Long-Term Evolution of Histone Families: Old Notions and New Insights into Their Mechanisms of Diversification Across Eukaryotes

Eirín‐López, José M.; González-Romero, Rodrigo; Dryhurst, Deanna; Méndez, Josefina; Ausió, Juan

doi:10.1007/978-3-642-00952-5_8

Cited by 42 publications

(41 citation statements)

References 112 publications

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“…Instead, it supports a conserved ancestral role for histone variant lineages, based on the widespread presence of macroH2A and other specialized variants across metazoan animals. [33][34][35]45,46,62,63 Under this hypothesis, canonical histones (multiple copy, intronless, non polyadenylated genes) would have derived from ancestral variants (single copy, introns, polyadenylated genes) in order to produce enough protein product during the Sphase of the cell cycle to accommodate the newly synthesized DNA into nucleosomes. Overall, the results presented in this work help to configure a new evolutionary scenario in which histone variants, rather than modern "deviants" of canonical histones, would constitute ancient components of eukaryotic chromatin.…”

Section: Discussionmentioning

confidence: 99%

“…12,28,31,32 For a long time macroH2A was thought to be an invention of vertebrates, culminating (together with H2A.B) the functional diversification of variants within the H2A family. [33][34][35][36] The hypothetical existence of a functional invertebrate macroH2A bears 2 critical implications: first, the evolutionary origin of this variant would have to be redefined; second, the role of macroH2A in chromatin structure and epigenetic regulation would require further examination in a broader evolutionary context. Unfortunately, no conclusive experimental information is currently available for the non-vertebrate counterpart of this histone variant.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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Histone variants play a critical role in chromatin structure and epigenetic regulation. These "deviant" proteins have been historically considered as the evolutionary descendants of ancestral canonical histones, helping specialize the nucleosome structure during eukaryotic evolution. Such view is now challenged by 2 major observations: first, canonical histones present extremely unique features not shared with any other genes; second, histone variants are widespread across many eukaryotic groups. The present work further supports the ancestral nature of histone variants by providing the first in vivo characterization of a functional macroH2A histone (a variant long defined as a specific refinement of vertebrate chromatin) in a non-vertebrate organism (the mussel Mytilus) revealing its recruitment into heterochromatic fractions of actively proliferating tissues. Combined with in silico analyses of genomic data, these results provide evidence for the widespread presence of macroH2A in metazoan animals, as well as in the holozoan Capsaspora, supporting an evolutionary origin for this histone variant lineage before the radiation of Filozoans (including Filasterea, Choanoflagellata and Metazoa). Overall, the results presented in this work help configure a new evolutionary scenario in which histone variants, rather than modern "deviants" of canonical histones, would constitute ancient components of eukaryotic chromatin.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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“…In this sense, the differential position of the Ag-NOR/MM+/18S rDNA sites in the long arms of this pair in both genomes (i.e., pericentromeric and terminal) strongly indicates a paracentric inversion encompassing this rDNA region. Molina Cytogenet Genome Res DOI: 10.1159/000499748 6 Similar to ribosomal genes, the histone multigene family plays a crucial role in the genomes of eukaryotes [Eirín-López et al, 2009]. The position of histone genes in the chromosomes of many fish species has been shown to be evolutionarily more dynamic than previously thought [Pansonato-Alves et al, 2013;Costa et al, 2014;Daniel et al, 2015;Utsunomia et al, 2016], and eventually they were co-located with ribosomal genes [Costa et al, 2016].…”

Section: Discussionmentioning

confidence: 99%

Paracentric Inversions Differentiate the Conservative Karyotypes in Two Centropomus Species (Teleostei: Centropomidae)

Borges

Cioffi

Bertollo

et al. 2019

Cytogenet Genome Res

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Centropomus is the sole genus of the Centropomidae family (Teleostei), comprising 12 species widely distributed throughout the Western Atlantic and Eastern Pacific, with 6 of them occurring in the Western Atlantic in extensive sympatry. Their life history and phylogenetic relationships are well characterized; however, aspects of chromosomal evolution are still unknown. Here, cytogenetic analyses of 2 Centropomus species of great economic value (C. undecimalis and C. mexicanus) were performed using conventional (Giemsa, Ag-NOR, and fluorochrome staining, C- and replication banding) and molecular (chromosomal mapping of 18S and 5S rDNA, H2A-H2B and H3 hisDNA, and (TTAGGG)_n repeats) approaches. The karyotypes of both species were composed of 48 solely acrocentric chromosomes (2n = 48; FN = 48), but the single ribosomal site was located in varying positions in the long arms of the second largest chromosome pair. Replication bands were generally similar, although conspicuous differences were observed in some chromosome regions. In both species, the histone H3 genes were located on 3 apparently homeologous chromosome pairs, but the exact position of these clusters differed slightly. Interspecific hisDNA and rDNA site displacements can indicate the occurrence of multiple paracentric inversions during the evolutionary diversification of the Centropomus genomes. Although the karyotypes remained similar in both species, our data demonstrate an unsuspected microstructural reorganization between them, driven most likely by a series of paracentric inversions.

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“…Histone genes are quite conserved in different species but display heterogeneity with respect to the pattern of genome organization [Sellos et al, 1990;Cabrero et al, 2009;Eirín-López et al, 2009]. Although the distribution of these genes in the chromosomes of fishes is still poorly known, a single locus for primary DNAhis occurs in salmonids, located in the pericentromeric region of chromosomes [Pendás et al, 1994].…”

Section: Histone H2b-h2a and H3 Chromosomal Mappingmentioning

confidence: 99%

Unusual Dispersion of Histone Repeats on the Whole Chromosomal Complement and Their Colocalization with Ribosomal Genes in Rachycentron canadum (Rachycentridae, Perciformes)

Costa

Cioffi²,

Bertollo³

et al. 2014

Cytogenet Genome Res

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Rachycentron canadum, the only representative of the family Rachycentridae, has been the focus of biotechnological interest due to its significant potential in marine fish farming. The chromosome set of this species has been widely investigated with respect to the location of genes and multigene families. A FISH analysis was performed using 4 multigene families as probes, represented by 5S and 18S ribosomal genes and histones H2B-H2A and H3. Earlier data suggested that differential replication of heterochromatin could be partially associated with functional genes. Indeed, our results showed that the DNA contained in heterochromatic regions of R. canadum contains 5S and 18S ribosomal genes as well as the gene sequences of histones H2B-H2A and H3, which were colocalized. The distribution of H3 sequences in all heterochromatic regions, except in 13q, could indicate an important evolutionary role for this class of repetitive sequences. Besides, the presence of chromosome regions bearing multifunctional repetitive sequences formed by H2B-H2A/H3/18S rDNA and H2B-H2A/H3/5S rDNA clusters was demonstrated for the first time in fishes. The implications of differential histone gene extension and its functionality in the karyotype of R. canadum remain unknown.

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Long-Term Evolution of Histone Families: Old Notions and New Insights into Their Mechanisms of Diversification Across Eukaryotes

Cited by 42 publications

References 112 publications

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

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

Paracentric Inversions Differentiate the Conservative Karyotypes in Two <b><i>Centropomus</i></b> Species (Teleostei: Centropomidae)

Unusual Dispersion of Histone Repeats on the Whole Chromosomal Complement and Their Colocalization with Ribosomal Genes in <b><i>Rachycentron canadum</i></b> (Rachycentridae, Perciformes)

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