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Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination

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  • Sara Martins

    (Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University
    Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences)

  • Esther M. N. Dohmann

    (University of Lausanne)

  • Anne Cayrel

    (Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University
    Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences)

  • Alexander Johnson

    (Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University
    Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences)

  • Wolfgang Fischer

    (The Salk Institute for Biological Studies)

  • Florence Pojer

    (Protein Crystallography Core Facility, Ecole Polytechnique Fédérale de Lausanne)

  • Béatrice Satiat-Jeunemaître

    (Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University
    Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences)

  • Yvon Jaillais

    (Laboratoire de Reproduction et Développement des Plantes, INRA, CNRS, ENS Lyon, Université de Lyon)

  • Joanne Chory

    (The Salk Institute for Biological Studies
    Howard Hughes Medical Institute, The Salk Institute for Biological Studies)

  • Niko Geldner

    (University of Lausanne)

  • Grégory Vert

    (Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University
    Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences)

Abstract

Brassinosteroids are plant steroid hormones that control many aspects of plant growth and development, and are perceived at the cell surface by the plasma membrane-localized receptor kinase BRI1. Here we show that BRI1 is post-translationally modified by K63 polyubiquitin chains in vivo. Using both artificial ubiquitination of BRI1 and generation of an ubiquitination-defective BRI1 mutant form, we demonstrate that ubiquitination promotes BRI1 internalization from the cell surface and is essential for its recognition at the trans-Golgi network/early endosomes (TGN/EE) for vacuolar targeting. Finally, we demonstrate that the control of BRI1 protein dynamics by ubiquitination is an important control mechanism for brassinosteroid responses in plants. Altogether, our results identify ubiquitination and K63-linked polyubiquitin chain formation as a dual targeting signal for BRI1 internalization and sorting along the endocytic pathway, and highlight its role in hormonally controlled plant development.

Suggested Citation

  • Sara Martins & Esther M. N. Dohmann & Anne Cayrel & Alexander Johnson & Wolfgang Fischer & Florence Pojer & Béatrice Satiat-Jeunemaître & Yvon Jaillais & Joanne Chory & Niko Geldner & Grégory Vert, 2015. "Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination," Nature Communications, Nature, vol. 6(1), pages 1-11, May.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7151
    DOI: 10.1038/ncomms7151
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    Cited by:

    1. Sha Tang & Zhiying Zhao & Xiaotong Liu & Yi Sui & Dandan Zhang & Hui Zhi & Yuanzhu Gao & Hui Zhang & Linlin Zhang & Yannan Wang & Meicheng Zhao & Dongdong Li & Ke Wang & Qiang He & Renliang Zhang & We, 2023. "An E2-E3 pair contributes to seed size control in grain crops," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Karin Vogel & Tobias Bläske & Marie-Kristin Nagel & Christoph Globisch & Shane Maguire & Lorenz Mattes & Christian Gude & Michael Kovermann & Karin Hauser & Christine Peter & Erika Isono, 2022. "Lipid-mediated activation of plasma membrane-localized deubiquitylating enzymes modulate endosomal trafficking," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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