Department of Biology, Johns Hopkins University, Baltimore, United States
Suhua Feng
Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United States; Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, University of California, Los Angeles, Los Angeles, United States
James J Moresco
Center for the Genetics of Host Defense, University of Texas Southwestern Medical Center, Dallas, United States
Brooke E Montgomery
Department of Biology, Colorado State University, Fort Collins, United States
Emily Xu
Department of Biology, Johns Hopkins University, Baltimore, United States
Maya A Hammonds
Department of Biology, Johns Hopkins University, Baltimore, United States
Michael C Schatz
Department of Biology, Johns Hopkins University, Baltimore, United States; Department of Computer Science, Johns Hopkins University, Baltimore, United States
Department of Molecular Medicine, The Scripps Research Institute, La Jolla, United States
Steven E Jacobsen
Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United States; Howard Hughes Medical Institute, University of California, Los Angeles, Los Angeles, United States
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.
