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

Stajich, Jason E.; Wilke, Sarah K.; Ahrén, Dag LU ; Au, Chun Hang; Birren, Bruce W.; Borodovsky, Mark; Burns, Claire; Canbäck, Björn LU ; Casselton, Lorna A. and Cheng, C. K., et al. (2010) In Proceedings of the National Academy of Sciences 107(26). p.11889-11894
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 10(8) 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... (More)
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 10(8) 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. (Less)
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keywords
kinase, gene families, basidiomycete, dikaryon formation, meiotic, recombination
in
Proceedings of the National Academy of Sciences
volume
107
issue
26
pages
11889 - 11894
publisher
National Acad Sciences
external identifiers
  • wos:000279332300043
  • scopus:77955350734
ISSN
1091-6490
DOI
10.1073/pnas.1003391107
language
English
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yes
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c6c9cefb-2ce4-445f-99d1-86770133c5ca (old id 1628643)
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2010-07-21 16:13:32
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@article{c6c9cefb-2ce4-445f-99d1-86770133c5ca,
  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 10(8) 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.},
  author       = {Stajich, Jason E. and Wilke, Sarah K. and Ahrén, Dag and Au, Chun Hang and Birren, Bruce W. and Borodovsky, Mark and Burns, Claire and Canbäck, Björn and Casselton, Lorna A. and Cheng, C. K. and Deng, Jixin and Dietrich, Fred S. and Fargo, David C. and Farman, Mark L. and Gathman, Allen C. and Goldberg, Jonathan and Guigo, Roderic and Hoegger, Patrick J. and Hooker, James B. and Huggins, Ashleigh and James, Timothy Y. and Kamada, Takashi and Kilaru, Sreedhar and Kodira, Chinnapa and Kuees, Ursula and Kupfert, Doris and Kwan, H. S. and Lomsadze, Alexandre and Li, Weixi and Lilly, Walt W. and Ma, Li-Jun and Mackey, Aaron J. and Manning, Gerard and Martin, Francis and Muraguchi, Hajime and Natvig, Donald O. and Palmerini, Heather and Ramesh, Marilee A. and Rehmeyer, Cathy J. and Roe, Bruce A. and Shenoy, Narmada and Stanke, Mario and Ter-Hovhannisyan, Vardges and Tunlid, Anders and Velagapudi, Rajesh and Vision, Todd J. and Zeng, Qiandong and Zolan, Miriam E. and Pukkila, Patricia J.},
  issn         = {1091-6490},
  keyword      = {kinase,gene families,basidiomycete,dikaryon formation,meiotic,recombination},
  language     = {eng},
  number       = {26},
  pages        = {11889--11894},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences},
  title        = {Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus)},
  url          = {http://dx.doi.org/10.1073/pnas.1003391107},
  volume       = {107},
  year         = {2010},
}