Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution
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 u...
| Autores principales: | , , , , , , , , |
|---|---|
| Formato: | Artículo |
| Lenguaje: | Inglés |
| Publicado: |
Springer Nature
2021
|
| Materias: | |
| Acceso en línea: | http://hdl.handle.net/20.500.12123/8688 https://www.nature.com/articles/srep19036 https://doi.org/10.1038/srep19036 |
| _version_ | 1855484248573607936 |
|---|---|
| author | 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_browse | Alonso, Guillermo D. Ayub, Nicolás Daniel Bravo Almonacid, Fernando Felix Flawia, Mirtha M. Llorente, Briardo Meyer, Cristian Rodríguez-Concepción, Manuel Soto, Gabriela Cynthia de Souza, Flavio S. J. |
| 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_sort | Llorente, Briardo |
| collection | INTA Digital |
| 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. |
| format | Artículo |
| id | INTA8688 |
| institution | Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina) |
| language | Inglés |
| publishDate | 2021 |
| publishDateRange | 2021 |
| publishDateSort | 2021 |
| publisher | Springer Nature |
| publisherStr | Springer Nature |
| record_format | dspace |
| spelling | INTA86882021-02-18T16:33:34Z Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution 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 Plastids Cytoplasmic Organelles Prokaryotae Plastidios Orgánulos citoplásmicos Arabidopsis 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 2021-02-18T16:28:46Z 2021-02-18T16:28:46Z 2016-01 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://hdl.handle.net/20.500.12123/8688 https://www.nature.com/articles/srep19036 2045-2322 https://doi.org/10.1038/srep19036 eng 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) application/pdf Springer Nature Scientific Reports 6 : 19036 (Enero 2016) |
| spellingShingle | Plastids Cytoplasmic Organelles Prokaryotae Plastidios Orgánulos citoplásmicos Arabidopsis 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 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 |
| 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_short | 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 |
| topic | Plastids Cytoplasmic Organelles Prokaryotae Plastidios Orgánulos citoplásmicos Arabidopsis |
| url | http://hdl.handle.net/20.500.12123/8688 https://www.nature.com/articles/srep19036 https://doi.org/10.1038/srep19036 |
| work_keys_str_mv | AT llorentebriardo selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT desouzaflaviosj selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT sotogabrielacynthia selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT meyercristian selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT alonsoguillermod selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT flawiamirtham selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT bravoalmonacidfernandofelix selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT ayubnicolasdaniel selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT rodriguezconcepcionmanuel selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution |