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Comparative genomics reveals the origin of fungal hyphae and multicellularity

Author

Listed:
  • Enikő Kiss

    (Institute of Biochemistry
    University of Szeged, Faculty of Science and Informatics)

  • Botond Hegedüs

    (Institute of Biochemistry)

  • Máté Virágh

    (Institute of Biochemistry)

  • Torda Varga

    (Institute of Biochemistry
    University of Szeged, Faculty of Science and Informatics)

  • Zsolt Merényi

    (Institute of Biochemistry)

  • Tamás Kószó

    (Institute of Biochemistry)

  • Balázs Bálint

    (Institute of Biochemistry)

  • Arun N. Prasanna

    (Institute of Biochemistry
    4700 King Abdullah University of Science and Technology (KAUST))

  • Krisztina Krizsán

    (Institute of Biochemistry)

  • Sándor Kocsubé

    (University of Szeged, Faculty of Science and Informatics)

  • Meritxell Riquelme

    (Centro de Investigación Científica y de Educación Superior de Ensenada)

  • Norio Takeshita

    (University of Tsukuba)

  • László G. Nagy

    (Institute of Biochemistry)

Abstract

Hyphae represent a hallmark structure of multicellular fungi. The evolutionary origins of hyphae and of the underlying genes are, however, hardly known. By systematically analyzing 72 complete genomes, we here show that hyphae evolved early in fungal evolution probably via diverse genetic changes, including co-option and exaptation of ancient eukaryotic (e.g. phagocytosis-related) genes, the origin of new gene families, gene duplications and alterations of gene structure, among others. Contrary to most multicellular lineages, the origin of filamentous fungi did not correlate with expansions of kinases, receptors or adhesive proteins. Co-option was probably the dominant mechanism for recruiting genes for hypha morphogenesis, while gene duplication was apparently less prevalent, except in transcriptional regulators and cell wall - related genes. We identified 414 novel gene families that show correlated evolution with hyphae and that may have contributed to its evolution. Our results suggest that hyphae represent a unique multicellular organization that evolved by limited fungal-specific innovations and gene duplication but pervasive co-option and modification of ancient eukaryotic functions.

Suggested Citation

  • Enikő Kiss & Botond Hegedüs & Máté Virágh & Torda Varga & Zsolt Merényi & Tamás Kószó & Balázs Bálint & Arun N. Prasanna & Krisztina Krizsán & Sándor Kocsubé & Meritxell Riquelme & Norio Takeshita & L, 2019. "Comparative genomics reveals the origin of fungal hyphae and multicellularity," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12085-w
    DOI: 10.1038/s41467-019-12085-w
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    Cited by:

    1. Mirjana Domazet-Lošo & Tin Široki & Korina Šimičević & Tomislav Domazet-Lošo, 2024. "Macroevolutionary dynamics of gene family gain and loss along multicellular eukaryotic lineages," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    2. Md. Abdulla Al Mamun & Wei Cao & Shugo Nakamura & Jun-ichi Maruyama, 2023. "Large-scale identification of genes involved in septal pore plugging in multicellular fungi," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. 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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