Coordinated regulation of glutathione S-transferases confers metabolic flexibility in multi-insecticide-resistant Frankliniella occidentalis (Pergande)

IF 17.1 1区综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES

Journal of Advanced Research Pub Date : 2026-09-01 Epub Date: 2025-12-28 DOI:10.1016/j.jare.2025.12.052

Jing Wang, Sirui Chen, Yulei Wu, Haolan Yang, Xiaobin Zheng, Jiangjiang Yuan, Kanghua Qian, Hongyi Cao, Yingxi Tang, Xin Yang, Zhaojiang Guo, Wen Xie, Shaoli Wang, Qi Su, Pei Liang, Youjun Zhang, Qingjun Wu

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引用次数: 0

Abstract

Introduction

The evolution of multi-insecticide resistance in insect pests threatens global food security. Although glutathione S-transferases (GSTs) are implicated in detoxification, the coordinated mechanism by which specific gene subfamilies interact to confer broad-spectrum resistance remains inadequately characterized.

Objective

To dissect the functional allocation and cooperation of GST subfamilies in multi-insecticide-resistant strains of Frankliniella occidentalis.

Methods

We integrated comparative genomics (20 GST genes cloned), transcriptomics (qRT-PCR), RNAi-mediated silencing, molecular docking (AutoDock Vina), and in vitro metabolism assays (UPLC-MS/MS) across susceptible and resistant thrips strains.

Results

The two resistant strains (NIL-R and FS-R) exhibited moderate to high resistance to five insecticides (chlorfenapyr, emamectin benzoate, spinetoram, spinosad, and thiamethoxam), accompanied by significantly elevated GSTs activity. Phylogenetic analysis indicates that GSTs include 10 conserved delta and 7 diverse sigma members. The sigma subfamily has undergone a marked expansion due to gene duplication. Delta (FoGSTd1, d4, and d9) and sigma (FoGSTs1, s2, and s6) genes were significantly up-regulated in the resistant strains. RNAi showed specialized functional allocation among GSTs: delta GSTs mediated resistance to spinosad and chlorfenapyr, sigma GSTs were responsible for thiamethoxam resistance, and notably, cooperation between these subfamilies contributed to resistance against emamectin benzoate and spinetoram. Molecular docking and in vitro metabolism assays of FoGSTd9 and FoGSTs1 proteins further supported the functional allocation and cooperative roles of GST subfamilies.

Conclusion

Our results indicate that F. occidentalis may coordinate GST subfamilies to achieve metabolic flexibility in response to multi-insecticide pressure. This survival strategy, mediated by mechanistic functional allocation and cooperative interactions among subfamilies, may contribute to energy conservation and reduced adaptive costs. Disruption of this coordinated mechanism represents a potential approach for overcoming resistance in agricultural pest populations.

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谷胱甘肽s -转移酶的协调调节赋予多重抗杀虫剂西方富兰克林氏菌（Pergande）的代谢灵活性

害虫对多种杀虫剂的抗药性演变威胁着全球粮食安全。虽然谷胱甘肽s -转移酶（GSTs）与解毒有关，但特定基因亚家族相互作用赋予广谱抗性的协调机制仍未充分表征。目的探讨西富兰克林氏菌多重耐药菌株中GST亚科的功能分配与协同作用。方法采用比较基因组学（克隆了20个GST基因）、转录组学（qRT-PCR）、rnai介导的沉默、分子对接（AutoDock Vina）和体外代谢分析（UPLC-MS/MS）对敏感和耐药的蓟马菌株进行分析。结果2个耐药菌株（NIL-R和FS-R）对5种杀虫剂（氯虫腈、甲维菌素苯甲酸酯、spinetoram、spinosad和噻虫嗪）均表现出中高抗性，GSTs活性显著升高。系统发育分析表明，gst包含10个保守的delta成员和7个不同的sigma成员。由于基因复制，sigma亚家族经历了显著的扩展。Delta （FoGSTd1、d4、d9）和sigma （FoGSTs1、s2、s6）基因在耐药菌株中显著上调。RNAi在GSTs之间显示出特殊的功能分配：delta GSTs介导对spinosad和chlorfenapyr的抗性，sigma GSTs负责噻虫嗪的抗性，值得注意的是，这些亚家族之间的合作有助于对emamectin benzoate和spinetoram的抗性。FoGSTd9和FoGSTs1蛋白的分子对接和体外代谢实验进一步支持了GST亚家族的功能分配和协同作用。结论西花蓟马可能通过协调GST亚家族来实现对多种杀虫剂压力的代谢灵活性。这种生存策略由亚家族之间的机制功能分配和合作相互作用所调节，可能有助于节约能源和降低适应成本。破坏这种协调机制是克服农业害虫种群抗性的一种潜在方法。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Journal of Advanced Research Multidisciplinary-Multidisciplinary

CiteScore

21.60

自引率

0.90%

发文量

280

审稿时长

12 weeks

期刊介绍： Journal of Advanced Research (J. Adv. Res.) is an applied/natural sciences, peer-reviewed journal that focuses on interdisciplinary research. The journal aims to contribute to applied research and knowledge worldwide through the publication of original and high-quality research articles in the fields of Medicine, Pharmaceutical Sciences, Dentistry, Physical Therapy, Veterinary Medicine, and Basic and Biological Sciences. The following abstracting and indexing services cover the Journal of Advanced Research: PubMed/Medline, Essential Science Indicators, Web of Science, Scopus, PubMed Central, PubMed, Science Citation Index Expanded, Directory of Open Access Journals (DOAJ), and INSPEC.