一种双顺反子病毒通过抑制蛋白酶活性和草地贪夜蛾幼虫的取食来提高蛹的死亡率

doi:10.1016/j.jia.2023.12.030

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (8): 2723-2734.DOI: 10.1016/j.jia.2023.12.030

一种双顺反子病毒通过抑制蛋白酶活性和草地贪夜蛾幼虫的取食来提高蛹的死亡率

收稿日期:2023-09-19 接受日期:2023-12-01 出版日期:2024-08-20 发布日期:2024-07-29

A dicistrovirus increases pupal mortality in Spodoptera frugiperda by suppressing protease activity and inhibiting larval diet consumption

Meixue Sun^1*, Tong Li^2*, Yingjie Liu³, Kenneth Wilson⁴, Xingyu Chen¹, Robert I. Graham⁵, Xianming Yang⁶, Guangwei Ren^1#, Pengjun Xu^1#

¹Key Laboratory of Tobacco Pest Monitoring & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
²Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou 450000, China
³ Staff Development Institute of China National Tobacco Corporation, Zhengzhou 450000, China
⁴ Lancaster Environment Centre, Lancaster University, Lancaster LA14YW, UK
⁵ Department of Rural Land Use, Scotland's Rural College, Craibstone Campus, Aberdeen AB01AB, UK
⁶ State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Received:2023-09-19 Accepted:2023-12-01 Online:2024-08-20 Published:2024-07-29
About author:Meixue Sun, E-mail: 18254310586@163.com; Tong Li, E-mail: holy518125@126.com; #Correspondence Guangwei Ren, Tel: +86-532-88701012, E-mail: renguangwei@caas.cn; Pengjun Xu, Tel: +86-532-88701012, E-mail: xupengjun@163.com * These authors contributed equally to this study. *These authors contributed equally to this study.
Supported by:
This work was supported by the Major Special Projects for Green Pest Control, China (110202101028(LS-03), 201938, 110202201017(LS-01) and 110202001035(LS-04)), the National Natural Science Foundation of China (31901893) and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (ASTIP-TRIC04).

摘要/Abstract

摘要：

明确病毒与宿主之间的相互作用可更好地将病毒应用为生防治剂。寄生蜂携带的某些病毒通过保护寄生蜂若虫免受鳞翅目寄主免疫系统的攻击，提高了寄生蜂若虫的寄生效率。然而，在捕食性天敌中发现的病毒与其猎物之间的关系尚不清楚。在此，我们报道了一种最初从捕食性天敌蠋蝽Arma chinensis（半翅目，蝽科）中分离到的病毒（Arma chinensis virus-1, AcV-1）与其猎物之一草地贪夜蛾Spodoptera frugiperda（鳞翅目，夜蛾科）之间的相互作用关系。结果表明，AcV-1病毒通过抑制幼虫的取食和提高蛹的死亡率，对新寄主草地贪夜蛾产生了危害。同时，测序数据表明，该病毒改变了草地贪夜蛾的基因表达谱。KEGG分析显示，与蛋白质降解和免疫应答相关的蛋白酶体通路和吞噬体通路显著富集。虽然消化酶基因表达水平没有显著变化，但AcV-1病毒阳性个体的总蛋白酶活性显著降低，说明病毒通过下调消化酶活性抑制了草地贪夜蛾幼虫的取食。这些结果表明，最初从捕食性天敌中分离出来的病毒影响了其猎物与蛋白质降解和免疫相关的蛋白酶体通路和吞噬体通路，降低新寄主的适合度，为提高害虫控制效率提供了潜在的新策略。

Abstract:

Understanding interactions between viruses and their hosts is conducive to enabling better application of viruses as biocontrol agents. Certain viruses carried by parasitic wasps enhance the parasitic efficiency of wasp-larvae by protecting them against the immune system of their Lepidopteran host. However, the relationship between prey pests and viruses found in predatory natural enemies remains unclear. Herein, we report the interaction between Arma chinensis virus-1 (AcV-1), originally isolated from a predatory natural enemy, Arma chinensis (Hemiptera: Pentatomidae), and one of its prey species, Spodoptera frugiperda (Lepidoptera: Noctuidae). The results showed that the AcV-1 virus appeared harmful to the novel host S. frugiperda by inhibiting larval diet consumption and increasing pupal mortality. Meanwhile, sequencing data indicated that the virus altered the gene expression profiles of S. frugiperda. KEGG analysis showed that the proteasome and phagosome pathways related to protein degradation and immune response were significantly enriched. Although the expression levels of digestive enzyme genes did not change significantly, the total protease activity of AcV-1 virus-positive individuals was significantly decreased, suggesting that the virus inhibited diet consumption of S. frugiperda via the down-regulation of digestive enzyme activities. These results indicate that a virus initially isolated in a predatory natural enemy can decrease the fitness of its prey species. The virus was found to impact the host proteasome and phagosome pathways related to protein degradation and immunity, providing a potential mechanism to enhance controlling efficiency.

Key words: Arma chinensis virus-1 , diet consumption , fitness , transcriptome , protease activity

Meixue Sun, Tong Li, Yingjie Liu, Kenneth Wilson, Xingyu Chen, Robert I. Graham, Xianming Yang, Guangwei Ren, Pengjun Xu. 一种双顺反子病毒通过抑制蛋白酶活性和草地贪夜蛾幼虫的取食来提高蛹的死亡率[J]. Journal of Integrative Agriculture, 2024, 23(8): 2723-2734.

Meixue Sun, Tong Li, Yingjie Liu, Kenneth Wilson, Xingyu Chen, Robert I. Graham, Xianming Yang, Guangwei Ren, Pengjun Xu. A dicistrovirus increases pupal mortality in Spodoptera frugiperda by suppressing protease activity and inhibiting larval diet consumption[J]. Journal of Integrative Agriculture, 2024, 23(8): 2723-2734.

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一种双顺反子病毒通过抑制蛋白酶活性和草地贪夜蛾幼虫的取食来提高蛹的死亡率

A dicistrovirus increases pupal mortality in Spodoptera frugiperda by suppressing protease activity and inhibiting larval diet consumption

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