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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: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group
2016
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4707469/ https://www.ncbi.nlm.nih.gov/pubmed/26750147 http://dx.doi.org/10.1038/srep19036 |
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author | Llorente, Briardo de Souza, Flavio S. J. Soto, Gabriela Meyer, Cristian Alonso, Guillermo D. Flawiá, Mirtha M. Bravo-Almonacid, Fernando Ayub, Nicolás D. Rodríguez-Concepción, Manuel |
author_facet | Llorente, Briardo de Souza, Flavio S. J. Soto, Gabriela Meyer, Cristian Alonso, Guillermo D. Flawiá, Mirtha M. Bravo-Almonacid, Fernando Ayub, Nicolás D. Rodríguez-Concepción, Manuel |
author_sort | Llorente, Briardo |
collection | PubMed |
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 | Online Article Text |
id | pubmed-4707469 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | Nature Publishing Group |
record_format | MEDLINE/PubMed |
spelling | pubmed-47074692016-01-20 Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution Llorente, Briardo de Souza, Flavio S. J. Soto, Gabriela Meyer, Cristian Alonso, Guillermo D. Flawiá, Mirtha M. Bravo-Almonacid, Fernando Ayub, Nicolás D. Rodríguez-Concepción, Manuel Sci Rep Article 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. Nature Publishing Group 2016-01-11 /pmc/articles/PMC4707469/ /pubmed/26750147 http://dx.doi.org/10.1038/srep19036 Text en Copyright © 2016, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ |
spellingShingle | Article Llorente, Briardo de Souza, Flavio S. J. Soto, Gabriela Meyer, Cristian Alonso, Guillermo D. Flawiá, Mirtha M. Bravo-Almonacid, Fernando Ayub, Nicolás D. 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 | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4707469/ https://www.ncbi.nlm.nih.gov/pubmed/26750147 http://dx.doi.org/10.1038/srep19036 |
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