Nuclear stress bodies enable a germline-specific transcriptional stress response in Drosophila

Abstract

The germline ensures the continuity of genetic information across generations, but how this immortal lineage functions under stress conditions remains incompletely understood. Here, we identify that heat shock factor (Hsf), a conserved master regulator of the stress response, drives the expression of transposable elements (TEs), in addition to molecular chaperones upon heat shock in Drosophila gonads. In germ cells, this potential intra-genomic conflict is countered by the formation of nuclear stress bodies (nSBs) at non-coding satellite DNA repeats. Using chemical and genetic perturbations, we demonstrate that nSBs are both necessary and sufficient to delay Hsf-dependent transcription. Notably, this nSB-mediated delay, in tandem with the piRNA pathway, allows germ cells to selectively express molecular chaperones, but not transposable elements, upon heat shock. Overall, we propose that this unique transcriptional stress response preserves germline function and evolutionary fitness, especially in natural populations routinely exposed to environmental stress.