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.
Highlights
The specific deposition of histone variants into chromatin is an important epigenetic mechanism that contributes to gene regulation through chromatin architectural changes
In addition to trans-acting factors, we reported on the genomic organization of the carp ribosomal cistron [34], when cis-acting elements located in the intergenic spacer (IGS), named T0 ́ and T0, and core promoter (CP), can contribute to the modulation of rRNA synthesis
Because post-translational modifications (PTMs) of H2A.Z are associated with different chromatin states [27,40,41], we found a differential enrichment of H2A.Zub in the IGS and CP regions
Summary
The specific deposition of histone variants into chromatin is an important epigenetic mechanism that contributes to gene regulation through chromatin architectural changes. Fish are living under large fluctuations of physical parameters, such as photoperiod, water temperature, nutrition availability, oxygen concentration, and salinity, among others [2] In this context, the common carp provides a powerful, natural, non-manipulated model for studying several molecular and cellular responses as part of the acclimatization process [2,3]. In addition to packaging DNA, chromatin is a dynamic structure that adjusts to different cellular processes in response to biotic and abiotic environmental parameters [6] This flexible and efficient intercommunication between genomic DNA and exogenous influences can be explained by several epigenetic mechanisms, such as DNA methylation [7], ATP-dependent chromatin remodeling [8], noncoding RNAs [9], post-translational modifications (PTMs) of histones, and the replacement of canonical histones with non-allelic histone variants [10,11]. The nonrandom deposition of histone variants into chromatin that occurs independently of DNA replication, substantially contributes to gene regulation and architectural changes in chromosomes [12]
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