H3.1K27me1 maintains transcriptional silencing and genome stability by preventing GCN5-mediated histone acetylation.
Acetylation
Arabidopsis
/ genetics
Arabidopsis Proteins
/ genetics
Gene Silencing
Genome, Plant
Genomic Instability
Heterochromatin
/ genetics
Histone Acetyltransferases
/ genetics
Histones
/ genetics
Lysine
/ genetics
Methylation
Methyltransferases
/ genetics
Mutation
Plants, Genetically Modified
Transcription Factors
/ genetics
Journal
The Plant cell
ISSN: 1532-298X
Titre abrégé: Plant Cell
Pays: England
ID NLM: 9208688
Informations de publication
Date de publication:
31 05 2021
31 05 2021
Historique:
received:
04
08
2020
accepted:
25
11
2020
pubmed:
2
4
2021
medline:
21
8
2021
entrez:
1
4
2021
Statut:
ppublish
Résumé
Epigenetic mechanisms play diverse roles in the regulation of genome stability in eukaryotes. In Arabidopsis thaliana, genome stability is maintained during DNA replication by the H3.1K27 methyltransferases ARABIDOPSIS TRITHORAX-RELATED PROTEIN 5 (ATXR5) and ATXR6, which catalyze the deposition of K27me1 on replication-dependent H3.1 variants. The loss of H3.1K27me1 in atxr5 atxr6 double mutants leads to heterochromatin defects, including transcriptional de-repression and genomic instability, but the molecular mechanisms involved remain largely unknown. In this study, we identified the transcriptional co-activator and conserved histone acetyltransferase GCN5 as a mediator of transcriptional de-repression and genomic instability in the absence of H3.1K27me1. GCN5 is part of a SAGA-like complex in plants that requires the GCN5-interacting protein ADA2b and the chromatin remodeler CHR6 to mediate the heterochromatic defects in atxr5 atxr6 mutants. Our results also indicate that Arabidopsis GCN5 acetylates multiple lysine residues on H3.1 variants, but H3.1K27 and H3.1K36 play essential functions in inducing genomic instability in the absence of H3.1K27me1. Finally, we show that H3.1K36 acetylation by GCN5 is negatively regulated by H3.1K27me1 in vitro. Overall, this work reveals a key molecular role for H3.1K27me1 in maintaining transcriptional silencing and genome stability in heterochromatin by restricting GCN5-mediated histone acetylation in plants.
Identifiants
pubmed: 33793815
pii: 6025186
doi: 10.1093/plcell/koaa027
pmc: PMC8226292
mid: EMS147746
doi:
Substances chimiques
ADA2b protein, Arabidopsis
0
Arabidopsis Proteins
0
Heterochromatin
0
Histones
0
Transcription Factors
0
ATXR5 protein, Arabidopsis
EC 2.1.1.-
ATXR6 protein, Arabidopsis
EC 2.1.1.-
Methyltransferases
EC 2.1.1.-
GCN5 protein, Arabidopsis
EC 2.3.1.48
Histone Acetyltransferases
EC 2.3.1.48
Lysine
K3Z4F929H6
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
961-979Subventions
Organisme : Wellcome Trust
ID : 203149
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 104175/Z/14/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 101527/Z/13/Z
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R35 GM128661
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Informations de copyright
� American Society of Plant Biologists 2021. All rights reserved. For permissions, please email: journals.permissions@oup.com.
Références
Development. 2009 Sep;136(18):3131-41
pubmed: 19700617
Nucleic Acids Res. 2004 Dec 14;32(22):6511-8
pubmed: 15598823
Plant Physiol. 2004 Mar;134(3):995-1005
pubmed: 14963244
Science. 2014 Mar 14;343(6176):1249-53
pubmed: 24626927
Nucleic Acids Res. 2017 Jun 20;45(11):6375-6387
pubmed: 28383693
J Biol Chem. 2011 Mar 11;286(10):7983-7989
pubmed: 21239496
Plant Physiol. 2016 Mar;170(3):1566-77
pubmed: 26764380
Methods Mol Biol. 2018;1675:345-360
pubmed: 29052201
Mol Cell Biol. 2008 Jan;28(1):227-36
pubmed: 17938198
Mol Cell Proteomics. 2014 Nov;13(11):2896-910
pubmed: 25106422
FEBS J. 2015 Feb;282(4):630-46
pubmed: 25400280
Plant Cell. 2003 Mar;15(3):626-38
pubmed: 12615937
Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13839-44
pubmed: 10570159
Genomics. 2015 Oct;106(4):214-20
pubmed: 26021446
Nature. 1996 Sep 19;383(6597):269-72
pubmed: 8805705
PLoS One. 2017 Oct 26;12(10):e0185056
pubmed: 29073143
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Plant J. 2007 Nov;52(4):615-26
pubmed: 17877703
Mol Cell. 2011 May 6;42(3):330-41
pubmed: 21549310
Nat Genet. 2008 Jul;40(7):897-903
pubmed: 18552846
Mol Cell. 2014 Jan 9;53(1):49-62
pubmed: 24289921
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
Plant J. 1998 Dec;16(6):735-43
pubmed: 10069079
Front Plant Sci. 2015 Oct 14;6:865
pubmed: 26528322
Mol Cell. 2001 Aug;8(2):473-9
pubmed: 11545749
Nucleic Acids Res. 2001 Nov 1;29(21):4319-33
pubmed: 11691919
Plant Signal Behav. 2014;9(3):e28173
pubmed: 24614176
Nucleic Acids Res. 2010 Aug;38(15):4958-69
pubmed: 20385584
Plant Cell. 2009 Apr;21(4):1070-9
pubmed: 19376933
Mol Cell. 2003 Aug;12(2):461-73
pubmed: 14536085
Elife. 2020 Jul 20;9:
pubmed: 32687055
Genome Biol. 2014;15(12):550
pubmed: 25516281
Cold Spring Harb Perspect Biol. 2015 Apr 01;7(4):a016600
pubmed: 25833843
Methods Mol Biol. 2010;655:401-11
pubmed: 20734276
Genome Biol. 2005;6(8):227
pubmed: 16086857
Elife. 2018 Sep 07;7:
pubmed: 30192741
Nucleic Acids Res. 2002 Dec 1;30(23):5036-55
pubmed: 12466527
Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19266-71
pubmed: 20974918
PLoS One. 2013;8(2):e54896
pubmed: 23437046
J Mol Biol. 2018 May 11;430(10):1479-1494
pubmed: 29588169
Plant J. 2018 Jan;93(2):377-386
pubmed: 29161464
Nat Struct Mol Biol. 2009 Jul;16(7):763-8
pubmed: 19503079
Dev Cell. 2018 Jun 18;45(6):769-784.e6
pubmed: 29920280
Plant Physiol. 2003 Oct;133(2):462-9
pubmed: 14555774
Genes Dev. 2012 Mar 15;26(6):527-41
pubmed: 22426530
Nucleic Acids Res. 2020 Jun 19;48(11):5953-5966
pubmed: 32396165
Nature. 2010 Aug 19;466(7309):987-91
pubmed: 20631708
Nature. 2009 Oct 8;461(7265):762-7
pubmed: 19767730
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Plant Physiol. 2003 Jun;132(2):907-25
pubmed: 12805620
Nat Plants. 2017 Oct;3(10):814-824
pubmed: 28947800
PLoS Genet. 2012 Jul;8(7):e1002808
pubmed: 22792077
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Nat Commun. 2019 Apr 12;10(1):1705
pubmed: 30979870
PLoS One. 2015 Aug 11;10(8):e0134709
pubmed: 26263547
Plant J. 2006 Aug;47(3):395-407
pubmed: 16771839
PLoS Genet. 2016 Jun 02;12(6):e1006092
pubmed: 27253878
Trends Plant Sci. 2002 May;7(5):193-5
pubmed: 11992820
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
Genes Dev. 2003 Aug 1;17(15):1870-81
pubmed: 12897054
J Mol Biol. 2019 Mar 29;431(7):1370-1379
pubmed: 30826376
Nat Struct Mol Biol. 2012 Dec;19(12):1218-27
pubmed: 23211769
Plant Cell Physiol. 2017 Dec 1;58(12):2202-2216
pubmed: 29048607
Mol Plant. 2013 Sep;6(5):1463-72
pubmed: 23355544
Nat Cell Biol. 2008 Nov;10(11):1291-300
pubmed: 18931660
Curr Opin Cell Biol. 2009 Dec;21(6):778-84
pubmed: 19913398
Semin Cancer Biol. 2010 Aug;20(4):222-33
pubmed: 20541013
EMBO J. 1998 Jun 1;17(11):3155-67
pubmed: 9606197
Mol Cell Proteomics. 2010 May;9(5):838-50
pubmed: 20150217
Science. 1990 Feb 16;247(4944):841-5
pubmed: 2106160
Science. 1997 Jul 4;277(5322):91-4
pubmed: 9204906
Cell. 2012 Sep 28;151(1):181-93
pubmed: 23021224
Plant Cell. 2014 Jun 16;26(6):2351-2366
pubmed: 24934173
Cell Rep. 2014 Nov 6;9(3):1163-70
pubmed: 25437568
BMC Genomics. 2019 Jun 28;20(1):533
pubmed: 31253095
Mol Cell. 2003 Dec;12(6):1577-89
pubmed: 14690609
Mol Plant. 2015 Dec 7;8(12):1820-3
pubmed: 26524930