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Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi

Abstract : The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple mul-ticellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation , signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. complex multicellularity | evolution | fungi | comparative genomics | fruiting body development F ungi represent a diverse lineage of complex multicellular organisms with a unique evolutionary history compared with complex multicellular animals, embryophytes, florideophytes, and laminarean brown algae (1-4). Within the fungal kingdom, complex multicellularity is discussed mostly in the context of fruiting bodies, which are found in at least eight independent lin-eages (2), of which the Pezizomycotina (Ascomycota) and the Agaricomycetes (Basidiomycota) contain the vast majority of species. The mushroom-forming fungi (Agaricomycetes) comprise >21,000 species and originated 350 million years ago (5), approximately coinciding with the origin of tetrapods. Fruiting bodies of mushroom-forming fungi have immense importance in agriculture, ecology, and medicine; they represent an important and sustainable food source, with favorable medicinal properties (e.g., antitumor, immunomodulatory) (6). Mushroom-forming fungi share a single origin of fruiting body formation that probably dates to the most recent common ancestor of the Agaricomycetes, Dacrymycetes, and Tremellomycetes (2). Fruiting body development in mushroom-forming fungi has been subject to surprisingly few studies (see, e.g., refs. 7-10), resulting in a paucity of information on the genetic underpinnings of the origins of complex multicellularity in this group (2). During fruiting body development, fungi deploy mechanisms for hypha-to-hypha adhesion, communication (e.g., via Significance Complex multicellularity is a major evolutionary innovation in the history of life. Mushroom-forming fungi (Agaricomycetes) represent one of the most diverse complex multicellular clades, yet the genetic bases and evolutionary origins of their multicellular development are hardly known. We used readouts of gene expression in six species to find genes with a dynamic expression during the development of fruit-ing bodies. Comparisons across species and to 200 fungal genomes identified the gene families with a conserved expression dynamics in multicellular fruiting bodies and their ancient evolutionary origins. These data outline the major multicellularity-related and developmental processes of mushrooms, including the role of transcriptional reprogramming , gene coexpression networks, and alternative splicing , and reveal significant convergence with other complex multicellular lineages.
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Krisztina Krizsán, Éva Almási, Zsolt Merényi, Neha Sahu, Máté Virágh, et al.. Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2019, 116 (15), pp.7409-7418. ⟨10.1038/s41559-019-0833-2⟩. ⟨hal-02587458⟩

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