Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua

Abstract Synthetic insecticides have been widely used for the prevention and control of disease vectors and agricultural pests. However, frequent uses of insecticides have resulted in the development of insecticide resistance in these insect pests. The resistance adversely affects the efficacy of in...

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Main Authors: Bo Hu, Yuping Deng, Tao Lu, Miaomiao Ren, Kuitun Liu, Cong Rao, Hailiang Guo, Jianya Su
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-07560-8
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author Bo Hu
Yuping Deng
Tao Lu
Miaomiao Ren
Kuitun Liu
Cong Rao
Hailiang Guo
Jianya Su
author_facet Bo Hu
Yuping Deng
Tao Lu
Miaomiao Ren
Kuitun Liu
Cong Rao
Hailiang Guo
Jianya Su
author_sort Bo Hu
collection DOAJ
description Abstract Synthetic insecticides have been widely used for the prevention and control of disease vectors and agricultural pests. However, frequent uses of insecticides have resulted in the development of insecticide resistance in these insect pests. The resistance adversely affects the efficacy of insecticides, and seriously reduces the lifespan of insecticides. Therefore, resistance management requires new strategies to suppress insecticide resistance. Here, we confirm that CncC/Maf are the key regulators of various detoxification genes involved in insecticide resistance in Spodoptera exigua. Then, we develop a cell screening platform to identify the natural compound inhibitors of CncC/Maf and determine that sofalcone can act as a CncC/Maf inhibitor in vitro and in vivo. Bioassay results showed that sofalcone significantly enhanced the toxicity (more than 3-fold) of chlorpyrifos and lambda-cyhalothrin against S. exigua larvae. Finally, we demonstrate that sofalcone can greatly improve the susceptibility of S. exigua larvae to insecticides by inhibiting the activity of the ROS/CncC-dependent detoxifying enzymes and downregulating the expression levels of detoxification genes. CncC/Maf inhibitors can be used as broad-spectrum synergists to overcome insecticide resistance in pest populations. Altogether, our results demonstrate that reduced expression of detoxification genes resulting from suppression of transcriptional regulation of these genes contributes to controlling insecticide resistance, which provides a very novel and high-efficiency green resistance management strategy.
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institution Kabale University
issn 2399-3642
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spelling doaj-art-310d8495d900496f87d5653937d7f2812025-02-02T12:37:18ZengNature PortfolioCommunications Biology2399-36422025-01-018111310.1038/s42003-025-07560-8Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exiguaBo Hu0Yuping Deng1Tao Lu2Miaomiao Ren3Kuitun Liu4Cong Rao5Hailiang Guo6Jianya Su7Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyJiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyJiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and TechnologyCollege of Environment and Chemical Engineering, Jiangsu University of Science and TechnologyKey Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural UniversityKey Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural UniversityKey Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural UniversityKey Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural UniversityAbstract Synthetic insecticides have been widely used for the prevention and control of disease vectors and agricultural pests. However, frequent uses of insecticides have resulted in the development of insecticide resistance in these insect pests. The resistance adversely affects the efficacy of insecticides, and seriously reduces the lifespan of insecticides. Therefore, resistance management requires new strategies to suppress insecticide resistance. Here, we confirm that CncC/Maf are the key regulators of various detoxification genes involved in insecticide resistance in Spodoptera exigua. Then, we develop a cell screening platform to identify the natural compound inhibitors of CncC/Maf and determine that sofalcone can act as a CncC/Maf inhibitor in vitro and in vivo. Bioassay results showed that sofalcone significantly enhanced the toxicity (more than 3-fold) of chlorpyrifos and lambda-cyhalothrin against S. exigua larvae. Finally, we demonstrate that sofalcone can greatly improve the susceptibility of S. exigua larvae to insecticides by inhibiting the activity of the ROS/CncC-dependent detoxifying enzymes and downregulating the expression levels of detoxification genes. CncC/Maf inhibitors can be used as broad-spectrum synergists to overcome insecticide resistance in pest populations. Altogether, our results demonstrate that reduced expression of detoxification genes resulting from suppression of transcriptional regulation of these genes contributes to controlling insecticide resistance, which provides a very novel and high-efficiency green resistance management strategy.https://doi.org/10.1038/s42003-025-07560-8
spellingShingle Bo Hu
Yuping Deng
Tao Lu
Miaomiao Ren
Kuitun Liu
Cong Rao
Hailiang Guo
Jianya Su
Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua
Communications Biology
title Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua
title_full Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua
title_fullStr Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua
title_full_unstemmed Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua
title_short Inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in Spodoptera exigua
title_sort inhibition of transcriptional regulation of detoxification genes contributes to insecticide resistance management in spodoptera exigua
url https://doi.org/10.1038/s42003-025-07560-8
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