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Title: Megaphylogeny resolves global patterns of mushroom evolution

Abstract

Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfil diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.

Authors:
 [1];  [1]; ORCiD logo [1]; ORCiD logo [2];  [3]; ORCiD logo [4];  [2]; ORCiD logo [5]; ORCiD logo [6];  [7];  [8];  [9];  [10];  [8];  [11];  [12];  [13];  [1]; ORCiD logo [14];  [8] more »; ORCiD logo [15];  [16];  [17];  [7];  [18]; ORCiD logo [8];  [19];  [3];  [20];  [21];  [1];  [5];  [22];  [8];  [23];  [24];  [8];  [5];  [8];  [25];  [24];  [18];  [26];  [27];  [28];  [5];  [8];  [29];  [30];  [31]; ORCiD logo [32];  [33]; ORCiD logo [34];  [35];  [36]; ORCiD logo [37];  [5];  [33];  [38]; ORCiD logo [32];  [3]; ORCiD logo [1] « less
+ Show Author Affiliations
  1. Hungarian Academy of Sciences, Szeged (Hungary)
  2. Eötvös Loránd Univ., Budapest (Hungary)
  3. Clark Univ., Worcester, MA (United States)
  4. Univ. of Toronto, ON (Canada)
  5. Univ. of Szeged (Hungary)
  6. Szent István Univ., Budapest (Hungary)
  7. Hungarian Mycological Society, Budapest (Hungary)
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  9. Dr. Rafael Ma. Moscoso National Botanical Garden, Santo Domingo (Dominican Republic)
  10. Moravian Museum, Brno (Czech Republic)
  11. Western Australian Herbarium, Kensington, WA (Australia)
  12. Manaaki Whenua—Landcare Research, Auckland New Zealand)
  13. Sorbonne Univ. (France)
  14. State Herbarium of South Australia, Adelaide, SA (Australia)
  15. Manaaki Whenua—Landcare Research, Lincoln (New Zealand)
  16. Univ. of Salzburg (Austria)
  17. San Francisco State Univ., CA (United States)
  18. Naturalis Biodiversity Center, Leiden (Netherlands)
  19. Univ. of Tennessee, Knoxville, TN (United States)
  20. Polish Academy of Sciences, Kraków (Poland)
  21. Slovak National Museum, Bratislava (Slovakia)
  22. Finnish Environment Inst., Helsinki (Finland)
  23. Univ. of Buenos Aires (Argentina)
  24. Jodrell Lab., Kew (United Kingdom)
  25. Naturalis Biodiversity Center, Leiden (Netherlands); Univ. of Oslo (Norway)
  26. Univ. of Utrecht (Netherlands)
  27. US Forest Service, Madison, WI (United States)
  28. Univ. of Central Oklahoma, Edmond, OK (United States)
  29. Univ. of Helsinki (Finland);Univ. of Tartu (Estonia)
  30. Russian Academy of Sciences, Ekaterinburg (Russia)
  31. Swedish Museum of Natural History, Stockholm (Sweden)
  32. Univ. of Helsinki (Finland)
  33. Univ. of Szeged (Hungary); MTA-SZTE ‘Lendulet’ Fungal Pathogenicity Mechanisms Research Group, Szeged (Hungary)
  34. Mendel Univ., Brno (Czech Republic)
  35. Herbarium Rooseveltensis Amanitarum, Roosevelt, NJ (United States); New York Botanical Garden, New York, NY (United States)
  36. Univ. of California, Berkeley, CA (United States)
  37. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  38. Institut National de la Recherche Agronomique (INRA), Champenoux (France)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; Hungarian Academy of Sciences
OSTI Identifier:
1546658
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 3; Journal Issue: 4; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Varga, Torda, Krizsán, Krisztina, Földi, Csenge, Dima, Bálint, Sánchez-García, Marisol, Sánchez-Ramírez, Santiago, Szöllősi, Gergely J., Szarkándi, János G., Papp, Viktor, Albert, László, Andreopoulos, William, Angelini, Claudio, Antonín, Vladimír, Barry, Kerrie W., Bougher, Neale L., Buchanan, Peter, Buyck, Bart, Bense, Viktória, Catcheside, Pam, Chovatia, Mansi, Cooper, Jerry, Dämon, Wolfgang, Desjardin, Dennis, Finy, Péter, Geml, József, Haridas, Sajeet, Hughes, Karen, Justo, Alfredo, Karasiński, Dariusz, Kautmanova, Ivona, Kiss, Brigitta, Kocsubé, Sándor, Kotiranta, Heikki, LaButti, Kurt M., Lechner, Bernardo E., Liimatainen, Kare, Lipzen, Anna, Lukács, Zoltán, Mihaltcheva, Sirma, Morgado, Louis N., Niskanen, Tuula, Noordeloos, Machiel E., Ohm, Robin A., Ortiz-Santana, Beatriz, Ovrebo, Clark, Rácz, Nikolett, Riley, Robert, Savchenko, Anton, Shiryaev, Anton, Soop, Karl, Spirin, Viacheslav, Szebenyi, Csilla, Tomšovský, Michal, Tulloss, Rodham E., Uehling, Jessie, Grigoriev, Igor V., Vágvölgyi, Csaba, Papp, Tamás, Martin, Francis M., Miettinen, Otto, Hibbett, David S., and Nagy, László G. Megaphylogeny resolves global patterns of mushroom evolution. United States: N. p., 2019. Web. doi:10.1038/s41559-019-0834-1.
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Varga, Torda, Krizsán, Krisztina, Földi, Csenge, Dima, Bálint, Sánchez-García, Marisol, Sánchez-Ramírez, Santiago, Szöllősi, Gergely J., Szarkándi, János G., Papp, Viktor, Albert, László, Andreopoulos, William, Angelini, Claudio, Antonín, Vladimír, Barry, Kerrie W., Bougher, Neale L., Buchanan, Peter, Buyck, Bart, Bense, Viktória, Catcheside, Pam, Chovatia, Mansi, Cooper, Jerry, Dämon, Wolfgang, Desjardin, Dennis, Finy, Péter, Geml, József, Haridas, Sajeet, Hughes, Karen, Justo, Alfredo, Karasiński, Dariusz, Kautmanova, Ivona, Kiss, Brigitta, Kocsubé, Sándor, Kotiranta, Heikki, LaButti, Kurt M., Lechner, Bernardo E., Liimatainen, Kare, Lipzen, Anna, Lukács, Zoltán, Mihaltcheva, Sirma, Morgado, Louis N., Niskanen, Tuula, Noordeloos, Machiel E., Ohm, Robin A., Ortiz-Santana, Beatriz, Ovrebo, Clark, Rácz, Nikolett, Riley, Robert, Savchenko, Anton, Shiryaev, Anton, Soop, Karl, Spirin, Viacheslav, Szebenyi, Csilla, Tomšovský, Michal, Tulloss, Rodham E., Uehling, Jessie, Grigoriev, Igor V., Vágvölgyi, Csaba, Papp, Tamás, Martin, Francis M., Miettinen, Otto, Hibbett, David S., & Nagy, László G. Megaphylogeny resolves global patterns of mushroom evolution. United States. https://doi.org/10.1038/s41559-019-0834-1
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Varga, Torda, Krizsán, Krisztina, Földi, Csenge, Dima, Bálint, Sánchez-García, Marisol, Sánchez-Ramírez, Santiago, Szöllősi, Gergely J., Szarkándi, János G., Papp, Viktor, Albert, László, Andreopoulos, William, Angelini, Claudio, Antonín, Vladimír, Barry, Kerrie W., Bougher, Neale L., Buchanan, Peter, Buyck, Bart, Bense, Viktória, Catcheside, Pam, Chovatia, Mansi, Cooper, Jerry, Dämon, Wolfgang, Desjardin, Dennis, Finy, Péter, Geml, József, Haridas, Sajeet, Hughes, Karen, Justo, Alfredo, Karasiński, Dariusz, Kautmanova, Ivona, Kiss, Brigitta, Kocsubé, Sándor, Kotiranta, Heikki, LaButti, Kurt M., Lechner, Bernardo E., Liimatainen, Kare, Lipzen, Anna, Lukács, Zoltán, Mihaltcheva, Sirma, Morgado, Louis N., Niskanen, Tuula, Noordeloos, Machiel E., Ohm, Robin A., Ortiz-Santana, Beatriz, Ovrebo, Clark, Rácz, Nikolett, Riley, Robert, Savchenko, Anton, Shiryaev, Anton, Soop, Karl, Spirin, Viacheslav, Szebenyi, Csilla, Tomšovský, Michal, Tulloss, Rodham E., Uehling, Jessie, Grigoriev, Igor V., Vágvölgyi, Csaba, Papp, Tamás, Martin, Francis M., Miettinen, Otto, Hibbett, David S., and Nagy, László G. Mon . "Megaphylogeny resolves global patterns of mushroom evolution". United States. https://doi.org/10.1038/s41559-019-0834-1. https://www.osti.gov/servlets/purl/1546658.
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@article{osti_1546658,
title = {Megaphylogeny resolves global patterns of mushroom evolution},
author = {Varga, Torda and Krizsán, Krisztina and Földi, Csenge and Dima, Bálint and Sánchez-García, Marisol and Sánchez-Ramírez, Santiago and Szöllősi, Gergely J. and Szarkándi, János G. and Papp, Viktor and Albert, László and Andreopoulos, William and Angelini, Claudio and Antonín, Vladimír and Barry, Kerrie W. and Bougher, Neale L. and Buchanan, Peter and Buyck, Bart and Bense, Viktória and Catcheside, Pam and Chovatia, Mansi and Cooper, Jerry and Dämon, Wolfgang and Desjardin, Dennis and Finy, Péter and Geml, József and Haridas, Sajeet and Hughes, Karen and Justo, Alfredo and Karasiński, Dariusz and Kautmanova, Ivona and Kiss, Brigitta and Kocsubé, Sándor and Kotiranta, Heikki and LaButti, Kurt M. and Lechner, Bernardo E. and Liimatainen, Kare and Lipzen, Anna and Lukács, Zoltán and Mihaltcheva, Sirma and Morgado, Louis N. and Niskanen, Tuula and Noordeloos, Machiel E. and Ohm, Robin A. and Ortiz-Santana, Beatriz and Ovrebo, Clark and Rácz, Nikolett and Riley, Robert and Savchenko, Anton and Shiryaev, Anton and Soop, Karl and Spirin, Viacheslav and Szebenyi, Csilla and Tomšovský, Michal and Tulloss, Rodham E. and Uehling, Jessie and Grigoriev, Igor V. and Vágvölgyi, Csaba and Papp, Tamás and Martin, Francis M. and Miettinen, Otto and Hibbett, David S. and Nagy, László G.},
abstractNote = {Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfil diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.},
doi = {10.1038/s41559-019-0834-1},
journal = {Nature Ecology and Evolution},
number = 4,
volume = 3,
place = {United States},
year = {Mon Mar 18 00:00:00 EDT 2019},
month = {Mon Mar 18 00:00:00 EDT 2019}
}
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Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota)
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Fungi and the Rise of Mammals
journal, August 2012

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    Works referencing / citing this record:

    The late blooming amphipods: Global change promoted post-Jurassic ecological radiation despite Palaeozoic origin
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    • Perez, Rolando; Luccioni, Marina; Kamakaka, Rohinton
    • Fungal Biology and Biotechnology, Vol. 7, Issue 1
    • DOI: 10.1186/s40694-020-00092-2

    Data from: Megaphylogeny resolves global patterns of mushroom evolution
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    Data from: Megaphylogeny resolves global patterns of mushroom evolution
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    Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants
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    • Ayuso-Fernández, Iván; Rencoret, Jorge; Gutiérrez, Ana
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 36
    • DOI: 10.1073/pnas.1905040116

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    Two new species of Hohenbuehelia (Pleurotaceae) from China
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    Enabling community-based metrology for wood-degrading fungi
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    • Perez, Rolando; Luccioni, Marina; Kamakaka, Rohinton
    • Fungal Biology and Biotechnology, Vol. 7, Issue 1
    • DOI: 10.1186/s40694-020-00092-2
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