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

Piwi-interacting RNAs (piRNAs) play essential roles in silencing repetitive elements to promote fertility in metazoans. Nearly one-third of the ~15,000 piRNA loci in the C. elegans hermaphrodite are enriched during spermatogenesis, whereas >2,000 piRNAs are enriched during oogenesis. However, the mechanism underlying this sex-specific regulation is 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. Binding of SNPC-1.3 at male piRNA loci drives spermatogenic piRNA transcription and requires the core piRNA transcription factor SNPC-4. Loss of snpc-1.3 leads to depletion of spermatogenic 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, sexual dimorphic regulation of snpc-1.3 coordinates male and female piRNA expression during germline development. We performed small RNA-seq and ChIP-seq in C. elegans N2 worms and various mutants to explore the role of SNPC-1.3 and TRA-1 in regulating piRNA expression during spermatogenesis and oogenesis.