title: An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis.
abstract: The chloroplast originated from the endosymbiosis of an ancient photosynthetic bacterium by a eukaryotic cell. Remarkably, the chloroplast has retained elements of a bacterial stress response pathway that is mediated by the signaling nucleotides guanosine penta- and tetraphosphate (ppGpp). However, an understanding of the mechanism and outcomes of ppGpp signaling in the photosynthetic eukaryotes has remained elusive. Using the model plant Arabidopsis thaliana, we show that ppGpp is a potent regulator of chloroplast gene expression in vivo that directly reduces the quantity of chloroplast transcripts and chloroplast-encoded proteins. We then go on to demonstrate that the antagonistic functions of different plant RelA SpoT homologs together modulate ppGpp levels to regulate chloroplast function and show that they are required for optimal plant growth, chloroplast volume, and chloroplast breakdown during dark-induced and developmental senescence. Therefore, our results show that ppGpp signaling is not only linked to stress responses in plants but is also an important mediator of cooperation between the chloroplast and the nucleocytoplasmic compartment during plant growth and development.
authors.affiliation: Aix Marseille University, Biologie Végétale et Microbiologie Environnementales UMR 7265, Laboratoire de Génétique et Biophysique des Plantes, Marseille F-13009, France CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Marseille F-13009, France CEA, Bioscience and Biotechnology Institute of Aix-Marseille, Marseille F-13009, France.
authors.forename: Matteo
authors.initials: M
authors.lastname: Sugliani
authors.affiliation: Aix Marseille University, Biologie Végétale et Microbiologie Environnementales UMR 7265, Laboratoire de Génétique et Biophysique des Plantes, Marseille F-13009, France CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Marseille F-13009, France CEA, Bioscience and Biotechnology Institute of Aix-Marseille, Marseille F-13009, France University of Tunis El Manar, Faculté des Sciences de Tunis, Laboratory of Molecular Genetics, Immunology, and Biotechnology, 2092 El Manar Tunis, Tunisia.
authors.forename: Hela
authors.identifier: http://orcid.org/0000-0002-9304-0890
authors.initials: H
authors.lastname: Abdelkefi
authors.affiliation: Aix Marseille University, Biologie Végétale et Microbiologie Environnementales UMR 7265, Laboratoire de Génétique et Biophysique des Plantes, Marseille F-13009, France CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Marseille F-13009, France CEA, Bioscience and Biotechnology Institute of Aix-Marseille, Marseille F-13009, France.
authors.forename: Hang
authors.initials: H
authors.lastname: Ke
authors.affiliation: Laboratoire d'Ingénierie des Systèmes Macromoléculaires, CNRS/Aix-Marseille University, Marseille F-13009, France.
authors.forename: Emmanuelle
authors.initials: E
authors.lastname: Bouveret
authors.affiliation: Aix Marseille University, Biologie Végétale et Microbiologie Environnementales UMR 7265, Laboratoire de Génétique et Biophysique des Plantes, Marseille F-13009, France CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Marseille F-13009, France CEA, Bioscience and Biotechnology Institute of Aix-Marseille, Marseille F-13009, France.
authors.forename: Christophe
authors.initials: C
authors.lastname: Robaglia
authors.affiliation: Aix Marseille University, Biologie Végétale et Microbiologie Environnementales UMR 7265, Laboratoire de Génétique et Biophysique des Plantes, Marseille F-13009, France CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Marseille F-13009, France CEA, Bioscience and Biotechnology Institute of Aix-Marseille, Marseille F-13009, France.
authors.forename: Stefano
authors.initials: S
authors.lastname: Caffarri
authors.affiliation: Aix Marseille University, Biologie Végétale et Microbiologie Environnementales UMR 7265, Laboratoire de Génétique et Biophysique des Plantes, Marseille F-13009, France CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Marseille F-13009, France CEA, Bioscience and Biotechnology Institute of Aix-Marseille, Marseille F-13009, France ben.field@univ-amu.fr.
authors.forename: Ben
authors.identifier: http://orcid.org/0000-0003-2142-4606
authors.initials: B
authors.lastname: Field
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development* / Q000502:physiology; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D016922:Cellular Senescence; D002734:Chlorophyll / Q000378:metabolism; D002736:Chloroplasts / Q000378:metabolism*; D017930:Genes, Reporter; D006158:Guanosine Pentaphosphate / Q000378:metabolism*; D006159:Guanosine Tetraphosphate / Q000378:metabolism*; D009154:Mutation; D010641:Phenotype; D011993:Recombinant Fusion Proteins; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism; D015398:Signal Transduction; D013312:Stress, Physiological
chemical_list: D001426:Bacterial Proteins; D011993:Recombinant Fusion Proteins; D002734:Chlorophyll; D006159:Guanosine Tetraphosphate; D006158:Guanosine Pentaphosphate; D012273:Ribulose-Bisphosphate Carboxylase