Liu Xiaoming, Tian Zhiqiang, Cai Limei, Shen Zhongjian, Michaud J P, Zhu Lin, Yan Shuo, Ros Vera I D, Hoover Kelli, Li Zhen, Zhang Songdou, Liu Xiaoxia
MOA Key Laboratory of Pest Monitoring and Green Management, Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China.
College of Biological Sciences, China Agricultural University, Beijing, China.
Mol Ecol. 2022 May;31(9):2752-2765. doi: 10.1111/mec.16425. Epub 2022 Mar 15.
Baculoviruses can induce climbing behaviour in their caterpillar hosts to ensure they die at elevated positions to enhance virus transmission, providing an excellent model to study parasitic manipulation of host behaviour. Here, we demonstrate that climbing behaviour occurred mostly during daylight hours, and that the height at death of Helicoverpa armigera single nucleopolyhedrovirus (HearNPV)-infected larvae increases with the height of the light source. Phototaxic and electroretinogram (ERG) responses were enhanced after HearNPV-infection in host larvae, and ablation of stemmata in infected larvae prevented both phototaxis and climbing behaviour. Through transcriptome and quantitative PCR, we confirmed that two opsin genes (a blue light-sensitive gene, HaBL; and a long wave-sensitive gene, HaLW) as well as the TRPL (transient receptor potential-like channel protein) gene, all integral to the host's visual perception pathway, were significantly upregulated after HearNPV infection. Knockout of HaBL, HaLW, or TRPL genes using the CRISPR/Cas9 system resulted in significantly reduced ERG responses, phototaxis, and climbing behaviour in HearNPV-infected larvae. These results reveal that HearNPV alters the expression of specific genes to hijack host visual perception at fundamental levels-photoreception and phototransduction-in order to induce climbing behaviour in host larvae.
杆状病毒可诱导其毛虫宿主出现攀爬行为，以确保它们在较高位置死亡，从而增强病毒传播，这为研究寄生虫对宿主行为的操控提供了一个绝佳模型。在此，我们证明攀爬行为大多发生在白天，而且感染棉铃虫单核多角体病毒（HearNPV）的幼虫死亡时的高度会随着光源高度的增加而升高。宿主幼虫感染HearNPV后，其趋光性和视网膜电图（ERG）反应增强，而感染幼虫的单眼被切除后，趋光性和攀爬行为均受到抑制。通过转录组和定量PCR，我们证实，两个视蛋白基因（一个对蓝光敏感的基因HaBL和一个对长波敏感的基因HaLW）以及TRPL（类瞬时受体电位通道蛋白）基因，这些都是宿主视觉感知通路不可或缺的基因，在HearNPV感染后均显著上调。使用CRISPR/Cas9系统敲除HaBL、HaLW或TRPL基因，会导致感染HearNPV的幼虫的ERG反应、趋光性和攀爬行为显著降低。这些结果表明，HearNPV改变特定基因的表达，在光感受器和光转导等基本层面劫持宿主的视觉感知，从而诱导宿主幼虫出现攀爬行为。
