Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution

Autores
Llorente, Briardo; de Souza, Flavio S. J.; Soto, Gabriela Cynthia; Meyer, Cristian; Alonso, Guillermo D.; Flawia, Mirtha M.; Bravo Almonacid, Fernando Felix; Ayub, Nicolás Daniel; Rodríguez-Concepción, Manuel
Año de publicación
2016
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Instituto de Genética
Fil: Llorente, Briardo. Centre for Research in Agricultural Genomics (CRAG); España. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: de Souza, Flavio S. J. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Soto, Gabriela Cynthia. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Meyer, Cristian. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Alonso, Guillermo D. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular; Argentina
Fil: Flawia, Mirtha M. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular; Argentina
Fil: Bravo Almonacid, Fernando Felix. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina
Fil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rodríguez-Concepción, Manuel. Centre for Research in Agricultural Genomics (CRAG); España
Fuente
Scientific Reports 6 : 19036 (Enero 2016)
Materia
Plastids
Cytoplasmic Organelles
Prokaryotae
Plastidios
Orgánulos citoplásmicos
Arabidopsis
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/8688

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network_name_str INTA Digital (INTA)
spelling Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolutionLlorente, Briardode Souza, Flavio S. J.Soto, Gabriela CynthiaMeyer, CristianAlonso, Guillermo D.Flawia, Mirtha M.Bravo Almonacid, Fernando FelixAyub, Nicolás DanielRodríguez-Concepción, ManuelPlastidsCytoplasmic OrganellesProkaryotaePlastidiosOrgánulos citoplásmicosArabidopsisThe 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.Instituto de GenéticaFil: Llorente, Briardo. Centre for Research in Agricultural Genomics (CRAG); España. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: de Souza, Flavio S. J. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Soto, Gabriela Cynthia. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Meyer, Cristian. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Alonso, Guillermo D. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular; ArgentinaFil: Flawia, Mirtha M. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular; ArgentinaFil: Bravo Almonacid, Fernando Felix. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; ArgentinaFil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Rodríguez-Concepción, Manuel. Centre for Research in Agricultural Genomics (CRAG); EspañaSpringer Nature2021-02-18T16:28:46Z2021-02-18T16:28:46Z2016-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/8688https://www.nature.com/articles/srep190362045-2322https://doi.org/10.1038/srep19036Scientific Reports 6 : 19036 (Enero 2016)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)2025-09-29T13:45:08Zoai:localhost:20.500.12123/8688instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-29 13:45:08.572INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
title Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
spellingShingle Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
Llorente, Briardo
Plastids
Cytoplasmic Organelles
Prokaryotae
Plastidios
Orgánulos citoplásmicos
Arabidopsis
title_short Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
title_full Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
title_fullStr Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
title_full_unstemmed Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
title_sort Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
dc.creator.none.fl_str_mv Llorente, Briardo
de Souza, Flavio S. J.
Soto, Gabriela Cynthia
Meyer, Cristian
Alonso, Guillermo D.
Flawia, Mirtha M.
Bravo Almonacid, Fernando Felix
Ayub, Nicolás Daniel
Rodríguez-Concepción, Manuel
author Llorente, Briardo
author_facet Llorente, Briardo
de Souza, Flavio S. J.
Soto, Gabriela Cynthia
Meyer, Cristian
Alonso, Guillermo D.
Flawia, Mirtha M.
Bravo Almonacid, Fernando Felix
Ayub, Nicolás Daniel
Rodríguez-Concepción, Manuel
author_role author
author2 de Souza, Flavio S. J.
Soto, Gabriela Cynthia
Meyer, Cristian
Alonso, Guillermo D.
Flawia, Mirtha M.
Bravo Almonacid, Fernando Felix
Ayub, Nicolás Daniel
Rodríguez-Concepción, Manuel
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Plastids
Cytoplasmic Organelles
Prokaryotae
Plastidios
Orgánulos citoplásmicos
Arabidopsis
topic Plastids
Cytoplasmic Organelles
Prokaryotae
Plastidios
Orgánulos citoplásmicos
Arabidopsis
dc.description.none.fl_txt_mv 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.
Instituto de Genética
Fil: Llorente, Briardo. Centre for Research in Agricultural Genomics (CRAG); España. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: de Souza, Flavio S. J. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Soto, Gabriela Cynthia. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Meyer, Cristian. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Alonso, Guillermo D. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular; Argentina
Fil: Flawia, Mirtha M. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Fisiología, Biología Molecular y Celular; Argentina
Fil: Bravo Almonacid, Fernando Felix. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Héctor Torres; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina
Fil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rodríguez-Concepción, Manuel. Centre for Research in Agricultural Genomics (CRAG); España
description 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.
publishDate 2016
dc.date.none.fl_str_mv 2016-01
2021-02-18T16:28:46Z
2021-02-18T16:28:46Z
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/8688
https://www.nature.com/articles/srep19036
2045-2322
https://doi.org/10.1038/srep19036
url http://hdl.handle.net/20.500.12123/8688
https://www.nature.com/articles/srep19036
https://doi.org/10.1038/srep19036
identifier_str_mv 2045-2322
dc.language.none.fl_str_mv eng
language eng
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eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
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publisher.none.fl_str_mv Springer Nature
dc.source.none.fl_str_mv Scientific Reports 6 : 19036 (Enero 2016)
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