The C. elegans SNAPc component SNPC-4 coats piRNA domains and is globally required for piRNA abundance

The Piwi/Piwi-interacting RNA (piRNA) pathway protects the germline from the activity of foreign sequences such as transposons. Remarkably, tens of thousands of piRNAs arise from a minimal number of discrete genomic regions. The extent to which clustering of these small RNA genes contributes to their coordinated expression remains unclear. We show that C. elegans SNPC-4, the Myb-like DNA-binding subunit of the small nuclear RNA activating protein complex, binds piRNA clusters in a germline-specific manner and is required for global piRNA expression. SNPC-4 localization is mutually dependent with localization of piRNA biogenesis factor PRDE-1. SNPC-4 exhibits an atypical widely distributed binding pattern that "coats" piRNA domains. Discrete peaks within the domains occur frequently at RNA-polymerase-III-occupied transfer RNA (tRNA) genes, which have been implicated in chromatin organization. We suggest that SNPC-4 binding establishes a positive expression environment across piRNA domains, providing an explanation for the conserved clustering of individually transcribed piRNA genes.