Characteristic of resistance to dichlorvos and biochemical mechanisms in the greenhouse strains of Frankliniella occidentalis (Thysanoptera: Thripidae)

Volume 9, Issue 2
June 2020
Pages 195-207

Document Type : Original Research

Authors

1 Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran.

2 Iranian Research Institute of Plant Protection, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran.

Abstract
The western flower thrips (WFT), Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) is an invasive pest in greenhouse with high potential to cause damage to crops. There are a limited number of effective insecticides to manage this pest and several cases of chemical control failures have been reported in Iran which can be due to resistance to insecticides. To evaluate the status of insecticide resistance and possible resistance mechanisms, eight Iranian strains of F. occidentalis, collected from Tehran, Markazi, Alborz, Qazvin, Isfahan, Yazd (M and B) and Kerman provinces, were assayed against dichlorvos as a recommended insecticide for chemical control of thrips. Compared with the susceptible strain (Isfahan), two strains collected from Yazd had the lowest susceptibility to dichlorvos (Resistance Factor = 2.14 and 2.04 fold). Bioassay by synergists and enzyme assays demonstrated interfering of carboxyl esterase and glutathion S- transferase in Yazd M strain. The esterase inhibitor, triphenyl phosphite (TPP), and Glutathione S-transferase inhibitor, diethyl maleate (DEM), synergized the toxicity of dichlorvos in the Yazd M strain, (Synergistic Ratio = 5.28 and 1.79 fold, respectively). Also, carboxylesterase (for α- naphtyl acetate and ß- naphtyl acetate) and glutathion S- transferases activities in this population were 1.69, 7.31 and 0.97 fold higher than in the Isfahan strain. Furthermore, dichlorvos resistance did not significantly diminish after several months. Based on our results, we suggest that dichlorvos should be removed from the control program of this pest.

Keywords

Abbot, W. S. 1925. A method for computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265-567.
Baniameri, V. 2009. Status of IPM program in greenhouse crops in Iran, success and needs. Available from:http://baniameri.entomology.ir/Papers/PaperE8.pdf.
Bielza, P., Quinto, V., Contreras, J., Torne, M., Martin, A. and Espinosa, P. J. 2007. Resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande), in greenhouses of south-eastern Spain. Pest Management Science, 63: 682-687.
Bielza, P., Quinto, V., Grávalos, C., Fernández, E., Abellan, J. and Contreras, J. 2008. Stability of spinosad resistance in Frankliniella occidentalis (Pergande) under laboratory conditions. Bulletin of Entomological research, 98: 355-359.
Bourguet, D., Raymond, M., Berrada, S., and Fournier, D. 1997. Interaction between acetylcholinesterase and choline acetyltransferase: an hypothesis to explain unusual toxicological responses. Pesticide Science, 51(3): 276–282.
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: 248-254.
Brøadsgaard, H. F. 1994. Insecticide resistance in European and African strains of western flower thrips (Thysanoptera: Thripidae) tested in a new residue-on-glass test. Journal of Economic Entomology, 87: 1141-1146.
Castañeda, L. E., Figueroa, C. C., Contreras, E. F., Niemeyer, H. M. and Nespolo, R. F. 2009. Energetic costs of detoxification systems in herbivores feeding on chemically defended host plants: a correlational study in the grain aphid, Sitobion avenae. Journal of Experimental Biology, 212: 1185-1190.
Chen, X., Yuan, L., Du, Y., Zhang, Y. and Wang, J. 2011. Cross-resistance and biochemical mechanisms of abamectin resistance in the western flower thrips, Frankliniella occidentalis. Pesticide Biochemistry and Physiology, 101: 34-38.
Contreras, J., Espinosa, P. J., Quinto, V., Abellán, J., Grávalos, C., Fernández, E. and Bielza, P. 2010. Life-stage variation in insecticide resistance of the western flower thrips (Thysanoptera: Thripidae). Journal of Economic Entomology, 103(6): 2164-2168.
Contreras, J., Espinosa, P. J., Quinto, V., Grávalos, C., Fernández, E. and Bielza, P. 2008. Stability of insecticide resistance in Frankliniella occidentalis to acrinathrin, formetanate and methiocarb. Agricultural and Forest Entomology, 10: 273-278.
Demirozer, O., Tyler-Julian, K., Funderburk, J., Leppla, N. and Reitz, S. 2012. Frankliniella occidentalis (Pergande) integrated pest management programs for fruiting vegetables in Florida. Pest Management Science, 68: 1537-1545.
Devonshire, A. L. 1989. Insecticide resistance in Myzus persicae: from field to gene and back again. Pesticide Science, 26: 375-382.
Ellman, G. L., Courtney, K. D., Andres, V. and Featherstone, R. M. 1961. A new and rapid colorimetric determination of acetylcholinesterases activity. Biochemical Pharmacology, 7: 88-95.
Espinosa, P. J., Bielza, P., Contreras, J. and Lacasa, A. 2002. Insecticide resistance in field population of Frankliniella occidentalis (Pergande) in Murica (south-east Spain). Pest Management Science, 58: 967-971.
Espinosa, P. J., Contreras, J., Quinto, V., Grávalos, C., Fernández, E. and Bielza, P. 2005. Metabolic mechanism of insecticide resistance in the western flower thrips, Frankliniella occidentalis (Pergande). Pest Management Science, 61(10): 1009-1015.
Ferrari, J. A., Morse, J. G., Georghiou, G. P., and Sun, Y. 1993. Elevated esterase activity and acetylcholinesterase insensitivity in citrus thrips (Thysanoptera: Thripsidae) populations from the San Joaquin Valley of California. Journal of Economic Entomology, 86: 1645–1650.
Gholami, Z. and Sadeghi, A. 2016. Management Strategies for Western Flower Thrips in Vegetable Greenhouses in Iran: a Review. Plant Protection Science, 52(2): 87–98.
Gholami, Z., Sadeghi, A., Sheikhi Garjan, A., Nazemi Rafi, and Gholami, F. 2015. Susceptibility of western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae) to some synthetic and botanical insecticides under laboratory conditions. Journal of Crop Protection, 4 (Supplementary): 627-632.
Gong, Y. J., Wang, Z. H., Shi, B. C., Kang, Z. J., Zhu, L., Jin, G. H. and Wei, S. J. 2013. Correlation between Pesticide Resistance and Enzyme Activity in the Diamondback Moth, Plutella xylostella. Journal of Insect Science, 13(135): 1-13.
Guo, F., Zhang, Z. Q. and Zhao, Z. 1998. Pesticide resistance of Tetranychus cinnabarinus (Acari: Tetranychidae) in China: a review. Systematic and Applied Acarology, 3: 3-7
Habig, W. H., Pabst, M. J. and Jakoby, W. B. 1974. Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249: 7130-7139.
Immaraju, J. A., Morse, J. G., and Gaston, L. K. 1990. Mechanisms of organophosphate, pyrethroid and DDT resistance in citrus thrips (Thysanoptera: Thripsidae). Journal of Economic Entomology, 83: 1723–1732.
Immaraju, J. H., Paine, T. D., Bethke, J. A., Robb, K. L. and Newman, J. P. 1992. Western flower thrips (Thysanoptera: Thripidae) resistance to insecticides in coastal California greenhouses. Journal of Economic Entomology, 85: 9-14.
Jalili Moghadam, M. and Azmayesh Fard, P. 2004. Thrips of ornamental plants in Tehran and Mahallat. Proceeding of the 16th Iranian Plant Protection Congress. 29 August-2 September, Iran. pp. 16.
Jensen, S. E. 2000a. Mechanisms associated with methiocarb resistance in Frankliniella occidentalis (Thysanoptera: Thripsidae). Journal of Economic Entomology, 93: 464-471.
Jensen, S. E. 2000b. Insecticide resistance in the western flower thrips, Frankliniella occidentalis. Integrated Pest Management Reviews, 5: 131-146.
Lewis, T. 1997. Thrips as crop pests. Cab International. Wallingford, UK. Available from: https://www.cabdirect.org/cabdirect/abstract/19981100112.
Herron, G.A., and James, T.M. 2005. Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance. Australian Journal of Entomology, 44: 299-303.
Liu, Y., Zhang, H., Qiao, Ch., Lu, Z. and Cui, F. 2011. Correlation between carboxylesterase alleles and insecticide resistance in Culex pipiens complex from China. Parasites Vectors, 4: 236.
Lopez-Soler, N., Cervera, A., Quinto, V., Abellan, J., Bielza, P., Martínez-Pardo, R. and Garcera, M. D. 2011. Esterase inhibition by synergists in the western flower thrips Frankliniella occidentalis. Pest Management Science, 67: 1549-1556.
Macdonald, O. C. 1995. Response of western flower thrips to dichlorvos and malathion in the United Kingdom. In: Parker, M. and Lewis, T. (Eds.). Thrips Biology and Management. NATO ASI Series (Series A: Life Sciences). Boston, UK. pp. 347-350.
Maymo, A. C., Cervera, A., Sarabia, R., Martinez-Pardo, R. and Garcera, M. D. 2002. Evaluation of metabolic detoxifying enzyme activities and insecticide resistance in Frankliniella occidentalis. Pest Management Science, 58: 928-934.
Meng, X., Yang, X., Zhang, N., Jiang, H., Ge, H., Chen, M., Qian, K. and Wang, J. 2018. Knockdown of the GABA receptor RDL genes decreases abamectin susceptibility in the rice stem borer, Chilo suppressalis. Pesticide Biochemistry and Physiology, 153: 171-175.
Mirnezhad, M., Romero-Gonzalez, R. R., Leiss, K. A., Choi, Y. H., Verpoorte, R. and Klinkhamer, P. G. L. 2010. Metabolomic analysis of host plant resistance to Thrips in wild and cultivated Tomatoes. Phytochemical Analysis, 21(1): 110-117.
Montella, I. R., Schama, R. and Valle, D. 2012. The classification of esterases: an important gene family involved in insecticide resistance - A Review. Memórias do Instituto Oswaldo, 107(4): 437-449.
Nazemi, A., Khajehali, J. and Van Leeuwen, T. 2016. Incidence and characterization of resistance to pyrethroid and organophosphorus insecticides in Thrips tabaci (Thysanoptera: Thripidae) in onion fields in Isfahan, Iran. Pesticide Biochemistry and Physiology, 129: 28-35.
Newcomb, R. D., Campbell, P. M., Ollis, D. L., Cheah, E., Russell, R. J. and Oakeshott, J. G. 1997. A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proceedings of the National Academy of Science of the United States, 94: 7464-7468.
Raymond, M., Poulin, E., Boiroux, V., Dupont, E. and Pasteur, N. 1993. Stability of insecticide resistance due to amplification of esterase genes in Culex pipiens. Heredity, 70: 301-307.
Reitz, S. 2009. Biology and ecology of the western flower thrips (Thysanoptera: Thripidae): the making of a pest. Florida Entomologist, 92(1): 7-13.
Riley, D. G., Joseph, S. V., Srinivasan, R. and Diffie, S. 2011. Thrips vectors of tospoviruses. Journal of Integrated Pest Management, 2(1): I1-I10.
Robertson, J. L., Jones, M. M., Olguin, E. and Alberts, B. 2017. Bioassays with arthropods. CRC press, Boca Raton, FL, USA. Available from: https://www.taylorfrancis.com/books/9781315373775.
Rose, R. L., Barbhaiya, L., Roe, R., Rock, G. and Hodgson, E. 1995. Cytochrome P450-associated insecticide resistance and the development of biochemical diagnostic assays in Heliothis virescens. Pesticide Biochemistry and Physiology, 51: 178-191.
Saddiq, B., Afzal, M. B. S. and Shad, S. A. 2016. Studies on genetics, stability and possible mechanism of deltamethrin resistance in Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) from Pakistan. Journal of Genetics, 95: 1009-1016.
Saha, D., Roy, S. and Mukhopadhyay, A. 2012. Seasonal incidence and enzyme-based susceptibility to synthetic insecticides in two upcoming sucking insect pests of tea. Phytoparasitica, 40: 105.
Sanderson, J. P. and Roush, R. T. 1992. Monitoring insecticide resistance in greenhouse whitefly (Homoptera: Aleyrodidae) with yellow sticky cards. Journal of Economic Entomology, 85(3): 634-641.
SAS, 2004. SAS user’s guide statistics. Cary, NC: SAS Inst., Inc.
Scott, J. G. and Wen, Z. 2001. Cytochromes P450 of insects: the tip of the iceberg. Pest Management Science, 57: 958-967.
Software LO, 2007. Version 2.0. Polo plus: A user’s guide to probit or logit analysis. Petaluma, CA: LeOra Software Company.
Stevenson, B. J., Pignatelli, P., Nikou, D. and Paine, M. J. 2012. Pinpointing P450s associated with pyrethroid metabolism in the dengue vector, Aedes aegypti: developing new tools to combat insecticide resistance. Plos Neglected Tropical Diseases, 6: e1595.
Teese, M. G., Farnsworth, C. A., Li, Y., Coppin, C. W., Devonshire, A. L., Scott, C., East, P., Russell, R. J. and Oakeshott, J. G. 2013. Heterologous Expression and Biochemical Characterisation of Fourteen Esterases from Helicoverpa Armigera. PLoS ONE, 8(6): e65951.
van Asperen, K. A. 1962. Study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology, 8: 401-416.
Wang, Z. H., Gong, Y. J., Jin, J. H., Li, B. Y., Chen, J. C., Kang, Z. J., Zhu, L., Gao, Y. L., Reitz, S. and Wei, Sh. 2015. Field-evolved resistance to insecticides in the invasive western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in China. Pest Management Science, 72: 1440-1444.
Wu, Sh., Tang, L., Zhang, X., Xing, Zh., Lei, Zh. and Gao, Y. 2018. A decade of a thrips invasion in China: lessons learned. Ecotoxicology, 27: 1032–1038.
Yu, S. J. and Nguyen, S. N. 1992. Detection and biochemical characterization of insecticide resistance in the diamondback moth. Pesticide Biochemistry and Physiology, 44: 74-81.
Zhao, G., Liu, W., Brown, J. M. and Knowles, C. O. 1995. Insecticide resistance in field and laboratory strains of western flower thrips (Thysanoptera: Thripidae). Journal of Economic Entomology, 88: 1164-1170.
Zhao, G., Liu, W. and Knowles, C.O. 1994. Mechanisms associated with diazinon resistance in western flower thrips. Pesticide of Biochemistry Physiology, 49: 13-23.