Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>

The release of herbivore-induced plant volatiles (HIPVs) has been recognized to be an important strategy for plant adaptation to herbivore attack. However, whether these induced volatiles are beneficial to insect herbivores, particularly insect larvae, is largely unknown. We used the two important h...

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Main Authors: Peng Wang, Qiyue Zeng, Yi Zhao, Xiaomin Sun, Yongqiang Han, Rensen Zeng, Yuanyuan Song, Dongmei Chen, Yibin Lin
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/1/57
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author Peng Wang
Qiyue Zeng
Yi Zhao
Xiaomin Sun
Yongqiang Han
Rensen Zeng
Yuanyuan Song
Dongmei Chen
Yibin Lin
author_facet Peng Wang
Qiyue Zeng
Yi Zhao
Xiaomin Sun
Yongqiang Han
Rensen Zeng
Yuanyuan Song
Dongmei Chen
Yibin Lin
author_sort Peng Wang
collection DOAJ
description The release of herbivore-induced plant volatiles (HIPVs) has been recognized to be an important strategy for plant adaptation to herbivore attack. However, whether these induced volatiles are beneficial to insect herbivores, particularly insect larvae, is largely unknown. We used the two important highly polyphagous lepidopteran pests <i>Spodoptera frugiperda</i> and <i>S. litura</i> to evaluate the benefit on xenobiotic detoxification of larval exposure to HIPVs released by the host plant maize (<i>Zea mays</i>). Larval exposure of the invasive alien species <i>S. frugiperda</i> to maize HIPVs significantly enhanced their tolerance to all three of the well-known defensive compounds 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), chlorogenic acid, and tannic acid in maize and the two commonly used insecticides methomyl and chlorpyrifos. HIPV exposure also improved the larval tolerance of <i>S. litura</i> third instars to chlorogenic and tannic acids. Furthermore, larval exposure to either maize HIPVs or DIMBOA induced the activities of cytochrome P450 enzymes (P450s), glutathione-s-transferase (GST), and carboxylesterase (CarE) in the midguts and fat bodies of the two insects, while the induction was significantly higher by the two components together. In addition, the expression of four genes encoding uridine diphosphate (UDP)-glycosyltransferases (<i>UGT33F28</i>, <i>UGT40L8</i>) and P450s (<i>CYP4d8</i>, <i>CYP4V2</i>) showed similar induction patterns in <i>S. frugiperda.</i> Cis-3-hexen-1-ol, an important component in maize HIPVs, also showed the same functions as maize HIPVs, and its exposure increased larval xenobiotic tolerance and induced the detoxification enzymes and gene expression. Our findings demonstrate that HIPVs released by the pest-infested host plants are conductive to the xenobiotic tolerance of lepidopteran insect larvae. Hijacking the host plant HIPVs is an important strategy of the invasive alien polyphagous lepidopteran pest to counter-defend against the host plant’s chemical defense.
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spelling doaj-art-37b2d738a3f54820af529f72437d924a2025-01-10T13:19:37ZengMDPI AGPlants2223-77472024-12-011415710.3390/plants14010057Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>Peng Wang0Qiyue Zeng1Yi Zhao2Xiaomin Sun3Yongqiang Han4Rensen Zeng5Yuanyuan Song6Dongmei Chen7Yibin Lin8Ministry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Science, Southern University of Science and Technology, Shenzhen 518055, ChinaMinistry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaMinistry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Life Sciences and Resource Environment, Yichun University, Yichun 336000, ChinaMinistry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaMinistry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaMinistry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaMinistry of Education Key Laboratory for Genetics, Breeding and Multiple Utilization of Crop, Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaThe release of herbivore-induced plant volatiles (HIPVs) has been recognized to be an important strategy for plant adaptation to herbivore attack. However, whether these induced volatiles are beneficial to insect herbivores, particularly insect larvae, is largely unknown. We used the two important highly polyphagous lepidopteran pests <i>Spodoptera frugiperda</i> and <i>S. litura</i> to evaluate the benefit on xenobiotic detoxification of larval exposure to HIPVs released by the host plant maize (<i>Zea mays</i>). Larval exposure of the invasive alien species <i>S. frugiperda</i> to maize HIPVs significantly enhanced their tolerance to all three of the well-known defensive compounds 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), chlorogenic acid, and tannic acid in maize and the two commonly used insecticides methomyl and chlorpyrifos. HIPV exposure also improved the larval tolerance of <i>S. litura</i> third instars to chlorogenic and tannic acids. Furthermore, larval exposure to either maize HIPVs or DIMBOA induced the activities of cytochrome P450 enzymes (P450s), glutathione-s-transferase (GST), and carboxylesterase (CarE) in the midguts and fat bodies of the two insects, while the induction was significantly higher by the two components together. In addition, the expression of four genes encoding uridine diphosphate (UDP)-glycosyltransferases (<i>UGT33F28</i>, <i>UGT40L8</i>) and P450s (<i>CYP4d8</i>, <i>CYP4V2</i>) showed similar induction patterns in <i>S. frugiperda.</i> Cis-3-hexen-1-ol, an important component in maize HIPVs, also showed the same functions as maize HIPVs, and its exposure increased larval xenobiotic tolerance and induced the detoxification enzymes and gene expression. Our findings demonstrate that HIPVs released by the pest-infested host plants are conductive to the xenobiotic tolerance of lepidopteran insect larvae. Hijacking the host plant HIPVs is an important strategy of the invasive alien polyphagous lepidopteran pest to counter-defend against the host plant’s chemical defense.https://www.mdpi.com/2223-7747/14/1/57herbivore-induced plant volatiles<i>Spodoptera frugiperda</i>xenobioticcytochrome P450DIMBOA
spellingShingle Peng Wang
Qiyue Zeng
Yi Zhao
Xiaomin Sun
Yongqiang Han
Rensen Zeng
Yuanyuan Song
Dongmei Chen
Yibin Lin
Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>
Plants
herbivore-induced plant volatiles
<i>Spodoptera frugiperda</i>
xenobiotic
cytochrome P450
DIMBOA
title Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>
title_full Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>
title_fullStr Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>
title_full_unstemmed Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>
title_short Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of <i>Spodoptera frugiperda</i> and <i>S. litura</i>
title_sort maize herbivore induced volatiles enhance xenobiotic detoxification in larvae of i spodoptera frugiperda i and i s litura i
topic herbivore-induced plant volatiles
<i>Spodoptera frugiperda</i>
xenobiotic
cytochrome P450
DIMBOA
url https://www.mdpi.com/2223-7747/14/1/57
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