Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus)

Jason E. Stajich, Sarah K. Wilke, Dag Ahrén, Chun Hang Au, Bruce W. Birren, Mark Borodovsky, Claire Burns, Björn Canbäck, Lorna A. Casselton, C. K. Cheng, Jixin Deng, Fred S. Dietrich, David C. Fargo, Mark L. Farman, Allen C. Gathman, Jonathan Goldberg, Roderic Guigó, Patrick J. Hoegger, James B. Hooker, Ashleigh HugginsTimothy Y. James, Takashi Kamada, Sreedhar Kilaru, Chinnapa Kodira, Ursula Kües, Doris Kupfer, H. S. Kwan, Alexandre Lomsadze, Weixi Li, Walt W. Lilly, Li Jun Ma, Aaron J. Mackey, Gerard Manning, Francis Martin, Hajime Muraguchi, Donald O. Natvig, Heather Palmerini, Marilee A. Ramesh, Cathy J. Rehmeyer, Bruce A. Roe, Narmada Shenoy, Mario Stanke, Vardges Ter-Hovhannisyan, Anders Tunlid, Rajesh Velagapudi, Todd J. Vision, Qiandong Zeng, Miriam E. Zolan, Patricia J. Pukkila

Research output: Contribution to journalArticlepeer-review

342 Scopus citations

Abstract

The mushroom Coprinopsis cinerea is a classic experimental model for multicellular development in fungi because it grows on defined media, completes its life cycle in 2 weeks, produces some 108 synchronized meiocytes, and can be manipulated at all stages in development by mutation and transformation. The 37-megabase genome of C. cinerea was sequenced and assembled into 13 chromosomes. Meiotic recombination rates vary greatly along the chromosomes, and retrotransposons are absent in large regions of the genome with low levels of meiotic recombination. Single-copy genes with identifiable orthologs in other basidiomycetes are predominant in low-recombination regions of the chromosome. In contrast, paralogous multicopy genes are found in the highly recombining regions, including a large family of protein kinases (FunK1) unique to multicellular fungi. Analyses of P450 and hydrophobin gene families confirmed that local gene duplications drive the expansions of paralogous copies and the expansions occur in independent lineages of Agaricomycotina fungi. Gene-expression patterns from microarrays were used to dissect the transcriptional program of dikaryon formation (mating). Several members of the FunK1 kinase family are differentially regulated during sexual morphogenesis, and coordinate regulation of adjacent duplications is rare. The genomes of C. cinerea and Laccaria bicolor, a symbiotic basidiomycete, share extensive regions of synteny. The largest syntenic blocks occur in regions with low meiotic recombination rates, no transposable elements, and tight gene spacing, where orthologous single-copy genes are overrepresented. The chromosome assembly of C. cinerea is an essential resource in understanding the evolution of multicellularity in the fungi.

Original languageEnglish
Pages (from-to)11889-11894
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number26
DOIs
StatePublished - Jun 29 2010

Funding

FundersFunder number
National Institute of General Medical SciencesR01GM043930
National Institute of General Medical Sciences

    Keywords

    • Basidiomycete
    • Dikaryon formation
    • Gene families
    • Kinase
    • Meiotic recombination

    ASJC Scopus subject areas

    • General

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