Insect chemosensory proteins as targets in insecticide resistance and development

Abstract

Insect chemosensory proteins (CSPs) are thermostable proteins mainly found in insect species. They are integral components in the insect peripheral nervous system. Some CSP sequences and structures are species-specific. The functions of CSPs have been implied based on the evidence from fluorescent binding assays and expression analyses. In this review, we summarize the general biological and chemical properties of insect CSPs and present recent advancements in RNA interference, population genetics, and transgenesis for their functional characterization. We thus present new functional evidence of insect CSPs not only in olfaction but also in nonolfactory processes, particularly in insecticide resistance. Their expression is regulated during developmental stages and exhibits a wide tissue distribution. These proteins possess ligand binding sites for both semiochemicals and commonly used insecticides, making them viable targets for rational insecticide development. Although only a few crystal structures have been solved to date, this will be improved with the development of structure determination and prediction techniques, such as cryo-electron microscopy and AlphaFold. Newly rationally developed insecticides based on the differential expression of CSPs are expected to be nontoxic to vertebrates and specific to insect pest species.

Keywords

chemical ecology / chemosensory protein / insecticide / olfaction / pest management / semiochemical

References

[1] Pelosi, P., Zhou, J. J., Ban, L. P., & Calvello, M. (2006). Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences, 63(14), 1658-1676. https://doi.org/10.1007/s00018-005-5607-0

[2] Liu, N. Y., Li, Z. B., Zhao, N., Song, Q. S., Zhu, J. Y., & Yang, B. (2018). Identification and characterization of chemosensory gene families in the bark beetle, Tomicus yunnanensis. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 25, 73-85. https://doi.org/10.1016/j.cbd.2017.11.003

[3] Xuan, N., Guo, X., Xie, H. Y., Lou, Q. N., Lu, X. B., Liu, G. X., & Picimbon, J. F. (2015). Increased expression of CSP and CYP genes in adult silkworm females exposed to avermectins. Insect Science, 22(2), 203-219. https://doi.org/10.1111/1744-7917.12116

[4] Leal, W. S., Chen, A. M., Ishida, Y., Chiang, V. P., Erickson, M. L., Morgan, T. I., & Tsuruda, J. M. (2005). Kinetics and molecular properties of pheromone binding and release. Proceedings of the National Academy of Sciences of the United States of America, 102(15), 5386-5391. https://doi.org/10.1073/pnas.0501447102

[5] Ozaki, M., Wada-Katsumata, A., Fujikawa, K., Iwasaki, M., Yokohari, F., Satoji, Y., Nisimura, T., & Yamaoka, R. (2005). Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science, 309(5732), 311-314. https://doi.org/10.1126/science.1105244

[6] Sabatier, L., Jouanguy, E., Dostert, C., Zachary, D., Dimarcq, J. L., Bulet, P., & Imler, J. L. (2003). Pherokine-2 and -3: Two Drosophila molecules related to pheromone/odor-binding proteins induced by viral and bacterial infections. European Journal of Biochemistry, 270(16), 3398-3407. https://doi.org/10.1046/j.1432-1033.2003.03725.x

[7] Claridge-Chang, A., Wijnen, H., Naef, F., Boothroyd, C., Rajewsky, N., & Young, M. W. (2001). Circadian regulation of gene expression systems in the Drosophila head. Neuron, 32(4), 657-671. https://doi.org/10.1016/s0896-6273(01)00515-3

[8] Stathopoulos, A., & Levine, M. (2002). Whole-genome expression profiles identify gene batteries in Drosophila. Developmental Cell, 3(4), 464-465. https://doi.org/10.1016/s1534-5807(02)00300-3

[9] Forêt, S., Wanner, K. W., & Maleszka, R. (2007). Chemosensory proteins in the honey bee: Insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochemistry and Molecular Biology, 37(1), 19-28. https://doi.org/10.1016/j.ibmb.2006.09.009

[10] Zhou, J. J., Kan, Y., Antoniw, J., Pickett, J. A., & Field, L. M. (2006). Genome and EST analyses and expression of a gene family with putative functions in insect chemoreception. Chemical Senses, 31(5), 453-465. https://doi.org/10.1093/chemse/bjj050

[11] Sánchez-Gracia, A., Vieira, F. G., & Rozas, J. (2009). Molecular evolution of the major chemosensory gene families in insects. Heredity, 103(3), 208-216. https://doi.org/10.1038/hdy.2009.55

[12] Vieira, F. G., & Rozas, J. (2011). Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: Origin and evolutionary history of the chemosensory system. Genome Biology and Evolution, 3, 476-490. https://doi.org/10.1093/gbe/evr033

[13] Liu, G., Xuan, N., Rajashekar, B., Arnaud, P., Offmann, B., & Picimbon, J. F. (2020). Comprehensive history of CSP genes: Evolution, phylogenetic distribution and functions. Genes, 11(4), 413. https://doi.org/10.3390/genes11040413

[14] Xiao, Y., Sun, L., Wang, Q., Zhang, Q., Gu, S. H., Khashaveh, A., Liu, Z. W., & Zhang, Y. J. (2018). Molecular characterization and expression analysis of putative odorant carrier proteins in Adelphocoris lineolatus. Journal of Asia-Pacific Entomology, 21(3), 958-970. https://doi.org/10.1016/j.aspen.2018.07.016

[15] Gu, S. H., Wu, K. M., Guo, Y. Y., Field, L. M., Pickett, J. A., Zhang, Y. J., & Zhou, J. J. (2013). Identification and expression profiling of odorant binding proteins and chemosensory proteins between two wingless morphs and a winged morph of the cotton aphid Aphis gossypii glover. PLoS One, 8(9), e73524. https://doi.org/10.1371/journal.pone.0073524

[16] Wang, Q., Zhou, J. J., Liu, J. T., Huang, G. Z., Xu, W. Y., Zhang, Q., Chen, J. L., Zhang, Y. J., Li, X. C., & Gu, S. H. (2019). Integrative transcriptomic and genomic analysis of odorant binding proteins and chemosensory proteins in aphids. Insect Molecular Biology, 28(1), 1-22. https://doi.org/10.1111/imb.12513

[17] Kuang, Y., Shangguan, C., Yuan, S., Zhang, Q., Qiu, Z., Gao, L., & Yu, X. (2023). Candidate odorant-binding protein and chemosensory protein genes in the turnip aphid Lipaphis erysimi. Archives of Insect Biochemistry and Physiology, 113(4), e22022. https://doi.org/10.1002/arch.22022

[18] Xue, W., Fan, J., Zhang, Y., Xu, Q., Han, Z., Sun, J., & Chen, J. (2016). Identification and expression analysis of candidate odorant-binding protein and chemosensory protein genes by antennal transcriptome of Sitobion avenae. PLoS One, 11(8), e0161839. https://doi.org/10.1371/journal.pone.0161839

[19] Zhao, J. J., Zhang, Y., Fan, D. S., & Feng, J. N. (2017). Identification and expression profiling of odorant-binding proteins and chemosensory proteins of Daktulosphaira vitifoliae (Hemiptera: Phylloxeridae). Journal of Economic Entomology, 110(4), 1813-1820. https://doi.org/10.1093/jee/tox121

[20] Song, Y., Song, Z., Gu, H., Sun, H., & Zhao, J. (2021). Identification and expression analysis of odorant-binding proteins and chemosensory proteins in the antennal transcriptome of Yemma signatus (Hsiao, 1974). Phytoparasitica, 49(5), 917-933. https://doi.org/10.1007/s12600-021-00917-9

[21] Song, Y. Q., Sun, H. Z., & Du, J. (2018). Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Tropidothorax elegans Distant (Hemiptera: Lygaeidae). Scientific Reports, 8(1), 7803. https://doi.org/10.1038/s41598-018-26137-6

[22] Yang, K., He, P., & Dong, S. L. (2014). Different expression profiles suggest functional differentiation among chemosensory proteins in Nilaparvata lugens (Hemiptera: Delphacidae). Journal of Insect Science, 14(1), 270. https://doi.org/10.1093/jisesa/ieu132

[23] Chen, G. L., Pan, Y. F., Ma, Y. F., Wang, J., He, M., & He, P. (2018). Binding affinity characterization of an antennae-enriched chemosensory protein from the white-backed planthopper, Sogatella furcifera (Horváth), with host plant volatiles. Pesticide Biochemistry and Physiology, 152, 1-7. https://doi.org/10.1016/j.pestbp.2018.09.006

[24] Du, Y., Xu, K., Ma, W., Su, W., Tai, M., Zhao, H., Jiang, Y., & Li, X. (2019). Contact chemosensory genes identified in leg transcriptome of Apis cerana cerana (Hymenoptera: Apidae). Journal of Economic Entomology, 112(5), 2015-2029. https://doi.org/10.1093/jee/toz130

[25] Zhu, X., Yu, Q., Gan, X., Song, L., Zhang, K., Zuo, T., Zhang, J., Hu, Y., Chen, Q., & Ren, B. (2022). Transcriptome analysis and identification of chemosensory genes in Baryscapus dioryctriae (Hymenoptera: Eulophidae). Insects, 13(12), 1098. https://doi.org/10.3390/insects13121098

[26] Zhao, Y., Wang, F., Zhang, X., Zhang, S., Guo, S., Zhu, G., Liu, Q., & Li, M. (2016). Transcriptome and expression patterns of chemosensory genes in antennae of the parasitoid wasp Chouioia cunea. PLoS One, 11(2), e0148159. https://doi.org/10.1371/journal.pone.0148159

[27] Wang, S. N., Shan, S., Liu, J. T., Li, R. J., Lu, Z. Y., Dhiloo, K. H., Khashaveh, A., & Zhang, Y. J. (2018). Characterization of antennal chemosensilla and associated odorant binding as well as chemosensory proteins in the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidae). Scientific Reports, 8(1), 7649. https://doi.org/10.1038/s41598-018-25996-3

[28] Wang, R., Li, F., Zhang, W., Zhang, X., Qu, C., Tetreau, G., Sun, L., Luo, C., & Zhou, J. (2017). Identification and expression profile analysis of odorant binding protein and chemosensory protein genes in Bemisia tabaci MED by head transcriptome. PLoS One, 12(2), e0171739. https://doi.org/10.1371/journal.pone.0171739

[29] Xu, Q., Wu, Z., Zeng, X., & An, X. (2020). Identification and expression profiling of chemosensory genes in Hermetia illucens via a transcriptomic analysis. Frontiers in Physiology, 11, 720. https://doi.org/10.3389/fphys.2020.00720

[30] Wang, Z. X., Qi, Z. H., Chen, J., Wang, F. L., Gui, L. Y., & Zhang, G. H. (2021). Molecular characterization of chemosensory protein genes in Bactrocera minax (Diptera: Tephritidae). Entomological Research, 51(7), 349-356. https://doi.org/10.1111/1748-5967.12517

[31] Gong, D. P., Zhang, H. J., Zhao, P., Lin, Y., Xia, Q. Y., & Xiang, Z. H. (2007). Identification and expression pattern of the chemosensory protein gene family in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology, 37(3), 266-277. https://doi.org/10.1016/j.ibmb.2006.11.012

[32] Kulmuni, J., Wurm, Y., & Pamilo, P. (2013). Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates. Heredity, 110(6), 538-547. https://doi.org/10.1038/hdy.2012.122

[33] Sun, H., Song, Y., Du, J., Wang, X., & Cheng, Z. (2016). Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Athetis dissimilis (Lepidoptera: Noctuidae). Applied Entomology and Zoology, 51(3), 409-420. https://doi.org/10.1007/s13355-016-0413-8

[34] Liu, S., Shi, X. X., Zhu, Q. Z., Jiao, W. J., Zhu, Z. J., Yu, H., & Zhu, Z. R. (2015). Identification and expression profiles of putative chemosensory protein genes in Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Journal of Asia-Pacific Entomology, 18(1), 99-105. https://doi.org/10.1016/j.aspen.2014.12.006

[35] Walker, W. B., 3rd, Roy, A., Anderson, P., Schlyter, F., Hansson, B. S., & Larsson, M. C. (2019). Transcriptome analysis of gene families involved in chemosensory function in Spodoptera littoralis (Lepidoptera: Noctuidae). BMC Genomics, 20(1), 428. https://doi.org/10.1186/s12864-019-5815-x

[36] Liu, N. Y., Zhang, T., Ye, Z. F., Li, F., & Dong, S. L. (2015). Identification and characterization of candidate chemosensory gene families from Spodoptera exigua developmental transcriptomes. International Journal of Biological Sciences, 11(9), 1036-1048. https://doi.org/10.7150/ijbs.12020

[37] Liu, J., Liu, H., Yi, J., Mao, Y., Li, J., Sun, D., An, Y., & Wu, H. (2021). Transcriptome characterization and expression analysis of chemosensory genes in Chilo sacchariphagus (Lepidoptera: Crambidae), a key pest of sugarcane. Frontiers in Physiology, 12, 636353. https://doi.org/10.3389/fphys.2021.636353

[38] Li, H., Gu, T., Chen, C., Huang, K., Chen, R., & Hao, D. (2019). Identification and expression patterns of chemosensory proteins in the black-back prominent moth, Clostera restitura (Lepidoptera: Notodontidae). European Journal of Entomology, 116, 372-391. https://doi.org/10.14411/eje.2019.039

[39] Yang, H., Dong, J., Sun, Y., Hu, Z., Lv, Q., & Li, D. (2020). Antennal transcriptome analysis and expression profiles of putative chemosensory soluble proteins in Histia rhodope Cramer (Lepidoptera: Zygaenidae). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 33, 100654. https://doi.org/10.1016/j.cbd.2020.100654

[40] Agnihotri, A., Liu, N., & Xu, W. (2021). Chemosensory proteins (CSPs) in the cotton bollworm Helicoverpa armigera. Insects, 13(1), 29. https://doi.org/10.3390/insects13010029

[41] Li, Z., Liu, L., Zong, S., & Tao, J. (2021). Molecular characterization and expression profiling of chemosensory proteins in male Eogystia hippophaecolus (Lepidoptera: Cossidae). Journal of Entomological Science, 56(2), 217-234. https://doi.org/10.18474/0749-8004-56.2.217

[42] Zhang, Y. N., Jin, J. Y., Jin, R., Xia, Y. H., Zhou, J. J., Deng, J. Y., & Dong, S. L. (2013). Differential expression patterns in chemosensory and non-chemosensory tissues of putative chemosensory genes identified by transcriptome analysis of insect pest the purple stem borer Sesamia inferens (Walker). PLoS One, 8(7), e69715. https://doi.org/10.1371/journal.pone.0069715

[43] Wei, H. S., Li, K. B., Zhang, S., Cao, Y. Z., & Yin, J. (2017). Identification of candidate chemosensory genes by transcriptome analysis in Loxostege sticticalis Linnaeus. PLoS One, 12(4), e0174036. https://doi.org/10.1371/journal.pone.0174036

[44] Tian, Z., Sun, L., Li, Y., Quan, L., Zhang, H., Yan, W., Yue, Q., & Qiu, G. (2018). Antennal transcriptome analysis of the chemosensory gene families in Carposina sasakii (Lepidoptera: Carposinidae). BMC Genomics, 19(1), 544. https://doi.org/10.1186/s12864-018-4900-x

[45] Chen, W. B., Du, L. X., Gao, X. Y., Sun, L. L., Chen, L. L., Xie, G. Y., An, S. H., & Zhao, X. C. (2022). Identification of odorant-binding and chemosensory protein genes in Mythimna separata adult brains using transcriptome analyses. Frontiers in Physiology, 13, 839559. https://doi.org/10.3389/fphys.2022.839559

[46] Wu, L., Zhai, X., Li, L., Li, Q., Liu, F., & Zhao, H. (2021). Identification and expression profile of chemosensory genes in the small hive beetle Aethina tumida. Insects, 12(8), 661. https://doi.org/10.3390/insects12080661

[47] González-González, A., Rubio-Meléndez, M. E., Ballesteros, G. I., Ramírez, C. C., & Palma-Millanao, R. (2019). Sex- and tissue-specific expression of odorant-binding proteins and chemosensory proteins in adults of the scarab beetle Hylamorpha elegans (Burmeister) (Coleoptera: Scarabaeidae). PeerJ, 7, e7054. https://doi.org/10.7717/peerj.7054

[48] Li, Z., Dai, L., Chu, H., Fu, D., Sun, Y., & Chen, H. (2018). Identification, expression patterns, and functional characterization of chemosensory proteins in Dendroctonus armandi (Coleoptera: Curculionidae: Scolytinae). Frontiers in Physiology, 9, 291. https://doi.org/10.3389/fphys.2018.00291

[49] Li, X., Ju, Q., Jie, W., Li, F., Jiang, X., Hu, J., & Qu, M. (2015). Chemosensory gene families in adult antennae of Anomala corpulenta Motschulsky (Coleoptera: Scarabaeidae: Rutelinae). PLoS One, 10(4), e0121504. https://doi.org/10.1371/journal.pone.0121504

[50] Yuan, X., Jiang, Y. D., Wang, G. Y., Yu, H., Zhou, W. W., Liu, S., Yang, M. F., Cheng, J., Gurr, G. M., Way, M. O., & Zhu, Z. R. (2016). Odorant-binding proteins and chemosensory proteins from an invasive pest Lissorhoptrus oryzophilus (Coleoptera: Curculionidae). Environmental Entomology, 45(5), 1276-1286. https://doi.org/10.1093/ee/nvw111

[51] Li, H., Zhang, A., Chen, L. Z., Zhang, G., & Wang, M. Q. (2014). Construction and analysis of cDNA libraries from the antennae of Batocera horsfieldi and expression pattern of putative odorant binding proteins. Journal of Insect Science, 14(1), 57. https://doi.org/10.1093/jis/14.1.57

[52] Wu, Z., Tong, N., Li, Y., Guo, J., Lu, M., & Liu, X. (2022). Foreleg Ttranscriptomic analysis of the chemosensory gene families in Plagiodera versicolora (Coleoptera: Chrysomelidae). Insects, 13(9), 763. https://doi.org/10.3390/insects13090763

[53] Lechuga-Paredes, P., Segura-León, O. L., Cibrián-Tovar, J., Torres-Huerta, B., Velázquez-González, J. C., & Cruz-Jaramillo, J. L. (2023). Odorant-binding and chemosensory proteins in Anthonomus eugenii (Coleoptera: Curculionidae) and their tissue expression. International Journal of Molecular Sciences, 24(4), 3406. https://doi.org/10.3390/ijms24043406

[54] Pei, Y. W., Wu, Z. R., Zhang, H. N., Lu, M., & Liu, X. L. (2023). Transcriptome analysis and expression profiles of odorant binding proteins and chemosensory proteins in Orius sauteri. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 48, 101137. https://doi.org/10.1016/j.cbd.2023.101137

[55] Niu, D. J., Liu, Y., Dong, X. T., & Dong, S. L. (2016). Transcriptome based identification and tissue expression profiles of chemosensory genes in Blattella germanica (Blattaria: Blattidae). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 18, 30-43. https://doi.org/10.1016/j.cbd.2016.03.002

[56] He, M., Ma, Y. F., Guo, H., Liu, X. Z., Long, G. J., Wang, Q., Dewer, Y., Zhang, F., & He, P. (2022). Genome-wide identification and expression pattern analysis of novel chemosensory genes in the German cockroach Blattella germanica. Genomics, 114(2), 110310. https://doi.org/10.1016/j.ygeno.2022.110310

[57] Iovinella, I., Bozza, F., Caputo, B., Della Torre, A., & Pelosi, P. (2013). Ligand-binding study of Anopheles gambiae chemosensory proteins. Chemical Senses, 38(5), 409-419. https://doi.org/10.1093/chemse/bjt012

[58] Li, H., Tan, J., Song, X., Wu, F., Tang, M., Hua, Q., Zheng, H., & Hu, F. (2017). Sublethal doses of neonicotinoid imidacloprid can interact with honey bee chemosensory protein 1 (CSP1) and inhibit its function. Biochemical and Biophysical Research Communications, 486(2), 391-397. https://doi.org/10.1016/j.bbrc.2017.03.051

[59] Liu, G., Arnaud, P., Offmann, B., & Picimbon, J. F. (2017). Genotyping and bio-sensing chemosensory proteins in insects. Sensors, 17(8), 1801. https://doi.org/10.3390/s17081801

[60] Lin, X., Mao, Y., & Zhang, L. (2018). Binding properties of four antennae-expressed chemosensory proteins (CSPs) with insecticides indicates the adaption of Spodoptera litura to environment. Pesticide Biochemistry and Physiology, 146, 43-51. https://doi.org/10.1016/j.pestbp.2018.02.011

[61] Dong, X., Zhai, Y., Hu, M., Zhong, G., Huang, W., Zheng, Z., & Han, P. (2013). Proteomic and properties analysis of botanical insecticide rhodojaponin III-induced response of the diamondback moth, Plutella xyllostella (L.). PLoS One, 8(7), e67723. https://doi.org/10.1371/journal.pone.0067723

[62] Liu, Y. L., Guo, H., Huang, L. Q., Pelosi, P., & Wang, C. Z. (2014). Unique function of a chemosensory protein in the proboscis of two Helicoverpa species. Journal of Experimental Biology, 217(10), 1821-1826. https://doi.org/10.1242/jeb.102020

[63] Cui, L., Rui, C., Yang, D., Wang, Z., & Yuan, H. (2017). De novo transcriptome and expression profile analyses of the Asian corn borer (Ostrinia furnacalis) reveals relevant flubendiamide response genes. BMC Genomics, 18(1), 20. https://doi.org/10.1186/s12864-016-3431-6

[64] Bautista, M. A., Bhandary, B., Wijeratne, A. J., Michel, A. P., Hoy, C. W., & Mittapalli, O. (2015). Evidence for trade-offs in detoxification and chemosensation gene signatures in Plutella xylostella. Pest Management Science, 71(3), 423-432. https://doi.org/10.1002/ps.3822

[65] Pottier, M. A., Bozzolan, F., Chertemps, T., Jacquin-Joly, E., Lalouette, L., Siaussat, D., & Maïbèche-Coisne, M. (2012). Cytochrome P450s and cytochrome P450 reductase in the olfactory organ of the cotton leafworm Spodoptera littoralis. Insect Molecular Biology, 21(6), 568-580. https://doi.org/10.1111/j.1365-2583.2012.01160.x

[66] Ingham, V. A., Anthousi, A., Douris, V., Harding, N. J., Lycett, G., Morris, M., Vontas, J., & Ranson, H. (2020). A sensory appendage protein protects malaria vectors from pyrethroids. Nature, 577(7790), 376-380. https://doi.org/10.1038/s41586-019-1864-1

[67] Li, F., Venthur, H., Wang, S., Homem, R. A., & Zhou, J. J. (2021). Evidence for the involvement of the chemosensory protein AgosCSP5 in resistance to insecticides in the cotton aphid, Aphis gossypii. Insects, 12(4), 335. https://doi.org/10.3390/insects12040335

[68] Xu, H., Pan, Y., Li, J., Yang, F., Chen, X., Gao, X., Wen, S., & Shang, Q. (2022). Chemosensory proteins confer adaptation to the ryanoid anthranilic diamide insecticide cyantraniliprole in Aphis gossypii glover. Pesticide Biochemistry and Physiology, 184, 105076. https://doi.org/10.1016/j.pestbp.2022.105076

[69] Xu, H., Yan, K., Ding, Y., Lv, Y., Li, J., Yang, F., Chen, X., Gao, X., Pan, Y., & Shang, Q. (2022). Chemosensory proteins are associated with thiamethoxam and spirotetramat tolerance in Aphis gossypii glover. International Journal of Molecular Sciences, 23(4), 2356. https://doi.org/10.3390/ijms23042356

[70] Nomura, A., Kawasaki, K., Kubo, T., & Natori, S. (1992). Purification and localization of p10, a novel protein that increases in nymphal regenerating legs of Periplaneta americana (American cockroach). International Journal of Developmental Biology, 36(3), 391-398.

[71] McKenna, M. P., Hekmat-Scafe, D. S., Gaines, P., & Carlson, J. R. (1994). Putative Drosophila pheromone-binding proteins expressed in a subregion of the olfactory system. Journal of Biological Chemistry, 269(23), 16340-16347. https://doi.org/10.1016/s0021-9258(17)34013-9

[72] Robertson, H. M., Martos, R., Sears, C. R., Todres, E. Z., Walden, K. K., & Nardi, J. B. (1999). Diversity of odourant binding proteins revealed by an expressed sequence tag project on male Manduca sexta moth antennae. Insect Molecular Biology, 8(4), 501-518. https://doi.org/10.1046/j.1365-2583.1999.00146.x

[73] Angeli, S., Ceron, F., Scaloni, A., Monti, M., Monteforti, G., Minnocci, A., Petacchi, R., & Pelosi, P. (1999). Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. European Journal of Biochemistry, 262(3), 745-754. https://doi.org/10.1046/j.1432-1327.1999.00438.x

[74] Zhou, J. J., Vieira, F. G., He, X. L., Smadja, C., Liu, R., Rozas, J., & Field, L. M. (2010). Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Molecular Biology, 19(S2), 113-122. https://doi.org/10.1111/j.1365-2583.2009.00919.x

[75] Leal, W. S. (2013). Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58(1), 373-391. https://doi.org/10.1146/annurev-ento-120811-153635

[76] Pelosi, P., Iovinella, I., Felicioli, A., & Dani, F. R. (2014). Soluble proteins of chemical communication: An overview across arthropods. Frontiers in Physiology, 5, 320. https://doi.org/10.3389/fphys.2014.00320

[77] Venthur, H., & Zhou, J. J. (2018). Odorant receptors and odorant-binding proteins as insect pest control targets: A comparative analysis. Frontiers in Physiology, 9, 1163. https://doi.org/10.3389/fphys.2018.01163

[78] Pelosi, P., Iovinella, I., Zhu, J., Wang, G., & Dani, F. R. (2018). Beyond chemoreception: Diverse tasks of soluble olfactory proteins in insects. Biological Reviews of the Cambridge Philosophical Society, 93(1), 184-200. https://doi.org/10.1111/brv.12339

[79] Rihani, K., Ferveur, J. F., & Briand, L. (2021). The 40-year mystery of insect odorant-binding proteins. Biomolecules, 11(4), 509. https://doi.org/10.3390/biom11040509

[80] Ha, T. S., & Smith, D. P. (2022). Recent insights into insect olfactory receptors and odorant-binding proteins. Insects, 13(10), 926. https://doi.org/10.3390/insects13100926

[81] Saba, N. U., Ye, C., Zhang, W., Wu, T., Wang, Y., Zhang, X., Song, Z., Xing, L., & Su, X. (2022). The antennal sensilla and expression patterns of olfactory genes in the lower termite Reticulitermes aculabialis (Isoptera: Rhinotermitidae). Journal of Insect Science, 22(4), 11. https://doi.org/10.1093/jisesa/ieac045

[82] Li, H., Yang, Y., Xu, G., Wu, D., Lv, W., Jiang, Q., & Zhao, Y. (2016). Cloning, expression and localization of DacaCSP2 and DacaCSP3 during different reproductive stages in Daphnia carinata. Gene, 582(1), 59-68. https://doi.org/10.1016/j.gene.2016.01.048

[83] Pino, J., Godoy, R., Venthur, H., Larama, G., Quiroz, A., & Mutis, A. (2023). Identification and ligand binding of a chemosensory protein from sea louse Caligus rogercresseyi (Crustacea: Copepoda). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 265, 110830. https://doi.org/10.1016/j.cbpb.2023.110830

[84] Mita, K., Kasahara, M., Sasaki, S., Nagayasu, Y., Yamada, T., Kanamori, H., Namiki, N., Kitagawa, M., Yamashita, H., Yasukochi, Y., Kadono-Okuda, K., Yamamoto, K., Ajimura, M., Ravikumar, G., Shimomura, M., Nagamura, Y., Shin-I, T., Abe, H., Shimada, T., Morishita, S., & Sasaki, T. (2004). The genome sequence of silkworm, Bombyx mori. DNA Research, 11(1), 27-35. https://doi.org/10.1093/dnares/11.1.27

[85] Martín-Blázquez, R., Chen, B., Kang, L., & Bakkali, M. (2017). Evolution, expression and association of the chemosensory protein genes with the outbreak phase of the two main pest locusts. Scientific Reports, 7(1), 6653. https://doi.org/10.1038/s41598-017-07068-0

[86] Campanacci, V., Lartigue, A., Hällberg, B. M., Jones, T. A., Giudici-Orticoni, M. T., Tegoni, M., & Cambillau, C. (2003). Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proceedings of the National Academy of Sciences of the United States of America, 100(9), 5069-5074. https://doi.org/10.1073/pnas.0836654100

[87] Leal, W. S., Nikonova, L., & Peng, G. (1999). Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori. FEBS Letters, 464(1-2), 85-90. https://doi.org/10.1016/s0014-5793(99)01683-x

[88] Ban, L., Zhang, L., Yan, Y., & Pelosi, P. (2002). Binding properties of a locust's chemosensory protein. Biochemical and Biophysical Research Communications, 293(1), 50-54. https://doi.org/10.1016/S0006-291X(02)00185-7

[89] Tuccini, A., Maida, R., Rovero, P., Mazza, M., & Pelosi, P. (1996). Putative odorant-binding protein in antennae and legs of Carausius morosus (Insecta, Phasmatodea). Insect Biochemistry and Molecular Biology, 26(1), 19-24. https://doi.org/10.1016/0965-1748(95)00051-8

[90] Maleszka, R., & Stange, G. (1997). Molecular cloning, by a novel approach, of a cDNA encoding a putative olfactory protein in the labial palps of the moth Cactoblastis cactorum. Gene, 202(1-2), 39-43. https://doi.org/10.1016/s0378-1119(97)00448-4

[91] Maleszka, J., Forêt, S., Saint, R., & Maleszka, R. (2007). RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Development Genes and Evolution, 217(3), 189-196. https://doi.org/10.1007/s00427-006-0127-y

[92] Guo, W., Wang, X., Ma, Z., Xue, L., Han, J., Yu, D., & Kang, L. (2011). CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. PLoS Genetics, 7(2), e1001291. https://doi.org/10.1371/journal.pgen.1001291

[93] Zeng, X., Pan, Y., Tian, F., Li, J., Xu, H., Liu, X., Chen, X., Gao, X., Peng, T., Bi, R., & Shang, Q. (2021). Functional validation of key cytochrome P450 monooxygenase and UDP-glycosyltransferase genes conferring cyantraniliprole resistance in Aphis gossypii Glover. Pesticide Biochemistry and Physiology, 176, 104879. https://doi.org/10.1016/j.pestbp.2021.104879

[94] Shang, J., Tang, G., Yang, J., Lu, M., Wang, C. Z., & Wang, C. (2023). Sensing of a spore surface protein by a Drosophila chemosensory protein induces behavioral defense against fungal parasitic infections. Current Biology, 33(2), 276-286.e5. https://doi.org/10.1016/j.cub.2022.11.004

[95] Zhu, J., Iovinella, I., Dani, F. R., Liu, Y. L., Huang, L. Q., Liu, Y., Wang, C. Z., Pelosi, P., & Wang, G. (2016). Conserved chemosensory proteins in the proboscis and eyes of Lepidoptera. International Journal of Biological Sciences, 12(11), 1394-1404. https://doi.org/10.7150/ijbs.16517

[96] Jacquin-Joly, E., Vogt, R. G., François, M. C., & Nagnan-Le Meillour, P. (2001). Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chemical Senses, 26(7), 833-844. https://doi.org/10.1093/chemse/26.7.833

[97] Oduol, F., Xu, J., Niare, O., Natarajan, R., & Vernick, K. D. (2000). Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria. Proceedings of the National Academy of Sciences of the United States of America, 97(21), 11397-11402. https://doi.org/10.1073/pnas.180060997

[98] McDonald, M. J., & Rosbash, M. (2001). Microarray analysis and organization of circadian gene expression in Drosophila. Cell, 107(5), 567-578. https://doi.org/10.1016/s0092-8674(01)00545-1

[99] Liu, X., Luo, Q., Zhong, G., Rizwan-Ul-Haq, M., & Hu, M. (2010). Molecular characterization and expression pattern of four chemosensory proteins from diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Journal of Biochemistry, 148(2), 189-200. https://doi.org/10.1093/jb/mvq050

[100] Younas, A., Waris, M. I., Shaaban, M., Tahir Ul Qamar, M., & Wang, M. Q. (2022). Appraisal of MsepCSP14 for chemosensory functions in Mythimna separata. Insect Science, 29(1), 162-176. https://doi.org/10.1111/1744-7917.12909

[101] Liu, R., He, X., Lehane, S., Lehane, M., Hertz-Fowler, C., Berriman, M., Field, L. M., & Zhou, J. J. (2012). Expression of chemosensory proteins in the tsetse fly Glossina morsitans is related to female host-seeking behaviour. Insect Molecular Biology, 21(1), 41-48. https://doi.org/10.1111/j.1365-2583.2011.01114.x

[102] Briand, L., Swasdipan, N., Nespoulous, C., Bézirard, V., Blon, F., Huet, J. C., Ebert, P., & Penollet, J. C. (2002). Characterization of a chemosensory protein (ASP3c) from honeybee (Apis mellifera L.) as a brood pheromone carrier. European Journal of Biochemistry, 269(18), 4586-4596. https://doi.org/10.1046/j.1432-1033.2002.03156.x

[103] Zhou, X. H., Ban, L. P., Iovinella, I., Zhao, L. J., Gao, Q., Felicioli, A., Sagona, S., Pieraccini, G., Pelosi, P., Zhang, L., & Dani, F. R. (2013). Diversity, abundance, and sex-specific expression of chemosensory proteins in the reproductive organs of the locust Locusta migratoria manilensis. Biological Chemistry, 394(1), 43-54. https://doi.org/10.1515/hsz-2012-0114

[104] Zhang, Y. N., Ye, Z. F., Yang, K., & Dong, S. L. (2014). Antenna-predominant and male-biased CSP19 of Sesamia inferens is able to bind the female sex pheromones and host plant volatiles. Gene, 536(2), 279-286. https://doi.org/10.1016/j.gene.2013.12.011

[105] He, Y. Q., Feng, B., Guo, Q. S., & Du, Y. (2017). Age influences the olfactory profiles of the migratory oriental armyworm mythimna separate at the molecular level. BMC Genomics, 18(1), 32. https://doi.org/10.1186/s12864-016-3427-2

[106] Duan, S. G., Li, D. Z., & Wang, M. Q. (2019). Chemosensory proteins used as target for screening behaviourally active compounds in the rice pest Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Insect Molecular Biology, 28(1), 123-135. https://doi.org/10.1111/imb.12532

[107] Sun, L., Zhou, J. J., Gu, S. H., Xiao, H. J., Guo, Y. Y., Liu, Z. W., & Zhang, Y. J. (2015). Chemosensillum immunolocalization and ligand specificity of chemosensory proteins in the alfalfa plant bug Adelphocoris lineolatus (Goeze). Scientific Reports, 5(1), 8073. https://doi.org/10.1038/srep08073

[108] Gu, S. H., Wang, S. Y., Zhang, X. Y., Ji, P., Liu, J. T., Wang, G. R., Wu, K. M., Guo, Y. Y., Zhou, J. J., & Zhang, Y. J. (2012). Functional characterizations of chemosensory proteins of the alfalfa plant bug Adelphocoris lineolatus indicate their involvement in host recognition. PLoS One, 7(8), e42871. https://doi.org/10.1371/journal.pone.0042871

[109] Peng, X., Qu, M. J., Wang, S. J., Huang, Y. X., Chen, C., & Chen, M. H. (2021). Chemosensory proteins participate in insecticide susceptibility in Rhopalosiphum padi, a serious pest on wheat crops. Insect Molecular Biology, 30(2), 138-151. https://doi.org/10.1111/imb.12683

[110] Gao, P., Tan, J. J., Su, S., Wang, S. J., Peng, X., & Chen, M. H. (2023). Overexpression of the chemosensory protein CSP7 gene contributed to lambda-cyhalothrin resistance in theBbird cherry-oat aphid Rhopalosiphum padi. Journal of Agricultural and Food Chemistry, 71, 17005-17013. https://doi.org/10.1021/acs.jafc.3c05100

[111] Gao, P., Tan, J., Peng, X., Qu, M., & Chen, M. (2024). Key residues involved in the interaction between chlorpyrifos and a chemosensory protein in Rhopalosiphum padi: Implication for tracking chemical residues via insect olfactory proteins. The Science of the Total Environment, 928, 172361. https://doi.org/10.1016/j.scitotenv.2024.172361

[112] Yao, Q., Liang, Z., & Chen, B. (2023). Evidence for the Pparticipation of chemosensory proteins in response to insecticide challenge in Conopomorpha sinensis. Journal of Agricultural and Food Chemistry, 71(3), 1360-1368. https://doi.org/10.1021/acs.jafc.2c05973

[113] Li, Y., Ni, S., Wang, Y., Li, R., Sun, H., Ye, X., Tian, Z., Zhang, Y., & Liu, J. (2023). The chemosensory protein 1 contributes to indoxacarb resistance in Plutella xylostella (L.). Pest Management Science, 79(7), 2456-2468. https://doi.org/10.1002/ps.7415

[114] Wang, H., Zhao, R., Gao, J., Xiao, X., Yin, X., Hu, S., Zhang, Y., Liang, P., & Gu, S. (2024). Two cuticle-enriched chemosensory proteins confer multi-insecticide resistance in Spodoptera frugiperda. International Journal of Biological Macromolecules, 266, 130941. https://doi.org/10.1016/j.ijbiomac.2024.130941

[115] Yao, Y. J., Yin, N. N., Pu, L. M., Yang, A. J., & Liu, N. Y. (2024). Three chemosensory proteins enriched in antennae and tarsi of Rhaphuma horsfieldi differentially contribute to the binding of insecticides. Pesticide Biochemistry and Physiology, 199, 105797. https://doi.org/10.1016/j.pestbp.2024.105797

[116] Traverso, L., Latorre Estivalis, J. M., da Rocha Fernandes, G., Fronza, G., Lobbia, P., Mougabure Cueto, G., & Ons, S. (2022). Transcriptomic modulation in response to an intoxication with deltamethrin in a population of Triatoma infestans with low resistance to pyrethroids. PLoS Neglected Tropical Diseases, 16(6), e0010060. https://doi.org/10.1371/journal.pntd.0010060

[117] Xiong, W., Gao, S., Lu, Y., Wei, L., Mao, J., Xie, J., Cao, Q., Liu, J., Bi, J., Song, X., & Li, B. (2019). Latrophilin participates in insecticide susceptibility through positively regulating CSP10 and partially compensated by OBPC01 in Tribolium castaneum. Pesticide Biochemistry and Physiology, 159, 107-117. https://doi.org/10.1016/j.pestbp.2019.06.005

[118] Liu, G., Ma, H., Xie, H., Xuan, N., Guo, X., Fan, Z., Rajashekar, B., Arnaud, P., Offmann, B., & Picimbon, J. F. (2016). Biotype characterization, developmental profiling, insecticide response and binding property of Bemisia tabaci chemosensory proteins: Role of CSP in insect defense. PLoS One, 11(5), e0154706. https://doi.org/10.1371/journal.pone.0154706

[119] Zheng, R., Xie, M., Keyhani, N. O., & Xia, Y. (2023). An insect chemosensory protein facilitates locust avoidance to fungal pathogens via recognition of fungal volatiles. International Journal of Biological Macromolecules, 253(6), 127389. https://doi.org/10.1016/j.ijbiomac.2023.127389

[120] Lees, R., Praulins, G., Davies, R., Brown, F., Parsons, G., White, A., Ranson, H., Small, G., & Malone, D. (2019). A testing cascade to identify repurposed insecticides for next-generation vector control tools: Screening a panel of chemistries with novel modes of action against a malaria vector. Gates Open Research, 3, 1464. https://doi.org/10.12688/gatesopenres.12957.2

[121] Turner, J. A., Ruscoe, C. N., & Perrior, T. R. (2016). Discovery to development: Insecticides for malaria vector control. Chimia, 70(10), 684-693. https://doi.org/10.2533/chimia.2016.684

[122] Daina, A., Michielin, O., & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Scientific Reports, 7(1), 42717. https://doi.org/10.1038/srep42717

[123] Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583-589. https://doi.org/10.1038/s41586-021-03819-2

[124] Li, H., Hao, E., Li, Y., Yang, H., Sun, P., Lu, P., & Qiao, H. (2022). Antennal transcriptome analysis of olfactory genes and tissue expression profiling of odorant binding proteins in Semanotus bifasciatus (Cerambycidae: Coleoptera). BMC Genomics, 23(1), 461. https://doi.org/10.1186/s12864-022-08655-w

[125] Wang, J., Sakai, K., & Kiwa, T. (2022). Rational design of peptides derived from odorant-binding proteins for SARS-CoV-2-Rrelated volatile organic compounds recognition. Molecules, 27(12), 3917. https://doi.org/10.3390/molecules27123917

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2025 The Author(s). New Plant Protection published by John Wiley & Sons Australia, Ltd on behalf of Institute of Plant Protection, Chinese Academy of Agricultural Sciences.