IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31627-3.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31627-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-31627-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Xinyi Chen & Yiran Guo & Ting Zhao & Jiuwei Lu & Jian Fang & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2024. "Structural basis for the H2AK119ub1-specific DNMT3A-nucleosome interaction," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Linfeng Gao & Yiran Guo & Mahamaya Biswal & Jiuwei Lu & Jiekai Yin & Jian Fang & Xinyi Chen & Zengyu Shao & Mengjiang Huang & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2022. "Structure of DNMT3B homo-oligomer reveals vulnerability to impairment by ICF mutations," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Jiuwei Lu & Yiran Guo & Jiekai Yin & Jianbin Chen & Yinsheng Wang & Gang Greg Wang & Jikui Song, 2024. "Structure-guided functional suppression of AML-associated DNMT3A hotspot mutations," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Amika Kikuchi & Hiroki Onoda & Kosuke Yamaguchi & Satomi Kori & Shun Matsuzawa & Yoshie Chiba & Shota Tanimoto & Sae Yoshimi & Hiroki Sato & Atsushi Yamagata & Mikako Shirouzu & Naruhiko Adachi & Jafa, 2022. "Structural basis for activation of DNMT1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    6. Sun Shuying & Yu Xiaoqing, 2016. "HMM-Fisher: identifying differential methylation using a hidden Markov model and Fisher’s exact test," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 15(1), pages 55-67, March.
    7. Olbricht Gayla R. & Craig Bruce A. & Doerge Rebecca W., 2012. "Incorporating Genomic Annotation into a Hidden Markov Model for DNA Methylation Tiling Array Data," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 11(5), pages 1-37, November.
    8. Rakesh Chettier & Lesa Nelson & James W Ogilvie & Hans M Albertsen & Kenneth Ward, 2015. "Haplotypes at LBX1 Have Distinct Inheritance Patterns with Opposite Effects in Adolescent Idiopathic Scoliosis," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-11, February.
    9. Xue Yue & Zhiyuan Xie & Moran Li & Kai Wang & Xiaojing Li & Xiaoqing Zhang & Jian Yan & Yimeng Yin, 2022. "Simultaneous profiling of histone modifications and DNA methylation via nanopore sequencing," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Anyou Wang & Ying Du & Qianchuan He & Chunxiao Zhou, 2013. "A Quantitative System for Discriminating Induced Pluripotent Stem Cells, Embryonic Stem Cells and Somatic Cells," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-10, February.
    11. Yu Xiaoqing & Sun Shuying, 2016. "Comparing five statistical methods of differential methylation identification using bisulfite sequencing data," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 15(2), pages 173-191, April.
    12. Jiyuan Hu & Tengfei Li & Zidi Xiu & Hong Zhang, 2015. "MAFsnp: A Multi-Sample Accurate and Flexible SNP Caller Using Next-Generation Sequencing Data," PLOS ONE, Public Library of Science, vol. 10(8), pages 1-15, August.
    13. Allegra Angeloni & Skye Fissette & Deniz Kaya & Jillian M. Hammond & Hasindu Gamaarachchi & Ira W. Deveson & Robert J. Klose & Weiming Li & Xiaotian Zhang & Ozren Bogdanovic, 2024. "Extensive DNA methylome rearrangement during early lamprey embryogenesis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Jason A. Carter & Léonie Strömich & Matthew Peacey & Sarah R. Chapin & Lars Velten & Lars M. Steinmetz & Benedikt Brors & Sheena Pinto & Hannah V. Meyer, 2022. "Transcriptomic diversity in human medullary thymic epithelial cells," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    15. Steffen Mueller & Gail Dennison & Shujun Liu, 2021. "An Assessment on Ethanol-Blended Gasoline/Diesel Fuels on Cancer Risk and Mortality," IJERPH, MDPI, vol. 18(13), pages 1-23, June.
    16. Lacey Michelle R. & Baribault Carl & Ehrlich Melanie, 2013. "Modeling, simulation and analysis of methylation profiles from reduced representation bisulfite sequencing experiments," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 12(6), pages 723-742, December.
    17. Ruth V. Nichols & Brendan L. O’Connell & Ryan M. Mulqueen & Jerushah Thomas & Ashley R. Woodfin & Sonia Acharya & Gail Mandel & Dmitry Pokholok & Frank J. Steemers & Andrew C. Adey, 2022. "High-throughput robust single-cell DNA methylation profiling with sciMETv2," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    18. Ihab Ansari & Llorenç Solé-Boldo & Meshi Ridnik & Julian Gutekunst & Oliver Gilliam & Maria Korshko & Timur Liwinski & Birgit Jickeli & Noa Weinberg-Corem & Michal Shoshkes-Carmel & Eli Pikarsky & Era, 2023. "TET2 and TET3 loss disrupts small intestine differentiation and homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Jamie L. Endicott & Paula A. Nolte & Hui Shen & Peter W. Laird, 2022. "Cell division drives DNA methylation loss in late-replicating domains in primary human cells," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    20. Yinwen Zhang & Hosung Jang & Rui Xiao & Ioanna Kakoulidou & Robert S. Piecyk & Frank Johannes & Robert J. Schmitz, 2021. "Heterochromatin is a quantitative trait associated with spontaneous epiallele formation," Nature Communications, Nature, vol. 12(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31627-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.