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...
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Acceso en línea: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20452322_v6_n_p_Llorente http://hdl.handle.net/20.500.12110/paper_20452322_v6_n_p_Llorente |
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paper:paper_20452322_v6_n_p_Llorente2023-06-08T16:33:26Z Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution Llorente, Briardo Ernesto Soto, Gabriela Cynthia Flawiá, Mirtha María Ayub, Nicolás Daniel catechol oxidase signal peptide Arabidopsis bacterium cell nucleus classification cytology enzymology eukaryotic cell evolution fungus gene expression genetic selection genetics green alga horizontal gene transfer metabolism molecular model phylogeny physiology plant genome plastid prokaryotic cell protein transport symbiosis Arabidopsis Bacteria Biological Evolution Catechol Oxidase Cell Nucleus Chlorophyta Eukaryotic Cells Fungi Gene Expression Gene Transfer, Horizontal Genome, Plant Models, Molecular Phylogeny Plastids Prokaryotic Cells Protein Sorting Signals Protein Transport Selection, Genetic Symbiosis 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. Fil:Llorente, B. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Soto, G. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Flawiá, M.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Ayub, N.D. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. 2016 https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20452322_v6_n_p_Llorente http://hdl.handle.net/20.500.12110/paper_20452322_v6_n_p_Llorente |
institution |
Universidad de Buenos Aires |
institution_str |
I-28 |
repository_str |
R-134 |
collection |
Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA) |
topic |
catechol oxidase signal peptide Arabidopsis bacterium cell nucleus classification cytology enzymology eukaryotic cell evolution fungus gene expression genetic selection genetics green alga horizontal gene transfer metabolism molecular model phylogeny physiology plant genome plastid prokaryotic cell protein transport symbiosis Arabidopsis Bacteria Biological Evolution Catechol Oxidase Cell Nucleus Chlorophyta Eukaryotic Cells Fungi Gene Expression Gene Transfer, Horizontal Genome, Plant Models, Molecular Phylogeny Plastids Prokaryotic Cells Protein Sorting Signals Protein Transport Selection, Genetic Symbiosis |
spellingShingle |
catechol oxidase signal peptide Arabidopsis bacterium cell nucleus classification cytology enzymology eukaryotic cell evolution fungus gene expression genetic selection genetics green alga horizontal gene transfer metabolism molecular model phylogeny physiology plant genome plastid prokaryotic cell protein transport symbiosis Arabidopsis Bacteria Biological Evolution Catechol Oxidase Cell Nucleus Chlorophyta Eukaryotic Cells Fungi Gene Expression Gene Transfer, Horizontal Genome, Plant Models, Molecular Phylogeny Plastids Prokaryotic Cells Protein Sorting Signals Protein Transport Selection, Genetic Symbiosis Llorente, Briardo Ernesto Soto, Gabriela Cynthia Flawiá, Mirtha María Ayub, Nicolás Daniel Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution |
topic_facet |
catechol oxidase signal peptide Arabidopsis bacterium cell nucleus classification cytology enzymology eukaryotic cell evolution fungus gene expression genetic selection genetics green alga horizontal gene transfer metabolism molecular model phylogeny physiology plant genome plastid prokaryotic cell protein transport symbiosis Arabidopsis Bacteria Biological Evolution Catechol Oxidase Cell Nucleus Chlorophyta Eukaryotic Cells Fungi Gene Expression Gene Transfer, Horizontal Genome, Plant Models, Molecular Phylogeny Plastids Prokaryotic Cells Protein Sorting Signals Protein Transport Selection, Genetic Symbiosis |
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. |
author |
Llorente, Briardo Ernesto Soto, Gabriela Cynthia Flawiá, Mirtha María Ayub, Nicolás Daniel |
author_facet |
Llorente, Briardo Ernesto Soto, Gabriela Cynthia Flawiá, Mirtha María Ayub, Nicolás Daniel |
author_sort |
Llorente, Briardo Ernesto |
title |
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_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 |
publishDate |
2016 |
url |
https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20452322_v6_n_p_Llorente http://hdl.handle.net/20.500.12110/paper_20452322_v6_n_p_Llorente |
work_keys_str_mv |
AT llorentebriardoernesto selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT sotogabrielacynthia selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT flawiamirthamaria selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution AT ayubnicolasdaniel selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution |
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1768544202014064640 |