The C. elegans SNAPc Component SNPC-4 Coats piRNA Domains and Is Globally Required for piRNA Abundance

• Published in: Developmental cell 2014-10, Vol.31 (2), p.145-158
• Main Authors: Kasper, Dionna M., Wang, Guilin, Gardner, Kathryn E., Johnstone, Timothy G., Reinke, Valerie
• Format: Article
• Language: English
• Subjects: Animals; Base Sequence; Caenorhabditis elegans - genetics; Caenorhabditis elegans - metabolism; Caenorhabditis elegans Proteins - genetics; Cell Nucleus - metabolism; Chromatin - genetics; Chromosomal Proteins, Non-Histone - genetics; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Epigenesis, Genetic; RNA Polymerase III - genetics; RNA, Small Interfering - genetics; RNA, Small Interfering - metabolism; Sequence Analysis, RNA; Signal Transduction - genetics; Transcription Factors - genetics
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2014.09.015

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. [Display omitted] •SNPC-4 displays broadly distributed germline-specific binding across piRNA clusters•SNPC-4 is required for normal expression of mature piRNAs in C. elegans•SNPC-4 and piRNA biogenesis factor PRDE-1 exhibit codependency at piRNA domains•Discrete SNPC-4 peaks occur at Pol III-bound tRNA genes in piRNA domains C. elegans type I piRNA genes are located in evolutionarily conserved genomic clusters, despite being independent transcription units. Here, Kasper et al. demonstrate that the sequence-specific transcription factor SNPC-4 binds and coats entire piRNA domains and promotes piRNA expression through a germline-specific interaction with the early piRNA biogenesis factor PRDE-1.