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

Charlotte P Choi,Emily Xu,James J Moresco,Taiowa A Montgomery,Margaret R Starostik,Rebecca J Tay,Brooke E Montgomery,Maya A Hammonds,John K Kim,Michael C Schatz,Suhua Feng,Steven E Jacobsen,John R Yates

doi:10.7554/elife.60681

Abstract

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.

Highlights

Piwi-interacting RNAs, a distinct class of small noncoding RNAs, function to preserve germline integrity (Batista et al, 2008; Carmell et al, 2007; Cox et al, 1998; Deng and Lin, 2002; Kuramochi-Miyagawa et al, 2008; Lin and Spradling, 1997; Wang and Reinke, 2008)
Addition of auxin to the snpc-4::aid; Psun-1::TIR1 strain is expected to degrade SNPC4::auxin-inducible degron (AID), whereas strains with snpc-4::aid alone serve as a negative control; under these conditions, we examined a panel of spermatogenesis- and oogenesis-enriched Piwi-interacting RNAs (piRNAs) (Billi et al, 2013) during spermatogenesis and oogenesis
Our data indicate that C. elegans SNPC-1.3, a human SNAPC1 ortholog, functions as a male piRNA transcription factor

Summary

Introduction

Piwi-interacting RNAs (piRNAs), a distinct class of small noncoding RNAs, function to preserve germline integrity (Batista et al, 2008; Carmell et al, 2007; Cox et al, 1998; Deng and Lin, 2002; Kuramochi-Miyagawa et al, 2008; Lin and Spradling, 1997; Wang and Reinke, 2008). PiRNA biogenesis factors PRDE-1, TOFU-4, and TOFU-5 are expressed in germ cell nuclei and interact with SNPC-4 at clusters of piRNA loci (Goh et al, 2014; Kasper et al, 2014; Weick et al, 2014; Weng et al, 2019) These data suggest that SNPC-4 has been co-opted by germline-specific factors to transcribe piRNAs. The vast majority of the ~15,000 piRNAs in C. elegans are encoded within two large megabase genomic clusters on chromosome IV (Das et al, 2008; Ruby et al, 2006). Together, our study reports the first example of a sex-specific piRNA transcription factor that drives the expression of male-specific piRNAs

Results

Discussion

Materials and methods