Epigenetic regulation of the ribosomal cistron seasonally modulates enrichment of H2A.Z and H2A.Zub in response to different environmental inputs in carp (Cyprinus carpio)

Abstract

BackgroundThe specific deposition of histone variants into chromatin is an important epigenetic mechanism that contributes to gene regulation through chromatin architectural changes. The histone variant H2A.Z is essential in higher eukaryotes, and its incorporation within chromatin is a relevant process for gene expression and genome stability. However, the dual positive and negative roles of H2A.Z in gene regulation still remain unclear. We previously reported that acclimatization in common carp fish (Cyprinus carpio) involves cyclical seasonal gene reprogramming as an adaptation response to its natural environment, when rRNA synthesis and processing are profoundly affected. Epigenetic mechanisms primarily contribute to the transcriptional modulation of ribosomal genes concomitant with the acclimatization process, thus significantly regulating this process. The aim of this study was to describe the presence of several H2A.Z subtypes in carp, and assess the role of H2A.Z on the ribosomal cistron in summer- and winter-acclimatized carp.ResultsThis paper reports for the first time about the transcriptional expression of four different H2A.Z subtypes belonging to the same organism. Remarkably, a novel H2A.Z.7 was found, which corresponds to a tissue-specific histone subtype that contains seven amino acid residues longer than the canonical H2A.Z. Moreover, H2A.Z enrichment through the ribosomal cistron was significantly higher during summer, when rRNA transcription and processing are highly active, than it was in winter. Similar patterns of H2A.Z enrichment are found in two seasonally active promoters for genes transcribed by RNA polymerase II, the L41 and Δ9-desaturase genes. Interestingly, ubiquitylated-H2A.Z (H2A.Zub) was strongly enriched on regulatory regions of the ribosomal cistron in summer-acclimatized carp. Additionally, H2A.Z was present in both heterochromatin and euchromatin states on ribosomal cistron and RNA polymerase II promoters.ConclusionsOur study revealed seasonally-dependent H2A.Z enrichment for active ribosomal cistron and RNA polymerase II promoters during the carp environmental adaptation. Moreover, seasonal H2A.Zub enrichment appears as a specific mechanism contributing to the regulation of chromatin architecture under natural conditions. The existence of several H2A.Z subtypes in carp suggests that the epigenetic regulation in this species constitutes a complex and finely tuned mechanism developed to cope with seasonal environmental changes that occur in its habitat.

Histone Variants and Epigenetics

“…This shorter H2A.Z isoform destabilizes nucleosomes and is most enriched in brain , in which H2A.Z, like H3.3, is known to be especially abundant (Pina and Suau 1987). Although this particular isoform appears to be limited to primates, evidence for a longer alternatively spliced isoform with potential for nucleosome destabilization was reported in carp brain (Simonet et al 2013). With the increasing popularity of RNA-seq for identification of alternatively processed variants, we expect that other examples of potential H2A.Z functional diversification will be discovered.…”

Characterization of mussel H2A.Z.2: a new H2A.Z variant preferentially expressed in germinal tissues fromMytilus

“…(Bonisch et al 2012;Dryhurst et al 2009;Simonet et al 2013) and plants (Yi et al 2006), this is the first report describing multiple H2A.Z variants in non-vertebrate animals.…”

“…Based on the differences observed between H2A.Z.1 and H2A.Z.2 promoter regions, it seems likely that the functional specialization provided by these two variants is at least in part determined by differences in their expression patterns Simonet et al 2013;Yi et al 2006), as well as by nucleotide differences between their coding regions causing slight amino acid variation Horikoshi et al 2013;Nishibuchi et al 2014). …”

“…During the course of evolution, H2A.Z has experienced additional rounds of functional specialization, giving rise to new H2A.Z isoforms and/or variants refining the transcriptional regulatory mechanisms within the cell nucleus of certain groups of organisms Simonet et al 2013;Yi et al 2006). Indeed, most vertebrates exhibit two non-allelic H2A.Z variants encoded by independent genes (H2A.Z.1 and H2A.Z.2).…”

“…Additional H2A.Z histones have been described in other organisms, including up to four different H2A.Z variants in the teleost fish Cyprinus carpio (Simonet et al 2013) and at least three different H2A.Z variants in plants (Yi et al 2006). Based on the differences observed between H2A.Z.1 and H2A.Z.2 promoter regions, it seems likely that the functional specialization provided by these two variants is at least in part determined by differences in their expression patterns Simonet et al 2013;Yi et al 2006), as well as by nucleotide differences between their coding regions causing slight amino acid variation Horikoshi et al 2013;Nishibuchi et al 2014).…”