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

• Published in: eLife Vol. 10
• Main Authors: Choi, Charlotte P, Tay, Rebecca J, Starostik, Margaret R, Feng, Suhua, Moresco, James J, Montgomery, Brooke E, Xu, Emily, Hammonds, Maya A, Schatz, Michael C, Montgomery, Taiowa A, Yates, 3rd, John R, Jacobsen, Steven E, Kim, John K
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 15.02.2021; eLife Sciences Publications, Ltd
• Subjects: Animals; Biosynthesis; Caenorhabditis elegans - genetics; Caenorhabditis elegans - growth & development; Caenorhabditis elegans - metabolism; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Chromosomes and Gene Expression; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Ectopic expression; Female; Fertility; Gene Expression Regulation; Gene Expression Regulation, Developmental; Gene loci; Genetics and Genomics; Germ Cells - growth & development; Germ Cells - metabolism; germline development; Insects; Male; Mammals; Mutation; Oogenesis; piRNA; Proteins; RNA polymerase; RNA, Small Interfering - genetics; RNA, Small Interfering - metabolism; Sex determination; Sexual dimorphism; snRNA; Species Specificity; Spermatogenesis; TRA-1; transcription; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Worms; C. elegans; TRA-1; genetics; transcription; chromosomes; piRNA; spermatogenesis; genomics; germline development; gene expression; sex determination
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.60681

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 . 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 leads to depletion of male piRNAs and defects in male-dependent fertility. Furthermore, TRA-1, a master regulator of sex determination, binds to the promoter and represses its expression during oogenesis. Loss of TRA-1 targeting causes ectopic expression of and male piRNAs during oogenesis. Thus, sexually dimorphic regulation of expression coordinates male and female piRNA expression during germline development.