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Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals

Eukaryotic genomes must accomplish both compact packaging for genome stability and inheritance, as well as accessibility for gene expression. They do so using post-translational modifications of four ancient canonical histone proteins (H2A, H2B, H3, and H4) and by deploying histone variants with spe...

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Autores principales: Molaro, Antoine, Young, Janet M., Malik, Harmit S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880237/
https://www.ncbi.nlm.nih.gov/pubmed/29549088
http://dx.doi.org/10.1101/gr.229799.117
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author Molaro, Antoine
Young, Janet M.
Malik, Harmit S.
author_facet Molaro, Antoine
Young, Janet M.
Malik, Harmit S.
author_sort Molaro, Antoine
collection PubMed
description Eukaryotic genomes must accomplish both compact packaging for genome stability and inheritance, as well as accessibility for gene expression. They do so using post-translational modifications of four ancient canonical histone proteins (H2A, H2B, H3, and H4) and by deploying histone variants with specialized chromatin functions. Some histone variants are conserved across all eukaryotes, whereas others are lineage-specific. Here, we performed detailed phylogenomic analyses of “short H2A histone” variants found in mammalian genomes. We discovered a previously undescribed typically-sized H2A variant in monotremes and marsupials, H2A.R, which may represent the common ancestor of the short H2As. We also discovered a novel class of short H2A histone variants in eutherian mammals, H2A.Q. We show that short H2A variants arose on the X Chromosome in the common ancestor of all eutherian mammals and diverged into four evolutionarily distinct clades: H2A.B, H2A.L, H2A.P, and H2A.Q. However, the repertoires of short histone H2A variants vary extensively among eutherian mammals due to lineage-specific gains and losses. Finally, we show that all four short H2As are subject to accelerated rates of protein evolution relative to both canonical and other variant H2A proteins including H2A.R. Our analyses reveal that short H2As are a unique class of testis-restricted histone variants displaying an unprecedented evolutionary dynamism. Based on their X-Chromosomal localization, genetic turnover, and testis-specific expression, we hypothesize that short H2A variants may participate in genetic conflicts involving sex chromosomes during reproduction.
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spelling pubmed-58802372018-10-01 Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals Molaro, Antoine Young, Janet M. Malik, Harmit S. Genome Res Research Eukaryotic genomes must accomplish both compact packaging for genome stability and inheritance, as well as accessibility for gene expression. They do so using post-translational modifications of four ancient canonical histone proteins (H2A, H2B, H3, and H4) and by deploying histone variants with specialized chromatin functions. Some histone variants are conserved across all eukaryotes, whereas others are lineage-specific. Here, we performed detailed phylogenomic analyses of “short H2A histone” variants found in mammalian genomes. We discovered a previously undescribed typically-sized H2A variant in monotremes and marsupials, H2A.R, which may represent the common ancestor of the short H2As. We also discovered a novel class of short H2A histone variants in eutherian mammals, H2A.Q. We show that short H2A variants arose on the X Chromosome in the common ancestor of all eutherian mammals and diverged into four evolutionarily distinct clades: H2A.B, H2A.L, H2A.P, and H2A.Q. However, the repertoires of short histone H2A variants vary extensively among eutherian mammals due to lineage-specific gains and losses. Finally, we show that all four short H2As are subject to accelerated rates of protein evolution relative to both canonical and other variant H2A proteins including H2A.R. Our analyses reveal that short H2As are a unique class of testis-restricted histone variants displaying an unprecedented evolutionary dynamism. Based on their X-Chromosomal localization, genetic turnover, and testis-specific expression, we hypothesize that short H2A variants may participate in genetic conflicts involving sex chromosomes during reproduction. Cold Spring Harbor Laboratory Press 2018-04 /pmc/articles/PMC5880237/ /pubmed/29549088 http://dx.doi.org/10.1101/gr.229799.117 Text en © 2018 Molaro et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Molaro, Antoine
Young, Janet M.
Malik, Harmit S.
Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals
title Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals
title_full Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals
title_fullStr Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals
title_full_unstemmed Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals
title_short Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals
title_sort evolutionary origins and diversification of testis-specific short histone h2a variants in mammals
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880237/
https://www.ncbi.nlm.nih.gov/pubmed/29549088
http://dx.doi.org/10.1101/gr.229799.117
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