Paternally Expressed Imprinted Genes under Positive Darwinian Selection in Arabidopsis thaliana.
endosperm
genomic conflict
genomic imprinting
plant evolution
positive Darwinian selection
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:
01 06 2019
01 06 2019
Historique:
pubmed:
27
3
2019
medline:
19
7
2019
entrez:
27
3
2019
Statut:
ppublish
Résumé
Genomic imprinting is an epigenetic phenomenon where autosomal genes display uniparental expression depending on whether they are maternally or paternally inherited. Genomic imprinting can arise from parental conflicts over resource allocation to the offspring, which could drive imprinted loci to evolve by positive selection. We investigate whether positive selection is associated with genomic imprinting in the inbreeding species Arabidopsis thaliana. Our analysis of 140 genes regulated by genomic imprinting in the A. thaliana seed endosperm demonstrates they are evolving more rapidly than expected. To investigate whether positive selection drives this evolutionary acceleration, we identified orthologs of each imprinted gene across 34 plant species and elucidated their evolutionary trajectories. Increased positive selection was sought by comparing its incidence among imprinted genes with nonimprinted controls. Strikingly, we find a statistically significant enrichment of imprinted paternally expressed genes (iPEGs) evolving under positive selection, 50.6% of the total, but no such enrichment for positive selection among imprinted maternally expressed genes (iMEGs). This suggests that maternally- and paternally expressed imprinted genes are subject to different selective pressures. Almost all positively selected amino acids were fixed across 80 sequenced A. thaliana accessions, suggestive of selective sweeps in the A. thaliana lineage. The imprinted genes under positive selection are involved in processes important for seed development including auxin biosynthesis and epigenetic regulation. Our findings support a genomic imprinting model for plants where positive selection can affect paternally expressed genes due to continued conflict with maternal sporophyte tissues, even when parental conflict is reduced in predominantly inbreeding species.
Identifiants
pubmed: 30913563
pii: 5380439
doi: 10.1093/molbev/msz063
pmc: PMC6526901
doi:
Substances chimiques
Arabidopsis Proteins
0
DNA-Directed RNA Polymerases
EC 2.7.7.6
NRPD1A protein, Arabidopsis
EC 2.7.7.6
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1239-1253Informations de copyright
© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
Proc Biol Sci. 1998 Dec 22;265(1413):2393-7
pubmed: 10075542
Genes Dev. 1999 Nov 15;13(22):2971-82
pubmed: 10580004
Bioinformatics. 2000 Jul;16(7):573-82
pubmed: 11038328
Mol Biol Evol. 2001 Aug;18(8):1585-92
pubmed: 11470850
Proc Biol Sci. 2001 Sep 22;268(1479):1861-7
pubmed: 11564340
J Mol Biol. 2001 Dec 7;314(4):937-51
pubmed: 11734009
Nature. 2002 Apr 4;416(6880):531-4
pubmed: 11932744
Mol Biol Evol. 2002 Jun;19(6):908-17
pubmed: 12032247
Genome Biol. 2002 Aug 30;3(9):reviews1026
pubmed: 12225592
Proc Biol Sci. 2002 Sep 7;269(1502):1841-6
pubmed: 12350273
Mol Biol Evol. 2002 Nov;19(11):1973-80
pubmed: 12411606
J Physiol. 2003 Feb 15;547(Pt 1):35-44
pubmed: 12562908
Nature. 2003 Mar 27;422(6930):433-8
pubmed: 12660784
Trends Genet. 2003 May;19(5):248-52
pubmed: 12711215
J Theor Biol. 2003 Apr 21;221(4):559-64
pubmed: 12713940
Nat Rev Genet. 2003 May;4(5):359-68
pubmed: 12728278
Nat Rev Genet. 2003 May;4(5):369-79
pubmed: 12728279
Bioinformatics. 2003 Jun 12;19(9):1155-61
pubmed: 12801878
Genome Res. 2003 Sep;13(9):2178-89
pubmed: 12952885
Science. 2004 Jan 23;303(5657):521-3
pubmed: 14631047
Nucleic Acids Res. 2004 Jan 1;32(Database issue):D354-9
pubmed: 14681433
Science. 2004 Feb 13;303(5660):971-5
pubmed: 14963320
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Am Nat. 2004 May;163(5):635-53
pubmed: 15122484
J Mol Evol. 1992 Feb;34(2):126-9
pubmed: 1556748
Annu Rev Genet. 2004;38:553-85
pubmed: 15568986
Genetics. 2004 Dec;168(4):2317-27
pubmed: 15611195
Nat Genet. 2005 Jan;37(1):28-30
pubmed: 15619622
AIDS Res Hum Retroviruses. 2005 Jan;21(1):98-102
pubmed: 15665649
Mol Biol Evol. 2005 May;22(5):1208-22
pubmed: 15703242
Nat Genet. 2005 Jul;37(7):761-5
pubmed: 15924141
Am Nat. 2005 Sep;166(3):330-8
pubmed: 16224688
Annu Rev Genet. 2005;39:197-218
pubmed: 16285858
Reproduction. 2006 Jan;131(1):11-22
pubmed: 16388004
Nat Rev Genet. 2006 Feb;7(2):98-108
pubmed: 16418745
BMC Evol Biol. 2006 Mar 24;6:29
pubmed: 16563161
Plant Cell. 2006 Jun;18(6):1360-72
pubmed: 16648367
Science. 2006 Jun 16;312(5780):1614-20
pubmed: 16778047
Bioinformatics. 2006 Nov 1;22(21):2688-90
pubmed: 16928733
PLoS Biol. 2006 Nov;4(12):e380
pubmed: 17105351
J Mol Evol. 2007 Jan;64(1):101-12
pubmed: 17160640
PLoS One. 2007 Apr 18;2(4):e383
pubmed: 17440619
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Nature. 2007 Jul 19;448(7151):349-52
pubmed: 17637669
Trends Genet. 2007 Nov;23(11):533-9
pubmed: 18029048
Epigenetics. 2008 Jan-Feb;3(1):14-20
pubmed: 18259119
Brief Bioinform. 2008 Jul;9(4):286-98
pubmed: 18372315
Plant J. 2008 Aug;55(4):596-606
pubmed: 18433438
J R Soc Interface. 2008 Nov 6;5(28):1279-89
pubmed: 18664425
Plant Cell. 2008 Sep;20(9):2387-98
pubmed: 18796636
PLoS One. 2008;3(11):e3746
pubmed: 19015730
Nature. 1991 Jun 20;351(6328):652-4
pubmed: 1904993
PLoS Genet. 2008 Dec;4(12):e1000304
pubmed: 19081788
Mol Biol Evol. 2009 Apr;26(4):843-57
pubmed: 19126870
Mol Biol Evol. 2009 May;26(5):1073-9
pubmed: 19188264
New Phytol. 2009 Aug;183(3):565-74
pubmed: 19413690
Nature. 2009 Jul 9;460(7252):283-6
pubmed: 19494814
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
Science. 2009 Jun 12;324(5933):1447-51
pubmed: 19520961
Biochem Soc Trans. 2009 Aug;37(Pt 4):756-61
pubmed: 19614589
Development. 2009 Oct;136(20):3399-404
pubmed: 19783734
Bioinformatics. 2010 Jan 15;26(2):263-5
pubmed: 19926669
Science. 2009 Nov 20;326(5956):1118-20
pubmed: 19965432
Neurogenetics. 2010 May;11(2):153-61
pubmed: 20020165
BMC Evol Biol. 2010 Feb 11;10:39
pubmed: 20149245
Trends Genet. 1991 Feb;7(2):45-9
pubmed: 2035190
PLoS Genet. 2010 Mar 26;6(3):e1000890
pubmed: 20361058
Proc Biol Sci. 2010 Sep 22;277(1695):2885-93
pubmed: 20444721
Bioinformatics. 2010 Oct 1;26(19):2462-3
pubmed: 20798170
Mol Biol Evol. 2011 Jan;28(1):63-70
pubmed: 20837603
Mamm Genome. 2010 Oct;21(9-10):486-98
pubmed: 20931201
Evolution. 2011 Feb;65(2):537-53
pubmed: 21029079
Mol Biol Evol. 2011 Mar;28(3):1193-203
pubmed: 21059790
Evolution. 2011 May;65(5):1413-27
pubmed: 21166792
Trends Plant Sci. 2011 Feb;16(2):108-16
pubmed: 21177137
Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1755-62
pubmed: 21257907
BMC Evol Biol. 2011 Feb 18;11:47
pubmed: 21332978
PLoS Genet. 2011 Feb;7(2):e1001303
pubmed: 21379330
Genome Res. 2011 Jun;21(6):863-74
pubmed: 21393387
PLoS Genet. 2011 Jun;7(6):e1002126
pubmed: 21698132
Genome Biol Evol. 2011;3:687-701
pubmed: 21705473
BMC Plant Biol. 2011 Aug 12;11:113
pubmed: 21838868
PLoS One. 2011;6(8):e23687
pubmed: 21858209
Nat Genet. 2011 Aug 28;43(10):956-63
pubmed: 21874002
Nat Biotechnol. 2011 Nov 06;30(1):83-9
pubmed: 22057054
Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86
pubmed: 22110026
Curr Biol. 2012 Jan 24;22(2):160-5
pubmed: 22245001
Annu Rev Plant Biol. 2012;63:331-52
pubmed: 22404470
PLoS Genet. 2012;8(7):e1002764
pubmed: 22807683
PLoS One. 2012;7(12):e51769
pubmed: 23272162
Proc Natl Acad Sci U S A. 2013 Jan 29;110(5):E435-44
pubmed: 23319655
Annu Rev Cell Dev Biol. 2013;29:189-211
pubmed: 23641801
Am Nat. 2013 Jun;181(6):787-98
pubmed: 23669541
Mol Biol Evol. 2013 Nov;30(11):2475-86
pubmed: 23997108
Dev Cell. 2013 Sep 16;26(5):525-35
pubmed: 24012484
Proc Natl Acad Sci U S A. 2013 Sep 24;110(39):15836-41
pubmed: 24019480
Heredity (Edinb). 2014 Aug;113(2):96-103
pubmed: 24129605
Mol Biol Evol. 2014 Mar;31(3):574-83
pubmed: 24273323
Heredity (Edinb). 2014 Aug;113(2):129-37
pubmed: 24619179
PLoS Genet. 2014 Mar 27;10(3):e1004222
pubmed: 24675740
Philos Trans R Soc Lond B Biol Sci. 2014 Aug 5;369(1648):null
pubmed: 24958926
Cold Spring Harb Perspect Biol. 2014 Jul 24;6(9):a017525
pubmed: 25059710
Genome Biol Evol. 2014 Jul;6(7):1830-42
pubmed: 25115008
Mol Biol Evol. 2014 Nov;31(11):3026-39
pubmed: 25158800
Plant Reprod. 2015 Mar;28(1):17-32
pubmed: 25656951
Genome Biol Evol. 2015 May 13;7(6):1546-58
pubmed: 25971280
Mol Biol Evol. 1989 Sep;6(5):526-38
pubmed: 2677599
Plant Cell. 2016 Jun;28(6):1343-60
pubmed: 27233529
New Phytol. 2016 Dec;212(4):1094-1105
pubmed: 27431917
Plant Cell. 2016 Aug;28(8):1815-27
pubmed: 27465027
Nat Plants. 2016 Sep 19;2:16145
pubmed: 27643534
Plant Physiol. 2017 Jan;173(1):143-154
pubmed: 27895206
Plant Cell. 2017 Apr;29(4):608-617
pubmed: 28314828
Plant J. 2017 Dec;92(6):1044-1058
pubmed: 29024088
Cell Rep. 2017 Dec 19;21(12):3364-3372
pubmed: 29262317
Genome Biol Evol. 2018 Mar 1;10(3):895-900
pubmed: 29608724
Sci Rep. 2019 Feb 4;9(1):1320
pubmed: 30718537
Proc Biol Sci. 1997 May 22;264(1382):739-46
pubmed: 9178545
Proc Biol Sci. 1997 Nov 22;264(1388):1657-62
pubmed: 9404029
Mol Biol Evol. 1998 May;15(5):568-73
pubmed: 9580986