title: Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution.
abstract: The plastid organelle comprises a high proportion of nucleus-encoded proteins that were acquired from different prokaryotic donors via independent horizontal gene transfers following its primary endosymbiotic origin. What forces drove the targeting of these alien proteins to the plastid remains an unresolved evolutionary question. To better understand this process we screened for suitable candidate proteins to recapitulate their prokaryote-to-eukaryote transition. Here we identify the ancient horizontal transfer of a bacterial polyphenol oxidase (PPO) gene to the nuclear genome of an early land plant ancestor and infer the possible mechanism behind the plastidial localization of the encoded enzyme. Arabidopsis plants expressing PPO versions either lacking or harbouring a plastid-targeting signal allowed examining fitness consequences associated with its subcellular localization. Markedly, a deleterious effect on plant growth was highly correlated with PPO activity only when producing the non-targeted enzyme, suggesting that selection favoured the fixation of plastid-targeted protein versions. Our results reveal a possible evolutionary mechanism of how selection against heterologous genes encoding cytosolic proteins contributed in incrementing plastid proteome complexity from non-endosymbiotic gene sources, a process that may also impact mitochondrial evolution.
authors.affiliation: Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, 08193 Barcelona, Spain.|Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.
authors.forename: Briardo
authors.initials: B
authors.lastname: Llorente
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.
authors.forename: Flavio S J
authors.initials: FSJ
authors.lastname: de Souza
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.
authors.forename: Gabriela
authors.initials: G
authors.lastname: Soto
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.
authors.forename: Cristian
authors.initials: C
authors.lastname: Meyer
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.|Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EGA Buenos Aires, Argentina.
authors.forename: Guillermo D
authors.initials: GD
authors.lastname: Alonso
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.|Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EGA Buenos Aires, Argentina.
authors.forename: Mirtha M
authors.initials: MM
authors.lastname: Flawiá
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres, Consejo Nacional de Investigaciones Científicas y Técnicas (INGEBI-CONICET), C1428ADN Buenos Aires, Argentina.|Departamento de Ciencia y Tecnología. Universidad Nacional de Quilmes, B1876BXD Bernal, Argentina.
authors.forename: Fernando
authors.initials: F
authors.lastname: Bravo-Almonacid
authors.affiliation: Instituto de Genética Ewald A. Favret, Centro de Investigación en Ciencias Veterinarias y Agronómicas, Instituto Nacional de Tecnología Agropecuaria (CICVyA-INTA), B1712WAA Castelar, Argentina.|Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), C1033AAJ Buenos Aires, Argentina.
authors.forename: Nicolás D
authors.initials: ND
authors.lastname: Ayub
authors.affiliation: Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, 08193 Barcelona, Spain.
authors.forename: Manuel
authors.initials: M
authors.lastname: Rodríguez-Concepción
mesh_terms: D017360:Arabidopsis / Q000145:classification / Q000201:enzymology / Q000235:genetics*; D001419:Bacteria / Q000145:classification / Q000201:enzymology / Q000235:genetics; D005075:Biological Evolution; D004156:Catechol Oxidase / Q000235:genetics* / Q000378:metabolism; D002467:Cell Nucleus / Q000201:enzymology / Q000235:genetics; D000460:Chlorophyta / Q000145:classification / Q000201:enzymology / Q000235:genetics; D005057:Eukaryotic Cells / Q000166:cytology; D005658:Fungi / Q000145:classification / Q000201:enzymology / Q000235:genetics; D015870:Gene Expression; D022761:Gene Transfer, Horizontal; D018745:Genome, Plant; D008958:Models, Molecular; D010802:Phylogeny; D018087:Plastids / Q000201:enzymology / Q000235:genetics*; D011387:Prokaryotic Cells / Q000166:cytology / Q000201:enzymology; D021382:Protein Sorting Signals; D021381:Protein Transport; D012641:Selection, Genetic; D013559:Symbiosis / Q000502:physiology
chemical_list: D021382:Protein Sorting Signals; D004156:Catechol Oxidase