The characterization of macroH2A beyond vertebrates supports an ancestral origin and conserved role for histone variants in chromatin

Rivera-Casas, Ciro; González-Romero, Rodrigo; Cheema, Manjinder S.; Ausió, Juan; Eirín‐López, José M.

doi:10.1080/15592294.2016.1172161

Cited by 40 publications

(35 citation statements)

References 73 publications

(119 reference statements)

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“…H2As examined. The most obvious of these differences have been noted previously (Gautier, et al 2004;Gonzalez-Romero, et al 2008;Ishibashi, et al 2010;Bonisch and Hake 2012;Talbert, et al 2012;Rivera-Casas, et al 2016;Buschbeck and Hake 2017).…”

Section: Distinguishing Structural Features Of Short H2a Variant Protmentioning

confidence: 75%

“…Some variants, such as H2A.Z and cenH3, diverged from canonical histones early in eukaryotic evolution. Other variants, such as H2A.X, might have arisen independently in several lineages, whereas variants such as macroH2A are present only in some lineages (Malik and Henikoff 2003;Talbert and Henikoff 2010;Rivera-Casas, et al 2016). Despite these diverse origins, most histone variants evolve under strong purifying selection Talbert, et al 2012).…”

Section: Introductionmentioning

confidence: 99%

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

Molaro

Young

Malik

2017

Preprint

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Eukaryotic genomes must accomplish the tradeoff between compact packaging for genome stability and inheritance, and 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. While some histone variants are highly conserved across eukaryotes, others carry out lineage-specific functions. Here, we characterize the evolution of male germline-specific "short H2A variants", which wrap shorter DNA fragments than canonical H2A. In addition to three previously described H2A.B, H2A.L and H2A.P variants, we describe a novel, extremely short H2A histone variant: H2A.Q. We show that H2A.B, H2A.L, H2A.P and H2A.Q are most closely related to a novel, more canonical mmH2A variant found only in monotremes and marsupials. Using phylogenomics, we trace the origins and early diversification of short histone variants into four distinct clades to the ancestral X chromosome of placental mammals. We show that short H2A variants further diversified by repeated lineage-specific amplifications and losses, including pseudogenization of H2A.L in many primates. We also uncover evidence for concerted evolution of H2A.B and H2A.L genes by gene conversion in many species, involving loci separated by large distances. Finally, we find that short H2As evolve more rapidly than any other histone variant, with evidence that positive selection has acted upon H2A.P in primates. Based on their X chromosomal location and pattern of genetic innovation, we speculate that short H2A histone variants are engaged in a form of genetic conflict involving the mammalian sex chromosomes. IntroductionNucleosomes are the basic unit of chromatin in practically all eukaryotes. A typical nucleosome particle wraps 150bp of DNA around an octamer of four histone proteins: H3, H4, H2A and H2B (Kornberg 1974;Kornberg and Thomas 1974;Malik and Henikoff 2003). These four canonical "core" histone proteins have a stereotypical structure characterized by alpha-helices comprising a "histone fold domain" (HFD) (Luger, et al. 1997). During nucleosome assembly, the HFD mediates dimerization of H3 with H4, and that of H2A with H2B, and contains the nucleosome-DNA interface. Nucleosomes thus comprise a central core of a H3-H4 tetramer, flanked by two H2A-H2B dimers. In contrast to their HFD, the N-and C-terminal tails of canonical histones are far less structured and remain solvent-exposed in the nucleosome.. CC-BY-NC 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/165936 doi: bioRxiv preprint first posted online Jul. 20, 2017; 3 Nucleosomes can prevent other cellular factors, such as transcription factors, from interacting with DNA. While the post-translational modification of histone tails play an important role in regulating these interactions, eukaryotic genomes also establish diverse chroma...

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Section: Distinguishing Structural Features Of Short H2a Variant Protmentioning

confidence: 75%

Section: Introductionmentioning

confidence: 99%

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

Molaro

Young

Malik

2017

Preprint

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“…Some histone variants, such as H2A.Z and CENPA, diverged from canonical histones early in eukaryotic evolution and are present in nearly all eukaryotic lineages. Other variants originated more recently and are found in just one lineage, e.g., macroH2A in Filozoans (a lineage that includes animals and choanoflagellates) (Malik and Henikoff 2003;Talbert and Henikoff 2010;Rivera-Casas et al 2016). Most histone variants are highly conserved and evolve under strong purifying selection (Piontkivska et al 2002;Rooney et al 2002;Talbert et al 2012).…”

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confidence: 99%

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

Molaro¹,

Young²,

Malik³

2018

Genome Res.

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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, , which may represent the common ancestor of the short H2As. We also discovered a novel class of short H2A histone variants in eutherian mammals, 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: ,, , and 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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“…For example, the variant H3.3 is present in actively transcribed chromatin, whereas mac-roH2A.1 and the isoform H2A.2 can have either positive or negative effects on transcription depending on the gene of interest. These variants appear to be conserved across phylogenetic groups [2,10].…”

Section: Epigenetic Mechanismsmentioning

confidence: 99%

The Role of Epigenomics in Aquatic Toxicology

Brander

Biales

Connon

2017

Enviro Toxic and Chemistry

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Abstract-Over the past decade, the field of molecular biology has rapidly incorporated epigenetic studies to evaluate organismenvironment interactions that can result in chronic effects. Such responses arise from early life stage stress, the utilization of genetic information over an individual's life time, and transgenerational inheritance. Knowledge of epigenetic mechanisms provides the potential for a comprehensive evaluation of multigenerational and heritable effects from environmental stressors, such as contaminants. Focused studies have provided a greater understanding of how many responses to environmental stressors are driven by epigenetic modifiers. We discuss the promise of epigenetics and suggest future research directions within the field of aquatic toxicology, with a particular focus on the potential for identifying key heritable marks with consequential impacts at the organism and population levels. Environ

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The characterization of macroH2A beyond vertebrates supports an ancestral origin and conserved role for histone variants in chromatin

Cited by 40 publications

References 73 publications

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

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

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

The Role of Epigenomics in Aquatic Toxicology

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