Piwi-interacting RNAs (piRNAs) are predominantly expressed in germ cells and function in gametogenesis in various species. However, Piwi-deficient female mice are fertile and mouse oocytes express a panel of small RNAs that do not appear to be widely representative of mammals. Thus, the function of piRNAs in mammalian oogenesis remains largely unclear. Here, we generated Piwil1- and Mov10l1-deficient golden hamsters and found that all female and male mutants were sterile, with severe defects in embryogenesis and spermatogenesis, respectively. In Piwil1-deficient female hamsters, the oocytes and embryos displayed aberrant transposon accumulation and extensive transcriptomic dysregulation, and the embryos were arrested at the two-cell stage with impaired zygotic genome activation. Moreover, PIWIL1-piRNAs exert a non-redundant function in silencing endogenous retroviruses in the oocytes and embryos. Together, our findings demonstrate that piRNAs are indispensable for generating functional germ cells in golden hamsters and show the value of this model species for piRNA studies in gametogenesis, especially those related to female infertility.

Piwi 相互作用的 RNA (piRNA) 主要在生殖细胞中表达，并在各种物种的配子发生中发挥作用。然而，Piwi缺陷雌性小鼠具有生育能力，并且小鼠卵母细胞表达一组似乎不能广泛代表哺乳动物的小 RNA。因此，piRNAs 在哺乳动物卵子发生中的功能仍不清楚。在这里，我们生成了 Piwil1和Mov10l1 缺陷金仓鼠，发现所有雌性和雄性突变体都是不育的，分别在胚胎发生和精子发生方面存在严重缺陷。在Piwil1-缺乏雌性仓鼠，卵母细胞和胚胎表现出异常的转座子积累和广泛的转录组失调，胚胎在双细胞阶段停滞，合子基因组激活受损。此外，PIWIL1-piRNA 在沉默卵母细胞和胚胎中的内源性逆转录病毒方面发挥非冗余功能。总之，我们的研究结果表明 piRNA 对于在金仓鼠中产生功能性生殖细胞是必不可少的，并显示了这种模式物种在配子发生中 piRNA 研究的价值，尤其是与雌性不育相关的那些。