Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus).
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.
Stajich
Jason E
JE
Department of Plant Pathology and Microbiology, University of California, Riverside, CA 92521, USA. jason.stajich@ucr.edu
Wilke
Sarah K
SK
Ahrén
Dag
D
Au
Chun Hang
CH
Birren
Bruce W
BW
Borodovsky
Mark
M
Burns
Claire
C
Canbäck
Björn
B
Casselton
Lorna A
LA
Cheng
C K
CK
Deng
Jixin
J
Dietrich
Fred S
FS
Fargo
David C
DC
Farman
Mark L
ML
Gathman
Allen C
AC
Goldberg
Jonathan
J
Guigó
Roderic
R
Hoegger
Patrick J
PJ
Hooker
James B
JB
Huggins
Ashleigh
A
James
Timothy Y
TY
Kamada
Takashi
T
Kilaru
Sreedhar
S
Kodira
Chinnapa
C
Kües
Ursula
U
Kupfer
Doris
D
Kwan
H S
HS
Lomsadze
Alexandre
A
Li
Weixi
W
Lilly
Walt W
WW
Ma
Li-Jun
LJ
Mackey
Aaron J
AJ
Manning
Gerard
G
Martin
Francis
F
Muraguchi
Hajime
H
Natvig
Donald O
DO
Palmerini
Heather
H
Ramesh
Marilee A
MA
Rehmeyer
Cathy J
CJ
Roe
Bruce A
BA
Shenoy
Narmada
N
Stanke
Mario
M
Ter-Hovhannisyan
Vardges
V
Tunlid
Anders
A
Velagapudi
Rajesh
R
Vision
Todd J
TJ
Zeng
Qiandong
Q
Zolan
Miriam E
ME
Pukkila
Patricia J
PJ
D001483:Base Sequence; D002874:Chromosome Mapping; D015825:Chromosomes, Fungal / Q000235:genetics*; D003302:Coprinus / Q000166:cytology / Q000235:genetics* / Q000254:growth & development; D003577:Cytochrome P-450 Enzyme System / Q000235:genetics; D017931:DNA Primers / Q000235:genetics; D019143:Evolution, Molecular; D005656:Fungal Proteins / Q000235:genetics; D020440:Gene Duplication; D016681:Genome, Fungal; D008540:Meiosis / Q000235:genetics; D008969:Molecular Sequence Data; D005810:Multigene Family; D010802:Phylogeny; D011494:Protein Kinases / Q000235:genetics; D012331:RNA, Fungal / Q000235:genetics; D011995:Recombination, Genetic; D018626:Retroelements / Q000235:genetics
D017931:DNA Primers; D005656:Fungal Proteins; D012331:RNA, Fungal; D018626:Retroelements; D003577:Cytochrome P-450 Enzyme System; D011494:Protein Kinases