title: Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination.
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.
authors.affiliation: 1] Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France [2] Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France.
authors.forename: Sara
authors.initials: S
authors.lastname: Martins
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, UNIL-Sorge, 1015 Lausanne, Switzerland.
authors.forename: Esther M N
authors.initials: EM
authors.lastname: Dohmann
authors.affiliation: 1] Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France [2] Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France.
authors.forename: Anne
authors.initials: A
authors.lastname: Cayrel
authors.affiliation: 1] Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France [2] Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France.
authors.forename: Alexander
authors.initials: A
authors.lastname: Johnson
authors.affiliation: The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, California 92037, USA.
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Fischer
authors.affiliation: Protein Crystallography Core Facility, Ecole Polytechnique Fédérale de Lausanne, SV 3827 Station 19, 1015 Lausanne, Switzerland.
authors.forename: Florence
authors.initials: F
authors.lastname: Pojer
authors.affiliation: 1] Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France [2] Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France.
authors.forename: Béatrice
authors.initials: B
authors.lastname: Satiat-Jeunemaître
authors.affiliation: Laboratoire de Reproduction et Développement des Plantes, INRA, CNRS, ENS Lyon, Université de Lyon, 46 allée d'Italie, 69364 Lyon 07, France.
authors.forename: Yvon
authors.initials: Y
authors.lastname: Jaillais
authors.affiliation: 1] The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, California 92037, USA [2] Howard Hughes Medical Institute, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, California 92037, USA.
authors.forename: Joanne
authors.initials: J
authors.lastname: Chory
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, UNIL-Sorge, 1015 Lausanne, Switzerland.
authors.forename: Niko
authors.initials: N
authors.lastname: Geldner
authors.affiliation: 1] Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Paris-Sud University, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France [2] Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, Saclay Plant Sciences, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France.
authors.forename: Grégory
authors.initials: G
authors.lastname: Vert
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D060406:Brassinosteroids / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism / Q000648:ultrastructure; D011992:Endosomes / Q000378:metabolism / Q000648:ultrastructure; D018506:Gene Expression Regulation, Plant; D008239:Lysine / Q000378:metabolism; D008856:Microscopy, Fluorescence / Q000379:methods; D009154:Mutation; D010766:Phosphorylation; D030821:Plants, Genetically Modified; D025821:Polyubiquitin / Q000235:genetics / Q000378:metabolism*; D011494:Protein Kinases / Q000235:genetics / Q000378:metabolism*; D011499:Protein Processing, Post-Translational; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D021381:Protein Transport; D059748:Proteolysis; D015398:Signal Transduction; D054875:Ubiquitination; D014617:Vacuoles / Q000378:metabolism* / Q000648:ultrastructure; D021601:trans-Golgi Network / Q000378:metabolism / Q000648:ultrastructure
chemical_list: D029681:Arabidopsis Proteins; D060406:Brassinosteroids; D025821:Polyubiquitin; D011494:Protein Kinases; C463660:BAK1 protein, Arabidopsis; C108270:BRI1 protein, Arabidopsis; D017346:Protein Serine-Threonine Kinases; D008239:Lysine