Liaoning Key Laboratory of Economic and Applied Entomology, College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, China.
Liaoning Key Laboratory of Economic and Applied Entomology, College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, China.
Curr Biol. 2024 Jun 3;34(11):2359-2372.e9. doi: 10.1016/j.cub.2024.04.035. Epub 2024 Apr 30.
Host reproduction can be manipulated by bacterial symbionts in various ways. Parthenogenesis induction is the most effective type of reproduction manipulation by symbionts for their transmission. Insect sex is determined by regulation of doublesex (dsx) splicing through transformer2 (tra2) and transformer (tra) interaction. Although parthenogenesis induction by symbionts has been studied since the 1970s, its underlying molecular mechanism is unknown. Here we identify a Wolbachia parthenogenesis-induction feminization factor gene (piff) that targets sex-determining genes and causes female-producing parthenogenesis in the haplodiploid parasitoid Encarsia formosa. We found that Wolbachia elimination repressed expression of female-specific dsx and enhanced expression of male-specific dsx, which led to the production of wasp haploid male offspring. Furthermore, we found that E. formosa tra is truncated and non-functional, and Wolbachia has a functional tra homolog, termed piff, with an insect origin. Wolbachia PIFF can colocalize and interact with wasp TRA2. Moreover, Wolbachia piff has coordinated expression with tra2 and dsx of E. formosa. Our results demonstrate the bacterial symbiont Wolbachia has acquired an insect gene to manipulate the host sex determination cascade and induce parthenogenesis in wasps. This study reveals insect-to-bacteria horizontal gene transfer drives the evolution of animal sex determination systems, elucidating a striking mechanism of insect-microbe symbiosis.
宿主繁殖可以通过细菌共生体以各种方式进行操纵。孤雌生殖诱导是共生体传播的最有效类型的繁殖操纵。昆虫的性别由 doublesex（dsx）剪接通过 transformer2（tra2）和 transformer（tra）相互作用来决定。尽管自 20 世纪 70 年代以来就已经研究了共生体诱导的孤雌生殖，但它的潜在分子机制尚不清楚。在这里，我们确定了一个沃尔巴克氏体孤雌生殖诱导雌性化因子基因（piff），该基因靶向性别决定基因，并导致单倍体寄生蜂 Encarsia formosa 产生雌性孤雌生殖。我们发现沃尔巴克氏体消除抑制了雌性特异性 dsx 的表达并增强了雄性特异性 dsx 的表达，导致产生了蜂类单倍体雄性后代。此外，我们发现 E. formosa tra 被截断且无功能，而沃尔巴克氏体具有功能正常的 tra 同源物，称为 piff，具有昆虫起源。沃尔巴克氏体 PIFF 可以与黄蜂 TRA2 共定位并相互作用。此外，沃尔巴克氏体 piff 与 E. formosa 的 tra2 和 dsx 具有协调表达。我们的结果表明，细菌共生体沃尔巴克氏体已经获得了一个昆虫基因，以操纵宿主性别决定级联并在黄蜂中诱导孤雌生殖。这项研究揭示了昆虫到细菌的水平基因转移驱动了动物性别决定系统的进化，阐明了昆虫与微生物共生的惊人机制。
