细胞色素P450基因CYP6DW3和CYP4C64参与烟粉虱MED隐种（Q型）对双丙环虫酯的抗性

doi:10.1016/j.jia.2024.07.027

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (5): 1905-1915.DOI: 10.1016/j.jia.2024.07.027

细胞色素P450基因CYP6DW3和CYP4C64参与烟粉虱MED隐种（Q型）对双丙环虫酯的抗性

收稿日期:2024-04-01 修回日期:2024-07-19 接受日期:2024-06-20 出版日期:2025-05-20 发布日期:2025-04-18

Involvement of the cytochrome P450 genes CYP6DW3 and CYP4C64 in afidopyropen resistance in Bemisia tabaci Mediterranean (Q biotype)

Li-jun Ma^1*, Juan Tang^2*, Qing-he Zhang², Bing-li Gao², Cheng Qu², Ran Wang^2#, Chen Luo^1#

¹ College of Plant Protection, Yangzhou University, Yangzhou 225009, China
² Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China

Received:2024-04-01 Revised:2024-07-19 Accepted:2024-06-20 Online:2025-05-20 Published:2025-04-18
About author:Lijun Ma, Tel: +86-514-87978110, E-mail: ma_lijun@foxmail.com; Juan Tang, Tel: +86-514-87978110, E-mail: tangjuan981005@163.com; #Correspondence Chen Luo, Tel: +86-514-87978110, E-mail: Luochen@yzu.edu.cn; Ran Wang, Tel: +86-10-51503338, E-mail: rwang1105@126.com * These authors contributed equally to this study.
Supported by:
This study was partly supported by research grants from the Outstanding Youth Foundation of the Beijing Academy of Agriculture and Forestry Sciences, China (YXQN202301), the National Natural Science Foundation of China (32272522), and the Beijing Natural Science Foundation, China (6232005).

摘要/Abstract

摘要：

烟粉虱Bemisia tabaci寄主植物广泛，是一种世界性的重要害虫，已对多种杀虫剂产生高抗性。双丙环虫酯是近年商品化的丙烯类杀虫剂，其作用方式新颖，选择性强，被用于烟粉虱的防治。我们前期对一个烟粉虱田间种群进行抗性筛选，获得了双丙环虫酯高抗性种群（HD-Afi种群）。本研究发现在HD-Afi种群中，双丙环虫酯和其他常见化学剂交互抗性小, 但HD-Afi种群的P450酶活性是敏感种群HD-S的2.18倍；在12个候选P450基因中，CYP6DW3和CYP4C64基因在HD-Afi种群中显著上调。RNA干扰CYP6DW3和CYP4C64基因可显著增加烟粉虱成虫对双丙环虫酯的敏感性，证实两个基因与烟粉虱对双丙环虫酯的抗性相关。同源性建模和分子对接分析表明，双丙环虫酯与CYP6DW3和CYP4C64的结合稳定，结合自由能分别为-6.87和-6.11 kcal mol^-1。本研究结果表明CYP6DW3和CYP4C64基因的诱导促进了烟粉虱对双丙环虫酯的解毒代谢，造成烟粉虱抗性的发展。

Abstract:

The tobacco whitefly, Bemisia tabaci, is a notorious pest affecting various crops globally, and it exhibits high levels of resistance to various insecticides. Afidopyropen is a recently commercialized pyropene insecticide for B. tabaci control with high selectivity and a novel mode of action. We previously identified a high level of afidopyropen resistance in a field-collected population after selection in the lab, and named it the HD-Afi strain. In the present study, minimal cross-resistance in the HD-Afi strain was found between afidopyropen and other common chemical agents. However, the P450 enzyme activity in HD-Afi was 2.18 times the level in susceptible strain HD-S. Expression analysis revealed that two of 12 candidate P450 genes, namely CYP6DW3 and CYP4C64, were significantly up-regulated in HD-Afi. Silencing CYP6DW3 and CYP4C64 by RNA interference (RNAi) substantially increased the susceptibility of whitefly adults, confirming their involvement in afidopyropen resistance. Homology modeling and molecular docking analyses demonstrated stable binding of afidopyropen to CYP6DW3 and CYP4C64, with binding free energies of –6.87 and –6.11 kcal mol^–1, respectively. The findings of this study suggest that the induction of CYP6DW3 and CYP4C64 facilitates afidopyropen detoxification, contributing to the development of resistance in B. tabaci.

Key words: Bemisia tabaci , afidopyropen , insecticide detoxification , cytochrome P450 monooxygenase

Lijun Ma, Juan Tang, Qinghe Zhang, Bingli Gao, Cheng Qu, Ran Wang, Chen Luo. 细胞色素P450基因CYP6DW3和CYP4C64参与烟粉虱MED隐种（Q型）对双丙环虫酯的抗性[J]. Journal of Integrative Agriculture, 2025, 24(5): 1905-1915.

Lijun Ma, Juan Tang, Qinghe Zhang, Bingli Gao, Cheng Qu, Ran Wang, Chen Luo. Involvement of the cytochrome P450 genes CYP6DW3 and CYP4C64 in afidopyropen resistance in Bemisia tabaci Mediterranean (Q biotype)[J]. Journal of Integrative Agriculture, 2025, 24(5): 1905-1915.

参考文献

Arthur A L, Kirkland L, Chirgwin E, van Rooyen A, Uminaa P A. 2022. Baseline susceptibility of Australian Myzus persicae (Hemiptera: Aphididae) to novel insecticides flonicamid and afidopyropen. Crop Protection, 158, 105992.

De Barro P J, Liu S S, Boykin L M, Dinsdale A B. 2011. Bemisia tabaci: A statement of species status. Annual Review of Entomology, 56, 1–19.

Basit M. 2019. Status of insecticide resistance in Bemisia tabaci: Resistance, cross-resistance, stability of resistance, genetics and fitness costs. Phytoparasitica, 47, 207–225.

Berenbaum M R, Johnson R M. 2015. Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science, 10, 51−58.

Chen X D, Ashfaq M, Stelinski L L. 2018. Susceptibility of Asian citrus psyllid, Diaphorina citri (Hemiptera: liviidae), to the insecticide afidopyropen: A new and potent modulator of insect transient receptor potential channels. Applied Entomology and Zoology, 53, 453–461.

Fujii T, Sanada-Morimura S, Oe T, Ide M, Thanh D V, Chien H V, Tuong P V, Loc P M, Cuong L Q, Liu Z W, Zhu Z R, Li J H, Wu G, Huang S H, Jr G F E, Sonoda S, Matsumuraa M. 2020. Long-term field insecticide susceptibility data and laboratory experiments reveal evidence for cross resistance to other neonicotinoids in the imidacloprid-resistant brown planthopper Nilaparvata lugens. Pest Management Science, 76, 480–486.

Guo L, Zhang Z, Xu W, Ma J Y, Liang N, Li C Y, Chu D. 2022. Expression profile of CYP402C1 and its role in resistance to imidacloprid in the whitefly, Bemisia tabaci. Insect Science, 30, 146–160.

Horowitz A R, Ghanim M, Roditakis E, Nauen R, Ishaaya I. 2020. Insecticide resistance and its management in Bemisia tabaci species. Journal of Pest Science, 93, 893–910.

Hou X A, Qiao T, Zhao Y L, Liu D. 2019. Dissipation and safety evaluation of afidopyropen and its metabolite residues in supervised cotton field. Ecotoxicology and Environmental Safety, 180, 227–233.

Joseph S V. 2020. Effect of afidopyropen against Myzus persicae (Hemiptera: Aphididae) and its predator, Adalia bipunctata (L.) in a greenhouse. Journal of Entomological Science, 55, 584–587.

Karunker I, Benting J, Lueke B, Ponge T, Nauen R, Roditakis E, Vontas J, Gorman K, Denholm I, Morin S. 2008. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochemistry and Molecular Biology, 38, 634–644.

Koch R L, da-Silva Q O, Aita R C, Hodgson E W, Potter B D, Nyoike T, EllersKirk C D. 2020. Efficacy of afidopyropen against soybean aphid (Hemiptera: Aphididae) and toxicity to natural enemies. Pest Management Science, 76, 375–383.

Leichter C A, Thompson N, Johnson B R, Scott J G. 2013. The high potency of ME-5343 to aphids is due to a unique mechanism of action. Pesticide Biochemistry and Physiology, 107, 169–176.

Liang J, Yang J, Hu J, Fu B, Gong P, Du T, Xue H, Wei X, Liu S, Huang M, Yin C, Ji Y, He C, Xie W, Wang R, Yang X, Zhang Y. 2022. Cytpchrome P450 CYP4G68 is associated with imidacloprid and thiamethoxam resistance in field whitefly, Bemisia tabaci (Hemiptera: Gennadius). Agriculture (Basel), 12, 473.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using realtime quantitative PCR and the 2–∆∆CT method. Methods, 25, 402–408.

Li X, Schuler M A, Berenbaum M R. 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52, 231–253.

Mahalanobish D, Dutta S, Roy D, Biswas A, Sarkar S, Mondal D, Gaber A, Hossain A, Sarkar P K. 2022. Field-evolved resistance and mechanisms in Bemisia tabaci Asia I to a novel pyropene insecticide, afidopyropen, in India. Crop Protection, 162, 106078.

Nauen R, Bass C, Feyereisen R, Vontas J. 2022. The role of cytochrome P450s in insect toxicology and resistance. Annual Review of Entomology, 67, 105–124.

Nauen R, Wölfel K, Lueke B, Myridakis A, Tsakireli D, Roditakis E, Tsagkarakou A, Stephanou E, Vontas J. 2015. Development of a lateral flow test to detect metabolic resistance in Bemisia tabaci mediated by CYP6CM1, a cytochrome P450 with broad spectrum catalytic efficiency. Pesticide Biochemistry and Physiology, 121, 3–11.

Nelson D R. 2018. Cytochrome P450 diversity in the tree of life. Biochimica et Biophysica Acta, 1866, 141–154.

Perier J D, Cremonez P S G, Champagne D E, Simmons A M, Riley D G. 2022. Whiteflies at the intersection of polyphagy and insecticide resistance. Annals of the Entomological Society of America, 115, 401–416.

Sabra S G, Abbas N, Hafez A M. 2023. First monitoring of resistance and corresponding mechanisms in the green peach aphid, Myzus persicae (Sulzer), to registered and unregistered insecticides in Saudi Arabia. Pesticide Biochemistry and Physiology, 194, 105504.

SPSS. 2011. Release 13.0 Version for Windows. Chicago, IL.

Wang Q, Luo C, Wang R. 2023. Insecticide resistance and its man-agement in two invasive cryptic species of Bemisia tabaci in China. International Journal of Molecular Sciences, 24, 6048.

Wang R, Che W N, Qu C, Wang J D, Luo C. 2022a. Identification and detection of CYP4G68 overexpression associated with cyantraniliprole resistance in Bemisia tabaci from China. Frontiers in Environmental Science, 10, 914636.

Wang R, Gao B, Che W, Qu C, Zhou X, Luo C. 2022b. First report of field resistance to afidopyropen, the novel pyropene insecticide, on Bemisia tabaci Mediterranean (Q Biotype) from China. Agronomy, 12, 724.

Wang R, Gao B, Zhang Q, Qu C, Luo C. 2023a. Knockdown of TRPV gene Nanchung decreases resistance to the novel pyropene insecticide, afidopyropen, in Bemisia tabaci. International Journal of Biological Macromolecules, 224, 1566–1575.

Wang R, Wang J D, Che W N, Fang Y, Luo C. 2020a. Baseline susceptibility and biochemical mechanism of resistance to flupyradifurone in Bemisia tabaci. Crop Protection, 132, 105132.

Wang R, Wang J D, Che W N, Sun Y, Li W X, Luo C. 2019. Characterization of field-evolved resistance to cyantraniliprole in Bemisia tabaci MED from China. Journal of Integrative Agriculture, 18, 2571–2578.

Wang R, Wang J, Zhang J, Che W, Feng H, Luo C. 2020b. Characterization of flupyradifurone resistance in the whitefly Bemisia tabaci Mediterranean (Q biotype). Pest Management Science, 76, 4286–4292.

Wang R, Zhang Q, Zhou X, Zhang M, Yang Q, Su Q, Luo C. 2022c. Characterization of field-evolved resistance to afidopyropen, a novel insecticidal toxin developed from microbial secondary metabolites. Bemisia tabaci. Toxins, 14, 453.

Wang R, Zhang Q H, Qu C, Wang Q, Wang J D, Luo C. 2023b. Toxicity, baseline of susceptibility, detoxifying mechanism and sublethal effects of chlorogenic acid, a potential botanical insecticide, on Bemisia tabaci. Frontiers in Plant Science, 14, 1150853.

Wei X, Hu J, Yang J, Yin C, Du T, Huang M, Fu B, Gong P, Liang J, Liu S, Xue H, He C, Ji Y, Du H, Zhang R, Wang C, Li J, Yang X, Zhang Y. 2023. Cytochrome P450 CYP6DB3 was involved in thiamethoxam and imidacloprid resistance in Bemisia tabaci Q (Hemiptera: Aleyrodidae). Pesticide Biochemistry and Physiolog, 194, 105468.

Xiao T, Lu K. 2022. Functional characterization of CYP6AE subfamily P450s associated with pyrethroid detoxification in Spodoptera litura. International Journal of Biological Macromolecules, 219, 452–462.

Xue H, Fu B, Huang M, He C, Liang J, Yang J, Wei X, Liu S, Du T, Ji Y, Yin C, Gong P, Hu J, Du H, Zhang R, Wang C, Khajehali J, Su Q, Yang X, Zhang Y. 2023. CYP6DW3 metabolizes imidacloprid to imidacloprid-urea in whitefly (Bemisia tabaci). Journal of Agricultural and Food Chemistry, 71, 2333–2343.

Yang T, Li T, Feng X, Li M, Liu S, Liu N. 2021. Multiple cytochrome P450 genes: Conferring high levels of permethrin resistance in mosquitoes, Culex quinquefasciatus. Scientific Reports, 11, 9041.

Yang X, Wei X, Yang J, Du T, Yin C, Fu B, Huang M, Liang J, Gong P, Liu S. 2021. Epitranscriptomic regulation of insecticide resistance. Science Advances, 7, eabe5903.

Yang X, Xie W, Wang S, Wu Q, Pan H, Li R, Yang N, Liu B, Xu B, Zhou X, Zhang Y. 2013. Two cytochrome P450 genes are involved in imidacloprid resistance in field populations of the whitefly, Bemisia tabaci, in China. Pesticide Biochemistry and Physiology, 107, 343–350.

Zhang Z, Shi H, Xu W, Liu J, Geng Z, Chu D, Guo L. 2021. Pymetrozine-resistant whitefly Bemisia tabaci (Gennadius) populations in China remain susceptible to afidopyropen. Crop Protection, 149, 105757.

Zhang Z, Wen Z, Li K, Xu W, Liang N, Yu X, Li C, Chu D, Guo L. 2022. Cytochrome P450 gene, CYP6CX3, is involved in the resistance to cyantraniliprole in Bemisia tabaci. Journal of Agricultural and Food Chemistry, 70, 12398–12407.

Zhou C, Cao Q, Li G, Ma D. 2020. Role of several cytochrome P450s in the resistance and cross-resistance against imidacloprid and acetamiprid of Bemisia tabaci (Hemiptera: Aleyrodidae) MEAM1 cryptic species in Xinjiang, China. Pesticide Biochemistry and Physiology, 163, 209–215.

细胞色素P450基因CYP6DW3和CYP4C64参与烟粉虱MED隐种（Q型）对双丙环虫酯的抗性

Involvement of the cytochrome P450 genes CYP6DW3 and CYP4C64 in afidopyropen resistance in Bemisia tabaci Mediterranean (Q biotype)

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics