title: Duplicate gene divergence by changes in microRNA binding sites in Arabidopsis and Brassica.
abstract: Gene duplication provides large numbers of new genes that can lead to the evolution of new functions. Duplicated genes can diverge by changes in sequences, expression patterns, and functions. MicroRNAs play an important role in the regulation of gene expression in many eukaryotes. After duplication, two paralogs may diverge in their microRNA binding sites, which might impact their expression and function. Little is known about conservation and divergence of microRNA binding sites in duplicated genes in plants. We analyzed microRNA binding sites in duplicated genes in Arabidopsis thaliana and Brassica rapa. We found that duplicates are more often targeted by microRNAs than singletons. The vast majority of duplicated genes in A. thaliana with microRNA binding sites show divergence in those sites between paralogs. Analysis of microRNA binding sites in genes derived from the ancient whole-genome triplication in B. rapa also revealed extensive divergence. Paralog pairs with divergent microRNA binding sites show more divergence in expression patterns compared with paralog pairs with the same microRNA binding sites in Arabidopsis. Close to half of the cases of binding site divergence are caused by microRNAs that are specific to the Arabidopsis genus, indicating evolutionarily recent gain of binding sites after target gene duplication. We also show rapid evolution of microRNA binding sites in a jacalin gene family. Our analyses reveal a dynamic process of changes in microRNA binding sites after gene duplication in Arabidopsis and highlight the role of microRNA regulation in the divergence and contrasting evolutionary fates of duplicated genes.
authors: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
authors: Sishuo
authors: S
authors: Wang
authors: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada keitha@mail.ubc.ca.
authors: Keith L
authors: KL
authors: Adams
mesh_terms: D017360:Arabidopsis / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics; D001665:Binding Sites; D001937:Brassica / Q000235:genetics*; D019143:Evolution, Molecular; D020440:Gene Duplication; D018506:Gene Expression Regulation, Plant; D020131:Genes, Duplicate; D017343:Genes, Plant; D035683:MicroRNAs / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D035683:MicroRNAs
keywords: gene duplication; gene regulation; microRNA binding sites; microRNAs; tandem duplicates; whole-genome duplication
references: Genetics. 1999 Apr;151(4):1531-45
references: 10101175
references: Bioinformatics. 2006 Nov 1;22(21):2688-90
references: 16928733
references: New Phytol. 2012 Nov;196(3):914-25
references: 22994911
references: Nat Genet. 2011 Aug 28;43(10):1035-9
references: 21873998
references: Bioinformatics. 2010 Oct 15;26(20):2617-9
references: 20739307
references: Mol Biol Evol. 2006 Jan;23(1):144-51
references: 16151181
references: Trends Genet. 2008 Feb;24(2):56-9
references: 18192068
references: Nat Rev Genet. 2007 Feb;8(2):93-103
references: 17230196
references: Curr Opin Genet Dev. 2007 Dec;17(6):505-12
references: 18006297
references: Genome Biol. 2006;7(2):R13
references: 16507168
references: RNA. 2008 May;14(5):814-21
references: 18367716
references: RNA. 2008 Dec;14(12):2455-9
references: 18952822
references: Plant J. 2008 Jul;55(1):131-51
references: 18363789
references: Mol Biol Evol. 2001 May;18(5):691-9
references: 11319253
references: Plant Cell. 2011 Dec;23(12):4185-207
references: 22158467
references: Genome Res. 2006 Feb;16(2):182-9
references: 16365379
references: Cell. 2009 Feb 20;136(4):669-87
references: 19239888
references: Trends Plant Sci. 2012 Apr;17(4):196-203
references: 22365280
references: Dev Cell. 2005 Apr;8(4):517-27
references: 15809034
references: Nucleic Acids Res. 2012 Jan;40(Database issue):D1202-10
references: 22140109
references: Plant Cell. 2012 Feb;24(2):778-93
references: 22307853
references: Plant Mol Biol. 2013 Mar;81(4-5):447-60
references: 23341152
references: New Phytol. 2006;171(3):451-68
references: 16866953
references: Nat Rev Genet. 2008 Feb;9(2):102-14
references: 18197166
references: BMC Genomics. 2008 Oct 02;9:454
references: 18831738
references: New Phytol. 2009 Aug;183(3):557-64
references: 19555435
references: Nucleic Acids Res. 2014 Jan;42(Database issue):D78-85
references: 24304892
references: Mol Biol Evol. 2007 Aug;24(8):1586-91
references: 17483113
references: Trends Plant Sci. 2011 May;16(5):258-64
references: 21466971
references: Genome Res. 2003 Feb;13(2):137-44
references: 12566392
references: Cell. 2002 Aug 23;110(4):513-20
references: 12202040
references: Nucleic Acids Res. 2004 Sep 08;32(16):4776-85
references: 15356295
references: Mol Biol Evol. 2011 Aug;28(8):2359-69
references: 21389272
references: Genetics. 2005 Oct;171(2):765-81
references: 16020789
references: Nat Genet. 2004 Dec;36(12):1282-90
references: 15565108
references: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references: 15034147
references: BMC Bioinformatics. 2013 Jun 03;14:174
references: 23725466
references: Annu Rev Plant Biol. 2006;57:19-53
references: 16669754
references: Annu Rev Cell Dev Biol. 2009;25:21-44
references: 19575669
references: Nucleic Acids Res. 2011 Jul;39(Web Server issue):W155-9
references: 21622958
references: PLoS One. 2012;7(5):e36442
references: 22567157
references: Funct Integr Genomics. 2005 Jul;5(3):129-35
references: 15875226
references: Plant Cell. 2011 Feb;23(2):431-42
references: 21317375
references: Nat Rev Genet. 2010 Feb;11(2):97-108
references: 20051986
references: Bioinformatics. 1998;14(9):755-63
references: 9918945
references: Genome Biol. 2004;5(9):R65
references: 15345049
references: BMC Genomics. 2012 Jun 11;13 Suppl 3:S3
references: 22759612
references: Plant Physiol. 2004 Oct;136(2):3009-22
references: 15489284
references: Mol Cell. 2004 Jun 18;14(6):787-99
references: 15200956
references: Bioinformatics. 2010 Jun 15;26(12):1566-8
references: 20430753
references: Brief Bioinform. 2011 Mar;12(2):115-21
references: 20858738
references: Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):2967-71
references: 20080574
references: Genome Biol. 2008;9(8):R132
references: 18727826
references: Genome Res. 2005 Apr;15(4):516-25
references: 15781573
references: Plant Cell. 2013 Jul;25(7):2383-99
references: 23881412
references: Plant Physiol. 2011 Dec;157(4):1583-95
references: 22003084
references: Bioinformatics. 2011 Apr 15;27(8):1164-5
references: 21335321
references: Cell Res. 2007 Mar;17(3):212-8
references: 17130846
references: Bioinformatics. 2012 Aug 1;28(15):2059-61
references: 22628521
references: Genome Res. 2006 Apr;16(4):510-9
references: 16520461
references: Mol Biol Evol. 2011 Sep;28(9):2421-4
references: 21441354
references: J Exp Bot. 2010 May;61(9):2271-80
references: 20388745
references: Trends Plant Sci. 2008 Jul;13(7):343-9
references: 18502167
references: Mol Biol Evol. 2011 Sep;28(9):2429-34
references: 21478371
references: Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17835-40
references: 19805056
references: Cell. 2009 Jan 23;136(2):215-33
references: 19167326
references: Plant J. 2013 Nov;76(3):519-29
references: 23937661
references: J Mol Evol. 1999 May;48(5):597-604
references: 10198125
references: Proc Biol Sci. 1994 May 23;256(1346):119-24
references: 8029240
references: Trends Genet. 2010 Oct;26(10):425-30
references: 20708291
references: Nucleic Acids Res. 2006 Jan 1;34(Database issue):D140-4
references: 16381832
references: Science. 2013 Oct 4;342(6154):118-23
references: 24092744
references: Nat Rev Genet. 2011 Nov 18;12(12):846-60
references: 22094948
references: Mol Cell. 2013 Nov 21;52(4):591-601
references: 24267452
references: Genome Biol Evol. 2012;4(3):230-9
references: 22223755
references: Plant Cell. 2012 Mar;24(3):859-74
references: 22408077