title: Expression of nuclear and mitochondrial genes encoding ATP synthase is synchronized by disassembly of a multisynthetase complex.
abstract: In eukaryotic cells, oxidative phosphorylation involves multisubunit complexes of mixed genetic origin. Assembling these complexes requires an organelle-independent synchronizing system for the proper expression of nuclear and mitochondrial genes. Here we show that proper expression of the F1FO ATP synthase (complex V) depends on a cytosolic complex (AME) made of two aminoacyl-tRNA synthetases (cERS and cMRS) attached to an anchor protein, Arc1p. When yeast cells adapt to respiration the Snf1/4 glucose-sensing pathway inhibits ARC1 expression triggering simultaneous release of cERS and cMRS. Free cMRS and cERS relocate to the nucleus and mitochondria, respectively, to synchronize nuclear transcription and mitochondrial translation of ATP synthase genes. Strains releasing asynchronously the two aminoacyl-tRNA synthetases display aberrant expression of nuclear and mitochondrial genes encoding subunits of complex V resulting in severe defects of the oxidative phosphorylation mechanism. This work shows that the AME complex coordinates expression of enzymes that require intergenomic control.
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France; UPR Architecture et Réactivité de l'ARN, Institut de Biologie Moléculaire et Cellulaire, Université de Strasbourg, CNRS, 15 Rue René Descartes, 67084 Strasbourg Cedex, France. Electronic address: mathieu.frechin@uzh.ch.
authors.forename: Mathieu
authors.initials: M
authors.lastname: Frechin
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France.
authors.forename: Ludovic
authors.initials: L
authors.lastname: Enkler
authors.affiliation: Centre National de la Recherche Scientifique, Institut de Biochimie et Génétique Cellulaires, UMR 5095, 1 Rue Camille Saint-Saëns, 33077 Bordeaux, France; Institut de Biochimie et Génétique Cellulaires, UMR 5095, Université Bordeaux, 146 Rue Léo Saignat, 33076 Bordeaux, France.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Tetaud
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France.
authors.forename: Daphné
authors.initials: D
authors.lastname: Laporte
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France.
authors.forename: Bruno
authors.initials: B
authors.lastname: Senger
authors.affiliation: Centre National de la Recherche Scientifique, Institut de Biochimie et Génétique Cellulaires, UMR 5095, 1 Rue Camille Saint-Saëns, 33077 Bordeaux, France; Institut de Biochimie et Génétique Cellulaires, UMR 5095, Université Bordeaux, 146 Rue Léo Saignat, 33076 Bordeaux, France.
authors.forename: Corinne
authors.initials: C
authors.lastname: Blancard
authors.affiliation: Plateforme Protéomique de l'Esplanade, Université de Strasbourg, CNRS- FRC1589, IBMC, 15 Rue René Descartes, 67084 Strasbourg Cedex, France.
authors.forename: Philippe
authors.initials: P
authors.lastname: Hammann
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France.
authors.forename: Gaétan
authors.initials: G
authors.lastname: Bader
authors.affiliation: European Molecular Biology Laboratory (EMBL), Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
authors.forename: Sandra
authors.initials: S
authors.lastname: Clauder-Münster
authors.affiliation: European Molecular Biology Laboratory (EMBL), Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany; Stanford Genome Technology Center, Stanford University, Palo Alto, CA 94304, USA and Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.
authors.forename: Lars M
authors.initials: LM
authors.lastname: Steinmetz
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France.
authors.forename: Robert Pierre
authors.initials: RP
authors.lastname: Martin
authors.affiliation: Centre National de la Recherche Scientifique, Institut de Biochimie et Génétique Cellulaires, UMR 5095, 1 Rue Camille Saint-Saëns, 33077 Bordeaux, France; Institut de Biochimie et Génétique Cellulaires, UMR 5095, Université Bordeaux, 146 Rue Léo Saignat, 33076 Bordeaux, France. Electronic address: jp.dirago@ibgc.cnrs.fr.
authors.forename: Jean-Paul
authors.initials: JP
authors.lastname: di Rago
authors.affiliation: Génétique Moléculaire, Génomique, Microbiologie, UMR 7156, CNRS, Université de Strasbourg, 21 Rue René Descartes, 67084 Strasbourg Cedex, France. Electronic address: h.becker@unistra.fr.
authors.forename: Hubert Dominique
authors.initials: HD
authors.lastname: Becker
mesh_terms: D002467:Cell Nucleus / Q000235:genetics; D015870:Gene Expression; D015966:Gene Expression Regulation, Fungal; D008928:Mitochondria / Q000235:genetics; D009097:Multienzyme Complexes; D055503:Protein Multimerization; D006180:Proton-Translocating ATPases / Q000235:genetics* / Q000378:metabolism; D016601:RNA-Binding Proteins / Q000502:physiology; D012441:Saccharomyces cerevisiae / Q000201:enzymology / Q000235:genetics*; D029701:Saccharomyces cerevisiae Proteins / Q000502:physiology
chemical_list: C102145:ARC1 protein, S cerevisiae; D009097:Multienzyme Complexes; D016601:RNA-Binding Proteins; D029701:Saccharomyces cerevisiae Proteins; D006180:Proton-Translocating ATPases