Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)

<i>Spodoptera</i><i>exigua</i>, a multifeeding insect pest, has developed a high level of resistance to chlorantraniliprole, which is a benzoylurea insecticide that targets the ryanodine receptors (RyRs). Herein, the resistant strain (SE-Sel) and sensitive strain (SE-Sus) wer...

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Main Authors: Changwei Gong, Xinge Yao, Qunfang Yang, Xuegui Wang, Yuming Zhang, Yumeng Wang, Litao Shen
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/9/5027
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spelling doaj-f89d469a01904ef5931886cf0aa1922f2021-05-31T23:33:34ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-05-01225027502710.3390/ijms22095027Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)Changwei Gong0Xinge Yao1Qunfang Yang2Xuegui Wang3Yuming Zhang4Yumeng Wang5Litao Shen6Biorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, ChinaBiorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, ChinaBiorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, ChinaBiorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, ChinaBiorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, ChinaBiorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, ChinaBiorational Pesticide Research Laboratory, Agricultural College, Sichuan Agricultural University, Chengdu 611130, China<i>Spodoptera</i><i>exigua</i>, a multifeeding insect pest, has developed a high level of resistance to chlorantraniliprole, which is a benzoylurea insecticide that targets the ryanodine receptors (RyRs). Herein, the resistant strain (SE-Sel) and sensitive strain (SE-Sus) were obtained by bidirectional screening for six generations. The potential oviposited eggs and oviposition rate of the SE-Sel strain were dramatically lower than those of the SE-Sus strain; on the contrary, the weights of prepupae and preadult were significantly increased. As a post-mating response, the higher number of non-oviposited eggs in the SE-Sel strain was caused by a lower mating rate. In addition, the expression levels of <i>vitellogenin</i> (<i>SeVg</i>) and its receptor (<i>SeVgR</i>) in the SE-Sel strain were consistently lower than those in the SE-Sus strain. An RyR<sup>I4743M</sup> mutation, contributing to the resistance to chlorantraniliprole, was located in the S3 transmembrane segments and might have affected the release of calcium ions; it led to the upregulated expression of the neuropeptide <i>SeNPF</i> and its receptor <i>SeNPFR</i>, and the mating and oviposition rate were significantly recovered when the <i>SeNPF</i> was knocked down though RNA interference (RNAi) in the male adult of the SE-Sel strain. Moreover, the expression of the juvenile hormone-binding proteins <i>SeJHBWDS3</i> and <i>SeJHBAN</i> in the male adult of the SE-Sel strain was significantly decreased, which proved the existence of a fitness cost from another angle. Therefore, these results indicate that the fitness cost accompanied by chlorantraniliprole resistance in <i>S. exigua</i> may be related to the decrease in mating desire due to <i>SeNPF</i> overexpression.https://www.mdpi.com/1422-0067/22/9/5027ryanodine receptorsvitellogeninpost-mating responsemating rateoviposition
collection DOAJ
language English
format Article
sources DOAJ
author Changwei Gong
Xinge Yao
Qunfang Yang
Xuegui Wang
Yuming Zhang
Yumeng Wang
Litao Shen
spellingShingle Changwei Gong
Xinge Yao
Qunfang Yang
Xuegui Wang
Yuming Zhang
Yumeng Wang
Litao Shen
Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)
International Journal of Molecular Sciences
ryanodine receptors
vitellogenin
post-mating response
mating rate
oviposition
author_facet Changwei Gong
Xinge Yao
Qunfang Yang
Xuegui Wang
Yuming Zhang
Yumeng Wang
Litao Shen
author_sort Changwei Gong
title Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)
title_short Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)
title_full Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)
title_fullStr Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)
title_full_unstemmed Fitness Costs of Chlorantraniliprole Resistance Related to the <i>SeNPF</i> Overexpression in the <i>Spodoptera exigua</i> (Lepidoptera: Noctuidae)
title_sort fitness costs of chlorantraniliprole resistance related to the <i>senpf</i> overexpression in the <i>spodoptera exigua</i> (lepidoptera: noctuidae)
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2021-05-01
description <i>Spodoptera</i><i>exigua</i>, a multifeeding insect pest, has developed a high level of resistance to chlorantraniliprole, which is a benzoylurea insecticide that targets the ryanodine receptors (RyRs). Herein, the resistant strain (SE-Sel) and sensitive strain (SE-Sus) were obtained by bidirectional screening for six generations. The potential oviposited eggs and oviposition rate of the SE-Sel strain were dramatically lower than those of the SE-Sus strain; on the contrary, the weights of prepupae and preadult were significantly increased. As a post-mating response, the higher number of non-oviposited eggs in the SE-Sel strain was caused by a lower mating rate. In addition, the expression levels of <i>vitellogenin</i> (<i>SeVg</i>) and its receptor (<i>SeVgR</i>) in the SE-Sel strain were consistently lower than those in the SE-Sus strain. An RyR<sup>I4743M</sup> mutation, contributing to the resistance to chlorantraniliprole, was located in the S3 transmembrane segments and might have affected the release of calcium ions; it led to the upregulated expression of the neuropeptide <i>SeNPF</i> and its receptor <i>SeNPFR</i>, and the mating and oviposition rate were significantly recovered when the <i>SeNPF</i> was knocked down though RNA interference (RNAi) in the male adult of the SE-Sel strain. Moreover, the expression of the juvenile hormone-binding proteins <i>SeJHBWDS3</i> and <i>SeJHBAN</i> in the male adult of the SE-Sel strain was significantly decreased, which proved the existence of a fitness cost from another angle. Therefore, these results indicate that the fitness cost accompanied by chlorantraniliprole resistance in <i>S. exigua</i> may be related to the decrease in mating desire due to <i>SeNPF</i> overexpression.
topic ryanodine receptors
vitellogenin
post-mating response
mating rate
oviposition
url https://www.mdpi.com/1422-0067/22/9/5027
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