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

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 variant of a conserved subunit of the snRNA activating protein complex, as a male-specific piRNA transcription factor inC. elegans. Binding of SNPC-1.3 at male piRNA loci drives spermatogenic piRNA transcription and requires the core piRNA transcription factor SNPC-4. Loss ofsnpc-1.3leads to depletion of male piRNAs and defects in male-dependent fertility. Furthermore, TRA-1, a master regulator of sex determination, binds to thesnpc-1.3promoter and represses its expression during oogenesis. Loss of TRA-1 targeting causes ectopic expression ofsnpc-1.3and male piRNAs during oogenesis. Thus, sexual dimorphic regulation ofsnpc-1.3coordinates male and female piRNA expression during germline development.