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Piwi-interacting RNAs (piRNAs) play essential roles in silencing repetitive elements to promote fertility in metazoans. Studies in worms, flies, and mammals reveal that piRNAs are expressed in a sex-specific manner. However, the mechanisms underlying this sex-specific regulation are unknown. Here we identify SNPC-1.3, a male germline-enriched variant of a conserved subunit of the small nuclear RNA-activating protein complex, as a male-specific piRNA transcription factor in  Caenorhabditis elegans . SNPC-1.3 colocalizes with the core piRNA transcription factor, SNPC-4, in nuclear foci of the male germline. Binding of SNPC-1.3 at male piRNA loci drives spermatogenic piRNA transcription and requires SNPC-4. Loss of  snpc-1.3  leads to depletion of male piRNAs and defects in male-dependent fertility. Furthermore, TRA-1, a master regulator of sex determination, binds to the  snpc-1.3  promoter and represses its expression during oogenesis. Loss of TRA-1 targeting causes ectopic expression of  snpc-1.3  and male piRNAs during oogenesis. Thus, sexually dimorphic regulation of  snpc-1.3  expression coordinates male and female piRNA expression during germline development.

SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans