The evolutionary dynamics of operon distributions in eukaryote genomes.
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.
Cutter
Asher D
AD
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
Agrawal
Aneil F
AF
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*
RNA. 2008 Apr;14(4):760-70
18256244
Nucleic Acids Res. 2006 Jul 05;34(11):3378-88
16822859
PLoS Biol. 2007 Jul;5(7):e167
17608563
J Struct Funct Genomics. 2003;3(1-4):35-44
12836683
Genetics. 2009 Apr;181(4):1219-28
19204375
Curr Top Dev Biol. 2009;86:43-66
19361689
Development. 2004 Jan;131(2):311-23
14668411
Cell. 1993 May 7;73(3):521-32
8098272
Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5698-703
17372217
Genome Res. 2007 Oct;17(10):1478-85
17712020
Genome Res. 2003 Feb;13(2):238-43
12566401
Mol Biol Evol. 2003 Dec;20(12):2097-103
12949121
Genetics. 2008 Apr;178(4):2093-104
18430935
Genome Res. 2005 Aug;15(8):1127-35
16077012
Brief Funct Genomic Proteomic. 2004 Nov;3(3):199-211
15642184
PLoS Genet. 2006 Nov 24;2(11):e198
17121468
Annu Rev Genet. 1989;23:251-87
2559652
Mol Biol Evol. 2009 Jun;26(6):1199-234
19289596
Mol Cell. 2008 Jul 11;31(1):79-90
18571451
Genome Biol. 2008 Oct 14;9(10):R152
18854010
Nature. 2002 Jun 20;417(6891):851-4
12075352
Cell. 2006 Dec 15;127(6):1193-207
17174894
Mol Ecol. 2010 Feb;19(4):798-809
20088888
Annu Rev Cell Dev Biol. 2007;23:405-33
17506698
Mol Cell. 2008 Jul 11;31(1):67-78
18571452
Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6118-23
11983904
Nature. 1994 Nov 17;372(6503):270-2
7969472
Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9751-6
9275196
Curr Biol. 2008 Jun 24;18(12):861-7
18501605
Science. 2002 Dec 13;298(5601):2157-67
12481130
Genome Res. 2008 Mar;18(3):412-21
18218978
Curr Biol. 2008 Oct 14;18(19):1476-82
18818082
Mol Biol Evol. 2006 Dec;23(12):2303-15
16936139
PLoS Biol. 2003 Nov;1(2):E45
14624247
Nat Rev Genet. 2003 Feb;4(2):112-20
12560808
Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2579-81
10077550
Genomics. 2008 Mar;91(3):243-8
18082363