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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Autores principales: Llorente, Briardo Ernesto, Soto, Gabriela Cynthia, Flawiá, Mirtha María, Ayub, Nicolás Daniel
Publicado: 2016
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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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spelling 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
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AT flawiamirthamaria selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution
AT ayubnicolasdaniel selectivepressureagainsthorizontallyacquiredprokaryoticgenesasadrivingforceofplastidevolution
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