Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes

BackgroundAedes (Stegomyia) albopictus (Skuse) is an invasive and widespread mosquito species that can transmit dengue, chikungunya, yellow fever, and Zika viruses. Its control heavily relies on the use of insecticides. However, the efficacy of the insecticide-based intervention is threatened by the...

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Main Authors: Xiaojie Zhou, Jing Li, Ruoyao Ni, Xinghui Qiu, Yong Zhang, Ying Tong
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Physiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2024.1498313/full
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author Xiaojie Zhou
Jing Li
Ruoyao Ni
Xinghui Qiu
Yong Zhang
Ying Tong
author_facet Xiaojie Zhou
Jing Li
Ruoyao Ni
Xinghui Qiu
Yong Zhang
Ying Tong
author_sort Xiaojie Zhou
collection DOAJ
description BackgroundAedes (Stegomyia) albopictus (Skuse) is an invasive and widespread mosquito species that can transmit dengue, chikungunya, yellow fever, and Zika viruses. Its control heavily relies on the use of insecticides. However, the efficacy of the insecticide-based intervention is threatened by the increasing development of resistance to available insecticides. Understanding the current status and potential mechanisms of insecticide resistance is an important prerequisite for devising strategies to maintain the sustainability of vector control programs. In this study, we investigated the current status and probable candidate detoxification genes associated with insecticide resistance in the Asian tiger mosquito in Beijing, the capital city of China.MethodsBioassays were conducted on three field populations of Ae. albopictus collected from urban communities in Beijing by exposure to diagnostic doses of permethrin, deltamethrin, malathion, and propoxur. Differentially expressed genes (DEGs) associated with insecticide resistance were screened by transcriptomic analysis using Illumina RNA sequencing data (RNA-seq) from 12 independent RNA libraries constructed from female strains of the three field populations and one susceptible strain.ResultsThe bioassay results indicated that all the three field populations were resistant to propoxur (carbamate), deltamethrin, and permethrin (pyrethroids), but susceptible to malathion (organophosphate). Eighteen (18) cytochrome P450s (P450s), five (5) glutathione S-transferases (GSTs), four (4) carboxy/cholinesterases (CCEs), eight (8) UDP-glycosyltransferases (UGTs), and three (3) ATP-binding cassette transporters (ABCs) were found to be significantly overexpressed in the three field populations relative to the susceptible strain via transcriptomic analysis.ConclusionThis study demonstrates that the Ae. albopictus field populations in Beijing exhibit multiple phenotypic resistance to commonly used pyrethroids and carbamate. The identification of a number of DEGs associated with insecticide resistance indicates that the mechanisms underlying resistance in field populations are complicated, and detoxifying enzymes may play important roles. The multiple resistance status detected in the three field populations suggests that resistance management strategies such as insecticide rotation and non-chemical-based measures should be implemented in order to sustain effective control of the disease vector and vector-borne diseases.
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spelling doaj-art-cec35d5643054eaea5fc3536d54806eb2025-08-20T02:49:01ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-12-011510.3389/fphys.2024.14983131498313Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genesXiaojie Zhou0Jing Li1Ruoyao Ni2Xinghui Qiu3Yong Zhang4Ying Tong5Institute of Disinfection and Pest Control, Beijing Center for Disease Prevention and Control, Beijing, ChinaInstitute of Disinfection and Pest Control, Beijing Center for Disease Prevention and Control, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaInstitute of Disinfection and Pest Control, Beijing Center for Disease Prevention and Control, Beijing, ChinaInstitute of Disinfection and Pest Control, Beijing Center for Disease Prevention and Control, Beijing, ChinaBackgroundAedes (Stegomyia) albopictus (Skuse) is an invasive and widespread mosquito species that can transmit dengue, chikungunya, yellow fever, and Zika viruses. Its control heavily relies on the use of insecticides. However, the efficacy of the insecticide-based intervention is threatened by the increasing development of resistance to available insecticides. Understanding the current status and potential mechanisms of insecticide resistance is an important prerequisite for devising strategies to maintain the sustainability of vector control programs. In this study, we investigated the current status and probable candidate detoxification genes associated with insecticide resistance in the Asian tiger mosquito in Beijing, the capital city of China.MethodsBioassays were conducted on three field populations of Ae. albopictus collected from urban communities in Beijing by exposure to diagnostic doses of permethrin, deltamethrin, malathion, and propoxur. Differentially expressed genes (DEGs) associated with insecticide resistance were screened by transcriptomic analysis using Illumina RNA sequencing data (RNA-seq) from 12 independent RNA libraries constructed from female strains of the three field populations and one susceptible strain.ResultsThe bioassay results indicated that all the three field populations were resistant to propoxur (carbamate), deltamethrin, and permethrin (pyrethroids), but susceptible to malathion (organophosphate). Eighteen (18) cytochrome P450s (P450s), five (5) glutathione S-transferases (GSTs), four (4) carboxy/cholinesterases (CCEs), eight (8) UDP-glycosyltransferases (UGTs), and three (3) ATP-binding cassette transporters (ABCs) were found to be significantly overexpressed in the three field populations relative to the susceptible strain via transcriptomic analysis.ConclusionThis study demonstrates that the Ae. albopictus field populations in Beijing exhibit multiple phenotypic resistance to commonly used pyrethroids and carbamate. The identification of a number of DEGs associated with insecticide resistance indicates that the mechanisms underlying resistance in field populations are complicated, and detoxifying enzymes may play important roles. The multiple resistance status detected in the three field populations suggests that resistance management strategies such as insecticide rotation and non-chemical-based measures should be implemented in order to sustain effective control of the disease vector and vector-borne diseases.https://www.frontiersin.org/articles/10.3389/fphys.2024.1498313/fulltranscriptomeinsecticide resistancecytochrome P450metabolic resistanceAedes albopictus
spellingShingle Xiaojie Zhou
Jing Li
Ruoyao Ni
Xinghui Qiu
Yong Zhang
Ying Tong
Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes
Frontiers in Physiology
transcriptome
insecticide resistance
cytochrome P450
metabolic resistance
Aedes albopictus
title Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes
title_full Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes
title_fullStr Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes
title_full_unstemmed Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes
title_short Insecticide resistance in the field populations of the Asian tiger mosquito Aedes albopictus in Beijing: resistance status and associated detoxification genes
title_sort insecticide resistance in the field populations of the asian tiger mosquito aedes albopictus in beijing resistance status and associated detoxification genes
topic transcriptome
insecticide resistance
cytochrome P450
metabolic resistance
Aedes albopictus
url https://www.frontiersin.org/articles/10.3389/fphys.2024.1498313/full
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