piRNA-mediated gene regulation and adaptation to sex-specific transposon expression inD. melanogastermale germline

SUMMARY Small non-coding piRNAs act as sequence-specific guides to repress complementary targets in Metazoa. Prior studies in Drosophila ovaries have demonstrated the function of piRNA pathway in transposon silencing and therefore genome defense. However, the ability of piRNA program to respond to different transposon landscape and the role of piRNAs in regulating host gene expression remain poorly understood. Here, we comprehensively analyzed piRNA expression and defined the repertoire of their targets in Drosophila melanogaster testes. Comparison of piRNA programs between sexes revealed sexual dimorphism in piRNA programs that parallel sex-specific transposon expression. Using a novel bioinformatic pipeline, we identified new piRNA clusters and established complex satellites as dual-strand piRNA clusters. While sharing most piRNA clusters, two sexes employ them differentially to combat sex-specific transposon landscape. We found several host genes targeted by piRNAs in testis, including CG12717/pita , a SUMO protease gene. piRNAs encoded on Y chromosome silence pita , but not its paralog, to exert sex- and paralog-specific gene regulation. Interestingly, pita is targeted by endogenous siRNAs in a sibling species, Drosophila mauritiana , suggesting distinct but related silencing strategies invented in recent evolution to regulate a conserved protein-encoding gene.