Levels of Imidacloprid and Chlorpyrifos resistance and associated mechanisms in greenhouse populations of Trialeurodes vaporariorum (Hem., Aleyrodidae) from Iran

Document Type : Paper, English

Authors

1 Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Guilan, Rasht, Iran

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

Abstract

To evaluate resistance levels and potential resistance mechanisms to chlorpyrifos and imidacloprid in Trialeurodes vaporariorum, six populations were collected from greenhouse-growing regions of Iran and assessed using leaf-dip bioassays followed by probit analysis of LC50 values and their 95% confidence limits. Compared with the susceptible FR population, the FL population exhibited the highest resistance to chlorpyrifos (15.04-fold) and imidacloprid (13.62-fold). Synergism assays with piperonyl butoxide (PBO), triphenyl phosphate (TPP), and diethyl maleate (DEM) showed that PBO and TPP produced strong synergistic effects against both insecticides in the FL population, whereas DEM showed only limited synergistic effects. Enzyme activity assays corroborated the synergism results, indicating that elevated esterase (EST) and mixed-function oxidase (MFO) activities, but not glutathione S-transferase (GST) activity, were associated with resistance in T. vaporariorum. Acetylcholinesterase (AChE) kinetic analysis showed that the Km and Vmax values in the FL population were approximately twofold lower and 2.5-fold higher, respectively, than those in the FR population, suggesting altered AChE kinetic properties. In addition, AChE inhibition assays revealed reduced sensitivity to most inhibitors in the FL population, whereas increased sensitivity to fosthiazate was observed. Overall, the findings suggest that reduced AChE sensitivity, together with elevated EST and MFO activities, may contribute to resistance to chlorpyrifos and imidacloprid in Iranian populations of T. vaporariorum. These findings provide a basis for resistance monitoring and support the development of effective insecticide resistance management strategies.

Graphical Abstract

Levels of Imidacloprid and Chlorpyrifos resistance and associated mechanisms in greenhouse populations of Trialeurodes vaporariorum (Hem., Aleyrodidae) from Iran

Keywords

Main Subjects

Article Title [Persian]

سطوح مقاومت به ایمیداکلوپرید و کلرپیریفوس و مکانیسم‌های مرتبط در جمعیت‌های گلخانه‌ای Trialeurodes vaporariorum (Hem., Aleyrodidae) از ایران

Authors [Persian]

  • ابراهیم شفیعی 1
  • محمد قدمیاری 1
  • هادی مصلی نژاد 2
  • الهه شفیعی علویجه 1
1 گروه گیاه‌پزشکی، دانشکده علوم کشاورزی، دانشگاه گیلان، گیلان، رشت، ایران
2 موسسه تحقیقات گیاه‌پزشکی کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، تهران، ایران.
Abstract [Persian]

 برای ارزیابی سطوح مقاومت و مکانیسم‌های مقاومت بالقوه به کلرپیریفوس و ایمیداکلوپرید در Trialeurodes vaporariorum، شش جمعیت از مناطق کشت گلخانه‌ای ایران جمع‌آوری و با استفاده از زیست‌سنجی غوطه‌وری برگ و به دنبال آن تجزیه و تحلیل پروبیت مقادیر LC50 و حدود اطمینان 95٪ آنها ارزیابی شدند. در مقایسه با جمعیت حساس FR، جمعیت FL بالاترین مقاومت را به کلرپیریفوس (04/15 برابر) و ایمیداکلوپرید (62/13 برابر) نشان داد. سنجش‌های هم‌افزایی با پیپرونیل بوتوکسید (PBO)، تری‌فنیل فسفات (TPP) و دی‌اتیل مالئات (DEM) نشان داد که PBO و TPP اثرات هم‌افزایی قوی علیه هر دو حشره‌کش در جمعیت FL ایجاد می‌کنند، در حالی که DEM فقط اثرات هم‌افزایی محدودی نشان داد. سنجش فعالیت آنزیم، نتایج هم‌افزایی را تأیید کرد و نشان داد که افزایش فعالیت‌های استراز (EST) و اکسیداز با عملکرد مختلط (MFO)، اما نه فعالیت گلوتاتیون S-ترانسفراز (GST)، با مقاومت در T. vaporariorum مرتبط بودند. تجزیه و تحلیل سینتیکی استیل کولین استراز (AChE) نشان داد که مقادیر Km و Vmax در جمعیت FL تقریباً دو برابر کمتر و 2.5 برابر بیشتر از جمعیت FR بود، که نشان‌دهنده تغییر خواص سینتیکی AChE است. علاوه بر این، سنجش‌های مهار AChE کاهش حساسیت به اکثر مهارکننده‌ها را در جمعیت FL نشان داد، در حالی که افزایش حساسیت به فوستیازات مشاهده شد. به طور کلی، یافته‌ها نشان می‌دهد که کاهش حساسیت AChE، همراه با افزایش فعالیت‌های EST و MFO، ممکن است در مقاومت به کلرپیریفوس و ایمیداکلوپرید در جمعیت‌های ایرانی T. vaporariorum نقش داشته باشد. این یافته‌ها مبنایی برای نظارت بر مقاومت و پشتیبانی از توسعه استراتژی‌های موثر مدیریت مقاومت به حشره‌کش‌ها فراهم می‌کند.

Keywords [Persian]

  • سفید بالک گلخانه
  • بازدارنده آنزیمی
  • کلرپایریفوس
  • ایمیداکلوپرید
  • مقاومت

© 2026 by Author(s), Published by the Entomological Society of Iran

This Work is Licensed under Creative Commons Attribution-Non-Commercial 4.0 International Public License.

References

Ahangaran, A. & Alizadeh, P. (2008) Report of Citrus Pests and Diseases. Plant Protection Organization.
Alizadeh, A., Talebi-Jahromi, K., Hosseininaveh, V. & Ghadamyari, M. (2014) Toxicological and biochemical characterizations of AChE in phosalone-susceptible and resistant populations of the common pistachio psyllid, Agonoscena pistaciae. Journal of Insect Science, 14(1), 18. https://doi.org/10.1093/jis/14.1.18
Balaska, S., Fotakis, E. A., Kioulos, I., Grigoraki, L., Mpellou, S., Chaskopoulou, A. & Vontas, J. (2020) Bioassay and molecular monitoring of insecticide resistance status in Aedes albopictus populations from Greece, to support evidence-based vector control. Parasites & Vectors, 13(1), 1–13. https://doi.org/10.1186/s13071-020-04204-0
Basij, M., Talebi, K., Ghadamyari, M., Hosseininaveh, V. & Salami, S. A. (2017) Status of resistance of Bemisia tabaci (Hemiptera: Aleyrodidae) to neonicotinoids in Iran and detoxification by cytochrome P450-dependent monooxygenases. Neotropical Entomology, 46, 115–124. https://doi.org/10.1007/s13744-016-0437-
Bass, C., Denholm, I., Williamson, M. S. & Nauen, R. (2015) The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121, 78–87. https://doi.org/10.1016/j.pestbp.2015.04.004
Berrada, S., Fournier, D., Cuany, A. & Nguyen, T. X. (1994) Identification of resistance mechanisms in a selected laboratory strain of Cacopsylla pyri (Homoptera: Psyllidae): altered acetylcholinesterase and detoxifying oxidases. Pesticide Biochemistry and Physiology, 48(1), 41–47. https://doi.org/10.1006/pest.1994.1005
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), 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Byrne, D. N. & Bellows Jr, T. S. (1991) Whitefly biology. Annual Review of Entomology, 36(1), 431–457. https://doi.org/10.1146/annurev.en.36.010191.002243
Byrne, Devonshire (1997) Kinetics of insensitive Acetylcholinesterases in organophosphate-resistant Tobacco Whitefly, Bemisia tabaci(Gennadius) (Homoptera: Aleyrodidae). Pesticide Biochemistry and Physiology 58: 119–124. https://doi.org/10.1006/pest.1997.2292
Casida, J. E. & Durkin, K. A. (2013). Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 58, 99–117. https://doi.org/10.1146/annurev-ento-120811-153645
Choi, W.-I., Lee, E.-H., Choi, B.-R., Park, H.-M. & Ahn, Y.-J. (2003) Toxicity of plant essential oils to Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Journal of Economic Entomology, 96(5), 1479–1484. https://doi.org/10.1603/0022-0493-96.5.1479
Denholm, I. & Rowland, M. W. (1992). Tactics for managing pesticide resistance in arthropods: theory and practice. Annual Review of Entomology, 37(1), 91–112.  https://doi.org/10.1146/annurev.en.37.010192.000515
Devonshire, A. L. & Moores, G. D. (1984) Different forms of insensitive acetylcholinesterase in insecticide-resistant house flies (Musca domestica). Pesticide Biochemistry and Physiology, 21(3), 336–340. https://doi.org/10.1017/S0007485300000547
Dittrich, V., Ernst, G. H., Ruesch, O. & Uk, S. (1990) Resistance mechanisms in sweetpotato whitefly (Homoptera: Aleyrodidae) populations from Sudan, Turkey, Guatemala, and Nicaragua. Journal of Economic Entomology, 83(5), 1665–1670. https://doi.org/10.1093/jee/83.5.1665
Dittrich, V., Hassan, S. O. & Ernst, G. H. (1985) Sudanese cotton and the whitefly: a case study of the emergence of a new primary pest. Crop Protection, 4(2), 161–176. https://doi.org/10.1016/0261-2194(85)90015-8
Forgash, A. J. (1984) History, evolution, and consequences of insecticide resistance. Pesticide Biochemistry and Physiology, 22(2), 178–186. https://doi.org/10.1016/0048-3575(84)90087-7
Fournier, D. (2005) Mutations of acetylcholinesterase which confer insecticide resistance in insect populations. Chemico-Biological Interactions, 157, 257–261. https://doi.org/10.1016/j.cbi.2005.10.040
Fournier, D. & Mutero, A. (1994) Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 108(1), 19–31. https://doi.org/10.1016/1367-8280(94)90084-1
Ghadamyari, M., Mizuno, H., Oh, S., Talebi, K. & Kono, Y. (2008) Studies on pirimicarb resistance mechanisms in Iranian populations of the peach-potato aphid, Myzus persicae. Applied Entomology and Zoology, 43(1), 149–157. https://doi.org/10.1303/aez.2008.149
Gorman, K., Devine, G., Bennison, J., Coussons, P., Punchard, N. & Denholm, I. (2007) Report of resistance to the neonicotinoid insecticide imidacloprid in Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Pest Management Science: Formerly Pesticide Science, 63(6), 555–558. https://doi.org/10.1303/aez.2008.149
Habig, W. H., Pabst, M. J. & Jakoby, W. B. (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
Hall, L. M. & Malcolm, C. A. (1991) The acetylcholinesterase gene of Anopheles stephensi. Cellular and Molecular Neurobiology, 11(1), 131–141. https://doi.org/10.1007/bf00712805
İken, C. & Şahin, İ. (2017) Neonicotinoid resistance in Bemisia tabaci (Genn., 1889)(Hemiptera: Aleyrodidae) populations from Antalya, Turkey. Turkish Journal of Entomology, 41(2), 169–175. https://doi.org/10.1007/s10340-020-01210-0
Kang, C. Y., Wu, G. & Miyata, T. (2006) Synergism of enzyme inhibitors and mechanisms of insecticide resistance in Bemisia tabaci (Gennadius)(Hom., Aleyrodidae). Journal of Applied Entomology, 130(6‐7), 377–385. https://doi.org/10.1111/j.1439-0418.2006.01075.x
Kapantaidaki, D. E., Sadikoglou, E., Tsakireli, D., Kampanis, V., Stavrakaki, M., Schorn, C., Ilias, A., Riga, M., Tsiamis, G. & Nauen, R. (2018) Insecticide resistance in Trialeurodes vaporariorum populations and novel diagnostics for kdr mutations. Pest Management Science, 74(1), 59–69. https://doi.org/10.1002/ps.4674. Epub 2017 Sep 11
Mahdavi Moghadam, M., Ghadamyari, M. & Talebi, K. (2012) Resistance mechanisms to fenazaquin in Iranian populations of two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae). International Journal of Acarology, 38(2), 138–145. https://doi.org/110.1080/01647954.2011.583274
Manzari, S. & Fathipour, Y. (2021) Whiteflies. Polyphagous Pests of Crops, 183–230. https://doi.org/10.1007/978-981-15-8075-8_4
Martin, J. H., Mifsud, D. & Rapisarda, C. (2000) The whiteflies (Hemiptera: Aleyrodidae) of Europe and the Mediterranean basin. Bulletin of Entomological Research, 90(5), 407–448. https://doi.org/10.1017/S0007485300000547
Matu, F. K., Murungi, L. K., Mohamed, S. & Deletre, E. (2021) Behavioral response of the greenhouse whitefly (Trialeurodes vaporariorum) to plant volatiles of Ocimum basilicum and Tagetes minuta. Chemoecology, 31, 47–62. https://doi.org/10.1007/s00049-020-00327-z
Moores, G. D., Gao, X., Denholm, I. & Devonshire, A. L. (1996) Characterisation of insensitive acetylcholinesterase in insecticide-resistant cotton aphids, Aphis gossypii Glover (homoptera: Aphididae). Pesticide Biochemistry and Physiology, 56(2), 102–110. https://doi.org/10.1006/pest.1996.0064
Moreau, T. L. & Isman, M. B. (2011) Trapping whiteflies? A comparison of greenhouse whitefly (Trialeurodes vaporariorum) responses to trap crops and yellow sticky traps. Pest Management Science, 67(4), 408–413. https://doi.org/0.1002/ps.2078.
Mound, L. A. & Halsey, S. H. (1978) Whitefly of the world. A systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. John Wiley and Sons. https://doi.org/10.5962/bhl.title.118687
Mutero, A., Pralavorio, M., Bride, J. M. & Fournier, D. (1994) Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proceedings of the National Academy of Sciences, 91(13), 5922–5926. https://doi.org/10.1073/pnas.91.13.5922
Navas-Castillo, J., Fiallo-Olivé, E. & Sánchez-Campos, S. (2011) Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology, 49, 219–248. https://doi.org/10.1146/annurev-phyto-072910-095235
Norbakhsh, S. (2017) List of important pests, diseases and weeds of major agricultural products, recommended methods and pesticides for their control. Plant Protection Organization of Iran.
Pan, D., Dou, W., Yuan, G.-R., Zhou, Q.-H. & Wang, J. J. (2019) Monitoring the resistance of the citrus red mite (Acari: Tetranychidae) to four acaricides in different citrus orchards in China. Journal of Economic Entomology. https://doi.org/10.1093/jee/toz335.
Pandian, S. & Ramesh, M. (2020) Development of pesticide resistance in pests: A key challenge to the crop protection and environmental safety. Pesticides in Crop Production: Physiological and Biochemical Action, 1–13. https://doi.org/10.1002/9781119432241.ch1
Pappas, M. L., Migkou, F. & Broufas, G. D. (2013) Incidence of resistance to neonicotinoid insecticides in greenhouse populations of the whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) from Greece. Applied Entomology and Zoology, 48, 373–378. https://doi.org/10.1007/s13355-013-0197-z
Prabhaker, N., Coudriet, D. L. & Toscano, N. C. (1988) Effect of synergists on organophosphate and permethrin resistance in sweetpotato whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology, 81(1), 34–39. https://doi.org/10.5555/20143098373
Robertson, J. L., Jones, M. M., Olguin, E. & Alberts, B. (2017) Bioassays with arthropods. CRC press. https://doi.org/10.1201/9781315373775
Robertson, Preisler JL, Savin NE (1992) Pesticide bioassays with arthropods. Boca Raton: CRC 127 p.
Salehi-Sedeh, F., Khajehali, J., Nematollahi, M. R. & Askari-Saryazdi, G. (2020) Imidacloprid resistance status and role of detoxification enzymes in Bemisia tabaci (Hemiptera: Aleyrodidae) populations from Iran. Journal of Agricultural Science and Technology, 22(5), 1267–1277. https://doi.org/20.1001.1.16807073.2020.22.5.9.3
Senior, L. J. & McEwen, P. K. (1998) Laboratory study of Chrysoperla carnea (Stephens)(Neuropt., Chrysopidae) predation on Trialeurodes vaporariorum (Westwood)(Hom., Aleyrodidae). Journal of Applied Entomology, 122(1‐5), 99–101. https://doi.org/10.1111/j.1439-0418.1998.tb01469.x
Smissaert, H. R. (1964) Cholinesterase inhibition in spider mites susceptible and resistant to organophosphate. Science, 143(3602), 129–131. https://doi.org/10.1126/science.143.3602.129
Tiwari, S., Pelz-Stelinski, K., Mann, R. S. & Stelinski, L. L. (2011) Glutathione transferase and cytochrome P450 (general oxidase) activity levels in Candidatus Liberibacter asiaticus-infected and uninfected Asian citrus psyllid (Hemiptera: Psyllidae). Annals of the Entomological Society of America, 104(2), 297–305. https://doi.org/10.1603/AN10128
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/10.1016/0022-1910(62)90074-4
Van Leeuwen, T. & Dermauw, W. (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annual Review of Entomology, 61, 475–498. https://doi.org/10.1146/annurev-ento-010715-023907
Van Leeuwen, T., Vontas, J., Tsagkarakou, A. & Tirry, L. (2009) Mechanisms of acaricide resistance in the two-spotted spider mite Tetranychus urticae. In Biorational control of arthropod pests (pp. 347–393). Springer. https://doi.org/10.1007/978-90-481-2316-2_14
Van Leeuwen, T., Vontas, J., Tsagkarakou, A., Dermauw, W. & Tirry, L. (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochemistry and Molecular Biology, 40(8), 563–572. https://doi.org/10.1016/j.ibmb.2010.05.008
van Lenteren, J. C., van Roermund, H. J. W. & Sütterlin, S. (1996) Biological control of greenhouse whitefly (Trialeurodes vaporariorum) with the parasitoid Encarsia formosa: How does it work? Biological Control, 6(1), 1–10. https://doi.org/10.1006/bcon.1996.0001
Villatte, F., Augé, D., Touton, P., Delorme, R. & Fournier, D. (1999) Negative cross-insensitivity in insecticide-resistant cotton aphid Aphis gossypii Glover. Pesticide Biochemistry and Physiology, 65(1), 55–61. https://doi.org/10.1006/pest.1999.2427
Wen, Y., Liu, Z., Bao, H. & Han, Z. (2009) Imidacloprid resistance and its mechanisms in field populations of brown planthopper, Nilaparvata lugens Stål in China. Pesticide Biochemistry and Physiology, 94(1), 36–42. https://doi.org/10.1016/j.pestbp.2009.02.009
William, G. & Janet, C. (1997) Heme peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. Journal of the American Mosquito Control Association, 13(3), 233–237. PMID:9383763
Wilson, J. S. & Otsuki, T. (2004) To spray or not to spray: pesticides, banana exports, and food safety. Food Policy, 29(2), 131–146. https://doi.org/10.1016/j.foodpol.2004.02.003
Zamani, P., H Sajedi, R., Ghadamyari, M. & Memarizadeh, N. (2014) Resistance mechanisms to chlorpyrifos in Iranian populations of the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Journal of Agricultural Science and Technology, 16(2), 277–289. https://doi.org/20.1001.1.16807073.2014.16.2.16.2
Zhu, K. Y., Lee, S. H. & Clark, J. M. (1996) A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pesticide Biochemistry and Physiology, 55(2), 100–108. https://doi.org/10.1126/science.143.3602.129.
 
 
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Journal of Entomological Society of Iran
Volume 46, Issue 3
July 2026
Pages 287-302

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