piRNA-mediated gene regulation and adaptation to sex-specific transposon expression in male germline.

Small noncoding piRNAs act as sequence-specific guides to repress complementary targets in Metazoa. Prior studies in ovaries have demonstrated the function of the piRNA pathway in transposon silencing and therefore genome defense. However, the ability of the piRNA program to respond to different transposon landscapes 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 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, the two sexes employ them differentially to combat the sex-specific transposon landscape. We found two piRNA clusters that produce piRNAs antisense to four host genes in testis, including , a SUMO protease gene. piRNAs encoded on the Y chromosome silence , but not its paralog, to exert sex- and paralog-specific gene regulation. Interestingly, is targeted by endogenous siRNAs in a sibling species, , suggesting distinct but related silencing strategies invented in recent evolution to regulate a conserved protein-coding gene.