Brassinosteroid-regulated GSK3/Shaggy-like Kinases Phosphorylate Mitogen-activated Protein (MAP) Kinase Kinases, Which Control Stomata Development in Arabidopsis thaliana

Mamoona Khan (1, 2) , Wilfried Rozhon (1, 2) , Jean Bigeard (3) , Delphine Pflieger (4) , Sigrid Husar (2) , Andrea Pitzschke (5) , Markus Teige (2) , Claudia Jonak (6) , Heribert Hirt (3, 7) , Brigitte Poppenberger (1, 2)

1 TUM - Technische Universität Munchen - Technical University Munich - Université Technique de Munich
2 University of Vienna [Vienna]
3 URGV - Unité de recherche en génomique végétale
4 LAMBE - Laboratoire Analyse et Modélisation pour la Biologie et l'Environnement
5 BOKU - Universität für Bodenkultur Wien = University of Natural Resources and Life [Vienne, Autriche]
6 GMI - Gregor Mendel Institute of Molecular Plant Biology
7 KSU - King Saud University [Riyadh]

Brassinosteroids (BRs) are steroid hormones that coordinate fundamental developmental programs in plants. In this study we show that in addition to the well established roles of BRs in regulating cell elongation and cell division events, BRs also govern cell fate decisions during stomata development in Arabidopsis thaliana. In wild-type A. thaliana, stomatal distribution follows the one-cell spacing rule; that is, adjacent stomata are spaced by at least one intervening pavement cell. This rule is interrupted in BR-deficient and BR signaling-deficient A. thaliana mutants, resulting in clustered stomata. We demonstrate that BIN2 and its homologues, GSK3/Shaggy-like kinases involved in BR signaling, can phosphorylate the MAPK kinases MKK4 and MKK5, which are members of the MAPK module YODA-MKK4/5-MPK3/6 that controls stomata development and patterning. BIN2 phosphorylates a GSK3/Shaggy-like kinase recognition motif in MKK4, which reduces MKK4 activity against its substrate MPK6 in vitro. In vivo we show that MKK4andMKK5act downstream of BR signaling because their overexpression rescued stomata patterning defects in BR-deficient plants. A model is proposed in which GSK3-mediated phosphorylation of MKK4 and MKK5 enables for a dynamic integration of endogenous or environmental cues signaled by BRs into cell fate decisions governed by the YODA-MKK4/5-MPK3/6 module.

Mots clés: Arabidopsis thaliana; Brassinosteroids; Cell divisions; Cell fate decision; Environmental cues; Mitogen activated protein kinase; Over-expression; Cell proliferation; Cells; Cytology; Plants (botany); Steroid hormones; Enzymes; Arabidopsis protein; BIN2 protein; brassinosteroid; mitogen activated protein kinase 3; mitogen activated protein kinase 6; mitogen activated protein kinase kinase 4; mitogen activated protein kinase kinase 5; unclassified drug; Arabidopsis; article; cell division; cell elongation; cell fate; controlled study; enzyme activity; enzyme phosphorylation; enzyme repression; hormone action; in vitro study; in vivo study; nonhuman; plant development; plant stoma; priority journal; protein expression; protein function; protein protein interaction; wild type; Cloning; Molecular; Escherichia coli; Gene Expression Regulation; Enzymologic; Plant; Glutathione Transferase; Glycogen Synthase Kinase 3; Mitogen-Activated Protein Kinase Kinases; Models; Biological; Genetic; Phosphorylation; Plant Stomata; Plants; Genetically Modified; Recombinant Proteins; Signal Transduction; Steroids

Domaines: Chimie-Physique [physics.chem-ph]

Mamoona Khan, Wilfried Rozhon, Jean Bigeard, Delphine Pflieger, Sigrid Husar, et al.. Brassinosteroid-regulated GSK3/Shaggy-like Kinases Phosphorylate Mitogen-activated Protein (MAP) Kinase Kinases, Which Control Stomata Development in Arabidopsis thaliana. Journal of Biological Chemistry, 2013, 288 (11), pp.7519-7527. ⟨10.1074/JBC.M112.384453⟩. ⟨hal-02112599⟩