Abstract
Pericentromeric heterochromatin is generally composed of repetitive DNA forming a transcriptionally repressive environment. Dozens of genes were embedded into pericentromeric heterochromatin during evolution of Drosophilidae lineage while retaining activity. However, factors that contribute to insusceptibility of gene loci to transcriptional silencing remain unknown. Here, we find that the promoter region of genes that can be embedded in both euchromatin and heterochromatin exhibits a conserved structure throughout the Drosophila phylogeny and carries motifs for binding of certain chromatin remodeling factors, including insulator proteins. Using ChIP-seq data, we demonstrate that evolutionary gene relocation between euchromatin and pericentric heterochromatin occurred with preservation of sites of insulation of BEAF-32 in evolutionarily distant species, i.e. D. melanogaster and D. virilis. Moreover, promoters of virtually all protein-coding genes located in heterochromatin in D. melanogaster are enriched with insulator proteins BEAF-32, GAF and dCTCF. Applying RNA-seq of a BEAF-32 mutant, we show that the impairment of BEAF-32 function has a complex effect on gene expression in D. melanogaster, affecting even those genes that lack BEAF-32 association in their promoters. We propose that conserved intrinsic properties of genes, such as sites of insulation near the promoter regions, may contribute to adaptation of genes to the heterochromatic environment and, hence, facilitate the evolutionary relocation of genes loci between euchromatin and heterochromatin.
Highlights
Pericentromeric heterochromatin is generally composed of repetitive DNA forming a transcriptionally repressive environment
Using ChIP-seq data, we demonstrate that the insulator protein BEAF-32 occupies promoters of the same genes which are located in contrasting chromatin types in D. melanogaster and D. virilis, denoting the boundary of the nucleosome-free region available for RNA polymerase II recruitment and the surrounding heterochromatin
These include species of the melanogaster group (D. melanogaster and D. yakuba) and the obscura group (D. persimilis and D. miranda), with both groups belonging to the Sophophora subgenus, along with the virilis group (D. virilis and D. novamexicana) and the repleta group (D. mojavensis and D. hydei) that belong to the Drosophila subgenus (Table S1)
Summary
Pericentromeric heterochromatin is generally composed of repetitive DNA forming a transcriptionally repressive environment. We propose that conserved intrinsic properties of genes, such as sites of insulation near the promoter regions, may contribute to adaptation of genes to the heterochromatic environment and, facilitate the evolutionary relocation of genes loci between euchromatin and heterochromatin. Relocation of genes between euchromatin and heterochromatin during genome evolution is not unusual in the Drosophilidae lineage, the insusceptibility of heterochromatic genes to transcriptional silencing remains paradoxical and unexplained. It is still not clear whether pericentric gene loci have undergone adaptation to heterochromatic environment or originally had some intrinsic properties permitting local adaptation. One may hypothesize that gene loci capable of adaptation to heterochromatin probably share specific sites of insulation that ensure their expression in the repressive environment
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