Molecular mechanism of ATP-binding cassette transporter-mediated insecticide resistance

Yuntong Lv , Pengcheng Wang , Zihan Wei , Xueqing Yang

New Plant Protection ›› 2025, Vol. 2 ›› Issue (3) : e70018

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New Plant Protection ›› 2025, Vol. 2 ›› Issue (3) : e70018 DOI: 10.1002/npp2.70018
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Molecular mechanism of ATP-binding cassette transporter-mediated insecticide resistance

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Abstract

The growing problem of insecticide resistance poses a significant challenge to agricultural productivity. Investigations into the resistance mechanisms mediated by ATP-binding cassette (ABC) transporters have garnered considerable attention within toxicological research. Several ABC transporter subfamilies have been implicated in conferring resistance to both organosynthetic insecticides and Bacillus thuringiensis toxins. Research into insecticide resistance has broadened beyond gene expression analysis, including epigenetic modifications, cellular biology, and protein binding and transport dynamics. The advancement of RNA interference and CRISPR/Cas9 gene editing technologies has accelerated the functional analysis of ABC transporter genes. Furthermore, the emergence of artificial intelligence, such as AlphaFold 3.0, offers unprecedented opportunities for predicting the three-dimensional structures of these proteins, potentially elucidating the specific interactions between ABC transporters and insecticides. This review summarizes the recent advancements in the methodologies for functional analysis of ABC transporters, the molecular mechanisms underlying ABC transporter-mediated insecticide resistance, and the regulatory pathways governing resistance genes in insects. It aims to provide a theoretical foundation for comprehensively understanding the mechanisms of insecticide resistance in insects, and also offering novel insights for the development of innovative and effective resistance management strategies.

Keywords

ABC transporter / metabolic detoxification / regulation of gene expression / resistance mechanism / transport mechanism

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Yuntong Lv, Pengcheng Wang, Zihan Wei, Xueqing Yang. Molecular mechanism of ATP-binding cassette transporter-mediated insecticide resistance. New Plant Protection, 2025, 2(3): e70018 DOI:10.1002/npp2.70018

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References

[1]

Higgins, C. F. (1992). ABC transporters: From microorganisms to man. Annual Review of Cell Biology, 8(1), 67-113. https://doi.org/10.1146/annurev.cb.08.110192.000435

[2]

Dean, M., & Allikmets, R. (1995). Evolution of ATP-binding cassette transporter genes. Current Opinion in Genetics & Development, 5(6), 779-785. https://doi.org/10.1016/0959-437X(95)80011-S

[3]

Linton, K. J., & Higgins, C. F. (2007). Structure and function of ABC transporters: The ATP switch provides flexible control. Pflügers Archiv-European Journal of Physiology, 453(5), 555-567. https://doi.org/10.1007/s00424-006-0126-x

[4]

Higgins, C. F., & Linton, K. J. (2004). The ATP switch model for ABC transporters. Nature Structural & Molecular Biology, 11(10), 918-926. https://doi.org/10.1038/nsmb836

[5]

Hyde, S. C., Emsley, P., Hartshorn, M. J., Mimmack, M. M., Gileadi, U., Pearce, S. R., Gallagher, M. P., Gill, D. R., Hubbard, R. E., & Higgins, C. F. (1990). Structural model of ATP-binding proteing associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature, 346(6282), 362-365. https://doi.org/10.1038/346362a0

[6]

Oldham, M. L., Davidson, A. L., & Chen, J. (2008). Structural insights into ABC transporter mechanism. Current Opinion in Structural Biology, 18(6), 726-733. https://doi.org/10.1016/j.sbi.2008.09.007

[7]

Hollenstein, K., Dawson, R. J., & Locher, K. P. (2007). Structure and mechanism of ABC transporter proteins. Current Opinion in Structural Biology, 17(4), 412-418. https://doi.org/10.1016/j.sbi.2007.07.003

[8]

Rees, D. C., Johnson, E., & Lewinson, O. (2009). ABC transporters: The power to change. Nature Reviews Molecular Cell Biology, 10(3), 218-227. https://doi.org/10.1038/nrm2646

[9]

Leslie, E. M., Deeley, R. G., & Cole, S. P. C. (2005). Multidrug resistance proteins: Role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicology and Applied Pharmacology, 204(3), 216-237. https://doi.org/10.1016/j.taap.2004.10.012

[10]

Dermauw, W., & Van Leeuwen, T. (2014). The ABC gene family in arthropods: Comparative genomics and role in insecticide transport and resistance. Insect Biochemistry and Molecular Biology, 45, 89-110. https://doi.org/10.1016/j.ibmb.2013.11.001

[11]

Berger, E. A., & Heppel, L. A. (1974). Different mechanisms of energy coupling for the shock-sensitive and shock-resistant amino acid permeases of Escherichia coli. Journal of Biological Chemistry, 249(24), 7747-7755. https://doi.org/10.1016/S0021-9258(19)42031-0

[12]

Higgins, C. F., Haag, P. D., Nikaido, K., Ardeshir, F., Garcia, G., & Ames, G. F. L. (1982). Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium. Nature, 298(5876), 723-727. https://doi.org/10.1038/298723a0

[13]

Cordon-Cardo, C., O’Brien, J. P., Boccia, J., Casals, D., Bertino, J. R., & Melamed, M. R. (1990). Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues. Journal of Histochemistry and Cytochemistry, 38(9), 1277-1287. https://doi.org/10.1177/38.9.1974900

[14]

Holland, I. B. (2019). Rise and rise of the ABC transporter families. Research in Microbiology, 170(8), 304-320. https://doi.org/10.1016/j.resmic.2019.08.004

[15]

Thomas, C., & Tampé, R. (2020). Structural and mechanistic principles of ABC transporters. Annual Review of Biochemistry, 89(1), 605-636. https://doi.org/10.1146/annurev-biochem-011520-105201

[16]

Katayama, K., Noguchi, K., & Sugimoto, Y. (2014). Regulations of P-Glycoprotein/ABCB1/MDR1 in human cancer cells. New Journal of Science, 2014, 1-10. https://doi.org/10.1155/2014/476974

[17]

Dean, M., Hamon, Y., & Chimini, G. (2001). The human ATP-binding cassette (ABC) transporter superfamily. Journal of Lipid Research, 42(7), 1007-1017. https://doi.org/10.1016/S0022-2275(20)31588-1

[18]

Dean, M., & Annilo, T. (2005). Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annual Review of Genomics and Human Genetics, 6(1), 123-142. https://doi.org/10.1146/annurev.genom.6.080604.162122

[19]

Popovic, M., Zaja, R., Loncar, J., & Smital, T. (2010). A novel ABC transporter: The first insight into zebrafish (Danio rerio) ABCH1. Marine Environmental Research, 69, S11-S13. https://doi.org/10.1016/j.marenvres.2009.10.016

[20]

Després, L., David, J. P., & Gallet, C. (2007). The evolutionary ecology of insect resistance to plant chemicals. Trends in Ecology & Evolution, 22(6), 298-307. https://doi.org/10.1016/j.tree.2007.02.010

[21]

Kennedy, C. J., & Tierney, K. B. (2012). Xenobiotic protection/resistance mechanisms in organisms. In E. A. Laws (Ed.), Environmental Toxicology (pp. 689-721). Springer. https://doi.org/10.1007/978-1-4614-5764-0_23

[22]

Rösner, J., & Merzendorfer, H. (2020). Transcriptional plasticity of different ABC transporter genes from Tribolium castaneum contributes to diflubenzuron resistance. Insect Biochemistry and Molecular Biology, 116, 103282. https://doi.org/10.1016/j.ibmb.2019.103282

[23]

Lv, Y., Yan, K., Gao, X., Chen, X., Li, J., Ding, Y., Zhang, H., Pan, Y., & Shang, Q. (2022). Functional inquiry into ATP-binding cassette transporter genes contributing to spirotetramat resistance in Aphis gossypii Glover. Journal of Agricultural and Food Chemistry, 70(41), 13132-13142. https://doi.org/10.1021/acs.jafc.2c04263

[24]

Gahan, L. J., Pauchet, Y., Vogel, H., & Heckel, D. G. (2010). An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genetics, 6(12), e1001248. https://doi.org/10.1371/journal.pgen.1001248

[25]

Wang, Y., Adegawa, S., Miyamoto, K., Takasu, Y., Iizuka, T., Wada, S., Mang, D., Li, X., Kim, S., Sato, R., & Watanabe, K. (2021). ATP-binding cassette transporter subfamily C members 2, 3 and cadherin protein are susceptibility-determining factors in Bombyx mori for multiple Bacillus thuringiensis Cry1 toxins. Insect Biochemistry and Molecular Biology, 139, 103649. https://doi.org/10.1016/j.ibmb.2021.103649

[26]

Pignatelli, P., Ingham, V. A., Balabanidou, V., Vontas, J., Lycett, G., & Ranson, H. (2018). The Anopheles gambiae ATP-binding cassette transporter family: Phylogenetic analysis and tissue localization provide clues on function and role in insecticide resistance. Insect Molecular Biology, 27(1), 110-122. https://doi.org/10.1111/imb.12351

[27]

Glavinas, H., Méhn, D., Jani, M., Oosterhuis, B., Herédi-Szabó, K., & Krajcsi, P. (2008). Utilization of membrane vesicle preparations to study drug–ABC transporter interactions. Expert Opinion on Drug Metabolism & Toxicology, 4(6), 721-732. https://doi.org/10.1517/17425255.4.6.721

[28]

Abramson, J., Adler, J., Dunger, J., Evans, R., Green, T., Pritzel, A., Ronneberger, O., Willmore, L., Ballard, A. J., Bambrick, J., Bodenstein, S. W., Evans, D. A., Hung, C. C., O’Neill, M., Reiman, D., Tunyasuvunakool, K., Wu, Z., Žemgulytė, A., Arvaniti, E., … Hassabis, D. (2024). Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature, 630(8016), 493-500. https://doi.org/10.1038/s41586-024-07487-w

[29]

Khan, N., You, F. M., Datla, R., Ravichandran, S., Jia, B., & Cloutier, S. (2020). Genome-wide identification of ATP binding cassette (ABC) transporter and heavy metal associated (HMA) gene families in flax (Linum usitatissimum L.). BMC Genomics, 21(1), 722. https://doi.org/10.1186/s12864-020-07121-9

[30]

Tian, L., Song, T., He, R., Zeng, Y., Xie, W., Wu, Q., Wang, S., Zhou, X., & Zhang, Y. (2017). Genome-wide analysis of ATP-binding cassette (ABC) transporters in the sweetpotato whitefly, Bemisia tabaci. BMC Genomics, 18(1), 330. https://doi.org/10.1186/s12864-017-3706-6

[31]

Lebedeva, I. V., Pande, P., & Patton, W. F. (2011). Sensitive and specific fluorescent probes for functional analysis of the three major types of mammalian ABC transporters. PLoS One, 6(7), e22429. https://doi.org/10.1371/journal.pone.0022429

[32]

Ju, D., Hu, C., Lv, Y., Li, Y., Gao, P., & Yang, X. (2024). Establishing a fluorescence-based technique for ABC transporters functional analysis in metabolism of insecticides in a Lepidopteron. Environmental Technology & Innovation, 35, 103719. https://doi.org/10.1016/j.eti.2024.103719

[33]

Krumpochova, P., Sapthu, S., Brouwers, J. F., Haas, M., Vos, R., Borst, P., & Wetering, K. (2012). Transportomics: Screening for substrates of ABC transporters in body fluids using vesicular transport assays. The FASEB Journal, 26(2), 738-747. https://doi.org/10.1096/fj.11-195743

[34]

Qiao, H. H., Wang, F., Xu, R. G., Sun, J., Zhu, R., Mao, D., Ren, X., Wang, X., Jia, Y., Peng, P., Shen, D., Liu, L. P., Chang, Z., Wang, G., Li, S., Ji, J. Y., Liu, Q., & Ni, J. Q. (2018). An efficient and multiple target transgenic RNAi technique with low toxicity in Drosophila. Nature Communications, 9(1), 4160. https://doi.org/10.1038/s41467-018-06537-y

[35]

Homem, R. A., & Davies, T. G. E. (2018). An overview of functional genomic tools in deciphering insecticide resistance. Current Opinion in Insect Science, 27, 103-110. https://doi.org/10.1016/j.cois.2018.04.004

[36]

Lv, Y., Li, J., Yan, K., Ding, Y., Gao, X., Bi, R., Zhang, H., Pan, Y., & Shang, Q. (2022). Functional characterization of ABC transporters mediates multiple neonicotinoid resistance in a field population of Aphis gossypii Glover. Pesticide Biochemistry and Physiology, 188, 105264. https://doi.org/10.1016/j.pestbp.2022.105264

[37]

Kim, J. H., Gellatly, K. J., Lueke, B., Kohler, M., Nauen, R., Murenzi, E., Yoon, K. S., & Clark, J. M. (2018). Detoxification of ivermectin by ATP binding cassette transporter C4 and cytochrome P450 monooxygenase 6CJ1 in the human body louse, Pediculus humanus. Insect Molecular Biology, 27(1), 73-82. https://doi.org/10.1111/imb.12348

[38]

Scott, J. G., Michel, K., Bartholomay, L. C., Siegfried, B. D., Hunter, W. B., Smagghe, G., Zhu, K. Y., & Douglas, A. E. (2013). Towards the elements of successful insect RNAi. Journal of Insect Physiology, 59(12), 1212-1221. https://doi.org/10.1016/j.jinsphys.2013.08.014

[39]

Kunte, N., McGraw, E., Bell, S., Held, D., & Avila, L. (2020). Prospects, challenges and current status of RNAi through insect feeding. Pest Management Science, 76(1), 26-41. https://doi.org/10.1002/ps.5588

[40]

Li, J. J., Shi, Y., Wu, J. N., Li, H., Smagghe, G., & Liu, T. X. (2021). CRISPR/Cas9 in Lepidopteran insects: Progress, application and prospects. Journal of Insect Physiology, 135, 104325. https://doi.org/10.1016/j.jinsphys.2021.104325

[41]

Shan, J., Sun, X., Li, R., Zhu, B., Liang, P., & Gao, X. (2021). Identification of ABCG transporter genes associated with chlorantraniliprole resistance in Plutella xylostella (L.). Pest Management Science, 77(7), 3491-3499. https://doi.org/10.1002/ps.6402

[42]

Guo, Z., Sun, D., Kang, S., Zhou, J., Gong, L., Qin, J., Guo, L., Zhu, L., Bai, Y., Luo, L., & Zhang, Y. (2019). CRISPR/Cas9-mediated knockout of both the PxABCC2 and PxABCC3 genes confers high-level resistance to Bacillus thuringiensis Cry1Ac toxin in the diamondback moth, Plutella xylostella (L.). Insect Biochemistry and Molecular Biology, 107, 31-38. https://doi.org/10.1016/j.ibmb.2019.01.009

[43]

Zhou, J., Guo, Z., Kang, S., Qin, J., Gong, L., Sun, D., Guo, L., Zhu, L., Bai, Y., Zhang, Z., Zhou, X., & Zhang, Y. (2020). Reduced expression of the P-glycoprotein gene PxABCB1 is linked to resistance to Bacillus thuringiensis Cry1Ac toxin in Plutella xylostella (L.). Pest Management Science, 76(2), 712-720. https://doi.org/10.1002/ps.5569

[44]

Xiong, L., Liu, Z., Li, J., Yao, S., Li, Z., Chen, X., Shen, L., Zhang, Z., Li, Y., Hou, Q., Zhang, Y., You, M., Yuchi, Z., & You, S. (2023). Analysis of the effect of Plutella xylostella polycalin and ABCC2 transporter on Cry1Ac susceptibility by CRISPR/Cas9-mediated knockout. Toxins, 15(4), 273. https://doi.org/10.3390/toxins15040273

[45]

Litman, T., Zeuthen, T., Skovsgaard, T., & Stein, W. D. (1997). Structure-activity relationships of P-glycoprotein interacting drugs: Kinetic characterization of their effects on ATPase activity. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1361(2), 159-168. https://doi.org/10.1016/S0925-4439(97)00026-4

[46]

He, Q., Yan, Z., Si, F., Zhou, Y., Fu, W., & Chen, B. (2019). ATP-binding cassette (ABC) transporter genes involved in pyrethroid resistance in the malaria vector Anopheles sinensis: Genome-wide identification, characteristics, phylogenetics, and expression profile. International Journal of Molecular Sciences, 20(6), 1409. https://doi.org/10.3390/ijms20061409

[47]

Jin, M., Liao, C., Chakrabarty, S., Zheng, W., Wu, K., & Xiao, Y. (2019). Transcriptional response of ATP-binding cassette (ABC) transporters to insecticides in the cotton bollworm, Helicoverpa armigera. Pesticide Biochemistry and Physiology, 154, 46-59. https://doi.org/10.1016/j.pestbp.2018.12.007

[48]

Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L., & Schwede, T. (2009). The SWISS-MODEL repository and associated resources. Nucleic Acids Research, 37(Suppl_1), D387-D392. https://doi.org/10.1093/nar/gkn750

[49]

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. E. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10(6), 845-858. https://doi.org/10.1038/nprot.2015.053

[50]

Yang, Z., Zeng, X., Zhao, Y., & Chen, R. (2023). AlphaFold2 and its applications in the fields of biology and medicine. Signal Transduction and Targeted Therapy, 8(1), 115. https://doi.org/10.1038/s41392-023-01381-z

[51]

Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455-461. https://doi.org/10.1002/jcc.21334

[52]

Bhachoo, J., & Beuming, T. (2017). Investigating protein–peptide interactions using the Schrödinger computational suite. In O. Schueler-Furman & N. London (Eds.), Modeling peptide-protein interactions (Vol. 1561, pp. 235-254). Springer. https://doi.org/10.1007/978-1-4939-6798-8_14

[53]

De Vries, S. J., Van Dijk, M., & Bonvin, A. M. J. J. (2010). The HADDOCK web server for data-driven biomolecular docking. Nature Protocols, 5(5), 883-897. https://doi.org/10.1038/nprot.2010.32

[54]

DeLano, W. L. (2002). PyMOL: An open-source molecular graphics tool. CCP4 Newsletter on Protein Crystallography, 40(1), 82-92.

[55]

Spanakis, M., Tzamali, E., Tzedakis, G., Koumpouzi, C., Pediaditis, M., Tsatsakis, A., & Sakkalis, V. (2025). Artificial intelligence models and tools for the assessment of drug–herb interactions. Pharmaceuticals, 18(3), 282. https://doi.org/10.3390/ph18030282

[56]

Glaeser, H., Bailey, D. G., Dresser, G. K., Gregor, J. C., Schwarz, U. I., McGrath, J. S., Jolicoeur, E., Lee, W., Leake, B. F., Tirona, R. G., & Kim, R. B. (2007). Intestinal drug transporter expression and the impact of grapefruit juice in humans. Clinical Pharmacology & Therapeutics, 81(3), 362-370. https://doi.org/10.1038/sj.clpt.6100056

[57]

Dudas, B., & Miteva, M. A. (2024). Computational and artificial intelligence-based approaches for drug metabolism and transport prediction. Trends in Pharmacological Sciences, 45(1), 39-55. https://doi.org/10.1016/j.tips.2023.11.001

[58]

Li, X., Schuler, M. A., & Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52(1), 231-253. https://doi.org/10.1146/annurev.ento.51.110104.151104

[59]

Soderlund, D. M., & Bloomquist, J. R. (1990). Molecular mechanisms of insecticide resistance. In R. T. Roush & B. E. Tabashnik (Eds.), Pesticide Resistance in Arthropods (pp. 58-96). Springer US. https://doi.org/10.1007/978-1-4684-6429-0_4

[60]

Hemingway, J. (2000). The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochemistry and Molecular Biology, 30(11), 1009-1015. https://doi.org/10.1016/S0965-1748(00)00079-5

[61]

Hemingway, J., Field, L., & Vontas, J. (2002). An overview of insecticide resistance. Science, 298(5591), 96-97. https://doi.org/10.1126/science.1078052

[62]

Nauen, R., Bass, C., Feyereisen, R., & Vontas, J. (2022). The role of cytochrome P450s in insect toxicology and resistance. Annual Review of Entomology, 67(1), 105-124. https://doi.org/10.1146/annurev-ento-070621-061328

[63]

Pavlidi, N., Vontas, J., & 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. https://doi.org/10.1016/j.cois.2018.04.007

[64]

Li, X., Shi, H., Gao, X., & Liang, P. (2018). Characterization of UDP-glucuronosyltransferase genes and their possible roles in multi-insecticide resistance in Plutella xylostella (L.). Pest Management Science, 74(3), 695-704. https://doi.org/10.1002/ps.4765

[65]

Huang, Y., Chen, Z., Lan, J., Zhang, L., Chen, H., Jiang, L., Yu, H., Liu, N., Liao, C., & Han, Q. (2024). MDR49 coding for both P-glycoprotein and TMOF transporter functions in ivermectin resistance, trypsin activity inhibition, and fertility in the yellow fever mosquito, Aedes aegypti. Pesticide Biochemistry and Physiology, 201, 105899. https://doi.org/10.1016/j.pestbp.2024.105899

[66]

Rault, L. C., Johnson, E. J., O’Neal, S. T., Chen, R., McComic, S. E., Swale, D. R., & Anderson, T. D. (2019). Age- and sex-related ABC transporter expression in pyrethroid-susceptible and –resistant Aedes aegypti. Scientific Reports, 9(1), 19551. https://doi.org/10.1038/s41598-019-56134-2

[67]

Kefi, M., Balabanidou, V., Sarafoglou, C., Charamis, J., Lycett, G., Ranson, H., Gouridis, G., & Vontas, J. (2023). ABCH2 transporter mediates deltamethrin uptake and toxicity in the malaria vector Anopheles coluzzii. PLoS Pathogens, 19(8), e1011226. https://doi.org/10.1371/journal.ppat.1011226

[68]

Lv, Y., Pan, Y., Li, J., Ding, Y., Yu, Z., Yan, K., & Shang, Q. (2023). The C2H2 zinc finger transcription factor CF2-II regulates multi-insecticide resistance-related gut-predominant ABC transporters in Aphis gossypii Glover. International Journal of Biological Macromolecules, 253, 126765. https://doi.org/10.1016/j.ijbiomac.2023.126765

[69]

Pan, Y., Zeng, X., Wen, S., Gao, X., Liu, X., Tian, F., & Shang, Q. (2020). Multiple ATP-binding cassette transporters genes are involved in thiamethoxam resistance in Aphis gossypii glover. Pesticide Biochemistry and Physiology, 167, 104558. https://doi.org/10.1016/j.pestbp.2020.104558

[70]

Li, J., Lv, Y., Yan, K., Yang, F., Chen, X., Gao, X., Wen, S., Xu, H., Pan, Y., & Shang, Q. (2022). Functional analysis of cyantraniliprole tolerance ability mediated by ATP-binding cassette transporters in Aphis gossypii glover. Pesticide Biochemistry and Physiology, 184, 105104. https://doi.org/10.1016/j.pestbp.2022.105104

[71]

Yang, Y., Duan, A., Zhang, C., Zhang, Y., Wang, A., Xue, C., Wang, H., Zhao, M., & Zhang, J. (2022). Overexpression of ATP-binding cassette transporters ABCG10, ABCH3 and ABCH4 in Aphis craccivora (Koch) facilitates its tolerance to imidacloprid. Pesticide Biochemistry and Physiology, 186, 105170. https://doi.org/10.1016/j.pestbp.2022.105170

[72]

He, C., Liang, J., Liu, S., Wang, S., Wu, Q., Xie, W., & Zhang, Y. (2019). Changes in the expression of four ABC transporter genes in response to imidacloprid in Bemisia tabaci Q (Hemiptera: Aleyrodidae). Pesticide Biochemistry and Physiology, 153, 136-143. https://doi.org/10.1016/j.pestbp.2018.11.014

[73]

Xu, J., Zheng, J., Zhang, R., Wang, H., Du, J., Li, J., Zhou, D., Sun, Y., & Shen, B. (2023). Identification and functional analysis of ABC transporter genes related to deltamethrin resistance in Culex pipiens pallens. Pest Management Science, 79(10), 3642-3655. https://doi.org/10.1002/ps.7539

[74]

Guan, D., Yang, X., Jiang, H., Zhang, N., Wu, Z., Jiang, C., Shen, Q., Qian, K., Wang, J., & Meng, X. (2022). Identification and validation of ATP-binding cassette transporters involved in the detoxification of abamectin in rice stem borer, Chilo suppressalis. Journal of Agricultural and Food Chemistry, 70(15), 4611-4619. https://doi.org/10.1021/acs.jafc.2c00414

[75]

Meng, X., Yang, X., Wu, Z., Shen, Q., Miao, L., Zheng, Y., Qian, K., & Wang, J. (2020). Identification and transcriptional response of ATP-binding cassette transporters to chlorantraniliprole in the rice striped stem borer, Chilo suppressalis. Pest Management Science, 76(11), 3626-3635. https://doi.org/10.1002/ps.5897

[76]

Denecke, S., Fusetto, R., & Batterham, P. (2017). Describing the role of Drosophila melanogaster ABC transporters in insecticide biology using CRISPR-Cas9 knockouts. Insect Biochemistry and Molecular Biology, 91, 1-9. https://doi.org/10.1016/j.ibmb.2017.09.017

[77]

Denecke, S., Bảo Lương, H. N., Koidou, V., Kalogeridi, M., Socratous, R., Howe, S., Vogelsang, K., Nauen, R., Batterham, P., Geibel, S., & Vontas, J. (2022). Characterization of a novel pesticide transporter and P-glycoprotein orthologues in Drosophila melanogaster. Proceedings of the Royal Society B: Biological Sciences, 289(1975), 20220625. https://doi.org/10.1098/rspb.2022.0625

[78]

Sun, H., Buchon, N., & Scott, J. G. (2017). Mdr65 decreases toxicity of multiple insecticides in Drosophila melanogaster. Insect Biochemistry and Molecular Biology, 89, 11-16. https://doi.org/10.1016/j.ibmb.2017.08.002

[79]

Lira, E. C., Nascimento, A. R., Bass, C., Omoto, C., & Cônsoli, F. L. (2023). Transcriptomic investigation of the molecular mechanisms underlying resistance to the neonicotinoid thiamethoxam and the pyrethroid lambda-cyhalothrin in Euschistus heros (Hemiptera: Pentatomidae). Pest Management Science, 79(12), 5349-5361. https://doi.org/10.1002/ps.7745

[80]

Wang, L., Tao, S., Zhang, Y., Pei, X., Gao, Y., Song, X., Yu, Z., & Gao, C. (2022). Overexpression of ATP-binding cassette transporter Mdr49-like confers resistance to imidacloprid in the field populations of brown planthopper, Nilaparvata lugens. Pest Management Science, 78(2), 579-590. https://doi.org/10.1002/ps.6666

[81]

Zuo, Y. Y., Huang, J. L., Wang, J., Feng, Y., Han, T. T., Wu, Y. D., & Yang, Y. H. (2018). Knockout of a P-glycoprotein gene increases susceptibility to abamectin and emamectin benzoate in Spodoptera exigua. Insect Molecular Biology, 27(1), 36-45. https://doi.org/10.1111/imb.12338

[82]

Wang, L., Guo, S., Wen, B., Deng, Z., Ding, Q., & Li, X. (2025). Characterization of ATP-binding cassette transporters associated with emamectin benzoate tolerance: From the model insect Drosophila melanogaster to the agricultural pest Spodoptera frugiperda. Pest Management Science, 81(1), 340-350. https://doi.org/10.1002/ps.8437

[83]

Jin, M., Yang, Y., Shan, Y., Chakrabarty, S., Cheng, Y., Soberón, M., Bravo, A., Liu, K., Wu, K., & Xiao, Y. (2021). Two ABC transporters are differentially involved in the toxicity of two Bacillus thuringiensis Cry1 toxins to the invasive crop-pest Spodoptera frugiperda (J. E. Smith). Pest Management Science, 77(3), 1492-1501. https://doi.org/10.1002/ps.6170

[84]

Rösner, J., & Merzendorfer, H. (2022). Identification of two ABCC transporters involved in malathion detoxification in the red flour beetle, Tribolium castaneum. Insect Science, 29(4), 1096-1104. https://doi.org/10.1111/1744-7917.12981

[85]

Wu, M., Zhang, Y., Tian, T., Xu, D., Wu, Q., Xie, W., Zhang, Y., Crickmore, N., Guo, Z., & Wang, S. (2023). Assessment of the role of an ABCC transporter TuMRP1 in the toxicity of abamectin to Tetranychus urticae. Pesticide Biochemistry and Physiology, 195, 105543. https://doi.org/10.1016/j.pestbp.2023.105543

[86]

Amezian, D., Nauen, R., & Van Leeuwen, T. (2024). The role of ATP-binding cassette transporters in arthropod pesticide toxicity and resistance. Current Opinion in Insect Science, 63, 101200. https://doi.org/10.1016/j.cois.2024.101200

[87]

Buss, D. S., & Callaghan, A. (2008). Interaction of pesticides with p-glycoprotein and other ABC proteins: A survey of the possible importance to insecticide, herbicide and fungicide resistance. Pesticide Biochemistry and Physiology, 90(3), 141-153. https://doi.org/10.1016/j.pestbp.2007.12.001

[88]

Huang, Y., Xue, C., Wang, L., Bu, R., Mu, J., Wang, Y., & Liu, Z. (2023). Structural basis for substrate and inhibitor recognition of human multidrug transporter MRP4. Communications Biology, 6(1), 549. https://doi.org/10.1038/s42003-023-04935-7

[89]

Kang, X., Zhang, M., Wang, K., Qiao, X., & Chen, M. (2016). Molecular cloning, expression pattern of multidrug resistance associated protein 1 (mrp1, abcc1) gene, and the synergistic effects of verapamil on toxicity of two insecticides in the bird cherry-oat aphid. Archives of Insect Biochemistry and Physiology, 92(1), 65-84. https://doi.org/10.1002/arch.21334

[90]

Denecke, S., Fusetto, R., Martelli, F., Giang, A., Battlay, P., Fournier-Level, A., O’ Hair, R. A., & Batterham, P. (2017). Multiple P450s and variation in neuronal genes underpins the response to the insecticide imidacloprid in a population of Drosophila melanogaster. Scientific Reports, 7(1), 11338. https://doi.org/10.1038/s41598-017-11092-5

[91]

Li, Z., Mao, K., Jin, R., Cai, T., Qin, Y., Zhang, Y., He, S., Ma, K., Wan, H., Ren, X., & Li, J. (2022). miRNA novel_268 targeting NlABCG3 is involved in nitenpyram and clothianidin resistance in Nilaparvata lugens. International Journal of Biological Macromolecules, 217, 615-623. https://doi.org/10.1016/j.ijbiomac.2022.07.096

[92]

Li, Z., Cai, T., Qin, Y., Zhang, Y., Jin, R., Mao, K., Liao, X., Wan, H., & Li, J. (2020). Transcriptional response of ATP-binding cassette (ABC) transporters to insecticide in the brown planthopper, Nilaparvata lugens (Stål). Insects, 11(5), 280. https://doi.org/10.3390/insects11050280

[93]

Shan, J., Zhu, B., & Liang, P. (2023). Identification of ABCG transporter genes associated with multi-insecticide resistance in Plutella xylostella (L.). Entomologia Generalis, 43(3), 555-565. https://doi.org/10.1127/entomologia/2023/2099

[94]

Lu, Y., Wu, K., Jiang, Y., Guo, Y., & Desneux, N. (2012). Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature, 487(7407), 362-365. https://doi.org/10.1038/nature11153

[95]

Jin, L., Zhang, H., Lu, Y., Yang, Y., Wu, K., Tabashnik, B. E., & Wu, Y. (2015). Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nature Biotechnology, 33(2), 169-174. https://doi.org/10.1038/nbt.3100

[96]

Jurat-Fuentes, J. L., Heckel, D. G., & Ferré, J. (2021). Mechanisms of resistance to insecticidal proteins from Bacillus thuringiensis. Annual Review of Entomology, 66(1), 121-140. https://doi.org/10.1146/annurev-ento-052620-073348

[97]

Tabashnik, B. E., Gassmann, A. J., Crowder, D. W., & Carriére, Y. (2008). Insect resistance to Bt crops: Evidence versus theory. Nature Biotechnology, 26(2), 199-202. https://doi.org/10.1038/nbt1382

[98]

Tabashnik, B. E., Brévault, T., & Carrière, Y. (2013). Insect resistance to Bt crops: Lessons from the first billion acres. Nature Biotechnology, 31(6), 510-521. https://doi.org/10.1038/nbt.2597

[99]

Huang, J., Xu, Y., Zuo, Y., Yang, Y., Tabashnik, B. E., & Wu, Y. (2020). Evaluation of five candidate receptors for three Bt toxins in the beet armyworm using CRISPR-mediated gene knockouts. Insect Biochemistry and Molecular Biology, 121, 103361. https://doi.org/10.1016/j.ibmb.2020.103361

[100]

Wang, J., Ma, H., Zhao, S., Huang, J., Yang, Y., Tabashnik, B. E., & Wu, Y. (2020). Functional redundancy of two ABC transporter proteins in mediating toxicity of Bacillus thuringiensis to cotton bollworm. PLoS Pathogens, 16(3), e1008427. https://doi.org/10.1371/journal.ppat.1008427

[101]

Perera, O. P., Little, N. S., Abdelgaffar, H., Jurat-Fuentes, J. L., & Reddy, G. V. P. (2021). Genetic knockouts indicate that the ABCC2 protein in the bollworm Helicoverpa zea is not a major receptor for the Cry1Ac insecticidal protein. Genes, 12(10), 1522. https://doi.org/10.3390/genes12101522

[102]

Liu, Z., Fu, S., Ma, X., Baxter, S. W., Vasseur, L., Xiong, L., Huang, Y., Yang, G., You, S., & You, M. (2020). Resistance to Bacillus thuringiensis Cry1Ac toxin requires mutations in two Plutella xylostella ATP-binding cassette transporter paralogs. PLoS Pathogens, 16(8), e1008697. https://doi.org/10.1371/journal.ppat.1008697

[103]

Zhang, D., Jin, M., Yang, Y., Zhang, J., Yang, Y., Liu, K., Soberón, M., Bravo, A., Xiao, Y., & Wu, K. (2021). Synergistic resistance of Helicoverpa armigera to Bt toxins linked to cadherin and ABC transporters mutations. Insect Biochemistry and Molecular Biology, 137, 103635. https://doi.org/10.1016/j.ibmb.2021.103635

[104]

Kim, S., Wang, Y., Miyamoto, K., Takasu, Y., Wada, S., Iizuka, T., Sato, R., & Watanabe, K. (2022). Cadherin BtR175 and ATP-binding cassette transporter protein ABCC2 or ABCC3 facilitate Bacillus thuringiensis Cry1Aa intoxication in Bombyx mori. Journal of Insect Biotechnology and Sericology, 91, 1-12. https://doi.org/10.11416/jibs.91.1_001

[105]

Yang, X., Chen, W., Song, X., Ma, X., Cotto-Rivera, R. O., Kain, W., Chu, H., Chen, Y. R., Fei, Z., & Wang, P. (2019). Mutation of ABC transporter ABCA2 confers resistance to Bt toxin Cry2Ab in Trichoplusia ni. Insect Biochemistry and Molecular Biology, 112, 103209. https://doi.org/10.1016/j.ibmb.2019.103209

[106]

Tang, J., Lu, J., Zhang, C., Zhang, D., Yu, S., Fang, F., Naing, Z. L., Soe, E. T., Ding, Z., & Liang, G. (2023). Reduced expression of the P-glycoprotein gene HaABCB1 is linked to resistance to Bacillus thuringiensis Cry1Ac toxin but not Cry2Ab toxin in Helicoverpa armigera. International Journal of Biological Macromolecules, 253, 127668. https://doi.org/10.1016/j.ijbiomac.2023.127668

[107]

Lanning, C. L., Fine, R. L., Corcoran, J. J., Ayad, H. M., Rose, R. L., & Abou-Donia, M. B. (1996). Tobacco budworm P-glycoprotein: Biochemical characterization and its involvement in pesticide resistance. Biochimica et Biophysica Acta (BBA) - General Subjects, 1291(2), 155-162. https://doi.org/10.1016/0304-4165(96)00060-8

[108]

Aurade, R. M., Jayalakshmi, S. K., & Sreeramulu, K. (2010). P-glycoprotein ATPase from the resistant pest, Helicoverpa armigera: Purification, characterization and effect of various insecticides on its transport function. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1798(6), 1135-1143. https://doi.org/10.1016/j.bbamem.2010.02.019

[109]

Xiang, M., Zhang, L., Lu, Y., Tang, Q., Liang, P., Shi, X., Song, D., & Gao, X. (2017). A P-glycoprotein gene serves as a component of the protective mechanisms against 2-tridecanone and abamectin in Helicoverpa armigera. Gene, 627, 63-71. https://doi.org/10.1016/j.gene.2017.06.010

[110]

Tian, L., Yang, J., Hou, W., Xu, B., Xie, W., Wang, S., Zhang, Y., Zhou, X., & Wu, Q. (2013). Molecular cloning and characterization of a P-Glycoprotein from the Diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). International Journal of Molecular Sciences, 14(11), 22891-22905. https://doi.org/10.3390/ijms141122891

[111]

Akiyama, M. (2014). The roles of ABCA12 in epidermal lipid barrier formation and keratinocyte differentiation. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1841(3), 435-440. https://doi.org/10.1016/j.bbalip.2013.08.009

[112]

Yu, Z., Wang, Y., Zhao, X., Liu, X., Ma, E., Moussian, B., & Zhang, J. (2017). The ABC transporter ABCH-9C is needed for cuticle barrier construction in Locusta migratoria. Insect Biochemistry and Molecular Biology, 87, 90-99. https://doi.org/10.1016/j.ibmb.2017.06.005

[113]

Qiao, J. W., Wu, B. J., Wang, W. Q., Yuan, C. X., Su, S., Zhang, Z. F., Fan, Y. L., & Liu, T. X. (2024). The ATP-binding cassette transporter subfamily G member 4 mediates cuticular hydrocarbon transport to regulate drought tolerance in Acyrthosiphon pisum. International Journal of Biological Macromolecules, 278, 134605. https://doi.org/10.1016/j.ijbiomac.2024.134605

[114]

Balabanidou, V., Grigoraki, L., & Vontas, J. (2018). Insect cuticle: A critical determinant of insecticide resistance. Current Opinion in Insect Science, 27, 68-74. https://doi.org/10.1016/j.cois.2018.03.001

[115]

Moore, M. J. (2005). From Birth to Death: The complex lives of eukaryotic mRNAs. Science, 309(5740), 1514-1518. https://doi.org/10.1126/science.1111443

[116]

Lambert, S. A., Jolma, A., Campitelli, L. F., Das, P. K., Yin, Y., Albu, M., Chen, X., Taipale, J., Hughes, T. R., & Weirauch, M. T. (2018). The human transcription factors. Cell, 172(4), 650-665. https://doi.org/10.1016/j.cell.2018.01.029

[117]

Wittkopp, P. J., & Kalay, G. (2012). Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence. Nature Reviews Genetics, 13(1), 59-69. https://doi.org/10.1038/nrg3095

[118]

Amezian, D., Nauen, R., & Le Goff, G. (2021). Transcriptional regulation of xenobiotic detoxification genes in insects—An overview. Pesticide Biochemistry and Physiology, 174, 104822. https://doi.org/10.1016/j.pestbp.2021.104822

[119]

Guo, Z., Guo, L., Qin, J., Ye, F., Sun, D., Wu, Q., Wang, S., Crickmore, N., Zhou, X., Bravo, A., Soberón, M., & Zhang, Y. (2022). A single transcription factor facilitates an insect host combating Bacillus thuringiensis infection while maintaining fitness. Nature Communications, 13(1), 6024. https://doi.org/10.1038/s41467-022-33706-x

[120]

Guo, Z., Kang, S., Sun, D., Gong, L., Zhou, J., Qin, J., Guo, L., Zhu, L., Bai, Y., Ye, F., Wu, Q., Wang, S., Crickmore, N., Zhou, X., & Zhang, Y. (2020). MAPK-dependent hormonal signaling plasticity contributes to overcoming Bacillus thuringiensis toxin action in an insect host. Nature Communications, 11(1), 3003. https://doi.org/10.1038/s41467-020-16608-8

[121]

Sun, D., Zhu, L., Guo, L., Wang, S., Wu, Q., Crickmore, N., Zhou, X., Bravo, A., Soberón, M., Guo, Z., & Zhang, Y. (2022). A versatile contribution of both aminopeptidases N and ABC transporters to Bt Cry1Ac toxicity in the diamondback moth. BMC Biology, 20(1), 33. https://doi.org/10.1186/s12915-022-01226-1

[122]

Guo, Z., Zhu, L., Cheng, Z., Dong, L., Guo, L., Bai, Y., Wu, Q., Wang, S., Yang, X., Xie, W., Crickmore, N., Zhou, X., Lafont, R., & Zhang, Y. (2024). A midgut transcriptional regulatory loop favors an insect host to withstand a bacterial pathogen. The Innovation, 5(5), 100675. https://doi.org/10.1016/j.xinn.2024.100675

[123]

Ouyang, C., Ye, F., Wu, Q., Wang, S., Crickmore, N., Zhou, X., Guo, Z., & Zhang, Y. (2023). CRISPR/Cas9-based functional characterization of PxABCB1 reveals its roles in the resistance of Plutella xylostella (L.) to Cry1Ac, abamectin and emamectin benzoate. Journal of Integrative Agriculture, 22(10), 3090-3102. https://doi.org/10.1016/j.jia.2023.05.023

[124]

Guo, L., Cheng, Z., Qin, J., Sun, D., Wang, S., Wu, Q., Crickmore, N., Zhou, X., Bravo, A., Soberón, M., Guo, Z., & Zhang, Y. (2022). MAPK-mediated transcription factor GATAd contributes to Cry1Ac resistance in diamondback moth by reducing PxmALP expression. PLoS Genetics, 18(2), e1010037. https://doi.org/10.1371/journal.pgen.1010037

[125]

Guo, Z., Kang, S., Chen, D., Wu, Q., Wang, S., Xie, W., Zhu, X., Baxter, S. W., Zhou, X., Jurat-Fuentes, J. L., & Zhang, Y. (2015). MAPK signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in diamondback moth. PLoS Genetics, 11(4), e1005124. https://doi.org/10.1371/journal.pgen.1005124

[126]

Guo, Z., Kang, S., Wu, Q., Wang, S., Crickmore, N., Zhou, X., Bravo, A., Soberón, M., & Zhang, Y. (2021). The regulation landscape of MAPK signaling cascade for thwarting Bacillus thuringiensis infection in an insect host. PLoS Pathogens, 17(9), e1009917. https://doi.org/10.1371/journal.ppat.1009917

[127]

Guo, Z., Guo, L., Bai, Y., Kang, S., Sun, D., Qin, J., Ye, F., Wang, S., Wu, Q., Xie, W., Yang, X., Crickmore, N., Zhou, X., & Zhang, Y. (2023). Retrotransposon-mediated evolutionary rewiring of a pathogen response orchestrates a resistance phenotype in an insect host. Proceedings of the National Academy of Sciences of the United States of America, 120(14), e2300439120. https://doi.org/10.1073/pnas.2300439120

[128]

Xu, L., Qin, J., Fu, W., Wang, S., Wu, Q., Zhou, X., Crickmore, N., Guo, Z., & Zhang, Y. (2022). MAP4K4 controlled transcription factor POUM1 regulates PxABCG1 expression influencing Cry1Ac resistance in Plutella xylostella (L.). Pesticide Biochemistry and Physiology, 182, 105053. https://doi.org/10.1016/j.pestbp.2022.105053

[129]

Kalsi, M., & Palli, S. R. (2017). Cap n collar transcription factor regulates multiple genes coding for proteins involved in insecticide detoxification in the red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology, 90, 43-52. https://doi.org/10.1016/j.ibmb.2017.09.009

[130]

Gaddelapati, S. C., Kalsi, M., Roy, A., & Palli, S. R. (2018). Cap “n” collar C regulates genes responsible for imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata. Insect Biochemistry and Molecular Biology, 99, 54-62. https://doi.org/10.1016/j.ibmb.2018.05.006

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