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Functional role of TaGSTs1 in the detoxification of spinetoram and development of Tuta absoluta

Published online by Cambridge University Press:  25 August 2025

Amjad Ali
Affiliation:
Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, China
Jiaqi Wu
Affiliation:
Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, China
Jingang Xie
Affiliation:
Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, China
Yu Song
Affiliation:
Institute of Crop Variety Resources, Xinjiang Academy of Agricultural Sciences, Urumqi, China
Ning Liu
Affiliation:
Institute of Crop Variety Resources, Xinjiang Academy of Agricultural Sciences, Urumqi, China
Xiaoning Liu*
Affiliation:
Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, China
*
Corresponding author: Xiaoning Liu; Email: liuxn0103@xju.edu.cn

Abstract

Tuta absoluta has evolved resistance to many biological insecticides, resulting in significant annual agricultural and economic losses. Glutathione S-transferases (GSTs) are one of the major insect detoxification enzyme systems. However, the detoxification metabolism of GSTs in T. absoluta against biological insecticides remains poorly understood. In this study, We identified five key GST genes (TaGSTs1, TaGSTs2, TaGSTe1, TaGSTe3, and TaGSTd1) by screening from the comparative transcriptomes of two regional populations of T. absoluta in Xinjiang, China. Among the five GSTs, TaGSTs1 exhibited a significantly high expression level during the larval stage of T. absoluta following exposure to the LC50 dose of spinetoram. This gene was subsequently cloned, and its expression was knocked down using RNA interference to further analyse its role in the detoxification of spinetoram, as well as in the growth and development of T. absoluta. The results showed that TaGSTs1 contains a typical GST gene domain and was highly conserved within the Lepidoptera clade. Silencing of the TaGSTs1 gene led to a significant increase in the susceptibility of T. absoluta to spinetoram, as evidenced by an extension in the duration of leaf-mining and in the development time from the 2nd to the 4th instar larval stage, which were 35.7% and 19.6% longer, respectively, than those of ddH2O and dsGFP controls. Furthermore, the mortality rate of larvae treated with dsTaGSTs1 reached 57.3% by the 7th day. These findings indicate that TaGSTs1 plays a crucial role in the detoxification of spinetoram and in the growth and development of T. absoluta larvae.

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Research Paper
Copyright
© The Author(s), 2025. Published by Cambridge University Press.

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Co-first authors.

References

Amezian, D, Nauen, R and Le Goff, G (2021) Transcriptional regulation of xenobiotic detoxification genes in insects. Pesticides Biochemistry and Physiology 174, 104822.CrossRefGoogle ScholarPubMed
Askew, WT, Edwards, MG and Gatehouse, AMR (2024) Ex vivo delivery of dsRNA targeting ryanodine receptors for control of Tuta absoluta. Pest Management Science 80, 64006408.CrossRefGoogle ScholarPubMed
Biondi, A, Guedes, RNC, Wan, FH and Desneux, N (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: Past, present, and future. Entomology 63, 239258.CrossRefGoogle ScholarPubMed
Biondi, A, Zappalà, L, Stark, JD and Desneux, N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects. PLoS One 8(9), e76548.CrossRefGoogle ScholarPubMed
Campos, MR, Rodrigues, ARS, Silva, WM, Silva, TBM, Silva, VRF, Guedes, RNC and Siqueira, HAA (2014) Spinosad and the Tomato Borer Tuta absoluta: A Bioinsecticide, an invasive pest threat, and high insecticide resistance. PLOS ONE 9(8), e103235.CrossRefGoogle ScholarPubMed
Desneux, N, Luna, MG, Guillemaud, T and Urbaneja, A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: The new threat to tomato world production. Pest Management Science 84, 403408.CrossRefGoogle Scholar
Desneux, N, Wajnberg, E, Wyckhuys, KAG, Burgio, G, Arpaia, S, Narváez-Vasquez, CA, González-Cabrera, J, Catalán Ruescas, D, Tabone, E, Frandon, J, Pizzol, J, Poncet, C, Cabello, T and Urbaneja, A (2010) Biological invasion of European tomato crops by Tuta absoluta: Ecology, history of invasion and prospects for biological control. Pest Management Science 83, 197215.CrossRefGoogle Scholar
Gawande, ND, Subashini, S, Murugan, M and Subbarayalu, M (2014) Molecular screening of insecticides with sigma glutathione S-transferases (GST) in cotton aphid Aphis gossypii using docking. Bioinformation 11, 679683.CrossRefGoogle Scholar
Guedes, RNC and Picanço, MC (2012) The tomato borer Tuta absoluta in South America: Pest status, management and insecticide resistance. EPPO Bull 42, 211216.CrossRefGoogle Scholar
Hayes, JD, Flanagan, JU and Jowsey, IR (2005) Glutathione S-transferases. Annual Review Pharmacology 45, 5188.CrossRefGoogle Scholar
Hu, C, Liu, JY, Wang, W, Mota-Sanchez, D, He, S and Shi, Y (2022) Glutathione S-transferase genes are involved in lambda cyhalothrin resistance in Cydia pomonella via sequestration. Journal of Agriculture and Food Chemistry 70, 22652279.CrossRefGoogle ScholarPubMed
Hu, C, Wang, W, Ju, D, Chen, GM, Tan, XL, Mota-Sanchez, D and Yang, XQ (2020a) Functional characterization of a novel λ-cyhalothrin metabolising glutathione S-transferase, CpGSTe3, from the codling moth Cydia pomonella. Pest Management Science 76, 10391047.CrossRefGoogle Scholar
Hu, C, Wei, ZH, Li, PR, Harwood, JD, Li, XY and Yang, XQ (2020b) Identification and functional characterization of a sigma glutathione S-transferase CpGSTs2 involved in λ-cyhalothrin resistance in the codling moth Cydia pomonella. Agriculture and Food Chemistry 68, 1258512594.CrossRefGoogle Scholar
Kinyanjui, G, Khamis, FM, Ombura, FLO, Kenya, EU, Ekesi, S and Mohamed, SA (2021) Distribution, abundance and natural enemies of the invasive tomato leafminer, Tuta absoluta (Meyrick) in Kenya. Bulletin of Èntomology Resources 111, 658673.CrossRefGoogle ScholarPubMed
Koirala, BK, Moural, ST and Zhu, F (2022) Functional and structural diversity of insect glutathione S-transferases in xenobiotic adaptation. International Journal of Biological Science 18, 57135723.CrossRefGoogle Scholar
Labade, CP, Jadhav, AR, Ahire, M, Zinjarde, SS and Tamhane, VA (2018) Role of induced glutathione-S-transferase from Helicoverpa armigera (Lepidoptera:Noctuidae) HaGST-8 in detoxification of pesticides. Ecotoxicology and Environmental Safety Journal 147, 612621.CrossRefGoogle ScholarPubMed
Li, GW, Chen, XL, Xu, XL and Wu, JX (2018) Degradation of sex pheromone and plant volatile components by an antenna glutathione S-transferase in the oriental fruit moth, Grapholita molesta Busck (Lepidoptera: Tortricidae. Archives of Insect Biochem Physiology 999, e1512.Google Scholar
Li, H, Zhang, BX, Liu, FF, Liu, Z, Zhang, WT, Wang, Q, Sun, YX, Toufeeq, S and Rao, XJ (2022) Toxicological and transcriptomic effects in Mythimna separata (Lepidoptera: Noctuidae) exposed to chlorantraniliprole and functional characterization of glutathione S-transferases. Pest Management Science 78, 45174532.CrossRefGoogle ScholarPubMed
Li, X, Schuler, MA and Berenbaum, MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review Entomology 52, 231253.CrossRefGoogle ScholarPubMed
Li, YQ, Huang, A and Li, XJ (2024) RNAi targeting Naν and CPR via leaf delivery reduces adult emergence and increases the susceptibility to λ-cyholthin in Tuta absoluta (meyrick). Pesticides Biochemistry and Physiology 204, 106089.CrossRefGoogle Scholar
Liu, S, Zhang, YX, Wang, WL, Zhang, BX and Li, SG (2017b) Identification and characterization of seventeen glutathione S-transferase genes from the cabbage white butterfly Pieris rapae. Pesticide Biochemistry and Physiology 143, 102110.CrossRefGoogle Scholar
Liu, ZX, Xing, XR, Liang, XH, Ding, JH, Li, YJ, Shao, Y, Wu, FA, Wang, J and Sheng, S (2022) The role of glutathione-S-transferases in phoxim and chlorfenapyr tolerance in a major mulberry pest, Glyphodes pyloalis walker (Lepidoptera: Pyralidae). Pesticide Biochemistry and Physiology 181, 105004.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCt method. Methods 25, 402408.CrossRefGoogle Scholar
Lu, K, Song, Y and Zeng, R (2021) The role of Glutathion S-transferase mediated detoxification in insect adaptation to xenobiotics. Current Opinion Insect Science 43, 103107.CrossRefGoogle Scholar
Lu, XP, Wang, LL, Huang, Y, Dou, W, Chen, CT, Wei, D and Wang, JJ (2016) The epsilon glutathione S-transferases contribute to the malathion resistance in the oriental fruit fly, Bactrocera dorsalis (Hendel). Comparative Biochemistry and Physiology C 180, 4048.Google Scholar
Lumjuan, N, Rajatileka, S, Changsom, D, Wicheer, J, Leelapat, P, Prapanthadara, LA, Somboon, P, Lycett, G and Ranson, H (2011) The role of epsilon-3 glutathione transferases in in wing development in the Aedes aegypti. Insect Biochemistry and Molecular Biology 41, 203209.CrossRefGoogle Scholar
Pavlidi, N, Vontas, J and Van Leeuwen, T (2018) The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests. Insect Science 27, 97102.Google ScholarPubMed
Rane, RV, Ghodke, AB, Hoffmann, AA, Edwards, OR, Walsh, TK and Oakeshott, JG (2019) Detoxifying enzyme complements and host use phenotypes in 160 insect species. Current Opinion Insect Science 31, 131138.CrossRefGoogle ScholarPubMed
Sağlam, Ö, Çelik, A, Işıkber, AA, Bozkurt, H, Sakka, MK and Athanassiou, CG (2022) Efficacy of Spinetoram for the Control of Bean Weevil, Acanthoscelides obtectus (Coleoptera: Chrysomelidae) on Different Surfaces. Insects 13(8), 723.CrossRefGoogle ScholarPubMed
Shashank, PR, Twinkle, S, Chandrashekar, K, Meshram, NM, Suroshe, SS and Bajracharya, AS (2018) Genetic homogeneity in South American tomato pinworm, Tuta absoluta: A new invasive pest to oriental region. 3 Biotech 8, 350.CrossRefGoogle ScholarPubMed
Sue, M and Yajima, S (2018) Crystal structure of the delta-class glutathione transferase in Musca domestica. Biochemical and Biophysical Research Communications 502, 345350.CrossRefGoogle ScholarPubMed
Sun, L, Yin, J, Du, H, Liu, P and Cao, C (2020) Characterization of GST genes from the Hyphantria cunea and their response to the oxidative stress caused by the infection of Hyphantria cunea nucleopolyhedrovirus (HcNPV). Pesticide Biochemistry and Physiology 163, 254262.CrossRefGoogle Scholar
Tamilselvan, R, Kennedy, JS and Suganthi, A (2021) Monitoring the resistance and baseline susceptibility of Plutella xylostella (Lepidoptera: Plutellidae) against spinetoram in Tamil Nadu, India. Crop Protection 142, 105491.CrossRefGoogle Scholar
USDA–APHIS (2014) United States Department of Agriculture, Animal and Plant Health Inspection Service, Federal Order for U.S. imports of host materials of tomato leaf miner (Tuta absoluta). USDA Accessed 02 Oct 2017.Google Scholar
Vargas, H (1970) Observations about the biology and natural enemies of the tomato moth, Gnorimoschema absoluta (Meyrick) (Lepidoptera: Gelechiidae). Idesia 1, 75110.Google Scholar
Wang, J, Gao, JC and Guan, H (2021a) Occurrence and control suggestions of tomato leafminer in Xinjiang. China Plant Protection Guide 41, 8384+79.Google Scholar
Wang, JL, Xiao, YB, Gao, HT and Liu, TD (2014) A preliminary study on the effect of spinosyn and its spinosyn compound on field insect control. Grain and Food Industry 21(5), 8184+91.Google Scholar
Wang, K, Guo, C, Liu, Y, Wang, J and Wang, C (2022) Application and research progress of spinosyn insecticides and their resistance. World Pesticides 44(2), 1824.Google Scholar
Wang, Q, Rui, C, Wang, L, Nahiyoon, SA, Huang, W, Zhu, J, Ji, X, Yang, Q, Yuan, H and Cui, L (2021b) Field-evolved resistance to 11 insecticides and the mechanisms involved in Helicoverpa armigera (Lepidoptera: Noctuidae). Pest Management Science 77(11), 50865095.CrossRefGoogle Scholar
Wang, Y, Qiu, L, Ranson, H, Lumjuan, N, Hemingway, J and Setzer, WN (2008) Structure of an insect epsilon class glutathione S-transferase from the malaria vector Anopheles gambiae provides an explanation for the high DDT-detoxifying activity. Journal of Structural Biology 164, 228235.CrossRefGoogle ScholarPubMed
Xia, D, Zheng, R, Huang, J, Lu, S and Tang, Q (2022) Identification and functional analysis of glutathione S-transferases from Sitophilus zeamais in olfactory organ. Insects 13, 259.CrossRefGoogle ScholarPubMed
Yang, R (2016) Research progress of spinosyns. Chemical Management 6, 7273.Google Scholar
Yin, YQ, Zheng, LP, Li, FQ, Ma, TZ, Song, WH, Chen, F, Chen, FS, Liu, Y and Chen, AD (2021) Occurrence and field control effect of tomato leafminer in Midu County, Yunnan. Environmental Entomology 43, 559566.Google Scholar
Yu, X and Killiny, N (2018) RNA interference of two glutathione S-transferase genes, Diaphorina citri DcGSTe2 and DcGSTd1, increases the susceptibility of Asian citrus psyllid (Hemiptera: Liviidae) to the pesticides fenpropathrin and thiamethoxam. Pest Management Science 74, 638647.CrossRefGoogle Scholar
Zhang, BZ, Su, X, Xie, LF, Zhen, CA, Hu, GL, Jiang, K, Huang, ZY, Liu, RQ, Gao, YF, Chen, XL and Gao, XW (2020) Multiple detoxification genes confer imidacloprid resistance to Sitobion avenae Fabricius. Crop Protection 128, 105014.CrossRefGoogle Scholar
Zhang, J, Khan, SA, Heckel, DG and Bock, R (2017) Next-generation insect-resistant plants: RNAi-mediated crop protection. Trends in Biotechnology 35(9), 871882.CrossRefGoogle ScholarPubMed
Zhang, J, Ma, W, Yin, F, Park, Y, Zhu, KY, Zhang, X, Qin, X and Li, D (2022) Evaluations of two glutathione S-transferase epsilon genes for their contributions to metabolism of three selected insecticides in Locusta migratoria. Pesticides Biochemistry and Physiology 183, 105084.CrossRefGoogle ScholarPubMed
Zhou, WW, Liang, QM, Xu, Y, Gurr, GM, Bao, YY, Zhou, XP, Zhang, CX, Cheng, J and Zhu, ZR (2013) Genomic insights into the glutathione S-transferase gene family of two rice planthoppers, Nilaparvata lugens (Stål) and Sogatella furcifera (Horv´ ath) (Hemiptera: Delphacidae). PLoS One 8, e56604.CrossRefGoogle Scholar
Zou, X, Xu, Z, Zou, H, Liu, J, Chen, S and Feng, Q (2016) Glutathione S-transferase SlGSTe1 in Spodoptera litura may be associated with feeding adaptation of host plants. Insect Biochemistry and Molecular Biology 70, 3243.CrossRefGoogle ScholarPubMed
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