Evolution after Whole-Genome Duplication: Teleost MicroRNAs.
Japanese medaka Oryzias latipes
arm-switching
blackfin icefish Chaenocephalus aceratus
spotted gar Lepisosteus oculatus
three-spined stickleback Gasterosteus aculeatus
zebrafish Danio rerio
Journal
Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455
Informations de publication
Date de publication:
29 07 2021
29 07 2021
Historique:
pubmed:
20
4
2021
medline:
21
9
2021
entrez:
19
4
2021
Statut:
ppublish
Résumé
MicroRNAs (miRNAs) are important gene expression regulators implicated in many biological processes, but we lack a global understanding of how miRNA genes evolve and contribute to developmental canalization and phenotypic diversification. Whole-genome duplication events likely provide a substrate for species divergence and phenotypic change by increasing gene numbers and relaxing evolutionary pressures. To understand the consequences of genome duplication on miRNA evolution, we studied miRNA genes following the teleost genome duplication (TGD). Analysis of miRNA genes in four teleosts and in spotted gar, whose lineage diverged before the TGD, revealed that miRNA genes were retained in ohnologous pairs more frequently than protein-coding genes, and that gene losses occurred rapidly after the TGD. Genomic context influenced retention rates, with clustered miRNA genes retained more often than nonclustered miRNA genes and intergenic miRNA genes retained more frequently than intragenic miRNA genes, which often shared the evolutionary fate of their protein-coding host. Expression analyses revealed both conserved and divergent expression patterns across species in line with miRNA functions in phenotypic canalization and diversification, respectively. Finally, major strands of miRNA genes experienced stronger purifying selection, especially in their seeds and 3'-complementary regions, compared with minor strands, which nonetheless also displayed evolutionary features compatible with constrained function. This study provides the first genome-wide, multispecies analysis of the mechanisms influencing metazoan miRNA evolution after whole-genome duplication.
Identifiants
pubmed: 33871629
pii: 6237913
doi: 10.1093/molbev/msab105
pmc: PMC8321539
doi:
Substances chimiques
MicroRNAs
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3308-3331Subventions
Organisme : NIH HHS
ID : R24 OD011199
Pays : United States
Organisme : NIH HHS
ID : R01 OD011116
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM085318
Pays : United States
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
Curr Opin Genet Dev. 2007 Apr;17(2):145-50
pubmed: 17317150
Biochimie. 2019 May;160:193-199
pubmed: 30905732
PLoS Genet. 2018 Sep 10;14(9):e1007593
pubmed: 30199527
Nature. 2011 Jul 13;476(7359):228-31
pubmed: 21753754
Genome Biol Evol. 2011;3:667-73
pubmed: 21398425
RNA. 2014 Dec;20(12):1850-63
pubmed: 25332374
Biol Rev Camb Philos Soc. 2018 Nov;93(4):1955-1986
pubmed: 29797774
Mar Biotechnol (NY). 2016 Jun;18(3):436-47
pubmed: 27262998
PLoS One. 2010 Jun 30;5(6):e11387
pubmed: 20613982
Mol Biol Evol. 2015 May;32(5):1161-74
pubmed: 25576364
Nat Genet. 2016 Apr;48(4):427-37
pubmed: 26950095
Trends Genet. 2013 Feb;29(2):116-24
pubmed: 23128010
PLoS One. 2016 Apr 29;11(4):e0153324
pubmed: 27128807
Mol Biol Evol. 2014 Oct;31(10):2722-34
pubmed: 25063441
Annu Rev Anim Biosci. 2018 Feb 15;6:47-68
pubmed: 29447475
Genome Biol Evol. 2009 Nov 25;1:479-93
pubmed: 20333216
Nat Genet. 2013 May;45(5):567-72
pubmed: 23542700
Trends Genet. 2003 Sep;19(9):479-84
pubmed: 12957540
PLoS Comput Biol. 2011 Aug;7(8):e1002173
pubmed: 21901087
Nat Rev Genet. 2011 Nov 18;12(12):846-60
pubmed: 22094948
Nucleic Acids Res. 2017 Sep 19;45(16):9290-9301
pubmed: 28934507
Proc Natl Acad Sci U S A. 2009 May 5;106(18):7273-80
pubmed: 19351897
Nucleic Acids Res. 2014 Jan;42(Database issue):D68-73
pubmed: 24275495
Nat Genet. 2000 May;25(1):3-4
pubmed: 10802639
Trends Genet. 2018 Mar;34(3):165-167
pubmed: 29361313
Cell. 2007 Apr 20;129(2):303-17
pubmed: 17397913
Nat Biotechnol. 2017 Sep;35(9):872-878
pubmed: 28829439
Genome Biol Evol. 2015 Nov 01;7(11):3085-96
pubmed: 26527651
Genome Res. 2007 Sep;17(9):1254-65
pubmed: 17652425
Nat Commun. 2014 Apr 22;5:3657
pubmed: 24755649
Oncotarget. 2017 Jun 02;8(39):66629-66640
pubmed: 29029543
Evol Dev. 2013 Jul-Aug;15(4):293-304
pubmed: 23809703
Nat Commun. 2016 Apr 25;7:11438
pubmed: 27109497
Nat Rev Mol Cell Biol. 2013 Aug;14(8):475-88
pubmed: 23800994
BMC Genomics. 2012 Jun 06;13:218
pubmed: 22672736
Blood. 2009 Feb 19;113(8):1794-804
pubmed: 18849488
Nature. 2010 Feb 25;463(7284):1084-8
pubmed: 20118916
Curr Biol. 2013 Mar 18;23(6):523-8
pubmed: 23453955
Nat Rev Genet. 2013 Aug;14(8):535-48
pubmed: 23817310
Genome Res. 2003 Mar;13(3):382-90
pubmed: 12618368
Nucleic Acids Res. 2016 May 5;44(8):3865-77
pubmed: 26921406
Genomics. 2012 Sep;100(3):141-8
pubmed: 22735742
Mol Biol Evol. 2018 Mar 1;35(3):646-654
pubmed: 29237075
Nat Struct Mol Biol. 2008 Apr;15(4):354-63
pubmed: 18376413
Genome Biol. 2014;15(12):550
pubmed: 25516281
BMC Genomics. 2010 Apr 06;11:224
pubmed: 20370903
New Phytol. 2010 Apr;186(1):54-62
pubmed: 19925558
Mol Cell. 2014 Jun 5;54(5):766-76
pubmed: 24793693
Sci Rep. 2019 Mar 8;9(1):3913
pubmed: 30850632
J Exp Med. 2010 Jul 5;207(7):1351-8
pubmed: 20513743
RNA Biol. 2014;11(4):281-94
pubmed: 24643020
Biol Rev Camb Philos Soc. 2019 Apr;94(2):415-438
pubmed: 30151880
Nat Genet. 2013 Apr;45(4):415-21, 421e1-2
pubmed: 23435085
Sci Rep. 2017 Aug 1;7(1):7055
pubmed: 28765643
Proc Natl Acad Sci U S A. 2015 Dec 1;112(48):14918-23
pubmed: 26578810
Science. 1998 Nov 27;282(5394):1711-4
pubmed: 9831563
Front Genet. 2017 Mar 21;8:34
pubmed: 28377786
PLoS Biol. 2005 Oct;3(10):e314
pubmed: 16128622
PLoS Biol. 2011 Dec;9(12):e1001214
pubmed: 22162950
Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):14746-53
pubmed: 22908297
Gene. 2014 Aug 10;546(2):386-9
pubmed: 24835514
Mol Biol Evol. 2019 Aug 09;:
pubmed: 31397871
BMC Genomics. 2015 Nov 16;16:950
pubmed: 26574018
Dev Biol. 2016 Feb 1;410(1):1-13
pubmed: 26708096
Science. 2013 Jul 5;341(6141):71-3
pubmed: 23765281
Genome Biol Evol. 2014 Jul 22;6(8):1911-37
pubmed: 25053657
Annu Rev Genet. 2015;49:213-42
pubmed: 26473382
Genome Res. 2017 Oct;27(10):1665-1673
pubmed: 28904014
Mol Biol Evol. 2006 Nov;23(11):2008-16
pubmed: 16870682
Biol Reprod. 2013 Aug 15;89(2):34
pubmed: 23843232
BMC Genomics. 2013 Apr 02;14:214
pubmed: 23547919
Nucleic Acids Res. 2005 May 12;33(8):2697-706
pubmed: 15891114
J Evol Biol. 2021 Jun;34(6):977-988
pubmed: 33124163
Nat Neurosci. 2009 Apr;12(4):399-408
pubmed: 19287386
Nucleic Acids Res. 2008 Jan;36(Database issue):D154-8
pubmed: 17991681
Genome Biol. 2004;5(9):R68
pubmed: 15345052
Mol Cell. 2020 Apr 16;78(2):303-316.e4
pubmed: 32302542
Genome Res. 2004 Oct;14(10A):1902-10
pubmed: 15364901
Cell. 2012 Apr 27;149(3):515-24
pubmed: 22541426
Trends Genet. 2015 Nov;31(11):613-626
pubmed: 26453491
Nat Genet. 2006 Jun;38 Suppl:S20-4
pubmed: 16736020
Genetics. 1999 Apr;151(4):1531-45
pubmed: 10101175
Genome Biol Evol. 2016 Jun 03;8(5):1543-55
pubmed: 27189980
Bioinformatics. 2010 Apr 15;26(8):1119-21
pubmed: 20185404
Nucleic Acids Res. 2013 Sep;41(16):7745-52
pubmed: 23775791
Nucleic Acids Res. 2014 Aug;42(14):9424-35
pubmed: 25056318
Genes Dev. 2009 Mar 1;23(5):619-32
pubmed: 19240126
Cell. 2012 Mar 16;148(6):1172-87
pubmed: 22424228
Science. 2010 Jun 25;328(5986):1694-8
pubmed: 20448148
Curr Opin Genet Dev. 2014 Aug;27:1-6
pubmed: 24791686
Brief Funct Genomics. 2018 Jul 22;18(4):255-266
pubmed: 30785618
Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):E423-31
pubmed: 22308344
Mol Cell. 2007 Aug 3;27(3):435-48
pubmed: 17679093
Gene. 2013 Jan 10;512(2):383-91
pubmed: 23063939
Mol Biol Evol. 2019 Aug 1;36(8):1843
pubmed: 31099393
Cell. 2018 Mar 22;173(1):20-51
pubmed: 29570994
Dev Cell. 2012 May 15;22(5):1052-64
pubmed: 22595676
RNA. 2005 Mar;11(3):241-7
pubmed: 15701730
Science. 2015 Apr 3;348(6230):128-32
pubmed: 25838385
Mol Biol Evol. 2017 Jul 1;34(7):1812-1819
pubmed: 28387841
J Exp Zool B Mol Dev Evol. 2006 Nov 15;306(6):575-88
pubmed: 16838302
Biochim Biophys Acta Gene Regul Mech. 2020 Apr;1863(4):194373
pubmed: 30953728
Nucleic Acids Res. 2020 Jan 8;48(D1):D132-D141
pubmed: 31598695
Proc Natl Acad Sci U S A. 2015 Feb 3;112(5):1440-5
pubmed: 25605933
EMBO Rep. 2011 Feb;12(2):172-7
pubmed: 21212805
Nature. 2004 Oct 21;431(7011):946-57
pubmed: 15496914
Development. 2017 Jul 15;144(14):2548-2559
pubmed: 28720652
DNA Cell Biol. 2007 Apr;26(4):209-18
pubmed: 17465887
Nat Ecol Evol. 2019 Mar;3(3):469-478
pubmed: 30804520
Genes (Basel). 2019 Apr 25;10(4):
pubmed: 31027314
Cell. 2009 Jan 23;136(2):215-33
pubmed: 19167326
Proc Biol Sci. 2014 Jan 22;281(1778):20132881
pubmed: 24452024
Bioinformatics. 2020 Feb 1;36(3):698-703
pubmed: 31504201
Genome Res. 2013 Jan;23(1):34-45
pubmed: 23034410
Science. 2006 Apr 7;312(5770):75-9
pubmed: 16484454
Genome Biol Evol. 2010;2:686-96
pubmed: 20817720
Plant Cell. 2012 May;24(5):1776-92
pubmed: 22589464
Nat Genet. 2006 Jun;38(6):601-2
pubmed: 16736008
EMBO J. 2019 Jul 1;38(13):e101153
pubmed: 31268608
Database (Oxford). 2014 Oct 06;2014:
pubmed: 25288656
Diabetologia. 2013 Jul;56(7):1547-56
pubmed: 23595248
Nat Ecol Evol. 2020 Jun;4(6):820-830
pubmed: 32313176
Genome Biol Evol. 2011;3:55-65
pubmed: 21169229
Science. 2019 Dec 20;366(6472):
pubmed: 31806698
Proc Natl Acad Sci U S A. 2010 Aug 24;107(34):15163-8
pubmed: 20699384
Nat Neurosci. 2008 Jun;11(6):641-8
pubmed: 18454145
Nucleic Acids Res. 2019 Jan 8;47(D1):D867-D873
pubmed: 30407545
Cell. 2013 Dec 19;155(7):1556-67
pubmed: 24360277
Genes Dev. 2010 May 15;24(10):992-1009
pubmed: 20413612
Clin Cancer Res. 2010 Feb 15;16(4):1119-28
pubmed: 20145172
Curr Biol. 2017 Jun 5;27(11):R550-R557
pubmed: 28586692
Sci Rep. 2019 Sep 25;9(1):13848
pubmed: 31554838
Mar Genomics. 2016 Dec;30:27-34
pubmed: 27189439
Genome Res. 2009 May;19(5):734-43
pubmed: 19411598
Mol Cell. 2020 Apr 16;78(2):289-302.e6
pubmed: 32302541
Nat Genet. 2006 Feb;38(2):228-33
pubmed: 16380711
Evol Dev. 2011 Jan-Feb;13(1):15-27
pubmed: 21210939
BMC Genomics. 2006 Feb 15;7:25
pubmed: 16480513
BMC Evol Biol. 2013 Jul 06;13:142
pubmed: 24059862
Mol Biol Evol. 2006 Sep;23(9):1808-16
pubmed: 16809621
Mol Biol Evol. 2016 Sep;33(9):2232-47
pubmed: 27189568
Evol Dev. 2009 Jan-Feb;11(1):50-68
pubmed: 19196333
Semin Cell Dev Biol. 2018 Mar;75:3-12
pubmed: 28811264
Life (Basel). 2015 Mar 13;5(1):905-20
pubmed: 25780960
J Exp Clin Cancer Res. 2019 Feb 4;38(1):53
pubmed: 30717802
Nat Rev Genet. 2009 Oct;10(10):725-32
pubmed: 19652647
J Exp Zool B Mol Dev Evol. 2017 Nov;328(7):709-721
pubmed: 28944589
Nucleic Acids Res. 2017 Jan 4;45(D1):D635-D642
pubmed: 27899575
Genes Dev. 2005 Oct 1;19(19):2343-54
pubmed: 16166373
Annu Rev Anim Biosci. 2020 Feb 15;8:47-69
pubmed: 31525067
BMC Genomics. 2010 Oct 01;11:533
pubmed: 20920310
Genome Res. 2017 Oct;27(10):1769-1781
pubmed: 28877962
Oncotarget. 2014 Feb 28;5(4):872-81
pubmed: 24657911
Plant J. 2017 Feb;89(3):442-457
pubmed: 27743419
Mol Cell. 2016 Nov 3;64(3):565-579
pubmed: 27871486
Plant Cell. 2015 Mar;27(3):546-62
pubmed: 25747880
Nat Rev Genet. 2015 Jul;16(7):421-33
pubmed: 26077373
Trends Genet. 2012 Nov;28(11):544-9
pubmed: 22883467
Dev Cell. 2017 Mar 27;40(6):552-565.e5
pubmed: 28350988