Abstract
piRNAs are small non-coding RNAs that guide the silencing of transposons and other targets in animal gonads. In Drosophila female germline, many piRNA source loci dubbed "piRNA clusters" lack hallmarks of active genes and exploit an alternative path for transcription, which relies on the Rhino-Deadlock-Cutoff (RDC) complex. RDC was thought to be absent in testis, so it remains to date unknown how piRNA cluster transcription is regulated in the male germline. We found that components of RDC complex are expressed in male germ cells during early spermatogenesis, from germline stem cells (GSCs) to early spermatocytes. RDC is essential for expression of dual-strand piRNA clusters and transposon silencing in testis; however, it is dispensable for expression of Y-linked Suppressor of Stellate piRNAs and therefore Stellate silencing. Despite intact Stellate repression, males lacking RDC exhibited compromised fertility accompanied by germline DNA damage and GSC loss. Thus, piRNA-guided repression is essential for normal spermatogenesis beyond Stellate silencing. While RDC associates with multiple piRNA clusters in GSCs and early spermatogonia, its localization changes in later stages as RDC concentrates on a single X-linked locus, AT-chX. Dynamic RDC localization is paralleled by changes in piRNA cluster expression, indicating that RDC executes a fluid piRNA program during different stages of spermatogenesis. These results disprove the common belief that RDC is dispensable for piRNA biogenesis in testis and uncover the unexpected, sexually dimorphic and dynamic behavior of a core piRNA pathway machinery.
Highlights
Transposable elements (TEs) are selfish genetic elements that have the ability to propagate in the genome
Active transposons can move in the genome causing DNA damage and mutations, while inactive copies can contribute to chromosome organization and regulation of gene expression
While rhi is required for female fertility, it is dispensable for male fertility [13,14]
Summary
Transposable elements (TEs) are selfish genetic elements that have the ability to propagate in the genome. Transposition of TEs can cause overwhelming DNA damage and, eventually, genome instability This poses a particular threat to germ cells, and TE derepression often leads to reproductive defects like sterility. Canonical transcription must be repressed by factors like Maelstrom to allow proper piRNA production from dual-strand piRNA clusters [6]. Prior work has shown that such non-canonical transcription and co-transcriptional processing of piRNA precursors depend on the RDC complex, composed of Rhino (Rhi), Deadlock (Del) and Cutoff (Cuff) proteins, that bind dual-strand clusters [2,4]. Cuff is a homolog of the conserved cap-binding protein Rai that was reported to suppress both splicing [4] and transcriptional termination [3], in order to facilitate the production of long, unspliced piRNA precursors. The RDC complex conveys transcriptional competence to dual-strand piRNA clusters, and the majority of piRNA production collapses when one of its components is missing
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