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Contemporaneous radiations of fungi and plants linked to symbiosis

Author

Listed:
  • François Lutzoni

    (Duke University)

  • Michael D. Nowak

    (University of Oslo)

  • Michael E. Alfaro

    (University of California)

  • Valérie Reeb

    (University of Iowa)

  • Jolanta Miadlikowska

    (Duke University)

  • Michael Krug

    (Rheinische Friedrich-Wilhelms-Universität)

  • A. Elizabeth Arnold

    (University of Arizona
    University of Arizona)

  • Louise A. Lewis

    (University of Connecticut)

  • David L. Swofford

    (Duke University
    University of Florida)

  • David Hibbett

    (Clark University)

  • Khidir Hilu

    (Virginia Tech)

  • Timothy Y. James

    (University of Michigan)

  • Dietmar Quandt

    (Rheinische Friedrich-Wilhelms-Universität)

  • Susana Magallón

    (Universidad Nacional Autónoma de México)

Abstract

Interactions between fungi and plants, including parasitism, mutualism, and saprotrophy, have been invoked as key to their respective macroevolutionary success. Here we evaluate the origins of plant-fungal symbioses and saprotrophy using a time-calibrated phylogenetic framework that reveals linked and drastic shifts in diversification rates of each kingdom. Fungal colonization of land was associated with at least two origins of terrestrial green algae and preceded embryophytes (as evidenced by losses of fungal flagellum, ca. 720 Ma), likely facilitating terrestriality through endomycorrhizal and possibly endophytic symbioses. The largest radiation of fungi (Leotiomyceta), the origin of arbuscular mycorrhizae, and the diversification of extant embryophytes occurred ca. 480 Ma. This was followed by the origin of extant lichens. Saprotrophic mushrooms diversified in the Late Paleozoic as forests of seed plants started to dominate the landscape. The subsequent diversification and explosive radiation of Agaricomycetes, and eventually of ectomycorrhizal mushrooms, were associated with the evolution of Pinaceae in the Mesozoic, and establishment of angiosperm-dominated biomes in the Cretaceous.

Suggested Citation

  • François Lutzoni & Michael D. Nowak & Michael E. Alfaro & Valérie Reeb & Jolanta Miadlikowska & Michael Krug & A. Elizabeth Arnold & Louise A. Lewis & David L. Swofford & David Hibbett & Khidir Hilu &, 2018. "Contemporaneous radiations of fungi and plants linked to symbiosis," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-07849-9
    DOI: 10.1038/s41467-018-07849-9
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    Cited by:

    1. Christine Strullu-Derrien & Tomasz Goral & Alan R. T. Spencer & Paul Kenrick & M. Catherine Aime & Ester Gaya & David L. Hawksworth, 2023. "A fungal plant pathogen discovered in the Devonian Rhynie Chert," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. Biao-Feng Zhou & Shuai Yuan & Andrew A. Crowl & Yi-Ye Liang & Yong Shi & Xue-Yan Chen & Qing-Qing An & Ming Kang & Paul S. Manos & Baosheng Wang, 2022. "Phylogenomic analyses highlight innovation and introgression in the continental radiations of Fagaceae across the Northern Hemisphere," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Philipp Resl & Adina R. Bujold & Gulnara Tagirdzhanova & Peter Meidl & Sandra Freire Rallo & Mieko Kono & Samantha Fernández-Brime & Hörður Guðmundsson & Ólafur Sigmar Andrésson & Lucia Muggia & Helmu, 2022. "Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Camille Puginier & Cyril Libourel & Juergen Otte & Pavel Skaloud & Mireille Haon & Sacha Grisel & Malte Petersen & Jean-Guy Berrin & Pierre-Marc Delaux & Francesco Dal Grande & Jean Keller, 2024. "Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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