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DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development

Author

Listed:
  • Li He

    (Chinese Academy of Sciences)

  • Huan Huang

    (Chinese Academy of Sciences)

  • Mariem Bradai

    (Chinese Academy of Sciences)

  • Cheng Zhao

    (Chinese Academy of Sciences
    Karolinska Institutet)

  • Yin You

    (Chinese Academy of Sciences
    University of the Chinese Academy of Sciences)

  • Jun Ma

    (Chinese Academy of Sciences)

  • Lun Zhao

    (Chinese Academy of Sciences)

  • Rosa Lozano-Durán

    (Chinese Academy of Sciences
    Eberhard Karls University)

  • Jian-Kang Zhu

    (Chinese Academy of Sciences
    Southern University of Science and Technology)

Abstract

A contribution of DNA methylation to defense against invading nucleic acids and maintenance of genome integrity is uncontested; however, our understanding of the extent of involvement of this epigenetic mark in genome-wide gene regulation and plant developmental control is incomplete. Here, we knock out all five known DNA methyltransferases in Arabidopsis, generating DNA methylation-free plants. This quintuple mutant exhibits a suite of developmental defects, unequivocally demonstrating that DNA methylation is essential for multiple aspects of plant development. We show that CG methylation and non-CG methylation are required for a plethora of biological processes, including pavement cell shape, endoreduplication, cell death, flowering, trichome morphology, vasculature and meristem development, and root cell fate determination. Moreover, we find that DNA methylation has a strong dose-dependent effect on gene expression and repression of transposable elements. Taken together, our results demonstrate that DNA methylation is dispensable for Arabidopsis survival but essential for the proper regulation of multiple biological processes.

Suggested Citation

  • Li He & Huan Huang & Mariem Bradai & Cheng Zhao & Yin You & Jun Ma & Lun Zhao & Rosa Lozano-Durán & Jian-Kang Zhu, 2022. "DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28940-2
    DOI: 10.1038/s41467-022-28940-2
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    References listed on IDEAS

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    1. Asuka Miura & Shoji Yonebayashi & Koichi Watanabe & Tomoko Toyama & Hiroaki Shimada & Tetsuji Kakutani, 2001. "Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis," Nature, Nature, vol. 411(6834), pages 212-214, May.
    2. Zhengming Wang & David C. Baulcombe, 2020. "Transposon age and non-CG methylation," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Zachary Lippman & Anne-Valérie Gendrel & Michael Black & Matthew W. Vaughn & Neilay Dedhia & W. Richard McCombie & Kimberly Lavine & Vivek Mittal & Bruce May & Kristin D. Kasschau & James C. Carringto, 2004. "Role of transposable elements in heterochromatin and epigenetic control," Nature, Nature, vol. 430(6998), pages 471-476, July.
    4. Hidetoshi Saze & Junko Kitayama & Kazuya Takashima & Saori Miura & Yoshiko Harukawa & Tasuku Ito & Tetsuji Kakutani, 2013. "Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin," Nature Communications, Nature, vol. 4(1), pages 1-9, October.
    5. Leandro Quadrana & Mathilde Etcheverry & Arthur Gilly & Erwann Caillieux & Mohammed-Amin Madoui & Julie Guy & Amanda Bortolini Silveira & Stefan Engelen & Victoire Baillet & Patrick Wincker & Jean-Mar, 2019. "Transposition favors the generation of large effect mutations that may facilitate rapid adaption," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    6. Marie Mirouze & Jon Reinders & Etienne Bucher & Taisuke Nishimura & Korbinian Schneeberger & Stephan Ossowski & Jun Cao & Detlef Weigel & Jerzy Paszkowski & Olivier Mathieu, 2009. "Selective epigenetic control of retrotransposition in Arabidopsis," Nature, Nature, vol. 461(7262), pages 427-430, September.
    7. Ian R. Henderson & Steven E. Jacobsen, 2007. "Epigenetic inheritance in plants," Nature, Nature, vol. 447(7143), pages 418-424, May.
    8. Lun Zhao & Shuangqi Wang & Zhilin Cao & Weizhi Ouyang & Qing Zhang & Liang Xie & Ruiqin Zheng & Minrong Guo & Meng Ma & Zhe Hu & Wing-Kin Sung & Qifa Zhang & Guoliang Li & Xingwang Li, 2019. "Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    9. Sayuri Tsukahara & Akie Kobayashi & Akira Kawabe & Olivier Mathieu & Asuka Miura & Tetsuji Kakutani, 2009. "Bursts of retrotransposition reproduced in Arabidopsis," Nature, Nature, vol. 461(7262), pages 423-426, September.
    10. Hidetaka Ito & Hervé Gaubert & Etienne Bucher & Marie Mirouze & Isabelle Vaillant & Jerzy Paszkowski, 2011. "An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress," Nature, Nature, vol. 472(7341), pages 115-119, April.
    11. Asuka Higo & Noriko Saihara & Fumihito Miura & Yoko Higashi & Megumi Yamada & Shojiro Tamaki & Tasuku Ito & Yoshiaki Tarutani & Tomoaki Sakamoto & Masayuki Fujiwara & Tetsuya Kurata & Yoichiro Fukao &, 2020. "DNA methylation is reconfigured at the onset of reproduction in rice shoot apical meristem," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    12. Francesco Neri & Stefania Rapelli & Anna Krepelova & Danny Incarnato & Caterina Parlato & Giulia Basile & Mara Maldotti & Francesca Anselmi & Salvatore Oliviero, 2017. "Intragenic DNA methylation prevents spurious transcription initiation," Nature, Nature, vol. 543(7643), pages 72-77, March.
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    4. Kangxi Du & Jiabing Wu & Jiachen Wang & Wenhao Xie & Liufan Yin & Xiang Li & Chao Li & Aiwu Dong, 2024. "The chromatin remodeling factor OsINO80 promotes H3K27me3 and H3K9me2 deposition and maintains TE silencing in rice," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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