Stress affects the epigenetic marks added by natural transposable element insertions in Drosophila melanogaster

Abstract

Transposable elements are emerging as an important source of cis-acting regulatory sequences and epigenetic marks that could influence gene expression. However, few studies have dissected the role of specific transposable element insertions on epigenetic gene regulation. Bari-Jheh is a natural transposon that mediates resistance to oxidative stress by adding cis-regulatory sequences that affect expression of nearby genes. In this work, we integrated publicly available ChIP-seq and piRNA data with chromatin immunoprecipitation experiments to get a more comprehensive picture of Bari-Jheh molecular effects. We showed that Bari-Jheh was enriched for H3K9me3 in nonstress conditions, and for H3K9me3, H3K4me3 and H3K27me3 in oxidative stress conditions, which is consistent with expression changes in adjacent genes. We further showed that under oxidative stress conditions, H3K4me3 and H3K9me3 spread to the promoter region of Jheh1 gene. Finally, another insertion of the Bari1 family was associated with increased H3K27me3 in oxidative stress conditions suggesting that Bari1 histone marks are copy-specific. We concluded that besides adding cis-regulatory sequences, Bari-Jheh influences gene expression by affecting the local chromatin state.

Transposable elements in Drosophila

“…Percentages of divergence to consensus were evaluated from RepeatMasker output .align file using A. Kapusta script [154] upregulation of Jheh1 and Jheh2 [166]. Second, the spread of repressive epigenetic marks targeting TEs can reduce the expression of nearby genes (see below, host defenses against TEs), as it was also demonstrated in the Jheh cluster [167]. Lee and Karpen demonstrated recently that the spread of repressive epigenetic marks to nearby DNA occurs for more than half of euchromatic TEs, and can extend up to 20 kb [12].…”

Regulatory regions in natural transposable element insertions drive interindividual differences in response to immune challenges in Drosophila

“…For example, TEs have been shown to add transcription factor binding sites, and transcription start sites, leading to changes in expression of nearby genes (33)(34)(35)(36). TEs can also influence gene expression by inducing changes in the chromatin structure (37)(38)(39). These changes in expression induced by TE insertions have been associated with several organismal phenotypes such as stress resistance and fertility (40)(41)(42).…”

Biological invasion: The influence of the hidden side of the (epi)genome

“…When they examined the neighbouring genes to these insertions, they found they were genes previously known to be involved in adaptation to a variety of environmental factors (González et al, ). Other studies have also found direct links between the presence of the insertion and adaptive phenotypes related to insecticide resistance (Magwire, Bayer, Webster, Cao, & Jiggins, ; Merenciano, Ullastres, Cara, Barrón, & González, ), cold stress response, oxidative stress (Guio, Barrón, & González, ; Guio, Vieira, & González, ), xenobiotic stress (Mateo, Ullastres, & González, ) and resistance to sigma virus (Magwire et al, ). Thus, there is growing evidence that TEs can be under selection to alter patterns of expression on neighbouring genes, leading to adaptive changes in phenotypes.…”