Mechanistic basis for maintenance of CHG DNA methylation in plants.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 07 2022
Historique:
received: 15 10 2021
accepted: 26 06 2022
entrez: 5 7 2022
pubmed: 6 7 2022
medline: 8 7 2022
Statut: epublish

Résumé

DNA methylation is an evolutionarily conserved epigenetic mechanism essential for transposon silencing and heterochromatin assembly. In plants, DNA methylation widely occurs in the CG, CHG, and CHH (H = A, C, or T) contexts, with the maintenance of CHG methylation mediated by CMT3 chromomethylase. However, how CMT3 interacts with the chromatin environment for faithful maintenance of CHG methylation is unclear. Here we report structure-function characterization of the H3K9me2-directed maintenance of CHG methylation by CMT3 and its Zea mays ortholog ZMET2. Base-specific interactions and DNA deformation coordinately underpin the substrate specificity of CMT3 and ZMET2, while a bivalent readout of H3K9me2 and H3K18 allosterically stimulates substrate binding. Disruption of the interaction with DNA or H3K9me2/H3K18 led to loss of CMT3/ZMET2 activity in vitro and impairment of genome-wide CHG methylation in vivo. Together, our study uncovers how the intricate interplay of CMT3, repressive histone marks, and DNA sequence mediates heterochromatic CHG methylation.

Identifiants

pubmed: 35790763
doi: 10.1038/s41467-022-31627-3
pii: 10.1038/s41467-022-31627-3
pmc: PMC9256654
doi:

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

3877

Subventions

Organisme : NIAID NIH HHS
ID : R21 AI147057
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM124806
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM119721
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007133
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008349
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Nat Rev Mol Cell Biol. 2018 Aug;19(8):489-506
pubmed: 29784956
Nucleic Acids Res. 1993 May 25;21(10):2383-8
pubmed: 8389441
Bioinformatics. 2018 Sep 1;34(17):i884-i890
pubmed: 30423086
Nat Struct Mol Biol. 2014 Jan;21(1):64-72
pubmed: 24336224
Nat Commun. 2020 May 8;11(1):2294
pubmed: 32385248
Nucleic Acids Res. 1996 Jun 15;24(12):2260-7
pubmed: 8710494
Genes (Basel). 2018 Dec 11;9(12):
pubmed: 30544982
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Nat Rev Genet. 2009 May;10(5):295-304
pubmed: 19308066
Nucleic Acids Res. 2020 Apr 17;48(7):3949-3961
pubmed: 32083663
BMC Bioinformatics. 2009 Jul 27;10:232
pubmed: 19635165
Cell. 1995 Jul 14;82(1):143-53
pubmed: 7606780
Cell. 2012 Feb 17;148(4):816-31
pubmed: 22341451
Nat Rev Mol Cell Biol. 2015 Sep;16(9):519-32
pubmed: 26296162
Nucleic Acids Res. 2021 Sep 27;49(17):9755-9767
pubmed: 34403482
Science. 2012 Jun 15;336(6087):1445-8
pubmed: 22700931
Nat Rev Genet. 2010 Mar;11(3):204-20
pubmed: 20142834
Genome Res. 2010 Mar;20(3):320-31
pubmed: 20133333
Nat Rev Genet. 2014 Jun;15(6):394-408
pubmed: 24805120
Biopolymers. 1978 Oct;17(10):2341-60
pubmed: 24624489
Blood. 2015 Jan 8;125(2):346-57
pubmed: 25395428
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Annu Rev Genomics Hum Genet. 2015;16:55-77
pubmed: 26077819
Silence. 2013 Apr 05;4(1):1
pubmed: 23561294
J Biol Chem. 2005 May 27;280(21):20216-21
pubmed: 15784615
Methods Enzymol. 1997;276:307-26
pubmed: 27754618
Cell. 2012 Sep 28;151(1):167-80
pubmed: 23021223
Cell. 2013 Jan 17;152(1-2):352-64
pubmed: 23313553
Plant Cell. 2001 Aug;13(8):1919-28
pubmed: 11487702
Nature. 2009 Nov 19;462(7271):315-22
pubmed: 19829295
Nat Commun. 2018 Oct 31;9(1):4547
pubmed: 30382101
Nature. 2008 Mar 13;452(7184):215-9
pubmed: 18278030
Nature. 2018 Feb 15;554(7692):387-391
pubmed: 29414941
Science. 2001 Jun 15;292(5524):2077-80
pubmed: 11349138
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Cell. 2007 Mar 9;128(5):1003-12
pubmed: 17350582
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Science. 2010 May 14;328(5980):916-9
pubmed: 20395474
Nat Plants. 2017 Oct;3(10):814-824
pubmed: 28947800
Plant J. 2010 Feb 1;61(3):519-28
pubmed: 19891705
Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1948-54
pubmed: 12393927
PLoS Genet. 2016 Dec 20;12(12):e1006526
pubmed: 27997534
Nature. 2000 Jan 6;403(6765):41-5
pubmed: 10638745
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91
pubmed: 24799436
Science. 2012 Feb 10;335(6069):709-12
pubmed: 22323818
Nat Commun. 2020 Jul 24;11(1):3723
pubmed: 32709850
Biochemistry. 1988 Jul 12;27(14):5204-10
pubmed: 3167042
Nucleic Acids Res. 2017 Apr 20;45(7):3777-3784
pubmed: 28053115
Mol Cell. 2019 Jan 3;73(1):73-83.e6
pubmed: 30415948
Nat Commun. 2020 Jul 3;11(1):3355
pubmed: 32620778
Cell. 1994 Jan 28;76(2):357-69
pubmed: 8293469
J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674
pubmed: 19461840
Nat Plants. 2016 Oct 31;2(11):16169
pubmed: 27797352
Sci Adv. 2021 Jun 2;7(23):
pubmed: 34078593
Genome Res. 2013 Oct;23(10):1651-62
pubmed: 23739895
Genes Dev. 2002 Jan 1;16(1):6-21
pubmed: 11782440

Auteurs

Jian Fang (J)

Department of Biochemistry, University of California, Riverside, CA, 92521, USA.

Jianjun Jiang (J)

Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI, 53706, USA.
Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, WI, 53715, USA.

Sarah M Leichter (SM)

Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI, 53706, USA.
Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, WI, 53715, USA.

Jie Liu (J)

Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, WI, 53715, USA.

Mahamaya Biswal (M)

Department of Biochemistry, University of California, Riverside, CA, 92521, USA.

Nelli Khudaverdyan (N)

Department of Biochemistry, University of California, Riverside, CA, 92521, USA.

Xuehua Zhong (X)

Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI, 53706, USA. xuehua.zhong@wisc.edu.
Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, WI, 53715, USA. xuehua.zhong@wisc.edu.

Jikui Song (J)

Department of Biochemistry, University of California, Riverside, CA, 92521, USA. jikui.song@ucr.edu.

Articles similaires

Zea mays Triticum China Seasons Crops, Agricultural
Humans DNA Methylation Female Male Alcohol Oxidoreductases
Animals Epigenesis, Genetic DNA Methylation Skates, Fish CpG Islands

Classifications MeSH