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Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes

The coordination between nuclear and organellar genes is essential to many aspects of eukaryotic life, including basic metabolism, energy production, and ultimately, organismal fitness. Although nuclear genes are biparentally inherited, mitochondrial and chloroplast genes are almost exclusively mate...

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Autores principales: Hough, Josh, Ågren, J. Arvid, Barrett, Spencer C.H., Wright, Stephen I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4202333/
https://www.ncbi.nlm.nih.gov/pubmed/25193309
http://dx.doi.org/10.1093/gbe/evu197
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author Hough, Josh
Ågren, J. Arvid
Barrett, Spencer C.H.
Wright, Stephen I.
author_facet Hough, Josh
Ågren, J. Arvid
Barrett, Spencer C.H.
Wright, Stephen I.
author_sort Hough, Josh
collection PubMed
description The coordination between nuclear and organellar genes is essential to many aspects of eukaryotic life, including basic metabolism, energy production, and ultimately, organismal fitness. Although nuclear genes are biparentally inherited, mitochondrial and chloroplast genes are almost exclusively maternally inherited, and this asymmetry may lead to a bias in the chromosomal distribution of nuclear genes whose products act in the mitochondria or chloroplasts. In particular, because X-linked genes have a higher probability of cotransmission with organellar genes (2/3) compared with autosomal genes (1/2), selection for coadaptation has been predicted to lead to an overrepresentation of nuclear-mitochondrial and nuclear-chloroplast genes on the X chromosome relative to autosomes. In contrast, the occurrence of sexually antagonistic organellar mutations might lead to selection for movement of cytonuclear genes from the X chromosome to autosomes to reduce male mutation load. Recent broad-scale comparative studies of N-mt distributions in animals have found evidence for these hypotheses in some species, but not others. Here, we use transcriptome sequences to conduct the first study of the chromosomal distribution of cytonuclear interacting genes in a plant species with sex chromosomes (Rumex hastatulus; Polygonaceae). We found no evidence of under- or overrepresentation of either N-mt or N-cp genes on the X chromosome, and thus no support for either the coadaptation or the sexual-conflict hypothesis. We discuss how our results from a species with recently evolved sex chromosomes fit into an emerging picture of the evolutionary forces governing the chromosomal distribution of nuclear-mitochondrial and nuclear-chloroplast genes.
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spelling pubmed-42023332014-10-21 Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes Hough, Josh Ågren, J. Arvid Barrett, Spencer C.H. Wright, Stephen I. Genome Biol Evol Letter The coordination between nuclear and organellar genes is essential to many aspects of eukaryotic life, including basic metabolism, energy production, and ultimately, organismal fitness. Although nuclear genes are biparentally inherited, mitochondrial and chloroplast genes are almost exclusively maternally inherited, and this asymmetry may lead to a bias in the chromosomal distribution of nuclear genes whose products act in the mitochondria or chloroplasts. In particular, because X-linked genes have a higher probability of cotransmission with organellar genes (2/3) compared with autosomal genes (1/2), selection for coadaptation has been predicted to lead to an overrepresentation of nuclear-mitochondrial and nuclear-chloroplast genes on the X chromosome relative to autosomes. In contrast, the occurrence of sexually antagonistic organellar mutations might lead to selection for movement of cytonuclear genes from the X chromosome to autosomes to reduce male mutation load. Recent broad-scale comparative studies of N-mt distributions in animals have found evidence for these hypotheses in some species, but not others. Here, we use transcriptome sequences to conduct the first study of the chromosomal distribution of cytonuclear interacting genes in a plant species with sex chromosomes (Rumex hastatulus; Polygonaceae). We found no evidence of under- or overrepresentation of either N-mt or N-cp genes on the X chromosome, and thus no support for either the coadaptation or the sexual-conflict hypothesis. We discuss how our results from a species with recently evolved sex chromosomes fit into an emerging picture of the evolutionary forces governing the chromosomal distribution of nuclear-mitochondrial and nuclear-chloroplast genes. Oxford University Press 2014-09-04 /pmc/articles/PMC4202333/ /pubmed/25193309 http://dx.doi.org/10.1093/gbe/evu197 Text en © The Author(s) 2014. 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 Letter
Hough, Josh
Ågren, J. Arvid
Barrett, Spencer C.H.
Wright, Stephen I.
Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes
title Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes
title_full Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes
title_fullStr Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes
title_full_unstemmed Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes
title_short Chromosomal Distribution of Cytonuclear Genes in a Dioecious Plant with Sex Chromosomes
title_sort chromosomal distribution of cytonuclear genes in a dioecious plant with sex chromosomes
topic Letter
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4202333/
https://www.ncbi.nlm.nih.gov/pubmed/25193309
http://dx.doi.org/10.1093/gbe/evu197
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