Argonaute CSR-1A promotes H3K9me3 maintenance to protect somatic development in offspring

Paternal stress can be encoded into altered epigenetic information to influence their offspring. How environment-induced perturbation in sperm epigenome is reprogrammed to protect offspring is less well understood. In the nematode Caenorhabditis elegans, parental Argonaute and small RNA pathway defend offspring against viruses, starvation, and pathogenic bacteria. Here we report that, when challenged by universal heat-shock stress, paternal Argonaute CSR-1A potentiates recovery of spermic H3K9me3 to secure the late somatic developmental competence of offspring. CSR-1A employs its repetitive RG motif to engage with SET-25/32, putative histone 3 lysine 9 (H3K9) methyltransferases, and helps germ cell to rescue suppressive chromatin marks H3K9me3 following stress, protecting the late development of somatic cells in the progeny. Finally, among the genes regulated by CSR-1A, we identified dim-1, at which decreased H3K9me3 persists in the progeny, and RNAi of dim-1 mitigates the somatic defects associated with csr-1a loss under stress. Thus, CSR-1A coordinates the epigenetic machinery to shield the latter stages of a progeny's development from the influences of the paternal environment. We speculate that, driven by both natural environmental stressors and the unique characteristics of spermatogenic chromatin, the emergence of multiple RG motif-featured and spermatogenesis-specific CSR-1A and small RNA serves as an adaptive strategy to safeguard against variability in the orchestration of inherited developmental programs from the paternal lineage. To investigate how the csr-1a mutation causes morphological changes in the tails of C. elegans, we used fluorescence-activated cell sorting (FACS) to isolate rectal valve and rectal gland (abbreviations: RVRG or vir & rep) cells from 10 million offspring whose parents had been subjected to heat shock in wild type and csr-1a mutant strains.