Diversification of the Caenorhabditis heat shock response by Helitron transposable elements

Abstract

Heat Shock Factor 1 (HSF-1) is a key regulator of the heat shock response (HSR). Upon heat shock, HSF-1 binds well-conserved motifs, called Heat Shock Elements (HSEs), and drives expression of genes important for cellular protection during this stress. Remarkably, we found that substantial numbers of HSEs in multiple <i>Caenorhabditis</i> species reside within Helitrons, a type of DNA transposon. Consistent with Helitron-embedded HSEs being functional, upon heat shock they display increased HSF-1 and RNA polymerase II occupancy and up-regulation of nearby genes in <i>C. elegans</i>. Interestingly, we found that different genes appear to be incorporated into the HSR by species-specific Helitron insertions in <i>C. elegans</i> and <i>C. briggsae</i> and by strain-specific insertions among different wild isolates of <i>C. elegans</i>. Our studies uncover previously unidentified targets of HSF-1 and show that Helitron insertions are responsible for rewiring and diversifying the <i>Caenorhabditis</i> HSR.