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Mechanistic basis for maintenance of CHG DNA methylation in plants

Author

Listed:
  • Jian Fang

    (University of California)

  • Jianjun Jiang

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Sarah M. Leichter

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Jie Liu

    (University of Wisconsin-Madison)

  • Mahamaya Biswal

    (University of California)

  • Nelli Khudaverdyan

    (University of California)

  • Xuehua Zhong

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Jikui Song

    (University of California)

Abstract

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.

Suggested Citation

  • Jian Fang & Jianjun Jiang & Sarah M. Leichter & Jie Liu & Mahamaya Biswal & Nelli Khudaverdyan & Xuehua Zhong & Jikui Song, 2022. "Mechanistic basis for maintenance of CHG DNA methylation in plants," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31627-3
    DOI: 10.1038/s41467-022-31627-3
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    References listed on IDEAS

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    1. Ryan Lister & Mattia Pelizzola & Robert H. Dowen & R. David Hawkins & Gary Hon & Julian Tonti-Filippini & Joseph R. Nery & Leonard Lee & Zhen Ye & Que-Minh Ngo & Lee Edsall & Jessica Antosiewicz-Bourg, 2009. "Human DNA methylomes at base resolution show widespread epigenomic differences," Nature, Nature, vol. 462(7271), pages 315-322, November.
    2. Linfeng Gao & Max Emperle & Yiran Guo & Sara A. Grimm & Wendan Ren & Sabrina Adam & Hidetaka Uryu & Zhi-Min Zhang & Dongliang Chen & Jiekai Yin & Michael Dukatz & Hiwot Anteneh & Renata Z. Jurkowska &, 2020. "Comprehensive structure-function characterization of DNMT3B and DNMT3A reveals distinctive de novo DNA methylation mechanisms," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. Hiwot Anteneh & Jian Fang & Jikui Song, 2020. "Structural basis for impairment of DNA methylation by the DNMT3A R882H mutation," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    4. Zhi-Min Zhang & Rui Lu & Pengcheng Wang & Yang Yu & Dongliang Chen & Linfeng Gao & Shuo Liu & Debin Ji & Scott B Rothbart & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2018. "Structural basis for DNMT3A-mediated de novo DNA methylation," Nature, Nature, vol. 554(7692), pages 387-391, February.
    5. Shawn J. Cokus & Suhua Feng & Xiaoyu Zhang & Zugen Chen & Barry Merriman & Christian D. Haudenschild & Sriharsa Pradhan & Stanley F. Nelson & Matteo Pellegrini & Steven E. Jacobsen, 2008. "Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning," Nature, Nature, vol. 452(7184), pages 215-219, March.
    6. Cuijun Zhang & Xuan Du & Kai Tang & Zhenlin Yang & Li Pan & Peipei Zhu & Jinyan Luo & Yuwei Jiang & Hui Zhang & Huafang Wan & Xingang Wang & Fengkai Wu & W. Andy Tao & Xin-Jian He & Heng Zhang & Ray A, 2018. "Arabidopsis AGDP1 links H3K9me2 to DNA methylation in heterochromatin," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
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    Cited by:

    1. Jie Liu & Xuehua Zhong, 2024. "Epiallelic variation of non-coding RNA genes and their phenotypic consequences," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Zengyu Shao & Jiuwei Lu & Nelli Khudaverdyan & Jikui Song, 2024. "Multi-layered heterochromatin interaction as a switch for DIM2-mediated DNA methylation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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