piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster

piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster
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DOI:
10.1093/nar/gkz130
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发表时间:
2019-05-07
影响因子:
14.9
通讯作者:
Olenina, Ludmila V.
Olenina, Ludmila V.
中科院分区:
生物学2区
文献类型:
--
作者:
Kotov, Alexei A.;Adashev, Vladimir E.;Olenina, Ludmila V.

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PiRNA途径是一种适应性机制,通过抑制自私的基因组元件来维持基因组的稳定性。在果蝇雄性胚系中,雄性果蝇需要抑制Stel-Late(SU(Ste))位点产生的星状基因的piRNAs,但在其他果蝇中,SU(Ste)piRNAs及其靶标都缺失。我们发现,黑腹隐翅虫基因组包含多个X连锁的非编码基因组重复序列,这些重复序列与编码蛋白质的宿主基因VasA具有序列相似性。在雄性生殖系中,这些与VasA相关的AT-ChX重复序列产生了大量与VasA反义的piRNAs;然而,由于与AT-ChX piRNAs的不完全互补,VasA mRNA逃脱了沉默。出乎意料的是,我们在种间杂交种的睾丸中发现了针对毛果果蝇血管的AT-ChX piRNAs。在大多数杂交果蝇中,睾丸的大小和生殖线含量都显著减少。少数杂交种在精巢中保持着减数分裂前生殖细胞的野生型排列,但由于缺乏SU(Ste)piRNAs,有害的星状基因被去抑制,并观察到减数分裂失败。因此,piRNA途径有助于黑腹果蝇与近缘物种之间的生殖隔离,通过对两种不同寄主蛋白因子的错误调节而导致杂交雄性不育。
The piRNA pathway is an adaptive mechanism that maintains genome stability by repression of selfish genomic elements. In the male germline of Drosophila melanogaster repression of Stellate genes piRNAs generated from Supressor of Stel-late (Su(Ste)) locus is required for male but both Su(Ste) piRNAs and their targets are absent in other Drosophila species. We found that D. melanogaster genome contains multiple X-linked non-coding genomic repeats that have sequence similarity to the protein-coding host gene vasa. In the male germline, these vasa-related AT-chX repeats produce abundant piRNAs that are antisense to vasa; however, vasa mRNA escapes silencing due to imperfect complementarity to AT-chX piRNAs. Unexpectedly, we discovered AT-chX piRNAs target vasa of Drosophila mauritiana in the testes of interspecies hybrids. In the majority of hybrid flies, the testes were strongly reduced in size and germline content. A minority of hybrids maintained wild-type array of pre-meiotic germ cells in the testes, but in them harmful Stellate genes were derepressed due to the absence of Su(Ste) piRNAs, and meiotic failures were observed. Thus, the piRNA pathway contributes to reproductive isolation between D. melanogaster and closely related species, causing hybrid male sterility via misregulation of two different host protein factors.