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Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves

In Metazoa, four out of five complexes involved in oxidative phosphorylation (OXPHOS) are formed by subunits encoded by both the mitochondrial (mtDNA) and nuclear (nuDNA) genomes, leading to the expectation of mitonuclear coevolution. Previous studies have supported coadaptation of mitochondria-enco...

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Autores principales: Piccinini, Giovanni, Iannello, Mariangela, Puccio, Guglielmo, Plazzi, Federico, Havird, Justin C, Ghiselli, Fabrizio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136519/
https://www.ncbi.nlm.nih.gov/pubmed/33616640
http://dx.doi.org/10.1093/molbev/msab054
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author Piccinini, Giovanni
Iannello, Mariangela
Puccio, Guglielmo
Plazzi, Federico
Havird, Justin C
Ghiselli, Fabrizio
author_facet Piccinini, Giovanni
Iannello, Mariangela
Puccio, Guglielmo
Plazzi, Federico
Havird, Justin C
Ghiselli, Fabrizio
author_sort Piccinini, Giovanni
collection PubMed
description In Metazoa, four out of five complexes involved in oxidative phosphorylation (OXPHOS) are formed by subunits encoded by both the mitochondrial (mtDNA) and nuclear (nuDNA) genomes, leading to the expectation of mitonuclear coevolution. Previous studies have supported coadaptation of mitochondria-encoded (mtOXPHOS) and nuclear-encoded OXPHOS (nuOXPHOS) subunits, often specifically interpreted with regard to the “nuclear compensation hypothesis,” a specific form of mitonuclear coevolution where nuclear genes compensate for deleterious mitochondrial mutations due to less efficient mitochondrial selection. In this study, we analyzed patterns of sequence evolution of 79 OXPHOS subunits in 31 bivalve species, a taxon showing extraordinary mtDNA variability and including species with “doubly uniparental” mtDNA inheritance. Our data showed strong and clear signals of mitonuclear coevolution. NuOXPHOS subunits had concordant topologies with mtOXPHOS subunits, contrary to previous phylogenies based on nuclear genes lacking mt interactions. Evolutionary rates between mt and nuOXPHOS subunits were also highly correlated compared with non-OXPHO-interacting nuclear genes. Nuclear subunits of chimeric OXPHOS complexes (I, III, IV, and V) also had higher dN/dS ratios than Complex II, which is formed exclusively by nuDNA-encoded subunits. However, we did not find evidence of nuclear compensation: mitochondria-encoded subunits showed similar dN/dS ratios compared with nuclear-encoded subunits, contrary to most previously studied bilaterian animals. Moreover, no site-specific signals of compensatory positive selection were detected in nuOXPHOS genes. Our analyses extend the evidence for mitonuclear coevolution to a new taxonomic group, but we propose a reconsideration of the nuclear compensation hypothesis.
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spelling pubmed-81365192021-05-25 Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves Piccinini, Giovanni Iannello, Mariangela Puccio, Guglielmo Plazzi, Federico Havird, Justin C Ghiselli, Fabrizio Mol Biol Evol Discoveries In Metazoa, four out of five complexes involved in oxidative phosphorylation (OXPHOS) are formed by subunits encoded by both the mitochondrial (mtDNA) and nuclear (nuDNA) genomes, leading to the expectation of mitonuclear coevolution. Previous studies have supported coadaptation of mitochondria-encoded (mtOXPHOS) and nuclear-encoded OXPHOS (nuOXPHOS) subunits, often specifically interpreted with regard to the “nuclear compensation hypothesis,” a specific form of mitonuclear coevolution where nuclear genes compensate for deleterious mitochondrial mutations due to less efficient mitochondrial selection. In this study, we analyzed patterns of sequence evolution of 79 OXPHOS subunits in 31 bivalve species, a taxon showing extraordinary mtDNA variability and including species with “doubly uniparental” mtDNA inheritance. Our data showed strong and clear signals of mitonuclear coevolution. NuOXPHOS subunits had concordant topologies with mtOXPHOS subunits, contrary to previous phylogenies based on nuclear genes lacking mt interactions. Evolutionary rates between mt and nuOXPHOS subunits were also highly correlated compared with non-OXPHO-interacting nuclear genes. Nuclear subunits of chimeric OXPHOS complexes (I, III, IV, and V) also had higher dN/dS ratios than Complex II, which is formed exclusively by nuDNA-encoded subunits. However, we did not find evidence of nuclear compensation: mitochondria-encoded subunits showed similar dN/dS ratios compared with nuclear-encoded subunits, contrary to most previously studied bilaterian animals. Moreover, no site-specific signals of compensatory positive selection were detected in nuOXPHOS genes. Our analyses extend the evidence for mitonuclear coevolution to a new taxonomic group, but we propose a reconsideration of the nuclear compensation hypothesis. Oxford University Press 2021-02-22 /pmc/articles/PMC8136519/ /pubmed/33616640 http://dx.doi.org/10.1093/molbev/msab054 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Piccinini, Giovanni
Iannello, Mariangela
Puccio, Guglielmo
Plazzi, Federico
Havird, Justin C
Ghiselli, Fabrizio
Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves
title Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves
title_full Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves
title_fullStr Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves
title_full_unstemmed Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves
title_short Mitonuclear Coevolution, but not Nuclear Compensation, Drives Evolution of OXPHOS Complexes in Bivalves
title_sort mitonuclear coevolution, but not nuclear compensation, drives evolution of oxphos complexes in bivalves
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136519/
https://www.ncbi.nlm.nih.gov/pubmed/33616640
http://dx.doi.org/10.1093/molbev/msab054
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