Heat-induced transcriptional activation of LTR retrotransposons in the regenerative flatworm Macrostomum lignano.

The evolutionary arms race between transposable elements and their hosts contributes to genomic complexity. Because transposable element mobilization can be deleterious to individual cells and organisms, their activity is restricted by the host. Transposable elements can be reactivated during stress; however, the exact mechanisms vary and are rarely well understood. Here, we report that in the regenerative flatworm model organism Macrostomum lignano, long terminal repeat retrotransposon families (LTR-RTs) of the Ty3/Mdg4 superfamily clades Mag, CsRN1, and Gmr1/Osvaldo independently acquired canonical heat shock elements (HSEs) in their promoters. Using RNA-seq and qPCR, we found that four HSE-containing LTR-RT families showed significant and more than 250-fold increased transcription at elevated temperatures. Using transgenesis and HSE mutation analysis, we showed that HSEs are necessary for the heat sensitivity of LTR-RTs in vivo. While this phenomenon has been well described in a phylogenetically distant family of HSE-containing ONSEN Ty1/Copia plant LTR-RTs, and there are reports of measurable heat induction and the presence of HSE-like sequences in LTR-RTs in other animal taxa, this is the first report of a strong and potentially direct activation mechanism in flatworms. Our results suggest the convergent evolution of heat stress responses in LTR-RTs of animals and plants, broadening our understanding of the evolutionary strategies used by transposable elements.