A lateral oviduct secreted protein plays a vital role for egg movement through the female reproductive tract in the brown planthopper

The oviduct serves as a delivery tube for mature eggs ovulated from ovaries to egg-laying sites. Oviduct secreted components play important roles in ovulation and fertilization in mammals, however, no oviduct secreted protein has been characterized in an insect to date. Here, we identified a gene highly expressed in the lateral oviduct of the adult females in the brown planthopper (BPH), Nilaparvata lugens, the most destructive rice insect pest. Western blotting and immunofluorescence analyses revealed that the gene encodes a protein that is specifically expressed in the lateral oviduct as a component of the gel-like material secreted by the oviduct epithelial cells into the lumen of the swollen part of the lateral oviducts. The protein was tentatively named N. lugens oviduct secreted protein (Nlodsp). RNA interference (RNAi) against NlOdsp transcripts caused a failure of the lateral oviducts to deliver oocytes to the common oviduct that was, by consequence, plugged by 1?2 oocytes. Moreover, although oocytes in the Nlodsp-deficient ovariole were not released to the oviduct, they continued to develop, finally resulting in the presence of several matured oocytes in an ovariole. These defects evidently declined female fecundity. Together, our results demonstrate that NlOdsp plays an essential role in egg transport through the oviduct during ovulation. This work deepens our understanding of insect reproductive system and provides a potential target gene for RNAi-based insect pest control.

输卵管是将卵巢排出的成熟卵子输送到产卵部位的管道。在哺乳动物中，输卵管分泌的成分在排卵和受精过程中起着重要作用，然而，到目前为止，昆虫中还没有对输卵管分泌的蛋白质进行过特征描述。在此，我们在褐飞虱（Nilaparvata lugens，一种最具破坏性的水稻害虫）成年雌性的侧输卵管中鉴定出一个高表达的基因。蛋白质印迹和免疫荧光分析表明，该基因编码一种蛋白质，这种蛋白质作为输卵管上皮细胞分泌到侧输卵管肿胀部分管腔的凝胶状物质的一种成分，在侧输卵管中特异性表达。该蛋白质暂被命名为褐飞虱输卵管分泌蛋白（Nlodsp）。针对NlOdsp转录本的RNA干扰（RNAi）导致侧输卵管无法将卵母细胞输送到中输卵管，结果中输卵管被1 - 2个卵母细胞堵塞。此外，尽管缺乏Nlodsp的卵巢管中的卵母细胞没有释放到输卵管中，但它们继续发育，最终导致一个卵巢管中出现几个成熟的卵母细胞。这些缺陷明显降低了雌性的繁殖力。总之，我们的研究结果表明，NlOdsp在排卵过程中通过输卵管运输卵子方面起着至关重要的作用。这项工作加深了我们对昆虫生殖系统的理解，并为基于RNAi的害虫防治提供了一个潜在的靶基因。