title: The evolutionary dynamics of operon distributions in eukaryote genomes.
abstract: Genes in nematode and ascidian genomes frequently occur in operons--multiple genes sharing a common promoter to generate a polycistronic primary transcript--and such genes comprise 15-20% of the coding genome for Caenorhabditis elegans and Ciona intestinalis. Recent work in nematodes has demonstrated that the identity of genes within operons is highly conserved among species and that the unifying feature of genes within operons is that they are expressed in germline tissue. However, it is generally unknown what processes are responsible for generating the distribution of operon sizes across the genome, which are composed of up to eight genes per operon. Here we investigate several models for operon evolution to better understand their abundance, distribution of sizes, and evolutionary dynamics over time. We find that birth-death models of operon evolution reasonably describe the relative abundance of operons of different sizes in the C. elegans and Ciona genomes and generate predictions about the number of monocistronic, nonoperon genes that likely participate in the birth-death process. This theory, and applications to C. elegans and Ciona, motivates several new and testable hypotheses about eukaryote operon evolution.
authors.affiliation: Department of Ecology and Evolutionary Biology, Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario M5S 3B2, Canada. asher.cutter@utoronto.ca
authors.forename: Asher D
authors.initials: AD
authors.lastname: Cutter
authors.forename: Aneil F
authors.initials: AF
authors.lastname: Agrawal
mesh_terms: D000818:Animals; D005075:Biological Evolution; D017173:Caenorhabditis elegans / Q000235:genetics; D056890:Eukaryota; D005057:Eukaryotic Cells; D016678:Genome; D009348:Nematoda / Q000235:genetics; D009876:Operon / Q000235:genetics*
references.citation: RNA. 2008 Apr;14(4):760-70
references.pmid: 18256244
references.citation: Nucleic Acids Res. 2006 Jul 05;34(11):3378-88
references.pmid: 16822859
references.citation: PLoS Biol. 2007 Jul;5(7):e167
references.pmid: 17608563
references.citation: J Struct Funct Genomics. 2003;3(1-4):35-44
references.pmid: 12836683
references.citation: Genetics. 2009 Apr;181(4):1219-28
references.pmid: 19204375
references.citation: Curr Top Dev Biol. 2009;86:43-66
references.pmid: 19361689
references.citation: Development. 2004 Jan;131(2):311-23
references.pmid: 14668411
references.citation: Cell. 1993 May 7;73(3):521-32
references.pmid: 8098272
references.citation: Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5698-703
references.pmid: 17372217
references.citation: Genome Res. 2007 Oct;17(10):1478-85
references.pmid: 17712020
references.citation: Genome Res. 2003 Feb;13(2):238-43
references.pmid: 12566401
references.citation: Mol Biol Evol. 2003 Dec;20(12):2097-103
references.pmid: 12949121
references.citation: Genetics. 2008 Apr;178(4):2093-104
references.pmid: 18430935
references.citation: Genome Res. 2005 Aug;15(8):1127-35
references.pmid: 16077012
references.citation: Brief Funct Genomic Proteomic. 2004 Nov;3(3):199-211
references.pmid: 15642184
references.citation: PLoS Genet. 2006 Nov 24;2(11):e198
references.pmid: 17121468
references.citation: Annu Rev Genet. 1989;23:251-87
references.pmid: 2559652
references.citation: Mol Biol Evol. 2009 Jun;26(6):1199-234
references.pmid: 19289596
references.citation: Mol Cell. 2008 Jul 11;31(1):79-90
references.pmid: 18571451
references.citation: Genome Biol. 2008 Oct 14;9(10):R152
references.pmid: 18854010
references.citation: Nature. 2002 Jun 20;417(6891):851-4
references.pmid: 12075352
references.citation: Cell. 2006 Dec 15;127(6):1193-207
references.pmid: 17174894
references.citation: Mol Ecol. 2010 Feb;19(4):798-809
references.pmid: 20088888
references.citation: Annu Rev Cell Dev Biol. 2007;23:405-33
references.pmid: 17506698
references.citation: Mol Cell. 2008 Jul 11;31(1):67-78
references.pmid: 18571452
references.citation: Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6118-23
references.pmid: 11983904
references.citation: Nature. 1994 Nov 17;372(6503):270-2
references.pmid: 7969472
references.citation: Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9751-6
references.pmid: 9275196
references.citation: Curr Biol. 2008 Jun 24;18(12):861-7
references.pmid: 18501605
references.citation: Science. 2002 Dec 13;298(5601):2157-67
references.pmid: 12481130
references.citation: Genome Res. 2008 Mar;18(3):412-21
references.pmid: 18218978
references.citation: Curr Biol. 2008 Oct 14;18(19):1476-82
references.pmid: 18818082
references.citation: Mol Biol Evol. 2006 Dec;23(12):2303-15
references.pmid: 16936139
references.citation: PLoS Biol. 2003 Nov;1(2):E45
references.pmid: 14624247
references.citation: Nat Rev Genet. 2003 Feb;4(2):112-20
references.pmid: 12560808
references.citation: Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2579-81
references.pmid: 10077550
references.citation: Genomics. 2008 Mar;91(3):243-8
references.pmid: 18082363