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CYP4CJ6-mediated resistance to two neonicotinoid insecticides in Sitobion miscanthi (Takahashi)

Published online by Cambridge University Press:  17 February 2022

Gui-Lei Hu
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Liu-Yang Lu
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Ya-She Li
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Xu Su
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Wen-Yang Dong
Affiliation:
Department of Entomology, China Agricultural University, Beijing 100193, P.R. China
Bai-Zhong Zhang*
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Run-Qiang Liu
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Ming-Wang Shi
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Hong-Liang Wang
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
Xi-Ling Chen
Affiliation:
College of Resources and Environment, Henan Engineering Research Center of Biological Pesticide & Fertilizer Development and Synergistic Application, Henan Institute of Science and Technology, Xinxiang 453003, P.R. China
*
Author for correspondence: Bai-Zhong Zhang, Email: baizhongok@163.com

Abstract

The wheat aphid Sitobion miscanthi (CWA) is an important harmful pest in wheat fields. Insecticide application is the main method to effectively control wheat aphids. However, CWA has developed resistance to some insecticides due to its extensive application, and understanding resistance mechanisms is crucial for the management of CWA. In our study, a new P450 gene, CYP4CJ6, was identified from CWA and showed a positive response to imidacloprid and thiamethoxam. Transcription of CYP4CJ6 was significantly induced by both imidacloprid and thiamethoxam, and overexpression of CYP4CJ6 in the imidacloprid-resistant strain was also observed. The sensitivity of CWA to these two insecticides was increased after the knockdown of CYP4CJ6. These results indicated that CYP4CJ6 could be associated with CWA resistance to imidacloprid and thiamethoxam. Subsequently, the posttranscriptional regulatory mechanism was assessed, and miR-316 was confirmed to participate in the posttranscriptional regulation of CYP4CJ6. These results are crucial for clarifying the roles of P450 in the resistance of CWA to insecticides.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Asgari, S (2013) MicroRNA functions in insects. Insect Biochemistry and Molecular Biology 43, 388397.CrossRefGoogle ScholarPubMed
Betel, D, Wilson, M, Gabow, A, Marks, DS and Sander, C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Research 36, 149153.CrossRefGoogle ScholarPubMed
Brandt, A, Scharf, M, Pedra, JHF, Holmes, G, Dean, A, Kreitman, M and Pittendrigh, BR (2002) Differential expression and induction of two Drosophila cytochrome P450 genes near the Rst (2) DDT locus. Insect Molecular Biology 11, 337341.CrossRefGoogle ScholarPubMed
Broackes-Carter, FC, Nathalie, M, Deborah, G, Stephen, H, John, B and Ann, H (2002) Temporal regulation of CFTR expression during ovine lung development: implications for cf gene therapy. Human Molecular Genetics 2, 125.CrossRefGoogle Scholar
Buckingham, S, Lapied, B, Corronc, H and Sattelle, F (1997) Imidacloprid actions on insect neuronal acetylcholine receptors. Journal of Experimental Biology 200, 26852692.CrossRefGoogle ScholarPubMed
Byrne, FJ and Toscano, NC (2007) Lethal toxicity of systemic residues of imidacloprid against Homalodisca vitripennis (Homoptera: Cicadellidae) eggs and its parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae). Biological Control 43, 130135.CrossRefGoogle Scholar
Chen, X, Xia, X, Wang, H, Qiao, K and Wang, K (2013) Cross–resistance to clothianidin and acetamiprid in the imidacloprid resistant strain of Aphis gossypii (Hemiptera: Aphididae) and the related enzyme mechanisms. Acta Entomologica Sinica 56, 11431151.Google Scholar
Chen, XD, Ebert, TA, Pelz-Stelinski, KS and Stelinski, LL (2020) Fitness costs associated with thiamethoxam and imidacloprid resistance in three field populations of Diaphorina citri (Hemiptera: Liviidae) from Florida. Bulletin of Entomological Research 110, 512520.CrossRefGoogle ScholarPubMed
Choi, YM, An, S, Lee, EM, Kim, K, Choi, SJ, Kim, JS, Jang, HH, An, IS and Bae, S (2012) CYP1A1 is a target of miR-892a-mediated post-transcriptional repression. International Journal of Oncology 41, 331336.Google ScholarPubMed
Cui, L, Sun, L, Yang, D, Yan, X and Yuan, H (2012) Effects of cycloxaprid, a novel cis–nitromethylene neonicotinoid insecticide, on the feeding behaviour of Sitobion avenae. Pest Management Science 68, 14841491.CrossRefGoogle ScholarPubMed
Devine, GJ, Harling, ZK, Scarr, AW and Devonshire, AL (1996) Lethal and sublethal effects of imidacloprid on nicotine–tolerant Myzus nicotianae and Myzus persicae. Pesticide Science 48, 5762.3.0.CO;2-9>CrossRefGoogle Scholar
Duan, X, Peng, X, Qiao, X and Chen, M (2016) Life cycle and population genetics of bird cherry–oat aphids Rhopalosiphum padi in China: an important pest on wheat crops. Journal of Pest Science 90, 114.Google Scholar
Enright, AJ, John, B, Gaul, U, Tuschl, T, Sander, C and Marks, DS (2003) MicroRNA targets in Drosophila. Genome Biology 5, R1.CrossRefGoogle ScholarPubMed
George, KS and Gair, R (2010) Crop loss assessment on winter wheat attacked by the grain aphid, Sitobion avenae (F.). Plant Pathology 28, 143149.CrossRefGoogle Scholar
Goff, GL, Hilliou, F, Siegfried, BD, Boundy, S, Wajnberg, E, Sofer, L, Audant, P, ffrench-Constant, RH and Feyereisen, R (2006) Xenobiotic response in Drosophila melanogaster: sex dependence of P450 and GST gene induction. Insect Biochemistry and Molecular Biology 36, 674682.CrossRefGoogle ScholarPubMed
Gong, YH, Yu, XR, Shang, QL, Shi, XY and Gao, XW (2014) Oral delivery mediated RNA interference of a carboxylesterase gene results in reduced resistance to organophosphorus insecticides in the cotton aphid, Aphis gossypii glover. PLoS One 9, e102823.CrossRefGoogle ScholarPubMed
Harrison, TL, Zangerl, AR, Schuler, MA and Berenbaum, MR (2001) Developmental variation in cytochrome P450 expression in Papilio polyxenes in response to xanthotoxin, a hostplant allelochemical. Archives of Insect Biochemistry and Physiology 48, 179189.CrossRefGoogle ScholarPubMed
Hirata, K, Kiyota, R, Matsuura, A, Toda, S, Yamamoto, A and Iwasa, T (2015) Association between the R81T mutation in the nicotinic acetylcholine receptor β1 subunit of Aphis gossypii and the differential resistance to acetamiprid and imidacloprid. Journal of Pesticide Science 41, 2531.CrossRefGoogle Scholar
Hirata, K, Jouraku, A, Kuwazaki, S, Kanazawa, J and Iwasa, T (2017) The R81T mutation in the nicotinic acetylcholine receptor of Aphis gossypii is associated with neonicotinoid insecticide resistance with differential effects for cyano-and nitro-substituted neonicotinoids. Pesticide Biochemistry and Physiology 143, 5765.CrossRefGoogle ScholarPubMed
Hong, S, Guo, Q, Wang, W, Hu, S, Fang, F, Lv, Y, Yu, J, Zou, F, Lei, Z, Ma, K, Ma, L, Zhou, D, Sun, Y, Zhang, D, Shen, B and Zhu, C (2014) Identification of differentially expressed microRNAs in Culex pipiens and their potential roles in pyrethroid resistance. Insect Biochemistry and Molecular Biology 55, 3950.CrossRefGoogle ScholarPubMed
Hu, Z, Lin, Q, Chen, H, Li, Z, Yin, F and Feng, X (2014) Identification of a novel cytochrome P450 gene, CYP321E1 from the diamondback moth, Plutella xylostella (L.) and RNA interference to evaluate its role in chlorantraniliprole resistance. Bulletin of Entomological Research 104, 716723.CrossRefGoogle ScholarPubMed
Hu, XS, Liu, XF, Thieme, T, Zhang, GS, Liu, TX and Zhao, HY (2015) Testing the fecundity advantage hypothesis with Sitobion avenae, Rhopalosiphum padi, and Schizaphis graminum (hemiptera: aphididae) feeding on ten wheat accessions. Scientific Report 5, 18549.CrossRefGoogle ScholarPubMed
Jiang, X, Zhang, Q, Qin, Y, Yin, H, Zhang, S, Li, Q, Zhang, Y, Fan, J and Chen, J (2019) A chromosome-level draft genome of the grain aphid Sitobion miscanthi. Gigascience 8, giz101.CrossRefGoogle ScholarPubMed
Jones, CM, Daniels, M, Andrews, M, Slater, R, Lind, RJ, Gorman, K and Denholm, I (2011) Age-specific expression of a P450 monooxygenase (CYP6CM1) correlates with neonicotinoid resistance in Bemisia tabaci. Pesticide Biochemistry and Physiology 101, 5358.10.1016/j.pestbp.2011.07.004CrossRefGoogle Scholar
Karunker, I, Benting, J, Lueke, B, Ponge, T, Nauen, R, Roditakis, E and 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, 634644.CrossRefGoogle Scholar
Kim, JI, Kwon, M, Ki, GH, Kim, SY and Lee, SH (2015) Two mutations in nAChR beta subunit is associated with imidacloprid resistance in the Aphis gossypii. Journal of Asia–Pacific Entomology 18, 291296.CrossRefGoogle Scholar
Lei, Z, Lv, Y, Wang, W, Guo, Q, Zou, F, Hu, S, Fang, F, Tian, M, Liu, B, Liu, X, Ma, K, Ma, L, Zhou, D, Zhang, D, Sun, Y, Shen, B and Zhu, C (2015) MiR-278-3p regulates pyrethroid resistance in Culex pipiens pallens. Parasitology Research 114, 699706.CrossRefGoogle ScholarPubMed
Li, XC, Schuler, MA and Berenbaum, MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231253.CrossRefGoogle ScholarPubMed
Li, Y, Xu, Z, Shi, L, Shen, G and He, L (2016) Insecticide resistance monitoring and metabolic mechanism study of the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in Chongqing, China. Pesticide Biochemistry and Physiology 132, 2128.CrossRefGoogle Scholar
Liu, ZW, Han, ZJ, Wang, Y, Zhang, L, Zhang, H and Liu, C (2003) Selection for imidacloprid resistance in Nilaparvata lugens: cross–resistance patterns and possible mechanisms. Pest Management Science 59, 770775.Google Scholar
Liu, N, Li, M, Gong, Y, Liu, F and Li, T (2015) Cytochrome P450s-their expression, regulation, and role in insecticide resistance. Pesticide Biochemistry and Physiology 120, 7781.CrossRefGoogle ScholarPubMed
Lu, Y and Gao, X (2009) Multiple mechanisms responsible for differential susceptibilities of Sitobion avenae (Fabricius) and Rhopalosiphum padi (Linnaeus) to pirimicarb. Bulletin of Entomological Research 99, 611617.CrossRefGoogle Scholar
Ma, K, Li, F, Liu, Y, Liang, P, Chen, X and Gao, X (2017) Identification of microRNAs and their response to the stress of plant allelochemicals in Aphis gossypii (Hemiptera: Aphididae). BMC Molecular Biology 18, 5.CrossRefGoogle Scholar
Ma, K, Li, F, Tang, Q, Liang, P, Liu, Y, Zhang, B and Gao, X (2019 a) CYP4CJ1-mediated gossypol and tannic acid tolerance in Aphis gossypii glover. Chemosphere 219, 961970.CrossRefGoogle ScholarPubMed
Ma, K, Tang, Q, Zhang, B, Liang, P, Wang, B and Gao, X (2019 b) Overexpression of multiple cytochrome P450 genes associated with sulfoxaflor resistance in Aphis gossypii Glover. Pesticide Biochemistry and Physiology 157, 204210.CrossRefGoogle ScholarPubMed
Mezei, I, Bielza, P, Siebert, MW, Torne, M, Gomez, LE, Valverde-Garcia, P, Belando, A, Moreno, I, Grávalos, C, Cifuentes, D and Sparks, TC (2020) Sulfoxaflor efficacy in the laboratory against imidacloprid-resistant and susceptible populations of the green peach aphid, Myzus persicae: impact of the R81T mutation in the nicotinic acetylcholine receptor. Pesticide Biochemistry and Physiology 166, 104582.CrossRefGoogle ScholarPubMed
Mohammed, BR, Wilding, CS, Collier, PJ and Deeni, YY (2014) Cloning of Anopheles gambiae CYP6M2 gene promoter and construction of its luciferase reporter system. International Journal of Energy Research 3, 259264.Google Scholar
Peng, TF, Pan, YO, Gao, XW, Xi, JH, Zhang, L, Ma, KS, Wu, Y, Zhang, J and Shang, QL (2016) Reduced abundance of the CYP6CY3-targeting let-7 and miR-100 miRNAs accounts for host adaptation of Myzus persicae nicotianae. Insect Biochemistry and Molecular Biology 75, 8997.CrossRefGoogle ScholarPubMed
Pfaffl, MW (2001) A new mathematical model for relative quantification in real–time RT–PCR. Nucleic Acids Research 29, 4545.CrossRefGoogle ScholarPubMed
Pritchard, CC, Cheng, HH and Tewari, M (2012) MicroRNA profifiling: approaches and considerations. Nature Reviews Genetics 13, 358369.CrossRefGoogle Scholar
Puinean, AM, Foster, SP, Oliphant, L, Denholm, I, Field, LM, Millar, NS, Williamson, MS and Bass, C (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genetics 6, 1000999.CrossRefGoogle ScholarPubMed
Rehmsmeier, M, Steffen, P, Hochsmann, M and Giegerich, R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10, 15071517.CrossRefGoogle ScholarPubMed
Roat, TC, Santos-Pinto, JRAP, Miotelo, L, de Souza, CL, Palma, MS and Malaspina, O (2020) Using a toxicoproteomic approach to investigate the effects of thiamethoxam into the brain of Apis mellifera. Chemosphere 258, 127362.CrossRefGoogle ScholarPubMed
Schuld, M and Schmuck, R (2000) Effects of thiacloprid, a new chloronicotinyl insecticide, on the egg parasitoid Trichogramma cacoeciae. Ecotoxicology 9, 197205.CrossRefGoogle Scholar
Schuler, MA (2011) P450s in plant-insect interactions. BBA-Proteins Proteom 1814, 3645.CrossRefGoogle ScholarPubMed
Schuler, MA (2012) Insect P450s: mounted for battle in their war against toxins. Molecular Ecology 21, 41574159.CrossRefGoogle ScholarPubMed
Shi, YY, Zheng, HJ, Pan, QZ, Wang, ZL and Zeng, ZJ (2015) Differentially expressed microRNAs between queen and worker larvae of the honey bee (Apis mellifera). Apidologi 46, 3545.CrossRefGoogle Scholar
Sial, MU, Zhao, Z, Zhang, L, Zhang, Y, Mao, L and Jiang, H (2020) Loop-mediated isothermal amplification for the detection of R81T mutation in nAChR with crude genomic DNA extracted from individual Myzus persicae. Journal of Pest Science 93, 531541.CrossRefGoogle Scholar
Tamasi, V, Monostory, K, Prough, RA and Falus, A (2011) Role of xenobiotic metabolism in cancer: involvement of transcriptional and miRNA regulation of P450s. Cellular and Molecular Life Sciences 68, 11311146.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, 3947.CrossRefGoogle ScholarPubMed
Tavares, DA, Roat, TC, Carvalho, SM, Silva-Zacarin, ECM and Malaspina, O (2015) In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere 135, 370378.CrossRefGoogle Scholar
Tian, F, Li, C, Wang, Z, Liu, J and Zeng, X (2019) Identification of detoxification genes in imidacloprid-resistant Asian Citrus psyllid (Hemiptera:Lividae) and their expression patterns under stress of eight insecticides. Pest Management Science 75, 14001410.CrossRefGoogle ScholarPubMed
Wang, MF, Yuan, GH, Chen, JL, Lei, Z and Wu, Z (2006) Research advances of occurrence pattern damage characteristics of wheat aphid and resistance identification of wheat. Journal of Hennan Agricultural Sciences 7, 5860.Google Scholar
Wang, HY, Yang, Y, Su, JY, Shen, JL, Gao, CF and Zhu, YC (2008) Assessment of the impact of insecticides on Anagrus nilaparvatae (Pang et Wang) (Hymenoptera: Mymanidae), an egg parasitoid of the rice planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Crop Protection 27, 514522.CrossRefGoogle Scholar
Wang, G, Cui, LL, Jie, D, Francis, F, Yong, L and Tooker, J (2011) Combining intercropping with semiochemical releases: optimization of alternative control of Sitobion avenae in wheat crops in China. Entomologia Experimentalis Et Applicata 140, 189195.CrossRefGoogle Scholar
Wang, NX, Watson, GB, Loso, MR and Sparks, TC (2016) Molecular modeling of sulfoxaflor and neonicotinoid binding in insect nicotinic acetylcholine receptors: impact of the Myzus β1 R81T mutation. Pest Management Science 72, 14671474.CrossRefGoogle ScholarPubMed
Wang, K, Zhang, M, Huang, Y, Yang, Z, Su, S and Chen, M (2018) Characterisation of imidacloprid resistance in the bird cherry–oat aphid, Rhopalosiphum padi, a serious pest on wheat crops. Pest Management Science 74, 14571465.CrossRefGoogle ScholarPubMed
Xu, L, Wu, M and Han, ZJ (2014) Biochemical and molecular characterisation and cross–resistance in field and laboratory chlorpyrifos–resistant strains of Laodelphax striatellus (Hemiptera: Delphacidae) from eastern China. Pest Management Science 70, 11181129.CrossRefGoogle ScholarPubMed
Yang, EC, Chang, HC, Wu, WY and Chen, YW (2012) Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS One 7, e49472.CrossRefGoogle ScholarPubMed
Zhang, X, Zheng, Y, Cao, X, Ren, R, Yu, X and Jiang, H (2015) Identification and profiling of Manduca sexta microRNAs and their possible roles in regulating specific transcripts in fat body, hemocytes, and midgut. Insect Biochemistry and Molecular Biology 62, 1122.CrossRefGoogle ScholarPubMed
Zhang, BZ, Kong, FC, Cui, RK and Zeng, XN (2016 a) Gene expression of detoxification enzymes in insecticide-resistant and insecticide-susceptible Bemisia tabaci strains after diafenthiuron exposure. Journal of Agricultural Science 154, 742753.CrossRefGoogle Scholar
Zhang, B, Kong, F, Wang, H, Gao, X, Zeng, X and Shi, X (2016 b) Insecticide induction of o-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren). Journal of Integrative Agriculture 15, 135144.CrossRefGoogle Scholar
Zhang, BZ, Ma, KS, Liu, JJ, Lu, LY, Chen, XL, Zhang, SP and Gao, XW (2019) Differential expression of genes in greenbug (Schizaphis graminum Rondani) treated by imidacloprid and RNA interference. Pest Management Science 75, 17261733.CrossRefGoogle ScholarPubMed
Zhang, B, Su, X, Xie, L, Zhen, C, Hu, G, Jiang, K, Huang, ZY, Liu, R, Gao, Y, Chen, X and Gao, X (2020) Multiple detoxification genes confer imidacloprid resistance to Sitobion avenae Fabricius. Crop Protection 128, 105014.CrossRefGoogle Scholar
Zhang, B, Hu, G, Lu, L, Hu, S, Li, Y, Su, X, Dong, W, Zhen, C, Liu, R, Kong, F, Shi, M and Chen, X (2021) Identification of differentially expressed micrornas under imidacloprid exposure in sitobion miscanthi. Pesticide Biochemistry and Physiology 177, 104885.CrossRefGoogle ScholarPubMed
Zhou, H, Chen, J, Liu, Y, Frédéric, F, Eric, H, Claude, B, Sun, JR and Cheng, D (2013) Influence of garlic intercropping or active emitted volatiles in releasers on aphid and related beneficial in wheat fields in China. Journal of Integrative Agriculture 12, 467473.CrossRefGoogle Scholar