Skip to main content Accessibility help
×
Home

Enzymatic detoxification strategies for neurotoxic insecticides in adults of three tortricid pests

  • M.A. Navarro-Roldán (a1), D. Bosch (a2), C. Gemeno (a1) and M. Siegwart (a3)

Abstract

We examined the role of the most important metabolic enzyme families in the detoxification of neurotoxic insecticides on adult males and females from susceptible populations of Cydia pomonella (L.), Grapholita molesta (Busck), and Lobesia botrana (Denis & Schiffermüller). The interaction between the enzyme families – carboxylesterases (EST), glutathione-S-transferases (GST), and polysubstrate monooxygenases (PSMO) – with the insecticides – chlorpyrifos, λ-cyhalothrin, and thiacloprid – was studied. Insect mortality arising from the insecticides, with the application of enzyme inhibitors – S,S,S-tributyl phosphorotrithioate (DEF), diethyl maleate (DEM), and piperonyl butoxide (PBO) – was first determined. The inhibitors' influence on EST, GST, and PSMO activity was quantified. EST and PSMO (the phase-I enzymatic activities) were involved in the insecticide detoxification in the three species for both sexes, highlighting the role of EST, whereas GST (phase-II enzymes) was involved only in G. molesta insecticide detoxification. L. botrana exhibited, in general, the highest level of enzymatic activity, with a significantly higher EST activity compared with the other species. It was the only species with differences in the response between sexes, with higher GST and PSMO activity in females than in males, which can be explained as the lower susceptibility of the females to the tested insecticides. A positive correlation between PSMO activity and the thiacloprid LD50s in the different species-sex groups was observed explaining the species-specific differences in susceptibility to the product reported in a previous study.

Copyright

Corresponding author

*Author for correspondence Phone: +34 973 702531 Fax: +34 973 238264 E-mail: m.navarro.roldan@gmail.com

References

Hide All
Ahmad, M. & Hollingworth, R.M. (2004) Synergism of insecticides provides evidence of metabolic mechanisms of resistance in the oblique-banded leafroller Choristoneura rosaceana (Lepidoptera: Tortricidae). Pest Management Science 60(5), 465473.
Bernard, C.B. & Philogène, B.J. (1993) Insecticide synergists: role, importance, and perspectives. Journal of Toxicology and Environmental Health-Part A 38(2), 199223.
Biddinger, D.J., Hull, L.A. & McPheron, B.A. (1996) Cross-resistance and synergism in azinphosmethyl resistant and susceptible strains of tufted apple bud moth (Lepidoptera: Tortricidae) to various insect growth regulators and abamectin. Journal of Economic Entomology 89(2), 274287.
Bingham, G., Gunning, R.V., Delogu, G., Borzatta, V., Field, L.M. & Moores, G.D. (2008) Temporal synergism can enhance carbamate and neonicotinoid insecticidal activity against resistant crop pests. Pest Management Science 64(1), 8185.
Bosch, D., Avilla, J., Musleh, S. & Rodríguez, M.A. (2018) Target-site mutations (AChE and kdr), and PSMO activity in codling moth (Cydia pomonella (L.) (Lepidoptera: Tortricidae)) populations from Spain. Pesticide Biochemistry and Physiology 146: 5262.
Bouvier, J.C., Boivin, T., Beslay, D. & Sauphanor, B. (2002) Age-dependent response to insecticides and enzymatic variation in susceptible and resistant codling moth larvae. Archives of Insect Biochemistry and Physiology 51(2), 5566.
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1–2), 248254.
Brown, T.M. & Brogdon, W.G. (1987) Improved detection of insecticide resistance through conventional and molecular techniques. Annual Review of Entomology 32(1), 145162.
Casida, J.E. & Quistad, G.B. (2004) Why insecticides are more toxic to insects than people: the unique toxicology of insects. Journal of Pesticide Science 29, 8186.
Civolani, S., Boselli, M., Butturini, A., Chicca, M., Fano, E.A. & Cassanelli., S. (2014) Assessment of insecticide resistance of Lobesia botrana (Lepidoptera: Tortricidae) in Emilia-Romagna Region. Journal of Economic Entomology 107, 12451249.
Damos, P., Colomar, L.A.E. & Ioriatti, C. (2015) Integrated fruit production and pest management in Europe: the apple case study and how far we are from the original concept? Insects 6(3), 626657.
de Lame, F.M., Hong, J.J., Shearer, P.W. & Brattsten, L.B. (2001) Sex-related differences in the tolerance of oriental fruit moth (Grapholita molesta) to organophosphate insecticides. Pest Management Science 57(9), 827832.
Deng, Z.Z., Zhang, F., Wu, Z.L., Yu, Z.Y. & Wu, G. (2016) Chlorpyrifos-induced hormesis in insecticide-resistant and-susceptible Plutella xylostella under normal and high temperatures. Bulletin of Entomological Research 106(03), 378386.
Després, L., David, J.P. & Gallet, C. (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends in Ecology and Evolution 22(6), 298307.
Devonshire, A.L. & Moores, G.D. (1982) A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae). Pesticide Biochemical Physiology 18, 235246.
Dunley, J.E., & Welter, S.C. (2000) Correlated insecticide cross-resistance in azinphosmethyl resistant codling moth (Lepidoptera: Tortricidae). Journal of economic entomology 93(3), 955962.
Enayati, A.A., Ranson, H. & Hemingway, J. (2005) Insect glutathione transferases and insecticide resistance. Insect Molecular Biology 14(1), 38.
Faucon, F., Dusfour, I., Gaude., T, Navratil, V., Boyer, F., Chandre, F., Sirisopa, P., Thanispong, K., Juntarajumnong, W., Poupardin, R., Chareonviriyaphap, T., Girod, R., Corbel, V., Reynaud, S. & David, J.P. (2015) Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing. Genome Research 25, 13471359.
Feyereisen, R. (1999) Insect P450 enzymes. Annual Review of Entomology 44(1), 507533.
Guo, Y., Chai, Y., Zhang, L., Zhao, Z., Gao, L.L. & Ma, R. (2017) Transcriptome analysis and identification of major detoxification gene families and insecticide targets in Grapholita molesta (Busck) (Lepidoptera: Tortricidae). Journal of Insect Science 17(2), 4357.
Hatipoglu, A., Durmusoglu, E. & Gürkan, O. (2015) Manisa ili bağ alanlarında Salkım güvesi [Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae)] popülasyonlarının insektisit direncinin belirlenmesi. Türkiye Entomoloji Dergisi-Turkish Journal of Entomology 39(1), 5565.
Hemingway, J. (2000) The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochemistry and Molecular Biology 30(11), 10091015.
Hodgson, E & Levi, P.E. (1998), Interactions of piperonyl butoxide with cytochrome P450. pp. 4154 in Jones, D.G. (Ed.), Piperonyl Butoxide. London, Academic Press.
Ioriatti, C., Anfora, G., Tasin, M., de Cristofaro, A., Witzgall, P. & Lucchi, A. (2011) Chemical ecology and management of Lobesia botrana (Lepidoptera: Tortricidae). Journal of Economic Entomology 104(4), 11251137.
İşci, M. & Ay, R. (2017) Determination of resistance and resistance mechanisms to thiacloprid in Cydia pomonella L. (Lepidoptera: Tortricidae) populations collected from apple orchards in Isparta Province, Turkey. Crop Protection 91, 8288.
Ivaldi-Sender, C. (1974) Techniques simples pour elevage permanent de la tordeuse orientale, Grapholita molesta (Lep., Tortricidae), sur milieu artificiel. Annales de Zoologie Ecologie Animale 6, 337343.
Iwasa, T., Motoyama, N., Ambrose, J.T. & Roe, R.M. (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection 23, 371378.
Karoly, E.D., Rose, R.L., Thompson, D.M., Hodgson, E., Rock, G.C. & Roe, R.M. (1996) Monooxygenase, esterase, and glutathione transferase activity associated with azinphosmethyl resistance in the tufted apple bud moth, Platynota idaeusalis. Pesticide Biochemistry and Physiology 55(2), 109121.
Kirk, H., Dorn, S. & Mazzi, D. (2013) Worldwide population genetic structure of the oriental fruit moth (Grapholita molesta), a globally invasive pest. BMC Ecology 13(1), 12.
Krieger, R.I., Feeny, P.P. & Wilkinson, C.F. (1971) Detoxication enzymes in the guts of caterpillars: an evolutionary answer to plant defenses? Science 172(3983), 579581.
Levi, P.E., Hollingworth, R.M. & Hodgson, E. (1988) Differences in oxidative dearylation and desulfuration of fenitrothion by cytochrome P-450 isozymes and in the subsequent inhibition of monooxygenase activity. Pesticide Biochemistry and Physiology 32(3), 224231.
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231253.
(MAPAMA). Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente. (2017) Registro de Productos Fitosanitarios. Available online at http://www.mapama.gob.es/es/agricultura/temas/sanidad-vegetal/productos-fitosanitarios/registro/menu.asp (Accessed April 2017).
Matsumura, F. (1985) Metabolism of insecticides by animals and plants. In Toxicology of Insecticides. Mastumura, F. (Ed.) pp. 203298, Plenum Press, New York.
Metcalf, R.L. (1967) Mode of action of insecticide synergists. Annual Review of Entomology 12(1), 229256.
Montella, I.R., Schama, R. & Valle, D. (2012) The classification of esterases: an important gene family involved in insecticide resistance-A review. Memorias do Instituto Oswaldo Cruz 107(4), 437449.
Nauen, R. & Stumpf, N. (2002) Fluorometric microplate assay to measure glutathione S-transferase activity in insects and mites using monochlorobimane. Analytical Biochemistry 303(2), 194198.
Navarro-Roldán, M.A. (2017) Detoxification and sublethal effects of neurotoxic insecticides in Tortricid moths. PhD University of Lleida. 1, 1200. Available online at https://www.tesisenred.net/handle/10803/462995 (Accessed May 2019).
Navarro-Roldán, M.A., Avilla, J., Bosch, D., Valls, J. & Gemeno, C. (2017) Comparative effect of three neurotoxic insecticides with different modes of action on adult males and females of three tortricid moth pests. Journal of Economic Entomology doi: 10.1093/jee/tox113.
Parra-Morales, L.B., Alzogaray, R.A., Cichón, L., Garrido, S., Soleño, J. & Montagna, C.M. (2017) Effects of chlorpyrifos on enzymatic systems of Cydia pomonella (Lepidoptera: Tortricidae) adults. Insect Science 24, 455466.
Poupardin, R., Reynaud, S., Strode, C., Ranson, H., Vontas, J. & David, J.P. (2008) Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: impact on larval tolerance to chemical insecticides. Insect Biochemistry and Molecular Biology 38(5), 540551.
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/ (accessed 1 September 2017).
Reuveny, H. & Cohen, E. (2004) Evaluation of mechanisms of azinphos-methyl resistance in the codling moth Cydia pomonella (L.). Archives of Insect Biochemistry and Physiology 57(2), 92100.
Reyes, M. (2007) La résistance aux insecticides chez le carpocapse des pommes: mécanismes, détection et variabilité géographique. PhD University of Avignon. Avignon.
Reyes, M., Franck, P., Charmillot, P.J., Ioriatti, C., Olivares, J., Pasqualini, E. & Sauphanor, B. (2007) Diversity of insecticide resistance mechanisms and spectrum in European populations of the codling moth, Cydia pomonella. Pest Management Science 63(9), 890902.
Reyes, M., Barros-Parada, W., Ramírez, C.C. & Fuentes-Contreras, E. (2015) Organophosphate resistance and its main mechanism in populations of codling moth (Lepidoptera: Tortricidae) from Central Chile. Journal of Economic Entomology 108(1), 277285.
Roberts, T.R. & Hutson, D.H. (1998) Metabolic Pathways of Agrochemicals: Insecticides and Fungicides, (Vol. 1). Cambridge, UK, Royal Society of Chemistry.
Rodríguez, M.A., Bosch, D., Sauphanor, B. & Avilla, J. (2010) Susceptibility to organophosphate insecticides and activity of detoxifying enzymes in Spanish populations of Cydia pomonella (Lepidoptera: Tortricidae). Journal of Economic Entomology 103(2), 482491.
Rose, H.A. (1985) The relationship between feeding specialization and host plants to aldrin epoxidase activities of midgut homogenates in larval Lepidoptera. Ecological Entomology 10(4), 455467.
Sauphanor, B., Cuany, A., Bouvier, J.C., Brosse, V., Amichot, M. & Bergé, J.B. (1997) Mechanism of resistance to deltamethrin in Cydia pomonella (L.) (Lepidoptera: Tortricidae). Pesticide Biochemistry and Physiology 58(2), 109117.
Scott, J.G. (1999) Cytochromes P450 and insecticide resistance. Insect Biochemistry and Molecular Biology 29(9), 757777.
Shearer, P.W. & Usmani, K.A. (2001) Sex-related response to organophosphorus and carbamate insecticides in adult oriental fruit moth, Grapholita molesta. Pest Management Science 7(9), 822826.
Sial, A.A. & Brunner, J.F. (2012) Selection for resistance, reversion towards susceptibility and synergism of chlorantraniliprole and spinetoram in obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Pest Management Science 68, 462468.
Siegwart, M., Monteiro, L.B., Maugin, S., Olivares, J., Malfitano-Carvalho, S. & Sauphanor, B. (2011) Tools for resistance monitoring in oriental fruit moth (Lepidoptera: Tortricidae) and first assessment in Brazilian populations. Journal of Economic Entomology 104(2), 636645.
Snoeck, S., Greenhalgh, R., Tirry, L., Clark, R.M., Van Leeuwen, T. & Dermauw, W. (2017) The effect of insecticide synergist treatment on genome-wide gene expression in a polyphagous pest. Scientific Reports 7, 13440 Available online at http://www.nature.com/scientificreports.
Soderlund, D.M. & Bloomquist, J.R. (1990) Molecular mechanisms of insecticide resistance. pp. 5895 in Pesticide Resistance in Arthropods, Roush, R.T. and Tabashnik, B.E. (Eds), New York, Chapman and Hall.
Terriere, L.C. (1984) Induction of detoxication enzymes in insects. Annual Review of Entomology 29(1), 7188.
Ullrich, V. & Weber, P. (1972) The O-dealkylation of 7-ethoxycoumarin by liver microsomes. A direct fluorometric test. Hoppe-Seyler's Zeitschrift für physiologische Chemie 353(2), 11711177.
Usmani, K.A. & Knowles, C.O. (2001) Toxicity of pyrethroids and effect of synergists to larval and adult Helicoverpa zea, Spodoptera frugiperda, and Agrotis ipsilon (Lepidoptera: Noctuidae). Journal of Economic Entomology 94(4), 868873.
Vogelweith, F., Thiery, D., Quaglietti, B., Moret, Y. & Moreau, J. (2011). Host plant variation plastically impacts different traits of the immune system of a phytophagous insect. Functional Ecology 25, 12411247.
Vojoudi, S., Saber, M., Gharekhani, G. & Esfandiari, E. (2017) Toxicity and sublethal effects of hexaflumuron and indoxacarb on the biological and biochemical parameters of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Iran. Crop Protection 91, 100107.
Willoughby, L., Batterham, P. & Daborn, P.J. (2007) Piperonyl butoxide induces the expression of cytochrome P450 and glutathione S-transferase genes in Drosophila melanogaster. Pest Management Science 63(8), 803808.
Wu, G., Miyata, T., Kang, C.Y. & Xie, L.H. (2007) Insecticide toxicity and synergism by enzyme inhibitors in 18 species of pest insect and natural enemies in crucifer vegetable crops. Pest Management Science 63, 500510.
Xie, W., Wang, S., Wu, Q., Feng, Y., Pan, H., Jiao, X., Zhou, L., Yang, X., Fu, W., Teng, H., Xu, B. & Zhang, Y. (2011) Induction effects of host plants on insecticide susceptibility and detoxification enzymes of Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 67, 8793.
Xue, M., Pang, Y.H., Li, Q.L. & Liu, T.X. (2010) Effects of four host plants on susceptibility of Spodoptera litura (Lepidoptera: Noctuidae) larvae to five insecticides and activities of detoxification esterases. Pest Management Science 66, 12731279.
Yang, X., Margolies, D.C., Zhu, K.Y. & Buschman, L.L. (2001) Host plant-induced changes in detoxification enzymes and susceptibility to pesticides in the two spotted spider mite (Acari: Tetranychidae). Journal of Economic Entomology 94(2), 381387.
Young, S.J., Gunning, R.V. & Moores, G.D. (2005) The effect of piperonyl butoxide on pyrethroid-resistance-associated esterases in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pest Management Science 61(4), 397401.
Young, S.J., Gunning, R.V. & Moores, G.D. (2006) Effect of pretreatment with piperonyl butoxide on pyrethroid efficacy against insecticide-resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and Bemisia tabaci (Sternorrhyncha: Aleyrodidae). Pest Management Science 62(2), 114119.
Yu, S.J. (2004) Induction of detoxification enzymes by triazine herbicides in the fall armyworm, Spodoptera frugiperda (JE Smith). Pesticide Biochemistry and Physiology 80(2), 113122.
Yu, S.J. (2008) The Toxicology and Biochemistry of Insecticides, Boca Raton, FL, USA, CRC Press/Taylor and Francis.
Yu, S.J. & Hsu, E.L. (1993) Induction of detoxification enzymes in phytophagous insects: role of insecticide synergists, larval age, and species. Archives of Insect Biochemistry and Physiology 24(1), 2132.
Yu, S.J., Nguyen, S.N. & Abo-Elghar, G.E. (2003) Biochemical characteristics of insecticide resistance in the fall armyworm, Spodoptera frugiperda (JE Smith). Pesticide Biochemistry and Physiology 77(1), 111.
Zimmer, C.T., Panini, M., Singh, K.S., Randall, E.L., Field, L.M., Roditakis, E., Mazzoni, E. & Bass, C. (2017). Use of the synergist piperonyl butoxide can slow the development of alpha-cypermethrin resistance in the whitefly Bemisia tabaci. Insect Molecular Biology 26(2), 152163.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed