The mex-3 3' untranslated region is essential for reproduction during temperature stress

Organisms must sense temperature and modify their physiology to survive environmental stress. Elevated temperature reduces fertility in most sexually reproducing organisms. Maternally supplied mRNAs are required for embryogenesis. They encode proteins that govern early embryonic patterning. RNA-binding proteins are major effectors of maternal mRNA regulation. MEX-3 is a conserved RNA-binding protein essential for anterior patterning of Caenorhabditis elegans embryos. We previously demonstrated that the mex-3 3' untranslated region (3'UTR) represses MEX-3 abundance in the germline yet is mostly dispensable for fertility. Here, we show that the 3'UTR is essential during thermal stress. Deletion of the 3'UTR causes a highly penetrant, temperature-sensitive embryonic lethality phenotype distinct from the mex-3 null phenotype. Loss of the 3'UTR decreases MEX-3 abundance specifically in maturing oocytes and early embryos during temperature stress. Dysregulation of mex-3 reprograms the thermal stress response by reducing the expression of hundreds of heat-shock genes. We propose that a major function of the mex-3 3'UTR is to buffer MEX-3 expression during fluctuating temperature, ensuring the robustness of oocyte maturation and embryogenesis.