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Research article - Peer-reviewed, 2020

Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi

Sanchez-Garcia, Marisol; Ryberg, Martin; Kalsoom Khan, Faheema; Varga, Torda; Nagy, László G.; Hibbett, David S.

Abstract

With ∼36,000 described species, Agaricomycetes are among the most successful groups of Fungi. Agaricomycetes display great diversity in fruiting body forms and nutritional modes. Most have pileate-stipitate fruiting bodies (with a cap and stalk), but the group also contains crust-like resupinate fungi, polypores, coral fungi, and gasteroid forms (e.g., puffballs and stinkhorns). Some Agaricomycetes enter into ectomycorrhizal symbioses with plants, while others are decayers (saprotrophs) or pathogens. We constructed a megaphylogeny of 8,400 species and used it to test the following five hypotheses regarding the evolution of morphological and ecological traits in Agaricomycetes and their impact on diversification: 1) resupinate forms are plesiomorphic, 2) pileate-stipitate forms promote diversification, 3) the evolution of gasteroid forms is irreversible, 4) the ectomycorrhizal (ECM) symbiosis promotes diversification, and 5) the evolution of ECM symbiosis is irreversible. The ancestor of Agaricomycetes was a saprotroph with a resupinate fruiting body. There have been 462 transitions in the examined morphologies, including 123 origins of gasteroid forms. Reversals of gasteroid forms are highly unlikely but cannot be rejected. Pileate-stipitate forms are correlated with elevated diversification rates, suggesting that this morphological trait is a key to the success of Agaricomycetes. ECM symbioses have evolved 36 times in Agaricomycetes, with several transformations to parasitism. Across the entire 8,400-species phylogeny, diversification rates of ectomycorrhizal lineages are no greater than those of saprotrophic lineages. However, some ECM lineages have elevated diversification rates compared to their non-ECM sister clades, suggesting that the evolution of symbioses may act as a key innovation at local phylogenetic scales.

Keywords

Agaricomycetes; diversification; ectomycorrhizal fungi; gasteroid forms; megaphylogeny

Published in

Proceedings of the National Academy of Sciences
2020, volume: 117, number: 51, pages: 32528-32534

Authors' information

Swedish University of Agricultural Sciences, Department of Forest Mycology and Plant Pathology
Clark University
Ryberg, Martin
Uppsala University
Kalsoom Khan, Faheema
Uppsala University
Varga, Torda
Hungarian Academy of Sciences
Nagy, László G.
Hungarian Academy of Sciences
Hibbett, David S.
Clark University

Associated SLU-program

SLU Network Plant Protection

UKÄ Subject classification

Microbiology
Ecology

Publication Identifiers

DOI: https://doi.org/10.1073/pnas.1922539117

URI (permanent link to this page)

https://res.slu.se/id/publ/109878