Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl

Plants release an array of volatile chemicals into the air to communicate with other organisms in the environment. Insect attack triggers emission of herbivore-induced plant volatiles (HIPVs). How insect herbivores use these odors to plan their detoxification systems is vital for insect adaptation t...

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Main Authors: Choufei Wu, Chaohui Ding, Shi Chen, Xiaoying Wu, Liqin Zhang, Yuanyuan Song, Wu Li, Rensen Zeng
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/12/3/238
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author Choufei Wu
Chaohui Ding
Shi Chen
Xiaoying Wu
Liqin Zhang
Yuanyuan Song
Wu Li
Rensen Zeng
author_facet Choufei Wu
Chaohui Ding
Shi Chen
Xiaoying Wu
Liqin Zhang
Yuanyuan Song
Wu Li
Rensen Zeng
author_sort Choufei Wu
collection DOAJ
description Plants release an array of volatile chemicals into the air to communicate with other organisms in the environment. Insect attack triggers emission of herbivore-induced plant volatiles (HIPVs). How insect herbivores use these odors to plan their detoxification systems is vital for insect adaptation to environmental xenobiotics. Here we show that the larvae of <i>Helicoverpa armigera</i> (Hübner), a broadly polyphagous lepidopteran herbivore, have the capacity to use plant volatiles as cues to upregulate multiple detoxification systems, including cytochrome P450 monooxygenases (P450s), for detoxification of insecticides. Olfactory exposure of the fifth instars to two terpene volatiles limonene and nerolidol, and two green-leaf volatiles 2-heptanone and <i>cis</i>-3-hexenyl acetate significantly reduced larval susceptibility to the insecticide methomyl. However, larval pretreatment with piperonyl butoxide (PBO), a known P450 inhibitor, neutralized the effects of volatile exposure. Furthermore, larval exposure to the four plant volatiles enhanced activities of P450 enzymes in midguts and fatbodies, and upregulated expression of CYP6B2, CYP6B6 and CYP6B7, P450s involved in detoxification of the insecticide. Larval exposure to 2-heptanone and limonene volatiles also enhanced activities of glutathione-s-transferase and carboxylesterase. Our findings suggest that olfactory exposure to HIPVs enhances larval insecticide tolerance via induction of detoxification P450s.
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spelling doaj.art-ef806cfdf7924f029895a3c902975cc62023-11-21T10:10:24ZengMDPI AGInsects2075-44502021-03-0112323810.3390/insects12030238Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide MethomylChoufei Wu0Chaohui Ding1Shi Chen2Xiaoying Wu3Liqin Zhang4Yuanyuan Song5Wu Li6Rensen Zeng7Key Laboratory of Vector Biology and Pathogen Control of Zhejiang Province, School of Life Sciences, Huzhou University, Huzhou 313000, ChinaGuangdong Provincial Key Laboratory of Crop Genetic Improvement, Crops Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaCollege of Materials and Energy, South China Agricultural University, Wushan, Guangzhou 510642, ChinaKey Laboratory of Vector Biology and Pathogen Control of Zhejiang Province, School of Life Sciences, Huzhou University, Huzhou 313000, ChinaKey Laboratory of Vector Biology and Pathogen Control of Zhejiang Province, School of Life Sciences, Huzhou University, Huzhou 313000, ChinaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Agriculture, Fujian Agriculture and Forestry University, Jinshan, Fuzhou 350002, ChinaGuangdong Provincial Key Laboratory of Crop Genetic Improvement, Crops Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Agriculture, Fujian Agriculture and Forestry University, Jinshan, Fuzhou 350002, ChinaPlants release an array of volatile chemicals into the air to communicate with other organisms in the environment. Insect attack triggers emission of herbivore-induced plant volatiles (HIPVs). How insect herbivores use these odors to plan their detoxification systems is vital for insect adaptation to environmental xenobiotics. Here we show that the larvae of <i>Helicoverpa armigera</i> (Hübner), a broadly polyphagous lepidopteran herbivore, have the capacity to use plant volatiles as cues to upregulate multiple detoxification systems, including cytochrome P450 monooxygenases (P450s), for detoxification of insecticides. Olfactory exposure of the fifth instars to two terpene volatiles limonene and nerolidol, and two green-leaf volatiles 2-heptanone and <i>cis</i>-3-hexenyl acetate significantly reduced larval susceptibility to the insecticide methomyl. However, larval pretreatment with piperonyl butoxide (PBO), a known P450 inhibitor, neutralized the effects of volatile exposure. Furthermore, larval exposure to the four plant volatiles enhanced activities of P450 enzymes in midguts and fatbodies, and upregulated expression of CYP6B2, CYP6B6 and CYP6B7, P450s involved in detoxification of the insecticide. Larval exposure to 2-heptanone and limonene volatiles also enhanced activities of glutathione-s-transferase and carboxylesterase. Our findings suggest that olfactory exposure to HIPVs enhances larval insecticide tolerance via induction of detoxification P450s.https://www.mdpi.com/2075-4450/12/3/238<i>Helicoverpa armigera</i>plant volatileherbivore-induced plant volatiles cytochrome P450 monooxygenasesinsecticide tolerancedetoxification enzyme
spellingShingle Choufei Wu
Chaohui Ding
Shi Chen
Xiaoying Wu
Liqin Zhang
Yuanyuan Song
Wu Li
Rensen Zeng
Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl
Insects
<i>Helicoverpa armigera</i>
plant volatile
herbivore-induced plant volatiles cytochrome P450 monooxygenases
insecticide tolerance
detoxification enzyme
title Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl
title_full Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl
title_fullStr Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl
title_full_unstemmed Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl
title_short Exposure of <i>Helicoverpa armigera</i> Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl
title_sort exposure of i helicoverpa armigera i larvae to plant volatile organic compounds induces cytochrome p450 monooxygenases and enhances larval tolerance to the insecticide methomyl
topic <i>Helicoverpa armigera</i>
plant volatile
herbivore-induced plant volatiles cytochrome P450 monooxygenases
insecticide tolerance
detoxification enzyme
url https://www.mdpi.com/2075-4450/12/3/238
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