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

piRNA-mediated gene regulation and adaptation to sex-specific transposon expression in D. melanogaster male germline.
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DOI:
10.1101/gad.345041.120
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发表时间:
2021-06
影响因子:
10.5
通讯作者:
Aravin AA
Aravin AA
中科院分区:
生物学1区
文献类型:
--
作者:
Chen P;Kotov AA;Godneeva BK;Bazylev SS;Olenina LV;Aravin AA

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在这项研究中,Chen等人分析了果蝇精子发生过程中piRNA及其靶标的表达,并将其与雌性对应物进行了比较。使用测序方法和新的生物信息学管道,作者定义了新的皮尔纳簇,并显示了依赖于转座子性别特异性表达的piRNA适应。小的非编码piRNA作为序列特异性向导抑制后生动物中的互补靶标。先前在果蝇卵巢中的研究已经证明了皮尔纳途径在转座子沉默中的功能,因此也证明了基因组防御的功能。然而,皮尔纳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,我们全面分析了皮尔纳的表达,并定义了它们在果蝇睾丸中的靶点。性别之间的皮尔纳程序的比较揭示了平行于性别特异性转座子表达的皮尔纳程序中的性二态性。使用一种新的生物信息学管道,我们鉴定了新的皮尔纳簇,并建立了复杂的卫星作为双链皮尔纳簇。虽然共享大多数皮尔纳簇,但两性不同地使用它们来对抗性别特异性转座子景观。我们在睾丸中发现了两个皮尔纳簇,它们产生与四个宿主基因反义的piRNA,包括CG 12717/pirate,一个SUMO蛋白酶基因。在Y染色体上编码的piRNA沉默海盗,但不是其parallel,以发挥性别和旁系同源特异性基因调控。有趣的是,海盗的目标是由内源性siRNA在一个兄弟物种,毛里求斯果蝇,这表明不同的,但相关的沉默策略发明在最近的进化,以调节保守的蛋白质编码基因。
In this study, Chen et al. analyzed expression of piRNAs and their targets during Drosophila spermatogenesis and compared it with the female counterpart. Using sequencing approaches and a novel bioinformatic pipeline, the authors define novel piRNA clusters and show adaptation of piRNAs that is dependent on sex-specific expression of transposons. 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.
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