The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila

Abstract

PIWI-interacting RNAs (piRNAs) are predominantly produced in animal gonads to suppress transposons during germline development. Our understanding about the piRNA biogenesis and function is predominantly from studies of the Drosophila female germline. piRNA pathway function in the male germline, however, remains poorly understood. To study overall and stage-specific features of piRNAs during spermatogenesis, we analyzed small RNAs extracted from entire wild-type testes and stage-specific arrest mutant testes enriched with spermatogonia or primary spermatocytes. We show that most active piRNA clusters in the female germline do not majorly contribute to piRNAs in testes, and abundance patterns of piRNAs mapping to different transposon families also differ between male and female germlines. piRNA production is regulated in a stage-specific manner during spermatogenesis. The piRNAs in spermatogonia-enriched testes are predominantly transposon-mapping piRNAs, and almost half of those exhibit a ping-pong signature. In contrast, the primary spermatocyte-enriched testes have a dramatically high amount of piRNAs targeting repeats like suppressor of stellate and AT-chX. The transposon-mapping piRNAs in the primary spermatocyte stages lacking Argonaute3 expression also show a ping-pong signature, albeit to a lesser extent. Consistently, argonaute3 mutant testes also retain ping-pong signature-bearing piRNAs, suggesting that a noncanonical pingpong cycle might act during spermatogenesis. Our study shows stage-specific regulation of piRNA biogenesis during spermatogenesis: An active ping-pong cycle produces abundant transposon-mapping piRNAs in spermatogonia, while in primary spermatocytes, piRNAs act to suppress the repeats and transposons.

RDC complex executes a dynamic piRNA program duringDrosophilaspermatogenesis to safeguard male fertility

“…Notably, though not dependent on Rhi, transcription of Su(Ste) piRNA cluster was shown to span a narrow window from late spermatogonia to early spermatocyte as well (Aravin et al, 2004), likely reflecting the promoter activity that drives Su(Ste) transcription (Aravin et al, 2001). Dynamic expression of piRNA clusters during spermatogenesis is also supported by the study that showed spermatogonia and spermatocytes have distinct piRNA populations (Quénerch'du et al, 2016). In contrast to dynamic localization of RDC complex and cluster expression in testes, previous work depicted a static view of piRNA production in female gonads.…”

Physiological characterization of the emergence from diapause: A transcriptomics approach

“…5 ). The first two (Ago3 and ATP-dependent helicase) play key roles in the Piwi pathway, which regulates the repression of transposable elements during spermatogenesis 42 . The third protein-encoding gene, Testis serine protease, is involved in the sperm/egg interaction.…”

The conserved RNA helicase YTHDC2 regulates the transition from proliferation to differentiation in the germline

“…Recent studies suggest that pachytene piRNAs may play a role in eliminating a large number of mRNAs, including meiotic transcripts, in late spermatocytes and early spermatids ( Goh et al, 2015 ; Gou et al, 2014 ; Watanabe et al, 2015 ). Likewise, in Drosophila testes, an RNA precursor expressed in primary spermatocytes from repeats on the Y chromosome is processed into piRNAs that down-regulate expression of the X-linked gene Stellate ( Bozzetti et al, 1995 ; Quénerch'du et al, 2016 ). One possibility is that YTHDC2 may bind and sequester certain pachytene piRNA precursors in early spermatocytes and block them from being processed into mature piRNAs prematurely.…”