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The UBP5 histone H2A deubiquitinase counteracts PRCs-mediated repression to regulate Arabidopsis development

Author

Listed:
  • James Godwin

    (University of Galway
    Donald Danforth Plant Science Center)

  • Mohan Govindasamy

    (University of Galway)

  • Kiruba Nedounsejian

    (University of Galway)

  • Eduardo March

    (University of Galway)

  • Ronan Halton

    (University of Galway)

  • Clara Bourbousse

    (École Normale Supérieure, CNRS, INSERM, Université PSL)

  • Léa Wolff

    (École Normale Supérieure, CNRS, INSERM, Université PSL)

  • Antoine Fort

    (Technological University of The Shannon: Midlands, Athlone, Co.)

  • Michal Krzyszton

    (Institute of Biochemistry and Biophysics, PAS)

  • Jesús López Corrales

    (University of Galway)

  • Szymon Swiezewski

    (Institute of Biochemistry and Biophysics, PAS)

  • Fredy Barneche

    (École Normale Supérieure, CNRS, INSERM, Université PSL)

  • Daniel Schubert

    (Freie Universität Berlin)

  • Sara Farrona

    (University of Galway)

Abstract

Polycomb Repressive Complexes (PRCs) control gene expression through the incorporation of H2Aub and H3K27me3. In recent years, there is increasing evidence of the complexity of PRCs’ interaction networks and the interplay of these interactors with PRCs in epigenome reshaping, which is fundamental to understand gene regulatory mechanisms. Here, we identified UBIQUITIN SPECIFIC PROTEASE 5 (UBP5) as a chromatin player able to counteract the deposition of the two PRCs’ epigenetic hallmarks in Arabidopsis thaliana. We demonstrated that UBP5 is a plant developmental regulator based on functional analyses of ubp5-CRISPR Cas9 mutant plants. UBP5 promotes H2A monoubiquitination erasure, leading to transcriptional de-repression. Furthermore, preferential association of UBP5 at PRC2 recruiting motifs and local H3K27me3 gaining in ubp5 mutant plants suggest the existence of functional interplays between UBP5 and PRC2 in regulating epigenome dynamics. In summary, acting as an antagonist of the pivotal epigenetic repressive marks H2Aub and H3K27me3, UBP5 provides novel insights to disentangle the complex regulation of PRCs’ activities.

Suggested Citation

  • James Godwin & Mohan Govindasamy & Kiruba Nedounsejian & Eduardo March & Ronan Halton & Clara Bourbousse & Léa Wolff & Antoine Fort & Michal Krzyszton & Jesús López Corrales & Szymon Swiezewski & Fred, 2024. "The UBP5 histone H2A deubiquitinase counteracts PRCs-mediated repression to regulate Arabidopsis development," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44546-8
    DOI: 10.1038/s41467-023-44546-8
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    References listed on IDEAS

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    1. Xiaochang Yin & Francisco J. Romero-Campero & Pedro de Los Reyes & Peng Yan & Jing Yang & Guangmei Tian & XiaoZeng Yang & Xiaorong Mo & Shuangshuang Zhao & Myriam Calonje & Yue Zhou, 2021. "H2AK121ub in Arabidopsis associates with a less accessible chromatin state at transcriptional regulation hotspots," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Johanna C. Scheuermann & Andrés Gaytán de Ayala Alonso & Katarzyna Oktaba & Nga Ly-Hartig & Robert K. McGinty & Sven Fraterman & Matthias Wilm & Tom W. Muir & Jürg Müller, 2010. "Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB," Nature, Nature, vol. 465(7295), pages 243-247, May.
    3. Vaniyambadi V. Sridhar & Avnish Kapoor & Kangling Zhang & Jianjun Zhu & Tao Zhou & Paul M. Hasegawa & Ray A. Bressan & Jian-Kang Zhu, 2007. "Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination," Nature, Nature, vol. 447(7145), pages 735-738, June.
    4. Danny D. Sahtoe & Willem J. van Dijk & Reggy Ekkebus & Huib Ovaa & Titia K. Sixma, 2016. "BAP1/ASXL1 recruitment and activation for H2A deubiquitination," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
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