Chromatin phosphoproteomics unravels a function for AT-hook motif nuclear localized protein AHL13 in PAMP-triggered immunity

Autor: Axel Mithöfer, Emmanuelle Lastrucci, Maria A. Schlöffel, Delphine Pflieger, Marilia Almeida-Trapp, Kiruthiga Mariappan, Hanna Alhoraibi, Jean Bigeard, Andrea A. Gust, Heribert Hirt, Aala A. Abulfaraj, Ludovic Bonhomme, Mai Jarad, Ronny Völz, Stefan T. Arold, Naganand Rayapuram
Přispěvatelé: Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology (KAUST), Centre for Research in Agricultural Genomics (CRAG), Department of Biochemistry, FAculty of science, King Abdulaziz University-King Abdulaziz University, Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Department of Biological Sciences, College of Sciences and Arts-Rabigh Campus, Plant Immunity Research Center, Seoul National University [Seoul] (SNU), Research Group Plant Defense Physiology, Max Planck Institute for Chemical Ecology, Max-Planck-Gesellschaft-Max-Planck-Gesellschaft, Center for Plant Molecular Biology, Eberhard Karls Universität Tübingen = Eberhard Karls University of Tuebingen, Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Génétique Diversité et Ecophysiologie des Céréales (GDEC), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Clermont Auvergne (UCA), Computational Bioscience Research Center, Laboratoire Analyse, Modélisation et Matériaux pour la Biologie et l'Environnement (LAMBE - UMR 8587), Université d'Évry-Val-d'Essonne (UEVE)-Institut de Chimie du CNRS (INC)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-CY Cergy Paris Université (CY), Infrastructure Nationale de Protéomique, FR2048 ProFI, Max Perutz Laboratories, University of Vienna [Vienna], French National Research Agency (ANR)European CommissionANR-2010-JCJC-1608ANR-14-CE19-0014French National Research Agency (ANR)ANR10-INBS-08King Abdullah University of Science & TechnologyBAS/1/1062-01-01, ANR-10-LABX-0040,SPS,Saclay Plant Sciences(2010), Lallemant, Christopher, Saclay Plant Sciences - - SPS2010 - ANR-10-LABX-0040 - LABX - VALID, Agence Nationale de la Recherche (France), Centre Européen de Recherche en Biologie et en Médecine (France), King Abdullah University of Science and Technology, Institute of Plant Sciences Paris-Saclay, Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Rok vydání: 2021
Předmět:
Zdroj: Proc Natl Acad Sci U S A
Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences of the United States of America, 2021, 118 (3), pp.e2004670118. ⟨10.1073/pnas.2004670118⟩
Digital.CSIC. Repositorio Institucional del CSIC
instname
Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2021, 118 (3), pp.e2004670118. ⟨10.1073/pnas.2004670118⟩
ISSN: 1091-6490
0027-8424
DOI: 10.1073/pnas.2004670118⟩
Popis: In many eukaryotic systems during immune responses, mitogen-activated protein kinases (MAPKs) link cytoplasmic signaling to chromatin events by targeting transcription factors, chromatin remodeling complexes, and the RNA polymerase machinery. So far, knowledge on these events is scarce in plants and no attempts have been made to focus on phosphorylation events of chromatin-associated proteins. Here we carried out chromatin phosphoproteomics upon elicitor-induced activation of Arabidopsis. The events in WT were compared with those in mpk3, mpk4, and mpk6 mutant plants to decipher specific MAPK targets. Our study highlights distinct signaling networks involving MPK3, MPK4, and MPK6 in chromatin organization and modification, as well as in RNA transcription and processing. Among the chromatin targets, we characterized the AT-hook motif containing nuclear localized (AHL) DNA-binding protein AHL13 as a substrate of immune MAPKs. AHL13 knockout mutant plants are compromised in pathogen-associated molecular pattern (PAMP)-induced reactive oxygen species production, expression of defense genes, and PAMP-triggered immunity. Transcriptome analysis revealed that AHL13 regulates key factors of jasmonic acid biosynthesis and signaling and affects immunity toward Pseudomonas syringae and Botrytis cinerea pathogens. Mutational analysis of the phosphorylation sites of AHL13 demonstrated that phosphorylation regulates AHL13 protein stability and thereby its immune functions.
This work was supported by Agence Nationale de la Recherche ANR-2010-JCJC-1608 and ANR-14-CE19-0014 (to D.P.); Investissement d’Avenir Infrastructures Nationales en Biologie et Santé program (ProFI project, ANR-10-INBS-08); and by King Abdullah University of Science and Technology BAS/1/1062-01-01 (to H.H.). The Institute of Plant Sciences Paris-Saclay benefits from the support of the LabEx Saclay Plant Sciences (ANR-10-LABX-0040-SPS). M.A.-T. was supported by a Humboldt-Capes fellowship.
Databáze: OpenAIRE