<i>CYP6DW3</i> Metabolizes Imidacloprid to Imidacloprid-urea in Whitefly (<i>Bemisia tabaci</i>)

Xue, Hong; Fu, Buli; Huang, Mingjiao; He, Chao; Liang, Jinjin; Yang, Jing; Wei, Xuegao; Liu, Shaonan; Du, Taisheng; Ji, Yao; Chen, Yin; Gong, Pan; Hu, Jinyu; Du, He; Zhang, Rong; Wang, Chao; Khajehali, Jahangir; Su, Qi; Yang, Xin; Zhang, Youjun

doi:10.1021/acs.jafc.2c08353

Cited by 17 publications

(12 citation statements)

References 55 publications

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“…Mobile phases A and B were 80% methanol and 5% ammonium acetate (including 0.1% formic acid). A similar UPLC‐MS/MS condition was adopted with positive ion mode for all analyses as described 34 …”

Section: Methodsmentioning

confidence: 99%

“…A similar UPLC-MS/MS condition was adopted with positive ion mode for all analyses as described. 34 2.13 Evaluation of biological fitness associated with the resistance After identification of CYP4CS5 conferring thiamethoxam and clothianidin resistance, we next investigated whether such resistance is accompanied by fitness cost in the whitefly.…”

Section: Metabolism Of Thiamethoxam and Clothianidin In Vitromentioning

confidence: 99%

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CYP4CS5‐mediated thiamethoxam and clothianidin resistance is accompanied by fitness cost in the whitefly Bemisia tabaci

Hu,

Fu,

Liang

et al. 2023

Pest Management Science

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BackgroundUnderstanding the trade‐offs between insecticide resistance and the associated fitness is of particular importance to sustainable pest control. Being as one of the most devastating pest worldwide, the whitefly Bemisia tabaci has developed resistance to various insecticides, especially neonicotinoid group. Although neonicotinoid resistance is often conferred by P450s‐mediated metabolic resistance, the relationship between such resistance and the associated fitness phenotype remains largely elusive. By gene cloning, qRT‐PCR, RNA interference (RNAi), transgenic Drosophila melanogaster, metabolism capacity in vitro and ‘two sex‐age stage’ life table study, this study aims to explore the molecular role of a P450 gene CYP4CS5 in neonicotinoid resistance and to investigate whether such resistance mechanism carries fitness costs in the whitefly.ResultsOur bioassay tests showed that a total of 13 field‐collected populations of B. tabaci MED displayed low to moderate resistance to thiamethoxam and clothianidin. Compared to the laboratory susceptible strain, we then found that an important P450 CYP4CS5 was remarkably upregulated in the field resistant populations. Such overexpression of CYP4CS5 had a good match with the resistance level among the whitefly samples. Further exposure to the two neonicotinoids resulted in an increase in CYP4CS5 expression. These results implicate that overexpression of CYP4CS5 is closely correlated with thiamethoxam and clothianidin resistance. RNAi knockdown of CYP4CS5 increased mortality of the resistant and susceptible populations after treatment with thiamethoxam and clothianidin in bioassay, while obtained an opposite result when using a transgenic line of D. melanogaster expressing CYP4CS5. Metabolic assays in vitro revealed that CYP4CS5 exhibited certain capacity of metabolizing thiamethoxam and clothianidin. These in vivo and in vitro assays indicate an essential role of CYP4CS5 in conferring thiamethoxam and clothianidin resistance in whitefly. Additionally, our life‐table analysis demonstrate that the filed‐resistant whitefly exhibited a prolonged development time, shortened longevity and reduced fecundity compared to the susceptible, suggesting an existing fitness cost as a result of the resistance.ConclusionCollectively, in addition to the important role of CYP4CS5 in conferring thiamethoxam and clothianidin resistance, we fundamentally discover such resistance mechanism is associated with fitness costs in the whitefly. These findings not only contribute to the development of neonicotinoids resistance management strategies, but also provide a new target for sustainable whitefly control.This article is protected by copyright. All rights reserved.

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Section: Methodsmentioning

confidence: 99%

Section: Metabolism Of Thiamethoxam and Clothianidin In Vitromentioning

confidence: 99%

CYP4CS5‐mediated thiamethoxam and clothianidin resistance is accompanied by fitness cost in the whitefly Bemisia tabaci

Hu,

Fu,

Liang

et al. 2023

Pest Management Science

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“…In the past few years, studies into the underlying mechanism of resistance to IMD have made great progress, especially in the adult stages of B. tabaci , in which resistance is caused by the overexpression of P450s. In particular, CYP6CM1 and CYP6DW3 can metabolize IMD both in vitro and in vivo experiments 32–35 . Because of the morphological, behavioral and physiological differences between adult and nymphal whiteflies, little is currently known about the underlying mechanism conferring IMD resistance in these insects.…”

Section: Introductionmentioning

confidence: 99%

“…In particular, CYP6CM1 and CYP6DW3 can metabolize IMD both in vitro and in vivo experiments. [32][33][34][35] Because of the morphological, behavioral and physiological differences between adult and nymphal whiteflies, little is currently known about the underlying mechanism conferring IMD resistance in these insects. 20E, which is an age-specific substance in the immature stage, is particularly important for many biological processes in insects and, as mentioned above, may have a possible role in insecticide resistance.…”

Section: Introductionmentioning

confidence: 99%

20E biosynthesis gene CYP306A1 confers resistance to imidacloprid in the nymph stage of Bemisia tabaci by detoxification metabolism

Liu

Zhang

et al. 2023

Pest Management Science

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BackgroundDifference in physiology level between the immature and mature stages of insects likely contribute to different mechanisms of insecticide resistance. It is well acknowledged that insect 20‐hydroxyecdysone (20E) plays an important role in many biological processes in the immature stage, whether 20E confers insecticide resistance at this specific stage is still poorly understood. By gene cloning, reverse transcription quantitative real‐time PCR, RNA interference (RNAi) and in vitro metabolism experiments, this study aimed to investigate the potential role of 20E‐related genes in conferring imidacloprid (IMD) resistance in the immature stage of the whitefly Bemisia tabaci Mediterranean.ResultsAfter identification of low to moderate IMD resistance in the whitefly, we found CYP306A1 of the six 20E‐related genes was overexpressed in the nymph stage of the three resistant strains compared to a laboratory reference susceptible strain, but not in the adult stage. Further exposure to IMD resulted in an increase in CYP306A1 expression in the nymph stage. These results together imply that CYP306A1 may be implicated in IMD resistance in the nymph stage of the whitefly. RNAi knockdown of CYP306A1 increased the mortality of nymphs after treatment with IMD in bioassay, suggesting a pivotal role of CYP306A1 in conferring IMD resistance in the nymph stage. Additionally, our metabolism experiments in vivo showed that the content of IMD reduced by 20% along with cytochrome P450 reductase and heterologously expressed CYP306A1, which provides additional evidence for the important function of CYP306A1 in metabolizing IMD that leads to the resistance.ConclusionThis study uncovers a novel function of the 20E biosynthesis gene CYP306A1 in metabolizing imidacloprid, thus contributing to such resistance in the immature stage of the insect. These findings not only advance our understanding of 20E‐mediated insecticide resistance, but also provide a new target for sustainable pest control of global insect pests such as whitefly. © 2023 Society of Chemical Industry.

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“…The key metabolic enzyme cytochrome P450 (P450) plays a crucial role in the detoxification of various xenobiotics, including insecticides . Numerous studies have shown that the induced or constitutive expression of P450 genes in insecticide-resistant insect strains and/or in response to insecticide exposure confers insecticide resistance. , Investigations of the molecular basis of neonicotinoid resistance in whitefly, Bemisia tabaci, revealed that several P450 genes (including CYP6DW3 , CYP6CM1, and CYP4C64 ) are expressed at high levels in resistant strains, and their encoded products play pivotal roles in resistance. − Another study identified a cluster of nine CYP6AE subfamily genes encoding products that are capable of detoxifying several xenobiotics (xanthotoxin, 2-tridecanone, and indoxacarb) in vivo . Overexpression of CYP6P9a and CYP6P9b in Anopheles funestus conferred resistance to carbamates, and their encoded products were demonstrated to be able to metabolize carbamates …”

Section: Introductionmentioning

confidence: 99%

CYP4CL2 Confers Metabolic Resistance to Pyridaben in the Citrus Pest Mite Panonychus citri

Pan,

Xia,

et al. 2023

J. Agric. Food Chem.

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CYP6DW3 Metabolizes Imidacloprid to Imidacloprid-urea in Whitefly (Bemisia tabaci)

Cited by 17 publications

References 55 publications

CYP4CS5‐mediated thiamethoxam and clothianidin resistance is accompanied by fitness cost in the whitefly Bemisia tabaci

CYP4CS5‐mediated thiamethoxam and clothianidin resistance is accompanied by fitness cost in the whitefly Bemisia tabaci

20E biosynthesis gene CYP306A1 confers resistance to imidacloprid in the nymph stage of Bemisia tabaci by detoxification metabolism

CYP4CL2 Confers Metabolic Resistance to Pyridaben in the Citrus Pest Mite Panonychus citri

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