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快乐十分复式金额表:Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi
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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 fruiting 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.
The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular 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.
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Author contributions: K.K., D.S.H., and L.G.N. designed research; K.K., é.A., Z.M., N.S., M.V., B.B., J.C., and I.N. performed research; K.B., J.C., B. Henrissat, J.J., A.L., R.A.O., I.N., J.P., J.Y., Y.X., and I.V.G. contributed new reagents/analytic tools; K.K., é.A., Z.M., N.S., M.V., T.K., S.M., B.K., B.B., U.K., B. Hegedüs, B. Henrissat, and L.G.N. analyzed data; and K.K., M.V., U.K., K.B., I.V.G., D.S.H., and L.G.N. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Genome assembly and annotation of Rickenella mellea was deposited in the National Center for Biotechnology Information BioProject database (accession no. PRJNA334780). A Gene Expression Omnibus (GEO) archive of the sequenced transcriptome libraries was deposited in the NCBI’s GEO Archive at www.ncbi.nlm.nih.gov/geo (accession no. GSE125200).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1817822116/-/DCSupplemental.
Published under the PNAS license.