title: GUN1 Controls Accumulation of the Plastid Ribosomal Protein S1 at the Protein Level and Interacts with Proteins Involved in Plastid Protein Homeostasis.
abstract: Developmental or metabolic changes in chloroplasts can have profound effects on the rest of the plant cell. Such intracellular responses are associated with signals that originate in chloroplasts and convey information on their physiological status to the nucleus, which leads to large-scale changes in gene expression (retrograde signaling). A screen designed to identify components of retrograde signaling resulted in the discovery of the so-called genomes uncoupled (gun) mutants. Genetic evidence suggests that the chloroplast protein GUN1 integrates signals derived from perturbations in plastid redox state, plastid gene expression, and tetrapyrrole biosynthesis (TPB) in Arabidopsis (Arabidopsis thaliana) seedlings, exerting biogenic control of chloroplast functions. However, the molecular mechanism by which GUN1 integrates retrograde signaling in the chloroplast is unclear. Here we show that GUN1 also operates in adult plants, contributing to operational control of chloroplasts. The gun1 mutation genetically interacts with mutations of genes for the chloroplast ribosomal proteins S1 (PRPS1) and L11. Analysis of gun1 prps1 lines indicates that GUN1 controls PRPS1 accumulation at the protein level. The GUN1 protein physically interacts with proteins involved in chloroplast protein homeostasis based on coimmunoprecipitation experiments. Furthermore, yeast two-hybrid and bimolecular fluorescence complementation experiments suggest that GUN1 might transiently interact with several TPB enzymes, including Mg-chelatase subunit D (CHLD) and two other TPB enzymes known to activate retrograde signaling. Moreover, the association of PRPS1 and CHLD with protein complexes is modulated by GUN1. These findings allow us to speculate that retrograde signaling might involve GUN1-dependent formation of protein complexes.
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Luca
authors.identifier: http://orcid.org/0000-0003-2315-7695
authors.initials: L
authors.lastname: Tadini
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Paolo
authors.initials: P
authors.lastname: Pesaresi
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Tatjana
authors.identifier: http://orcid.org/0000-0001-6455-3470
authors.initials: T
authors.lastname: Kleine
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Fabio
authors.initials: F
authors.lastname: Rossi
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Arthur
authors.initials: A
authors.lastname: Guljamow
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Frederik
authors.initials: F
authors.lastname: Sommer
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Timo
authors.initials: T
authors.lastname: Mühlhaus
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Michael
authors.initials: M
authors.lastname: Schroda
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Simona
authors.initials: S
authors.lastname: Masiero
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Mathias
authors.identifier: http://orcid.org/0000-0002-9174-9548
authors.initials: M
authors.lastname: Pribil
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Maxi
authors.initials: M
authors.lastname: Rothbart
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Boris
authors.initials: B
authors.lastname: Hedtke
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.).
authors.forename: Bernhard
authors.identifier: http://orcid.org/0000-0002-9730-1074
authors.initials: B
authors.lastname: Grimm
authors.affiliation: Department Biology I, Ludwig-Maximilians-Universität München, D-82152 Planegg-Martinsried, Germany (L.T., T.K., A.G., M.P., D.L.);Department of Biosciences, University of Milan, I-20133 Milano, Italy (P.P., F.R., S.M.);Department of Biology, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany (F.S., T.M., M.S.);Institute of Biology, Humboldt-University of Berlin, D-10115 Berlin, Germany (M.R., B.H., B.G.); andCopenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark (D.L.) leister@lmu.de.
authors.forename: Dario
authors.identifier: http://orcid.org/0000-0003-1897-8421
authors.initials: D
authors.lastname: Leister
mesh_terms: D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D060365:Chloroplast Proteins / Q000235:genetics / Q000378:metabolism*; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D004843:Epistasis, Genetic; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D015151:Immunoblotting; D008190:Lyases / Q000235:genetics / Q000378:metabolism; D009154:Mutation; D030821:Plants, Genetically Modified; D018087:Plastids / Q000235:genetics / Q000378:metabolism; D011485:Protein Binding; D021122:Protein Subunits / Q000235:genetics / Q000378:metabolism; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012269:Ribosomal Proteins / Q000235:genetics / Q000378:metabolism*; D017386:Sequence Homology, Amino Acid; D045725:Tetrapyrroles / Q000096:biosynthesis
chemical_list: D029681:Arabidopsis Proteins; D060365:Chloroplast Proteins; D004268:DNA-Binding Proteins; C519677:GUN1 protein, Arabidopsis; D021122:Protein Subunits; D012269:Ribosomal Proteins; D045725:Tetrapyrroles; C015494:ribosomal protein S1; D008190:Lyases; C086788:magnesium chelatase
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