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
- Institución
- Instituto Nacional de Tecnología Agropecuaria
- OAI Identificador
- oai:localhost:20.500.12123/8688
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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 http://purl.org/coar/resource_type/c_6501 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 |
dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by-nc-sa/4.0/ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) |
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) |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
Springer Nature |
publisher.none.fl_str_mv |
Springer Nature |
dc.source.none.fl_str_mv |
Scientific Reports 6 : 19036 (Enero 2016) reponame:INTA Digital (INTA) instname:Instituto Nacional de Tecnología Agropecuaria |
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INTA Digital (INTA) |
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INTA Digital (INTA) |
instname_str |
Instituto Nacional de Tecnología Agropecuaria |
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INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria |
repository.mail.fl_str_mv |
tripaldi.nicolas@inta.gob.ar |
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