Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)

The bean flower thrips, Megalurothrips usitatus (Bagnall), has caused significant damage to leguminous crops in the Asian tropics and established populations in North America. Ineffective pest control has been reported in multiple regions, raising concerns about food safety risks due to improper ins...

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Main Authors: Hongyi Cao, Jiangjiang Yuan, Yanran Wan, Yingxi Tang, Xiaobin Zheng, Jing Wang, Kanghua Qian, Jiuming Feng, Sirui Chen, Youjun Zhang, Qingjun Wu
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325006529
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author Hongyi Cao
Jiangjiang Yuan
Yanran Wan
Yingxi Tang
Xiaobin Zheng
Jing Wang
Kanghua Qian
Jiuming Feng
Sirui Chen
Youjun Zhang
Qingjun Wu
author_facet Hongyi Cao
Jiangjiang Yuan
Yanran Wan
Yingxi Tang
Xiaobin Zheng
Jing Wang
Kanghua Qian
Jiuming Feng
Sirui Chen
Youjun Zhang
Qingjun Wu
author_sort Hongyi Cao
collection DOAJ
description The bean flower thrips, Megalurothrips usitatus (Bagnall), has caused significant damage to leguminous crops in the Asian tropics and established populations in North America. Ineffective pest control has been reported in multiple regions, raising concerns about food safety risks due to improper insecticide use. To evaluate insecticide susceptibility and the role of detoxification enzyme involvement, resistance monitoring and enzyme activity assays were conducted. RNA sequencing (RNA-seq) and weighted gene co-expression network analysis (WGCNA) techniques validated key gene functions. Results showed that the XW population was resistant to five insecticides, with resistance ratios ranging from 7.17 to 42.90 compared to the reference population. The NJ and YZ populations showed resistance to two and one insecticide, respectively, while the HP population was most susceptible. Elevated cytochrome P450s (CYP450), UDP-glycosyltransferases, and acetylcholinesterases activities were observed in the YZ population. Three CYP450 genes positively correlated with CYP450 activity. Carboxylesterases (CarE) activity was the highest in the XW population, with MusiPT_006325 positively correlated and MusiPT_006095/MusiPT_003750 negatively correlated with CarE activity. Glutathione-S-transferase activity was the highest in the HP population. WGCNA revealed positive correlations between MEblue, MEturquoise, and MEbrown modules and acetamiprid/ novaluron median lethal concentration (LC50) values, but negative correlations with β-cypermethrin, spinetoram, emamectin benzoate, thiamethoxam, and spirotetramat LC50 values. Ten CYP450 genes and three UGT genes were identified as hub genes. Our findings reveal insecticide resistance and the role of detoxification enzymes in M. usitatus, providing valuable insights for developing effective management strategies against this thrips species.
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spelling doaj-art-936d96a905c2478bbcd9c7f8b3e301352025-08-20T03:53:53ZengElsevierEcotoxicology and Environmental Safety0147-65132025-06-0129811831610.1016/j.ecoenv.2025.118316Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)Hongyi Cao0Jiangjiang Yuan1Yanran Wan2Yingxi Tang3Xiaobin Zheng4Jing Wang5Kanghua Qian6Jiuming Feng7Sirui Chen8Youjun Zhang9Qingjun Wu10State Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China; National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572024, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China; College of Plant Protection, Hebei Agricultural University, Hebei 071000, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China; National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572024, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China; National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572024, China; Corresponding author at: State Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China.The bean flower thrips, Megalurothrips usitatus (Bagnall), has caused significant damage to leguminous crops in the Asian tropics and established populations in North America. Ineffective pest control has been reported in multiple regions, raising concerns about food safety risks due to improper insecticide use. To evaluate insecticide susceptibility and the role of detoxification enzyme involvement, resistance monitoring and enzyme activity assays were conducted. RNA sequencing (RNA-seq) and weighted gene co-expression network analysis (WGCNA) techniques validated key gene functions. Results showed that the XW population was resistant to five insecticides, with resistance ratios ranging from 7.17 to 42.90 compared to the reference population. The NJ and YZ populations showed resistance to two and one insecticide, respectively, while the HP population was most susceptible. Elevated cytochrome P450s (CYP450), UDP-glycosyltransferases, and acetylcholinesterases activities were observed in the YZ population. Three CYP450 genes positively correlated with CYP450 activity. Carboxylesterases (CarE) activity was the highest in the XW population, with MusiPT_006325 positively correlated and MusiPT_006095/MusiPT_003750 negatively correlated with CarE activity. Glutathione-S-transferase activity was the highest in the HP population. WGCNA revealed positive correlations between MEblue, MEturquoise, and MEbrown modules and acetamiprid/ novaluron median lethal concentration (LC50) values, but negative correlations with β-cypermethrin, spinetoram, emamectin benzoate, thiamethoxam, and spirotetramat LC50 values. Ten CYP450 genes and three UGT genes were identified as hub genes. Our findings reveal insecticide resistance and the role of detoxification enzymes in M. usitatus, providing valuable insights for developing effective management strategies against this thrips species.http://www.sciencedirect.com/science/article/pii/S0147651325006529Megalurothrips usitatusVigna unguiculataInsecticide resistanceDetoxification enzymesRNA-seqWGCNA
spellingShingle Hongyi Cao
Jiangjiang Yuan
Yanran Wan
Yingxi Tang
Xiaobin Zheng
Jing Wang
Kanghua Qian
Jiuming Feng
Sirui Chen
Youjun Zhang
Qingjun Wu
Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)
Ecotoxicology and Environmental Safety
Megalurothrips usitatus
Vigna unguiculata
Insecticide resistance
Detoxification enzymes
RNA-seq
WGCNA
title Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)
title_full Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)
title_fullStr Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)
title_full_unstemmed Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)
title_short Transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips, Megalurothrips usitatus (Bagnall)
title_sort transcriptome analysis of insecticide resistance mechanisms in field populations of the bean flower thrips megalurothrips usitatus bagnall
topic Megalurothrips usitatus
Vigna unguiculata
Insecticide resistance
Detoxification enzymes
RNA-seq
WGCNA
url http://www.sciencedirect.com/science/article/pii/S0147651325006529
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