Abstract
Germline development is sensitive to nutrient availability and environmental perturbation. Heat shock transcription factor 1 (HSF1), a key transcription factor driving the cellular heat shock response (HSR), is also involved in gametogenesis. The precise function of HSF1 (HSF-1 in C. elegans) and its regulation in germline development are poorly understood. Using the auxin-inducible degron system in C. elegans, we uncovered a role of HSF-1 in progenitor cell proliferation and early meiosis and identified a compact but important transcriptional program of HSF-1 in germline development. Interestingly, heat stress only induces the canonical HSR in a subset of germ cells but impairs HSF-1 binding at its developmental targets. Conversely, insulin/insulin growth factor 1 (IGF-1) signaling dictates the requirement for HSF-1 in germline development and functions through repressing FOXO/DAF-16 in the soma to activate HSF-1 in germ cells. We propose that this non-cell-autonomous mechanism couples nutrient-sensing insulin/IGF-1 signaling to HSF-1 activation to support homeostasis in rapid germline growth.
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•HSF-1 activates proteostatic and pro-reproduction genes in germline development•Heat stress relocates HSF-1 from its developmental targets to helitrons in germ cells•Insulin/IGF-1 signaling in the soma non-autonomously activates HSF-1 in the germline•HSF-1 is required for insulin/IGF-1-promoted germline proliferation and fecundity
Using auxin-inducible degradation in Caenorhabditis elegans, Edwards et al. uncover germline-specific activities of HSF-1 that only induce the canonical heat shock response in a subset of germ cells upon stress but are coupled to nutrient-sensing insulin/IGF-1 signaling during development to enhance expression of key proteostatic genes in support of rapid germline proliferation.