High detoxification enzyme and gene expression level in tomato leafminer, Tuta absoluta, explains resistance to fenvalerate

Volume 14, Issue 1
February 2025
Pages 1-10

Document Type : Original Research

Authors

Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, Tehran 14115-336, Iran.

Abstract
The tomato leafminer, Tuta absoluta, is a pest that greatly harms crops. Regrettably, the application of insecticides has resulted in the emergence of resistance in the tomato leafminer. Metabolic resistance is the most prevalent form of resistance, characterized by heightened esterase activity, cytochrome P450 monooxygenase, and glutathione S-transferase enzymes encoded by specific genes. This study investigated the metabolic resistance mechanisms associated with fenvalerate resistance in the tomato leafminer and explored the genes' status. Tomato leafminer populations in Iran showed varying levels of resistance to fenvalerate; the Tehran and Urmia populations were the most resistant and sensitive, respectively. The activity level of detoxifying enzymes, particularly cytochrome P450 monooxygenase, was found to be increased in the resistant populations (i.e., Tehran) compared to the susceptible one (i.e., Urmia). Gene expression analyses showed higher transcript levels of P450, esterases, and GSTs expression levels in the resistant population compared to the susceptible population. Our findings indicated that detoxification enzymes, especially cytochrome P450 monooxygenase, and differential expression of related genes contribute to fenvalerate resistance. Identifying the specific mechanisms behind resistance could assist in pest control and resistance management programs.

Keywords

Subjects
Arouri, R., Le Goff, G., Hemden, H., Navarro-Llopis, V., M'Saad, M., Castañera, P., Feyereisen, R., Hernández-Crespo, P., & Ortego, F. (2015). Resistance to lambda-cyhalothrin in Spanish field populations of Ceratitis capitata and metabolic resistance mediated by P450 in a resistant strain. Pest Manag Sci, 71(9), 1281-1291. https://doi.org/10.1002/ps.3924
Baradaran, E., Moharramipour, S., Asgari, S., & Mehrabadi, M. (2019). Induction of DNA methyltransferase genes in Helicoverpa armigera following injection of pathogenic bacteria modulates expression of antimicrobial peptides and affects bacterial proliferation. Journal of Insect Physiology, 118, 103939. https://doi.org/https://doi.org/10.1016/j.jinsphys.2019.103939
Baradaran, E., Moharramipour, S., Asgari, S., & Mehrabadi, M. (2019). Upregulation of Helicoverpa armigera core RNA interference genes by bacterial infections and its effect on the insect-bacteria interaction. Insect Mol Biol, 28(2), 290-299. https://doi.org/10.1111/imb.12551
Campos, M. R., Silva, T. B., Silva, W. M., Silva, J. E., & Siqueira, H. A. (2015). Susceptibility of Tuta absoluta (Lepidoptera: Gelechiidae) Brazilian populations to ryanodine receptor modulators. Pest Manag Sci, 71(4), 537-544. https://doi.org/10.1002/ps.3835
Douris, V., Papapostolou, K. M., Ilias, A., Roditakis, E., Kounadi, S., Riga, M., Nauen, R., & Vontas, J. (2017). Investigation of the contribution of RyR target-site mutations in diamide resistance by CRISPR/Cas9 genome modification in Drosophila. Insect Biochem Mol Biol, 87, 127-135. https://doi.org/10.1016/j.ibmb.2017.06.013
Fan, R., Fan, Z., Sun, Z., Chen, Y., & Gui, F. (2023). Insecticide Susceptibility and Detoxification Enzyme Activity of Frankliniella occidentalis under Three Habitat Conditions. Insects, 14(7). https://doi.org/10.3390/insects14070643
Feyereisen, R. (2006). Evolution of insect P450. Biochem Soc Trans, 34(Pt 6), 1252-1255. https://doi.org/10.1042/bst0341252
Feyereisen, R. (2011). Arthropod CYPomes illustrate the tempo and mode in P450 evolution. Biochim Biophys Acta, 1814(1), 19-28. https://doi.org/10.1016/j.bbapap.2010.06.012
Finney, D. J. (1980). Probit Analysis. Cambridge University Press. https://books.google.com/books?id=o_lMwAEACAAJ
Galdino, T., Picanço, M., Fidelis, E., Silva, N., Resende Silva, G. A., & Lopes, M. (2011). Bioassay method for toxicity studies of insecticide formulations to Tuta absoluta (Meyrick, 1917). Ciência e Agrotecnologia, 35, 869-877. https://doi.org/10.1590/S1413-70542011000500002
Ghaderi, S., Fathipour, Y., & Asgari, S. (2017). Susceptibility of Seven Selected Tomato Cultivars to Tuta absoluta (Lepidoptera: Gelechiidae): Implications for Its Management. J Econ Entomol, 110(2), 421-429. https://doi.org/10.1093/jee/tow275
Gitonga, Z. M., Chabi-Olaye, A., Mithöfer, D., Okello, J. J., & Ritho, C. N. (2010). Control of invasive Liriomyza leafminer species and compliance with food safety standards by small scale snow pea farmers in Kenya. Crop Protection, 29(12), 1472-1477. https://doi.org/https://doi.org/10.1016/j.cropro.2010.08.007
Grant, C., Jacobson, R., Ilias, A., Berger, M., Vasakis, E., Bielza, P., Zimmer, C. T., Williamson, M. S., ffrench-Constant, R. H., Vontas, J., Roditakis, E., & Bass, C. (2019). The evolution of multiple-insecticide resistance in UK populations of tomato leafminer, Tuta absoluta. Pest Management Science, 75(8), 2079-2085. https://doi.org/https://doi.org/10.1002/ps.5381
Grant, C., Singh, K. S., Hayward, A., Hunt, B. J., Troczka, B. J., Pym, A., Ahn, S.-J., Zeng, B., Gao, C.-F., Leroux, A., Daum, E., Süess, P., Souza, D., Elias, J., ffrench-Constant, R. H., Vontas, J., Roditakis, E., Bielza, P., Zimmer, C. T., & Bass, C. (2023). Overexpression of the UDP-glycosyltransferase UGT34A23 confers resistance to the diamide insecticide chlorantraniliprole in the tomato leafminer, Tuta absoluta. Insect Biochemistry and Molecular Biology, 159, 103983. https://doi.org/https://doi.org/10.1016/j.ibmb.2023.103983
Guedes, R., Roditakis, E., Campos, M., Haddi, K., Bielza, P., Siqueira, H., Tsagkarakou, A., Vontas, J., & Nauen, R. (2019). Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. Journal of Pest Science, 92(4), 1329-1342. https://doi.org/10.1007/s10340-019-01086-9
Guo, L., Xie, W., Wang, S., Wu, Q., Li, R., Yang, N., Yang, X., Pan, H., & Zhang, Y. (2014). Detoxification enzymes of Bemisia tabaci B and Q: biochemical characteristics and gene expression profiles. Pest Manag Sci, 70(10), 1588-1594. https://doi.org/10.1002/ps.3751
Hemingway, J., & Ranson, H. (2000). Insecticide Resistance in Insect Vectors of Human Disease. Annual Review of Entomology, 45(1), 371-391. https://doi.org/10.1146/annurev.ento.45.1.371
Kasai, S., Weerashinghe, I. S., & Shono, T. (1998). P450 monooxygenases are an important mechanism of permethrin resistance in Culex quinquefasciatus Say larvae. Archives of Insect Biochemistry and Physiology, 37(1), 47-56. https://doi.org/https://doi.org/10.1002/(SICI)1520-6327(1998)37:1<47::AID-ARCH6>3.0.CO;2-S
Katherine, P., Johanna, S., & Anne, F. (2012). Pyrethroid Insecticides: Use, Environmental Fate, and Ecotoxicology. In P. Farzana (Ed.), Insecticides (pp. Ch. 11). IntechOpen. https://doi.org/10.5772/29495
Keen, J. H., Habig, W. H., & Jakoby, W. B. (1976). Mechanism for the several activities of the glutathione S-transferases. J Biol Chem, 251(20), 6183-6188.
Lietti, M., Botto, E., & Alzogaray, R. (2005). Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology - NEOTROP ENTOMOL, 34. https://doi.org/10.1590/S1519-566X2005000100016
Liu, M.-Y., Tzeng, Y.-J., & Sun, C.-N. (1981). Diamondback Moth Resistance to Several Synthetic Pyrethroids12. Journal of Economic Entomology, 74(4), 393-396. https://doi.org/10.1093/jee/74.4.393
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25(4), 402-408. https://doi.org/10.1006/meth.2001.1262
Mirhosseini, M. A., Fathipour, Y., Soufbaf, M., & Reddy, G. V. P. (2019). Implications of using two natural enemies of Tuta absoluta (Lepidoptera: Gelechiidae) toward tomato yield enhancement. Bull Entomol Res, 109(5), 617-625. https://doi.org/10.1017/s0007485318000998
Nauen, R., Bass, C., Feyereisen, R., & Vontas, J. (2022). The Role of Cytochrome P450s in Insect Toxicology and Resistance. Annu Rev Entomol, 67, 105-124. https://doi.org/10.1146/annurev-ento-070621-061328
Ranson, H., Claudianos, C., Ortelli, F., Abgrall, C., Hemingway, J., Sharakhova, M. V., Unger, M. F., Collins, F. H., & Feyereisen, R. (2002). Evolution of supergene families associated with insecticide resistance. Science, 298(5591), 179-181. https://doi.org/10.1126/science.1076781
Reyes, M., Rocha, K., Alarcón, L., Siegwart, M., & Sauphanor, B. (2012). Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to spinosad. Pesticide Biochemistry and Physiology, 102(1), 45-50. https://doi.org/https://doi.org/10.1016/j.pestbp.2011.10.008
Sayani, Z., Mikani, A., & Mosallanejad, H. (2019). Biochemical Resistance Mechanisms to Fenvalerate in Plutella xylostella (Lepidoptera: Plutellidae). Journal of Economic Entomology, 112(3), 1372-1377. https://doi.org/10.1093/jee/toz025
Scott, J. G., & Wen, Z. (2001). Cytochromes P450 of insects: the tip of the iceberg. Pest Management Science, 57(10), 958-967. https://doi.org/https://doi.org/10.1002/ps.354
Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., & Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol, 7, 539. https://doi.org/10.1038/msb.2011.75
Silva, G. A., Picanço, M. C., Bacci, L., Crespo, A. L., Rosado, J. F., & Guedes, R. N. (2011). Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci, 67(8), 913-920. https://doi.org/10.1002/ps.2131
Silva, J. E., Silva, W. M., Silva, T. B. M., Campos, M. R., Filho, A. B. E., & de Siqueira, H. Á. A. (2021). High resistance to insect growth disruptors and control failure likelihood in Brazilian populations of the tomato pinworm Tuta absoluta. Phytoparasitica, 49(4), 689-701. https://doi.org/10.1007/s12600-021-00895-y
Silva, T. B. M., Silva, W. M., Campos, M. R., Silva, J. E., Ribeiro, L. M. S., & Siqueira, H. A. A. (2016). Susceptibility levels of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to minor classes of insecticides in Brazil. Crop Protection, 79, 80-86. https://doi.org/https://doi.org/10.1016/j.cropro.2015.10.012
Siqueira, H. A. A., Guedes, R. N. C., Fragoso, D. B., & Magalhaes, L. C. (2001). Abamectin resistance and synergism in Brazilian populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). International Journal of Pest Management, 47(4), 247-251. https://doi.org/10.1080/09670870110044634
Siqueira, H. Á. A., Guedes, R. N. C., & Picanço, M. C. (2000). Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agricultural and Forest Entomology, 2(2), 147-153. https://doi.org/https://doi.org/10.1046/j.1461-9563.2000.00062.x
van Asperen, K. (1962). A study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology, 8(4), 401-416. https://doi.org/https://doi.org/10.1016/0022-1910(62)90074-4
Vlogiannitis, S., Mavridis, K., Dermauw, W., Snoeck, S., Katsavou, E., Morou, E., Harizanis, P., Swevers, L., Hemingway, J., Feyereisen, R., Van Leeuwen, T., & Vontas, J. (2021). Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. Proc Natl Acad Sci U S A, 118(6). https://doi.org/10.1073/pnas.2020380118
Wang, H., Shi, Y., Wang, L., Liu, S., Wu, S., Yang, Y., Feyereisen, R., & Wu, Y. (2018). CYP6AE gene cluster knockout in Helicoverpa armigera reveals role in detoxification of phytochemicals and insecticides. Nature Communications, 9(1), 4820. https://doi.org/10.1038/s41467-018-07226-6
Yu, S. J., & Nguyen, S. N. (1992). Detection and biochemical characterization of insecticide resistance in the diamondback moth. Pesticide Biochemistry and Physiology, 44(1), 74-81. https://doi.org/https://doi.org/10.1016/0048-3575(92)90011-N