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Molecular and structural basis of the chromatin remodeling activity by Arabidopsis DDM1

Author

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  • Akihisa Osakabe

    (The University of Tokyo
    Japan Science and Technology Agency)

  • Yoshimasa Takizawa

    (The University of Tokyo)

  • Naoki Horikoshi

    (The University of Tokyo)

  • Suguru Hatazawa

    (The University of Tokyo)

  • Lumi Negishi

    (The University of Tokyo)

  • Shoko Sato

    (The University of Tokyo)

  • Frédéric Berger

    (Vienna Biocenter (VBC))

  • Tetsuji Kakutani

    (The University of Tokyo)

  • Hitoshi Kurumizaka

    (The University of Tokyo
    The University of Tokyo)

Abstract

The histone H2A variant H2A.W occupies transposons and thus prevents access to them in Arabidopsis thaliana. H2A.W is deposited by the chromatin remodeler DDM1, which also promotes the accessibility of chromatin writers to heterochromatin by an unknown mechanism. To shed light on this question, we solve the cryo-EM structures of nucleosomes containing H2A and H2A.W, and the DDM1-H2A.W nucleosome complex. These structures show that the DNA end flexibility of the H2A nucleosome is higher than that of the H2A.W nucleosome. In the DDM1-H2A.W nucleosome complex, DDM1 binds to the N-terminal tail of H4 and the nucleosomal DNA and increases the DNA end flexibility of H2A.W nucleosomes. Based on these biochemical and structural results, we propose that DDM1 counters the low accessibility caused by nucleosomes containing H2A.W to enable the maintenance of repressive epigenetic marks on transposons and prevent their activity.

Suggested Citation

  • Akihisa Osakabe & Yoshimasa Takizawa & Naoki Horikoshi & Suguru Hatazawa & Lumi Negishi & Shoko Sato & Frédéric Berger & Tetsuji Kakutani & Hitoshi Kurumizaka, 2024. "Molecular and structural basis of the chromatin remodeling activity by Arabidopsis DDM1," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49465-w
    DOI: 10.1038/s41467-024-49465-w
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    as
    1. Pierre Bourguet & Colette L. Picard & Ramesh Yelagandula & Thierry Pélissier & Zdravko J. Lorković & Suhua Feng & Marie-Noëlle Pouch-Pélissier & Anna Schmücker & Steven E. Jacobsen & Frédéric Berger , 2021. "The histone variant H2A.W and linker histone H1 co-regulate heterochromatin accessibility and DNA methylation," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Grigoriy A. Armeev & Anastasiia S. Kniazeva & Galina A. Komarova & Mikhail P. Kirpichnikov & Alexey K. Shaytan, 2021. "Histone dynamics mediate DNA unwrapping and sliding in nucleosomes," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Cedric R. Clapier & Bradley R. Cairns, 2012. "Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes," Nature, Nature, vol. 492(7428), pages 280-284, December.
    4. William L. Hwang & Sebastian Deindl & Bryan T. Harada & Xiaowei Zhuang, 2014. "Histone H4 tail mediates allosteric regulation of nucleosome remodelling by linker DNA," Nature, Nature, vol. 512(7513), pages 213-217, August.
    5. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    6. Xiaoyu Liu & Meijing Li & Xian Xia & Xueming Li & Zhucheng Chen, 2017. "Mechanism of chromatin remodelling revealed by the Snf2-nucleosome structure," Nature, Nature, vol. 544(7651), pages 440-445, April.
    7. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    8. Meijing Li & Xian Xia & Yuanyuan Tian & Qi Jia & Xiaoyu Liu & Ying Lu & Ming Li & Xueming Li & Zhucheng Chen, 2019. "Mechanism of DNA translocation underlying chromatin remodelling by Snf2," Nature, Nature, vol. 567(7748), pages 409-413, March.
    9. Ian R. Henderson & Steven E. Jacobsen, 2007. "Epigenetic inheritance in plants," Nature, Nature, vol. 447(7143), pages 418-424, May.
    10. Svetlana O. Dodonova & Fangjie Zhu & Christian Dienemann & Jussi Taipale & Patrick Cramer, 2020. "Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function," Nature, Nature, vol. 580(7805), pages 669-672, April.
    11. Lijuan Yan & Li Wang & Yuanyuan Tian & Xian Xia & Zhucheng Chen, 2016. "Structure and regulation of the chromatin remodeller ISWI," Nature, Nature, vol. 540(7633), pages 466-469, December.
    12. Kai Ni & Jianke Ren & Xiaoping Xu & Yafeng He & Richard Finney & Simon M. G. Braun & Nathaniel A. Hathaway & Gerald R. Crabtree & Kathrin Muegge, 2020. "LSH mediates gene repression through macroH2A deposition," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
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