends in evolution of agaricomycetes fruit bodies are summarized. The well-known evolutionary trends of basidial mushrooms, gasteromycetization and cyphellization, are outlined. Special attention is paid to coprinoidization, a recently recognized trend of evolution of agaricoid mushrooms. The coprinoidization, an ability of fruit bodies for accelerated ontogeny, which independently evolved in several evolutionary lines of fungi of the order Agaricales (families Agaricaceae, Bolbitiaceae and Psathyrellaceae), is a way of adaptation of basidial macromycetes to extreme conditions. It enables them to colonize substrates with considerably fluctuating water content. The most noticeable common feature of coprinoid fruit bodies is their fast autolysis or collapse after sporogenesis. The main morphological changes which make possible such a mode of adaptation as well as its advantages and preferences are considered. It is shown that this way of evolutionary adaptation is the most advantageous for fimicolous macromycetes but is also beneficial for mushrooms growing on other types of substrata. The present data about origin of the first coprinoid taxa of fungi and time of their origin are considered. The presumable connection with expansion of dry open grasslands followed by evolutionary radiation and diversification of large grazing mammals during the Miocene is indicated.

Keywords: coprinoidization, fruit bodies morphology, autolysis, evolution

Full text: PDF (Ukr) 2.94M

1. Agerer R. Lachnella-Crinipellis, Stigmatolemma-Fistulina: zwei Verwandschaftsreihen? Z. Mykol., 1978, 44: 51–70.
2. Baura G., Szaro T.M., Bruns T.D. Gastrosuillus laricinus is a recent derivative of Suillus grevillei: molecular evidence. Mycologia, 1992, 84(4): 592–597. https://doi.org/10.2307/3760328
3. Berbee M.L., Taylor J.W. Dating the evolutionary radiations of the true fungi. Can. J. Bot., 1993, 71: 1114–1127. https://doi.org/10.1139/b93-131
4. Binder M., Bresinsky A. Derivation of a polymorphic lineage of Gasteromycetes from boletoid ancestors. Mycologia, 2002, 94: 85–98. https://doi.org/10.1080/15572536.2003.11833251 https://www.ncbi.nlm.nih.gov/pubmed/21156480
5. Binder M., Hibbett D.S., Larsson K.H., Larsson E., Langer E., Langer G. The phylogenetic distribution of resupinate forms across the major clades of mushroom-forming fungi (Homobasidiomycetes). Syst. Biodiv., 2005, 3: 113–157. https://doi.org/10.1017/S1477200005001623
6. Binder M., Hibbett D.S., Molitoris H.P. Phylogenetic relationships of the marine gasteromycete Nia vibrissa. Mycologia, 2001, 93(4): 679–688. https://doi.org/10.2307/3761822
7. Bodensteiner P., Binder M., Moncalvo J.M., Agerer R., Hibbett D.S., Phylogenetic relationships of cyphelloid homobasidiomycetes. Mol. Phylogen. Evol., 2004, 33: 501–515. https://doi.org/10.1016/j.ympev.2004.06.007 https://www.ncbi.nlm.nih.gov/pubmed/15336682
8. Bruns T.D., Szaro T.M., Gardes M., Cullings K.W., Pan J.J., Taylor D.L., Horton D.R., Kretzer A., Garbelotto M., Li Y. A sequence database for the identification of ectomycorrhizal basidiomycetes by phylogenetic analysis. Mol. Ecol., 1998, 7: 257–272. https://doi.org/10.1046/j.1365-294X.1998.00337.x
9. Clémençon H. Cytology and Plectology of the Hymenomycetes, Stuttgart: J. Cramer, 2004, 488 pp.
10. Didukh Ya.P., Romashchenko K.Y., Futorna O.A. Ukr. Bot. J., 2016, 73(1): 21–32. https://doi.org/10.15407/ukrbotj73.01.021
11. Donk M.A. Notes on ‘Cyphellaceae’. I. Persoonia, 1959, 1: 25–110.
12. Donk M.A. A conspectus of the families of the Aphyllophorales. Persoonia, 1964, 3: 199–324.
13. Donk M.A. Progress in the study of the classification of higher basidiomycetes. In: Evolution in the higher basidiomycetes. Ed. R.H. Petersen, Knoxville: Univ. Tenessee Press, 1971, pp. 3–25.
14. Fries N. Untersuchungen über Sporenkeimung und Mycelentwiklung bodenbewohnender Hymenomyceten. Symb. Bot. Upsal., 1943, 6: 1–81.
15. Garnica S., Weiss M., Walther G., Oberwinkler F. Reconstructing the evolution of agarics from nuclear gene sequences and basidiospore ultrastructure. Mycol. Res., 2007, 111: 1019–1029. https://doi.org/10.1016/j.mycres.2007.03.019 https://www.ncbi.nlm.nih.gov/pubmed/18022533
16. Hallen H.E., Watling R., Adams G.C. Taxonomy and toxicity of Conocybe lactea and related species. Mycol. Res., 2003, 107(8): 969–979. https://doi.org/10.1017/S0953756203008190 https://www.ncbi.nlm.nih.gov/pubmed/14531619
17. Hibbett D.S. Trends in morphological evolution in homobasidiomycetes inferred using maximum likelihood: a comparison of binary and multistate approaches. Syst. Biol., 2004, 53: 889–903. https://doi.org/10.1080/10635150490522610 https://www.ncbi.nlm.nih.gov/pubmed/15764558
18. Hibbett D.S. After the gold rush, or before the flood? Evolutionary morphology of mushroom-forming fungi (Agaricomycetes) in the early 21st century. Mycol. Res., 2007, 111: 1001–1018. https://doi.org/10.1016/j.mycres.2007.01.012 https://www.ncbi.nlm.nih.gov/pubmed/17964768
19. Hibbett D.S., Binder M. Evolution of complex fruiting-body morphologies in homobasidiomycetes. Proc. Biol. Sci., 2002, 269: 1963–1969. https://doi.org/10.1098/rspb.2002.2123 https://www.ncbi.nlm.nih.gov/pubmed/12396494 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1691125
20. Hibbett D.S., Grimaldi D., Donoghue M.J. Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of homobasidiomycetes. Amer. J. Bot., 1997a, 84: 981–991. https://doi.org/10.2307/2446289 https://www.ncbi.nlm.nih.gov/pubmed/21708653
21. Hibbett D.S., Pine E.M., Langer E., Langer G., Donoghue M.J. Evolution of gilled mushrooms and puffballs inferred from ribosomal DNA sequences. Proc. Natl. Acad. Sci. USA, 1997b, 94: 12002–12006. https://doi.org/10.1073/pnas.94.22.12002 https://www.ncbi.nlm.nih.gov/pubmed/9342352 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC23683
22. Hibbett D.S., Thorn R.G. Basidiomycota: Homobasidiomycetes. In: Mycota. Systematics and evolution. Eds D.J. McLauhlin, E.G. McLauhlin, P.A. Lemke, Berlin: Springer Verlag, 2001, vol. 7, pp. 121–168. https://doi.org/10.1007/978-3-662-10189-6_5
23. Hopple J.S.Jr., Vilgalys R. Phylogenetic relationships in the mushroom genus Coprinus and dark-spored allies based on sequence data from the nuclear gene coding for the large ribosomal subunit RNA: divergent domains, outgroups, and monophyly. Mol. Phylogen. Evol., 1999, 13: 1–19. https://doi.org/10.1006/mpev.1999.0634 https://www.ncbi.nlm.nih.gov/pubmed/10508535
24. Janis C.M., Damuth J., Theodor J.M. Miocene ungulates and terrestrial primary productivity: where have all the browsers gone? Proc. Natl Acad. Sci. USA, 2000, 97: 7899–7904. https://doi.org/10.1073/pnas.97.14.7899 https://www.ncbi.nlm.nih.gov/pubmed/10884422 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC16642
25. Johnson J. Phylogenetic relationships within Lepiota sensu lato based on morphological and molecular data. Mycologia, 1999, 91(3): 443–458. https://doi.org/10.2307/3761345
26. Kües U. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microb. Mol. Biol. Rev., 2000, 64: 316–353. https://doi.org/10.1128/MMBR.64.2.316-353.2000 https://www.ncbi.nlm.nih.gov/pubmed/10839819 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC98996
27. Kühner R. Les Hyménomycètes agaricoides (Agaricales, Tricholomatales, Pluteales, Russulales). Bull. Soc. Linn. Lyon., 1980, Num. spéc. 49: 1–1027.
28. Larsson K.H., Larsson E., Kõljalg U. High phylogenetic diversity among corticioid homobasidiomycetes. Mycol. Res., 2004, 108: 983–1002. https://doi.org/10.1017/S0953756204000851 https://www.ncbi.nlm.nih.gov/pubmed/15506012
29. Matheny P.B., Curtis J.M., Hofstetter V., Aime M.C., Moncalvo J.M., Ge Z.W., Yang Z.L., Slot J.C., Ammirati J.F., Baroni T.J., Bougher N.L., Hughes K.W., Lodge D.J., Kerrigan R.W., Seidl M.T., Aanen D.K., DeNitis M., Daniele G.M., Desjardin D.E., Kropp B.R., Norvell L.L., Parker A., Vellinga E.C., Vilgalys R., Hibbett D.S. Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia, 2006, 98: 982–995. https://doi.org/10.1080/15572536.2006.11832627 https://www.ncbi.nlm.nih.gov/pubmed/17486974
30. Moncalvo J.M., Vilgalys R., Redhead S.A., Johnson J.E., James T.Y. One hundred and seventeen clades of euagarics. Mol. Phylogen. Evol., 2002, 23: 357–400. https://doi.org/10.1016/S1055-7903(02)00027-1
31. Nagy L.G., Házi J., Szappanos B.B., Koscubé S., Bálint B., Rákhely G., Vágvölgyi C., Papp T. The evolution of defense mechanisms correlate with the explosive diversification of autodigesting Coprinellus mushrooms (Agaricales, Fungi). Systematic Biology Advance Access, 2012, vol. 61, 13 pp., available at: http://sysbio.oxfordjournals.org/ (accessed 31 January 2012).
32. Nagy L.G., Koscubé S., Papp T., Vágvölgyi C. Phylogeny and character evolution of the coprinoid mushroom genus Parasola as inferred from LSU and ITS nrDNA sequence data. Persoonia, 2009, 22: 28–37. https://doi.org/10.3767/003158509X422434 https://www.ncbi.nlm.nih.gov/pubmed/20198135 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2789540
33. Nagy L.G., Urban A., Örstadius L., Papp T., Larsson E., Vágvölgyi C. The evolution of autodigestion in the mushroom family Psathyrellaceae (Agaricales) inferred from Maximum Likelihood and Bayesian methods. Mol. Phylogenet. Evol., 2010, 57: 1037–1048. https://doi.org/10.1016/j.ympev.2010.08.022 https://www.ncbi.nlm.nih.gov/pubmed/20801224
34. Nagy G.L., Walther G., Házi J., Vágvölgyi C., Papp T. Understanding the evolutionary processes of fungal fruiting bodies: correlated evolution and divergence times in the Psathyrellaceae. Syst. Biol., 2011, 60(3): 303–317. https://doi.org/10.1093/sysbio/syr005 https://www.ncbi.nlm.nih.gov/pubmed/21368323
35. Oberwinkler F. The significance of the morphology of the basidium in the phylogeny of basidiomycetes. In: Basidium and Basidiocarp. Eds K. Wells, E.K. Wells, New York: Springer Verlag, 1982, pp. 9–35. https://doi.org/10.1007/978-1-4612-5677-9_2
36. Padamsee M., Matheny P.B., Dentinger B.T.M., McLaughlin D.J. The mushroom family Psathyrellaceae: Evidence for large-scale polyphyly of the genus Psathyrella. Mol. Phylogen. and Evol., 2008, 46: 415–429. https://doi.org/10.1016/j.ympev.2007.11.004 https://www.ncbi.nlm.nih.gov/pubmed/18248744
37. Peintner U., Bougher N.L., Castellano M.A., Moncalvo J.M., Moser M.M., Trappe J.M., Vilgalys R. Multiple origins of sequestrate fungi related to Cortinarius (Cortinariaceae). Amer. J. Bot., 2001, 88: 2168–2179. https://doi.org/10.2307/3558378 https://www.ncbi.nlm.nih.gov/pubmed/21669649
38. Poinar G.O., Singer R. Upper Eocene gilled mushroom from the Dominican Republic. Science, 1990, 248: 1099–1101. https://doi.org/10.1126/science.248.4959.1099 https://www.ncbi.nlm.nih.gov/pubmed/17733372
39. Redhead S.A., Vilgalys R., Moncalvo J.M., Johnson J., Hopple J.S. Coprinus Persoon and the disposition of Coprinus species sensu lato. Taxon, 2001, 50: 203–241. https://doi.org/10.2307/1224525
40. Singer R. The Agaricales in modern taxonomy, Konigstein: Koeltz Sci. Books, 1986, 981 pp.
41. Sussman A.S. Longevity and survivility of fungi. In: The Fungi. An Advanced Treatise. Eds G.C. Ainsworth, A.S. Sussman, New York: Acad. Press, 1968, vol. 3, pp. 447–486.
42. Thiers H.D. The secotioid syndrome. Mycologia, 1984, 76: 1–8. https://doi.org/10.2307/3792830
43. Tóth A., Hausknecht A., Krisai-Greilhuber I., Papp T., Vágvölgyi C., Nagy L.G. Iteratively refined guide trees help improving alignment and phylogenetic inference in the mushroom family Bolbitiaceae. PLoS ONE, 2013, 8(2): 1–14. https://doi.org/10.1371/journal.pone.0056143 https://www.ncbi.nlm.nih.gov/pubmed/23418526 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3572013
44. Watling R. Germination of basidiospores and production of fructifications of members of the agaric family Bolbitiaceae using herbarium material. Nature, 1963, 197: 717–718. https://doi.org/10.1038/197717a0
45. Zmitrovich I.V., Wasser S.P. Modern view on the origin and phylogenetic reconstruction of homobasidiomycetes fungi. In: Evolutionary theory and processes: modern horizons, papers in honour of Eviatar Nevo. Ed. S.P. Wasser, Kluwer: Kluwer Acad. Publ., 2004, pp. 231–263. https://doi.org/10.1007/978-94-017-0443-4_13