Small noncoding piRNAs act as sequence-specific guides to repress complementary targets in Metazoa. Prior studies in Drosophila 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 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, 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 CG12717/pirate, a SUMO protease gene. piRNAs encoded on the Y chromosome silence pirate, but not its paralog, to exert sex- and paralog-specific gene regulation. Interestingly, pirate 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-coding gene.

中文翻译：

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黑腹果蝇雄性种系中piRNA介导的基因调控和性别特异性转座子表达的适应


小的非编码 piRNA 作为序列特异性向导来抑制后生动物中的互补靶标。先前对果蝇卵巢的研究已经证明了 piRNA 通路在转座子沉默以及基因组防御中的功能。然而，piRNA 程序响应不同转座子景观的能力以及 piRNA 在调节宿主基因表达中的作用仍然知之甚少。在这里，我们全面分析了果蝇睾丸中 piRNA 的表达并定义了其靶标的全部。性别之间 piRNA 程序的比较揭示了 piRNA 程序中与性别特异性转座子表达平行的性别二态性。使用新颖的生物信息学流程，我们鉴定了新的 piRNA 簇，并建立了复杂的卫星作为双链 piRNA 簇。虽然共享大多数 piRNA 簇，但两性以不同的方式利用它们来对抗性别特异性转座子景观。我们发现两个 piRNA 簇可产生与睾丸中四个宿主基因反义的 piRNA，其中包括CG12717/pirate （一种 SUMO 蛋白酶基因）。 Y染色体上编码的piRNA沉默海盗，但不沉默它的旁系同源物，以发挥性别和旁系同源物特异性基因调控。有趣的是， pirate是其同胞物种Drosophila mauritiana中内源 siRNA 的靶标，这表明在最近的进化中发明了独特但相关的沉默策略来调节保守的蛋白质编码基因。