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

Automated summary

Research has identified SNPC-1.3 as a male-specific piRNA transcription factor in Caenorhabditis elegans, which is essential for spermatogenic piRNA transcription in conjunction with the core transcription factor SNPC-4. Loss of SNPC-1.3 results in depletion of male piRNAs and fertility defects. Additionally, the master regulator of sex determination, TRA-1, represses the expression of snpc-1.3 during oogenesis, with loss of TRA-1 targeting leading to ectopic expression of snpc-1.3 and male piRNAs. Thus, sexually dimorphic regulation of snpc-1.3 coordinates male and female piRNA expression during germline development.