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Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles

Organelle biogenesis and function is dependent on the concerted action of both organellar-encoded (if present) and nuclear-encoded proteins. Differences between homologous organelles across the Plant Kingdom arise, in part, as a result of differences in the cohort of nuclear-encoded proteins that ar...

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Autores principales: Costello, Rona, Emms, David M, Kelly, Steven
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7086175/
https://www.ncbi.nlm.nih.gov/pubmed/31750917
http://dx.doi.org/10.1093/molbev/msz275
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author Costello, Rona
Emms, David M
Kelly, Steven
author_facet Costello, Rona
Emms, David M
Kelly, Steven
author_sort Costello, Rona
collection PubMed
description Organelle biogenesis and function is dependent on the concerted action of both organellar-encoded (if present) and nuclear-encoded proteins. Differences between homologous organelles across the Plant Kingdom arise, in part, as a result of differences in the cohort of nuclear-encoded proteins that are targeted to them. However, neither the rate at which differences in protein targeting accumulate nor the evolutionary consequences of these changes are known. Using phylogenomic approaches coupled to ancestral state estimation, we show that the plant organellar proteome has diversified in proportion with molecular sequence evolution such that the proteomes of plant chloroplasts and mitochondria lose or gain on average 3.6 proteins per million years. We further demonstrate that changes in organellar protein targeting are associated with an increase in the rate of molecular sequence evolution and that such changes predominantly occur in genes with regulatory rather than metabolic functions. Finally, we show that gain and loss of protein target signals occurs at a higher rate following gene duplication, revealing that gene and genome duplication are a key facilitator of plant organelle evolution.
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spelling pubmed-70861752020-03-26 Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles Costello, Rona Emms, David M Kelly, Steven Mol Biol Evol Discoveries Organelle biogenesis and function is dependent on the concerted action of both organellar-encoded (if present) and nuclear-encoded proteins. Differences between homologous organelles across the Plant Kingdom arise, in part, as a result of differences in the cohort of nuclear-encoded proteins that are targeted to them. However, neither the rate at which differences in protein targeting accumulate nor the evolutionary consequences of these changes are known. Using phylogenomic approaches coupled to ancestral state estimation, we show that the plant organellar proteome has diversified in proportion with molecular sequence evolution such that the proteomes of plant chloroplasts and mitochondria lose or gain on average 3.6 proteins per million years. We further demonstrate that changes in organellar protein targeting are associated with an increase in the rate of molecular sequence evolution and that such changes predominantly occur in genes with regulatory rather than metabolic functions. Finally, we show that gain and loss of protein target signals occurs at a higher rate following gene duplication, revealing that gene and genome duplication are a key facilitator of plant organelle evolution. Oxford University Press 2020-04 2019-11-21 /pmc/articles/PMC7086175/ /pubmed/31750917 http://dx.doi.org/10.1093/molbev/msz275 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Costello, Rona
Emms, David M
Kelly, Steven
Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles
title Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles
title_full Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles
title_fullStr Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles
title_full_unstemmed Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles
title_short Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles
title_sort gene duplication accelerates the pace of protein gain and loss from plant organelles
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7086175/
https://www.ncbi.nlm.nih.gov/pubmed/31750917
http://dx.doi.org/10.1093/molbev/msz275
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