The VmCarEs-6 gene in the Therioaphis trifolii（Monell） enhances pesticide sensitivity by inhibiting detoxification metabolism

doi:10.1016/j.jia.2025.09.016

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The VmCarEs-6 gene in the Therioaphis trifolii（Monell） enhances pesticide sensitivity by inhibiting detoxification metabolism

Haoyang Hao^{1, 2}, Kaihui Zhu^{1, 3},Xianfeng Yin¹, Shaodan Wang^{1, 2}, Xu Liu¹ , Dejun Li^{1, 2}, Chunmei Yang¹, Zehua Zhang⁴, Mark. Richard NcNeill⁵, Shali Yasen^2#, Xiongbing Tu^1#

¹State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

²Key Laboratory of Pest Monitoring and Safety Control of Crops and Forests, College of Agronomy, Xinjiang Agricultural University, Urumqi 830052, Xinjiang Uygur Autonomous Region, China

³Department of Plant Biosecurity, China Agricultural University, Beijing 100193, China

⁴Western Agricultural Research Center of Chinese Academy of Agricultural Sciences, Xinjiang, 831100, China

⁵AgResearch Ltd., Lincoln Research Centre, Cnr Springs Rd and GeraldSt, Lincoin 7608, Canterbury New Zealand

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摘要

杀虫剂的长期过度使用导致了显著的环境影响和昆虫抗药性的进化。羧酸酯酶（CarEs）作为解毒代谢关键酶类，与害虫抗药性形成密切相关。本研究基于苜蓿斑蚜逆胁迫转录组数据筛选并克隆了VmCarEs-6基因，通过RNA干扰和抑制剂处理VmCarEs-6，检测苜蓿斑蚜应对化学农药的敏感性。通过ProtParam软件分析显示，VmCarEs-6基因编码564个氨基酸，具有多样化结构域；其表达具有时空特异性，3龄若蚜及胸部组织表达量最高，无翅成蚜表达显著高于有翅型。室内生测结果显示，暴露于高效氯氟氰菊酯、异丙威、辛硫磷和吡虫啉LC₅₀浓度后，苜蓿斑蚜体内VmCarEs-6表达显著上调。利用星形阳离子聚合物（star polycation，SPc）包裹双链RNA干扰VmCarEs-6基因后，高效氯氟氰菊酯（LCT）、异丙威（IPC）、辛硫磷（PHX）和吡虫啉（IMI）处理后蚜虫的死亡率较对照组分别增加35.6%、23.4%、31.1%和23.3%；羧酸酯酶抑制剂TPP与上述四种杀虫剂联用表现出增效作用，增效倍数分别提升1.54、1.28、1.24和1.17，与RNAi结果一致。田间试验结果表明，在施药后第5天，与单用化学农药相比，LCT+TPP、IPC+TPP、PHX+TPP、IMI+TPP混用防治效果分别提高了35.6%、21.5%、46.0%和70.1%，与室内生测结果一致。因此，通过RNA干扰和TPP处理对苜蓿斑蚜VmCarEs-6基因进行功能抑制，显著削弱了害虫的解毒代谢能力，进而提高了害虫的应对化学农药的敏感性，为解析刺吸式害虫抗药性机制与开发靶向防控产品提供了理论依据。

Abstract

The long-term overuse of insecticides has accelerated the evolutionary development of insect resistance. In this process, carboxylesterases as pivotal enzymes in detoxification metabolism, play a critical role in the formation of pest resistance, with their enhanced activity and altered expression levels being closely associated with the development of resistance mechanisms. In this study, the VmCarEs-6 gene was screened and cloned based on the transcriptomic data of Therioaphis trifolii under reverse stress conditions. The aim was to investigate the role of this gene in the sensitivity of T. trifolii to chemical pesticides through RNA interference and inhibitor treatments. Indoor bioassay results demonstrated that exposure to LC₅₀concentrations of lambda-cyhalothrin (LCT), isoprocarb (IPC), phoxim (PHX), and imidacloprid (IMI) significantly upregulated the expression of the VmCarEs-6 gene in T. trifolii. Following RNAi-mediated silencing of VmCarEs-6 using star polycation (SPc)-encapsulated double-stranded RNA, the mortality rates of aphids treated with the four insecticides increased by 35.6, 23.4, 31.1, and 23.3%, respectively, compared tothe control group. Additionally, the carboxylesterase inhibitor TPP exhibited a synergistic effect when combined with the aforementioned insecticides, with synergistic ratios increasing by 1.54, 1.28, 1.24, and 1.17, respectively, consistent with the RNAi results. Field trials further validated the indoor findings, showing that on the 5^thday after application, the control efficacy of LCT+TPP, IPC+TPP, PHX+TPP, and IMI+TPP combinations improved by 35.6, 21.5, 46.0, and 70.1%, respectively, compared to the use of chemical pesticides alone.The functional inhibition of the VmCarEs-6 gene in T. trifolii through RNAi and TPP treatment significantly impaired the pest's detoxification metabolism, thereby enhancing its sensitivity to chemical pesticides. This study provides a critical theoretical foundation for elucidating the mechanisms of resistance in piercing-sucking pests and developing targeted pest control products.

Keywords: Therioaphis trifolii VmCarEs-6 gene RNA interference star polycation enzyme inhibitor triphenyl phosphate (TPP)

Online: 12 September 2025

Fund:

This research was supported by the earmarked fund for CARS (CARS-34-18). Studies were carried out in laboratories at the Institute of Plant Protection, Chinese Academy of Agricultural Sciences.

About author: Haoyang Hao, E-mail: yhh0836@hotmail.com；#Correspongdence Xiongbing Tu, E-mail: txb1208@163.com; Shali Yasen, E-mail: ysxjau@sina.com

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Haoyang Hao, Kaihui Zhu, Xianfeng Yin, Shaodan Wang, Xu Liu, Dejun Li, Chunmei Yang, Zehua Zhang, Mark. Richard NcNeill, Shali Yasen, Xiongbing Tu. 2025. The VmCarEs-6 gene in the Therioaphis trifolii（Monell） enhances pesticide sensitivity by inhibiting detoxification metabolism. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.016

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