Mechanistic basis for maintenance of CHG DNA methylation in plants

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. H...

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Autores principales: Fang, Jian, Jiang, Jianjun, Leichter, Sarah M., Liu, Jie, Biswal, Mahamaya, Khudaverdyan, Nelli, Zhong, Xuehua, Song, Jikui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
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Article
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9256654/
https://www.ncbi.nlm.nih.gov/pubmed/35790763
http://dx.doi.org/10.1038/s41467-022-31627-3
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author Fang, Jian
Jiang, Jianjun
Leichter, Sarah M.
Liu, Jie
Biswal, Mahamaya
Khudaverdyan, Nelli
Zhong, Xuehua
Song, Jikui
author_facet Fang, Jian
Jiang, Jianjun
Leichter, Sarah M.
Liu, Jie
Biswal, Mahamaya
Khudaverdyan, Nelli
Zhong, Xuehua
Song, Jikui
author_sort Fang, Jian
collection PubMed
description 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.
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spelling pubmed-92566542022-07-07 Mechanistic basis for maintenance of CHG DNA methylation in plants Fang, Jian Jiang, Jianjun Leichter, Sarah M. Liu, Jie Biswal, Mahamaya Khudaverdyan, Nelli Zhong, Xuehua Song, Jikui Nat Commun Article 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. Nature Publishing Group UK 2022-07-05 /pmc/articles/PMC9256654/ /pubmed/35790763 http://dx.doi.org/10.1038/s41467-022-31627-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Fang, Jian
Jiang, Jianjun
Leichter, Sarah M.
Liu, Jie
Biswal, Mahamaya
Khudaverdyan, Nelli
Zhong, Xuehua
Song, Jikui
Mechanistic basis for maintenance of CHG DNA methylation in plants
title Mechanistic basis for maintenance of CHG DNA methylation in plants
title_full Mechanistic basis for maintenance of CHG DNA methylation in plants
title_fullStr Mechanistic basis for maintenance of CHG DNA methylation in plants
title_full_unstemmed Mechanistic basis for maintenance of CHG DNA methylation in plants
title_short Mechanistic basis for maintenance of CHG DNA methylation in plants
title_sort mechanistic basis for maintenance of chg dna methylation in plants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9256654/
https://www.ncbi.nlm.nih.gov/pubmed/35790763
http://dx.doi.org/10.1038/s41467-022-31627-3
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