The epigenetics effects of transposable elements are genomic context dependent and not restricted to gene silencing in Drosophila

Abstract

Abstract Background Transposable elements (TEs) represent a threat to genome integrity due to their proliferative capacity. Eukaryotic cells silence TEs through different molecular mechanisms, including the deposition of repressive histone marks. Previous studies have shown that TE repressive marks can spread to neighboring sequences. However, evidence for this spreading leading to nearby gene silencing remains limited. Similarly, whether TEs induce changes in the enrichment of active histone marks genome-wide, and the potential impact on gene expression have not been widely studied. Results In this work, we perform a comprehensive study of the epigenetic effects of 2235 TEs and their potential effects on nearby gene expression on Drosophila melanogaster head, gut, and ovary. While most TEs (816) induce the enrichment of the H3K9me3 repressive mark, with stronger epigenetic effects in the ovary, a substantial number (345 TEs) induce the enrichment of the H3K27ac active mark, particularly in the gut. We find that 70% of the H3K9me3 enriched TEs associated with expression changes downregulate the nearby gene, and 50% of the H3K27ac enriched TEs associated with expression changes lead to gene upregulation. These changes in expression affect specific regulatory networks only in the head. Furthermore, TE epigenetic effects on gene expression are genomic context dependent. Finally, we find that 221 TEs also affect gene expression by disrupting regions enriched for histone marks. Conclusions Overall, our results show that TEs contribute to the generation of regulatory novelty through epigenetic changes, with these epigenetic effects not restricted to gene silencing and being genomic context dependent.

Keywords

• H3K9me3
• H3K27ac
• Histone marks
• Drosophila
• Gene expression
• Tissue specificity