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Voltage-gated sodium channel gene mutation and P450 gene expression are associated with the resistance of Aphis spiraecola Patch (Hemiptera: Aphididae) to lambda-cyhalothrin

Published online by Cambridge University Press:  05 January 2024

Hong-cheng Tang ,
Yu-rong Zhou ,
Jun-feng Zuo ,
Yi-xuan Wang ,
Jaime C. Piñero ,
Xiong Peng  and
Mao-hua Chen Open the ORCID record for Mao-hua Chen [Opens in a new window]
Hong-cheng Tang
Affiliation:
Department of Entomology, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Key Laboratory of Crop Pest Integrated Pest Management on the Loess Plateau of Ministry of Agriculture and Rural Affairs, Key Lab Plant Protect Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling 712100, Shaanxi, China
Yu-rong Zhou
Affiliation:
Department of Entomology, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Key Laboratory of Crop Pest Integrated Pest Management on the Loess Plateau of Ministry of Agriculture and Rural Affairs, Key Lab Plant Protect Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling 712100, Shaanxi, China
Jun-feng Zuo
Affiliation:
Department of Entomology, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Key Laboratory of Crop Pest Integrated Pest Management on the Loess Plateau of Ministry of Agriculture and Rural Affairs, Key Lab Plant Protect Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling 712100, Shaanxi, China
Yi-xuan Wang
Affiliation:
Department of Entomology, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Key Laboratory of Crop Pest Integrated Pest Management on the Loess Plateau of Ministry of Agriculture and Rural Affairs, Key Lab Plant Protect Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling 712100, Shaanxi, China
Jaime C. Piñero
Affiliation:
Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003 USA
Xiong Peng*
Affiliation:
Department of Entomology, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Key Laboratory of Crop Pest Integrated Pest Management on the Loess Plateau of Ministry of Agriculture and Rural Affairs, Key Lab Plant Protect Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling 712100, Shaanxi, China
Mao-hua Chen*
Affiliation:
Department of Entomology, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Key Laboratory of Crop Pest Integrated Pest Management on the Loess Plateau of Ministry of Agriculture and Rural Affairs, Key Lab Plant Protect Resources and Pest Management of Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling 712100, Shaanxi, China
*
Corresponding authors: Mao-hua Chen; Email: maohua.chen@nwsuaf.edu.cn; Xiong Peng; Email: pengxiong@nwsaf.edu.cn
Corresponding authors: Mao-hua Chen; Email: maohua.chen@nwsuaf.edu.cn; Xiong Peng; Email: pengxiong@nwsaf.edu.cn
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Abstract

Aphis spiraecola Patch is one of the most economically important tree fruit pests worldwide. The pyrethroid insecticide lambda-cyhalothrin is commonly used to control A. spiraecola. In this 2-year study, we quantified the resistance level of A. spiraecola to lambda-cyhalothrin in different regions of the Shaanxi province, China. The results showed that A. spiraecola had reached extremely high resistance levels with a 174-fold resistance ratio (RR) found in the Xunyi region. In addition, we compared the enzymatic activity and expression level of P450 genes among eight A. spiraecola populations. The P450 activity of A. spiraecola was significantly increased in five regions (Xunyi, Liquan, Fengxiang, Luochuan, and Xinping) compared to susceptible strain (SS). The expression levels of CYP6CY7, CYP6CY14, CYP6CY22, P4504C1-like, P4506a13, CYP4CZ1, CYP380C47, and CYP4CJ2 genes were significantly increased under lambda-cyhalothrin treatment and in the resistant field populations. A L1014F mutation in the sodium channel gene was found and the mutation rate was positively correlated with the LC50 of lambda-cyhalothrin. In conclusion, the levels of lambda-cyhalothrin resistance of A. spiraecola field populations were associated with P450s and L1014F mutations. Our combined findings provide evidence on the resistance mechanism of A. spiraecola to lambda-cyhalothrin and give a theoretical basis for rational and effective control of this pest species.

Keywords

Aphis spiraecolalambda-cyhalothrinP450sodium channeltoxicity

Information

Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 1 , February 2024 , pp. 49 - 56
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Copyright
Copyright © Northwest A&F University, 2024. Published by Cambridge University Press

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References

Barres, B, Micoud, A, Corio-Costet, MF, Debieu, D, Fillinger-David, S, Walker, AS, Délye, C, Grosman, J and Siegwart, M (2016) Trends and challenges in pesticide resistance detection. Trends in Plant Science 21, 834–853.Google Scholar
Bass, C, Puinean, AM, Zimmer, CT, Denholm, I, Field, LM, Foster, SP, Gutbrod, O, Nauen, R, Slater, R and Williamson, MS (2014) The evolution of pesticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology 51, 41–51.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of micro-gram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle Scholar
CABI (2022) ‘Aphis spiraecola (Spirea aphid)’, CABI Compendium. CABI International. https://doi.org/10.1079/cabicompendium.6221.CrossRefGoogle Scholar
Chen, XW, Li, F, Chen, AQ, Ma, KS, Liang, P, Liu, Y, Song, DL and Gao, XW (2016) Both point mutations and low expression levels of the nicotinic acetylcholine receptor β1 subunit are associated with imidacloprid resistance in an Aphis gossypii. (Glover) population from a Bt cotton field in China. Pesticide Biochemistry and Physiology 141, 1–8.CrossRefGoogle Scholar
Chen, XW, Tie, MY, Chen, AQ, Ma, KS, Li, F, Liang, PZ, Liu, Y, Song, DL and Gao, XW (2017) Pyrethroid resistance associated with M918L mutation and detoxifying metabolism in Aphis gossypii from Bt cotton growing regions of China. Pest Management Science 73, 2353–2359.CrossRefGoogle Scholar
Dong, K, Du, Y, Rinkevich, F, Nomura, Y, Xu, P, Wang, L, Silver, K and Zhorov, BS (2014) Molecular biology of insect sodium channels and pyrethroid resistance. Insect Biochemistry and Molecular Biology 50, 1–17.CrossRefGoogle ScholarPubMed
Eastop, VF and Blackman, RL (1988) The identity of Aphis citricola van der Goot. Systematic Entomology 13, 157–160.CrossRefGoogle Scholar
Eleftherianos, I, Foster, SP, Williamson, MS and Denholm, I (2008) Characterization of the M918T sodium channel gene mutation associated with strong resistance to pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer). Bulletin of Entomological Research 98, 183–191.CrossRefGoogle ScholarPubMed
Fan, JQ, Han, PF, Gao, Y, Liu, ZF, Zhang, PJ, Yang, J and Fan, RJ (2019) Expression of the cytochrome P450 gene AcCYP6CY14 and its role in imidacloprid resistance in Aphis citricola. Chinese Journal of Applied Entomology 56, 298–306.Google Scholar
Field, LM, Davies, TE, O'Reilly, AO, Williamson, MS and Wallace, BA (2017) Voltage-gated sodium channels as targets for pyrethroid insecticides. European Biophysics Journal 46, 675–679.CrossRefGoogle ScholarPubMed
Fontaine, S, Caddoux, L, Brazier, C, Bertho, C, Bertolla, P, Micoud, A and Roy, L (2011) Uncommon associations in target resistance among French populations of Myzus persicae from oilseed rape crops. Pest Management Science 67, 881–885.CrossRefGoogle ScholarPubMed
Foster, SP, Paul, VL, Slater, R, Warren, A, Denholm, I, Field, LM and Williamson, MS (2014) A mutation (L1014F) in the voltage-gated sodium channel of the grain aphid, Sitobion avenae, is associated with resistance to pyrethroid insecticides. Pest Management Science 70, 1249–1253.CrossRefGoogle ScholarPubMed
Guillemaud, T, Brun, A, Anthony, N, Sauge, MH, Boll, R, Delorme, R, Fournier, D, Lapchin, L and Vanlerberghe-Masutti, F (2003) Incidence of insecticide resistance alleles in sexually-reproducing populations of the peach-potato aphid Myzus persicae (Hemiptera: Aphididae) from southern France. Bulletin of Entomological Research 93, 289–297.CrossRefGoogle ScholarPubMed
Hu, C, Liu, JY, Wang, W, Mota-Sanchez, D, He, S, Shi, Y and Yang, XQ (2022a) Glutathione S-Transferase genes are involved in lambda-cyhalothrin resistance in Cydia pomonella via sequestration. Journal of Agricultural and Food Chemistry 70, 2265–2279.CrossRefGoogle ScholarPubMed
Hu, GL, Lu, LY, Li, YS, Su, X, Dong, WY, Zhang, BZ, Liu, RQ, Shi, MW, Wang, HL and Chen, XL (2022b) CYP4CJ6-mediated resistance to two neonicotinoid insecticides in Sitobion miscanthi (Takahashi). Bulletin of Entomological Research 112, 646–655.CrossRefGoogle ScholarPubMed
Li, MY, Li, XA, Wang, C, Li, QC, Zhu, SG, Zhang, YH, Li, XR, Yang, FS and Zhu, X (2021) Selection and validation of reference genes for qRT-PCR analysis of Rhopalosiphum padi (Hemiptera: Aphididae). Frontiers in Physiology 12, 663338.CrossRefGoogle ScholarPubMed
Litchfield, J and Wilcoxon, F (1949) A simplified method of evaluating dose-effect experiments. Journal of Pharmacology and Experimental Therapeutics 96, 99–113.Google ScholarPubMed
Liu, N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annual Review of Entomology 60, 537–559.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT methods. Methods (San Diego, Calif.) 25, 402–408.CrossRefGoogle Scholar
Margaritopoulos, JT, Kati, AN, Voudouris, CC, Skouras, PJ and Tsitsipis, JA (2021) Long-term studies on the evolution of resistance of Myzus persicae (Hemiptera: Aphididae) to insecticides in Greece. Bulletin of Entomological Research 111, 1–16.CrossRefGoogle ScholarPubMed
Martinez-Torres, C, Foster, SP, Field, LM, Devonshire, AL and Williamson, MS (1999) A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Insect Molecular Biology 8, 339–346.CrossRefGoogle ScholarPubMed
Mingeot, D, Hautier, L and Jansen, JP (2021) Structuration of multilocus genotypes associated with insecticide resistance of the peach potato aphid, Myzus persicae (Sulzer), in potato fields in southern Belgium. Pest Management Science 77, 482–491.CrossRefGoogle ScholarPubMed
Mu, SM, Liu, ZD, Kong, FH, Gao, XW, Shi, AJ and Qiu, YQ (2002) Studies on apple yield loss rate and economic threshold caused by Aphis citricola. Journal of Shandong Agricultural University (Natural Science) 33, 87–88+100.Google Scholar
Munkhbayar, O, Liu, N, Li, M and Qiu, XH (2021) First report of voltage-gated sodium channel M918V and molecular diagnostics of nicotinic acetylcholine receptor R81T in the cotton aphid. Journal of Applied Entomology 145, 261–269.CrossRefGoogle Scholar
Nasuti, C, Cantalamessa, F, Falcioni, G and Gabbianelli, R (2003) Different effects of type I and type II pyrethroids on erythrocyte plasma membrane properties and enzymatic activity in rats. Toxicology 191, 233–244.CrossRefGoogle ScholarPubMed
Pavlidi, N, Vontas, J and Van Leeuwen, T (2018) The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests and disease vectors. Current Opinion in Insect Science 27, 97–102.CrossRefGoogle ScholarPubMed
Peng, TF, Pan, YO, Yang, C, Gao, XW, Xi, JH, Wu, YQ, Huang, X, Zhu, E, Xin, XC, Zhan, C and Shang, QL (2016) Over-expression of CYP6A2 is associated with spirotetramat resistance and cross-resistance in the resistant strain of Aphis gossypii Glover. Pesticide Biochemistry and Physiology 126, 64–69.CrossRefGoogle ScholarPubMed
Rinkevich, FD, Du, YZ and Dong, K (2013) Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pesticide Biochemistry and Physiology 106, 93–100.CrossRefGoogle ScholarPubMed
Scott, JG (2019) Life and death at the voltage-sensitive sodium channel: evolution in response to insecticide use. Annual Review of Entomology 64, 243–257.CrossRefGoogle ScholarPubMed
Scott, JG, Yoshimizu, MH and Kasai, S (2015) Pyrethroid resistance in Culex pipiens mosquitoes. Pesticide Biochemistry and Physiology 120, 68–76.CrossRefGoogle ScholarPubMed
Shen, JL and Wu, YD (1995) Insecticide Resistance in Cotton Bollworm and its Management. Beijing, China: China Agricultural Press, pp. 259–280.Google Scholar
Soderlund, DM and Bloomquist, JR (1989) Neurotoxic actions of pyrethroid insecticides. Annual Review of Entomology 34, 77–96.CrossRefGoogle ScholarPubMed
Su, S, Jian, CZ, Zhang, XH, Fang, SS, Peng, X, Piñero, JC and Chen, MH (2021) Sublethal effects of abamectin on the development, reproduction, detoxification enzyme activity, and related gene expression of the oriental fruit moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 114, 2430–2438.CrossRefGoogle ScholarPubMed
Tang, QL, Ma, KS, Hou, YM and Gao, XW (2017) Monitoring insecticide resistance and diagnostics of resistance mechanisms in the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) in China. Pesticide Biochemistry and Physiology 143, 39–47.CrossRefGoogle ScholarPubMed
Vontas, JG, Small, GJ and Hemingway, J (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal 357, 65–72.CrossRefGoogle ScholarPubMed
Wang, K, Huang, YN, Li, XY and Chen, MH (2018) Functional analysis of a carboxylesterase gene associated with sporocarp and cyhalothrin resistance in Rhopalosiphum padi (L.). Frontiers in Physiology 9, 992.CrossRefGoogle Scholar
Wang, ZG, Jiang, SS, Mota-Sanchez, D, Wang, W, Li, XR, Gao, YL, Lu, XP and Yang, XQ (2019) Cytochrome P450-mediated λ-cyhalothrin-resistance in a field strain of Helicoverpa armigera from northeast China. Journal of Agricultural and Food Chemistry 67, 3546–3553.CrossRefGoogle Scholar
Wang, K, Bai, JY, Zhao, JN, Su, S, Liu, L, Han, ZJ and Chen, MH (2020) Super-kdr mutation M918L and multiple cytochrome P450s associated with the resistance of Rhopalosiphum padi to pyrethroid. Pest Management Science 76, 2809–2817.CrossRefGoogle ScholarPubMed
Wang, ZJ, Liang, CR, Shang, ZY, Yu, QT and Xue, CB (2021) Insecticide resistance and resistance mechanisms in the melon aphid, Aphis gossypii, in Shandong, China. Pesticide Biochemistry and Physiology 172, 104768.CrossRefGoogle ScholarPubMed
Wang, K, Zhao, JN, Han, ZJ and Chen, MH (2022) Comparative transcriptome and RNA interference reveal CYP6DC1 and CYP380C47 related to lambda-cyhalothrin resistance in Rhopalosiphum padi. Pesticide Biochemistry and Physiology 183, 105088.CrossRefGoogle ScholarPubMed
Wei, ZH, Liu, M, Hu, C and Yang, XQ (2020) Overexpression of glutathione S-transferase genes in field lambda-cyhalothrin-resistant population of Cydia pomonella: reference gene selection and expression analysis. Journal of Agricultural and Food Chemistry 68, 5825–5834.CrossRefGoogle ScholarPubMed
Wolfe, R and Hanley, J (2002) If we're so different why do we keep overlapping? When 1 plus 1 doesn't make 2. Canadian Medical Association Journal 166, 65–66.Google ScholarPubMed
Xi, JH, Pan, YO, Bi, R, Gao, XW, Chen, XW, Peng, TF, Zhang, M, Zhang, H, Hu, XY and Shang, QL (2015) Elevated expression of esterase and cytochrome P450 are related with lambda-cyhalothrin resistance and lead to cross resistance in Aphis glycines Matsumura. Pesticide Biochemistry and Physiology 118, 77–81.CrossRefGoogle ScholarPubMed
Yang, XQ and Zhang, YL (2015) Investigation of insecticide-resistance status of Cydia pomonella in Chinese populations. Bulletin of Entomological Research 105, 316–325.CrossRefGoogle ScholarPubMed
Zhang, YL, Wang, LH, Guo, HF, Li, GQ, Zhang, ZC, Xie, L and Fang, JC (2012) A transcriptome-based screen of carboxylesterase-like genes that are involved in chlorpyrifos resistance in Laodelphax striatellus (fallén). Pesticide Biochemistry and Physiology 104, 224–228.CrossRefGoogle Scholar
Zuo, YY, Peng, X, Wang, K, Lin, FF, Li, YT and Chen, MH (2016a) Expression patterns, mutation detection, and RNA interference of Rhopalosiphum padi voltage-gated sodium channel genes. Scientific Reports 6, 30166.CrossRefGoogle ScholarPubMed
Zuo, YY, Wang, K, Zhang, M, Peng, X, Piñero, JC and Chen, MH (2016b) Regional susceptibilities of Rhopalosiphum padi (Hemiptera: Aphididae) to ten insecticides. Florida Entomologist 99, 269–275.CrossRefGoogle Scholar
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