Insecticide resistance of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) in cotton fields in Çukurova Region (Türkiye)

Year 2023, Volume: 47 Issue: 4 - Year: 2023 Volume: 47 Issue: 4, 387 - 399, 01.12.2023

Selçuk Ulusoy , Doğancan Kahya , Mustafa Gökhan , Okan Özgür

https://doi.org/10.16970/entoted.1344982

Abstract

This study aimed to reveal resistance levels of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) populations against dimethoate, λ-cyhalothrin and chlorpyrifos-ethyl used in cotton fields in Adana province in Çukurova Region (Türkiye). Bioassay, biochemical and molecular methods were used to determine resistance on the populations collected from 16 locations between 2020 and 2021. Six populations were resistant according to the susceptible Toktamış population with leaf dip discriminating dose bioassays. Compared to the susceptible population, four populations were found at decreased susceptibility (DS) resistance levels to dimethoate and one population to chlorpyrifos-ethyl. Only two populations resistance ratio were detected in MR (Moderate resistance) category to chlorpyrifos-ethyl. Resistance levels of other populations were observed as S (susceptible) category. Resistant populations had higher acetylcholinesterase, glutathione-S transferase and cytochrome P450 monooxygenase enzyme activities in biochemical analysis. The carboxylesterase gene transcription levels were higher in resistant populations. S431F and Kdr (knockdown) mutation were determined by the PCR-RLFP method, which is effective in organophosphate and pyrethroid insecticides resistance and 17% and 100% recessive alleles were detected in populations. The biochemical and mutation-induced resistance to dimethoate and chlorpyrifos-ethyl was detected. These results will contribute to developing strategies for resistance management of A. gossypii.

Keywords

Aphis gossypii, insecticide, resistance, Türkiye, organophosphate, pyrethroid

Supporting Institution

Republic Of Türkiye Ministry of Agriculture And Forestry, Project No: TAGEM/BSAD/B/20/A2/P2/1537.

Project Number

TAGEM/BSAD/B/20/A2/P2/1537

Thanks

We wish to express my gratitude to Dr. Işıl Özdemir for morphologically identifying aphid species. In addition, we would like to thank Dilek Ulusoy and İkbal Burcu Özgür for their significant contributions during this study.

Çukurova Bölgesi (Türkiye) pamuk alanlarında Aphis gossypii Glover, 1877 (Hemiptera: Aphididae)’nin insektisit direncinin belirlenmesi

Abstract

Bu çalışma ile, Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) popülasyonlarının Çukurova bölgesinde (Türkiye) Adana ilinde pamuk alanlarında kullanılan dimethoate, λ-cyhalothrin ve chlorpyrifos-ethyl’e karşı direnç seviyelerinin ortaya konması amaçlanmıştır. 2020 ile 2021 yılları arasında 16 koordinattan elde edilen popülasyonlar üzerinde bioassay, biyokimyasal ve moleküler yöntemler uygulanmıştır. Yaprak daldırma metodu ile ayırıcı doz çalışmaları yapılarak 16 popülasyon incelenmiş ve Toktamış popülasyonu hassas popülasyon olarak belirlenmiştir. Hassas popülasyona göre, dört popülasyonun dimethoate'a ve bir popülasyon chlorpyrifos-ethyl’e karşı direnci düşük seviye (DD) kategorisindedir. Yalnızca iki popülasyonun chlorpyrifos-ethyl'e karşı direnci orta seviye (OD) direnç kategorisindedir. Diğer popülasyonların direnç oranlarının hassas (D) seviye kategorisinde kaldığı tespit edilmiştir. Dirençli popülasyonların, biyokimyasal analizlerde daha yüksek asetilkolinesteraz, glutatyon-S transferaz ve sitokrom P450 monooksigenaz enzim aktivitelerine sahip oldukları gözlenmiştir. Karboksilesteraz gen ifadesi seviyeleri dirençli popülasyonlarda daha yüksektir. S431F ve Kdr (knockdown) mutasyonları, organofosforlu ve piretroit insektisitlere karşı etkili olan PCR-RLFP yöntemi ile belirlenmiş olup, popülasyonlarda sırasıyla %17 ve %100 oranında baskın alellere rastlanmıştır. Bu çalışmada dimethoate ve chlorpyrifos-ethyl'e karşı biyokimyasal ve mutasyon kaynaklı direnç olduğu düşünülmektedir. Bu sonuçlar, bölgede A. gossypii’ye karşı direnç yönetimi stratejilerinin geliştirilmesinde katkı sağlayacaktır.

Keywords

Aphis gossypii, direnç, insektisit, Türkiye, organikfosfatlılar, piretroit

Supporting Institution

Tarımsal Araştırmalar ve Politikalar Genel Müdürlüğü

Project Number

TAGEM/BSAD/B/20/A2/P2/1537

References

• Abel, E. L., T. K. Bammler & D. L. Eaton, 2004. Biotransformation of methyl parathion by glutathione S-transferases. Toxicological Sciences. 79 (2): 224-232.
• Alpkent, Y. N., E. İnak, S. Ulusoy & R. Ay, 2020. Acaricide resistance and mechanisms in Tetranychus urticae populations from greenhouses in Turkey. Systematic and Applied Acarology, 25 (1): 155-168.
• Alpkent, Y. N., A. Yılmaz & S. Ertürk, 2023. Determination of malathion resistance in Sitophilus oryzae L., 1763 and Sitophilus granarius L., 1758 (Coleoptera: Curculionidae) populations in Türkiye. Turkish Journal of Entomology, 47 (2): 235-243.
• Amad, M., M. I. Arif & I. Denholm, 2003. High resistance of field populations of the cotton aphid Aphis gossypii Glover (Homoptera: Aphididae) to pyrethroid insecticides in Pakistan. Journal of Economic Entomology, 96 (3): 875-878.
• Andrews, M. C., A. Callaghan, L. M. Field, M. S. Williamson & G. D. Moores, 2004. Identification of mutations conferring insecticide-insensitive AChE in the cotton-melon aphid, Aphis gossypii Glover. Insect Molecular Biology, 13: 555-561.
• Anonymous, 2023. Arthropod Pesticide Resistance Database. (Web page: https://www.pesticideresistance.org/display.php?page=species&arId=218) (Date accessed: 21.10.2023).
• Bautista, M. A., T. Miyata, K. Miura & T. Tanaka, 2009. RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the Diamondback Moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochemistry and Molecular Biology, 39 (1): 38-46.
• Benting, J & R. Nauen, 2004. Biochemical evidence that an S431F mutation in acetylcholinesterase‐1 of Aphis gossypii mediates resistance to pirimicarb and omethoate. Pest Management Science, 60 (11): 1051-1055.
• 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.
• Busvine, J. R., 1951. Mechanism of resistance to insecticide in houseflies. Nature, 168 (5): 193-195.
• Cao, C, J. Zhang, X. Gao, P. Liang & H. Guo, 2008a. Over expression of carboxylesterase gene associated with organophosphorous insecticide resistance in cotton aphids, Aphis gossypii (Glover). Pesticide Biochemistry and Physiology, 90 (3): 175-180.
• Cao, C. W., J. Zhang, X. W. Gao, P. Liang & H. L. Guo, 2008b. Differential mRNA expression levels and gene sequences of carboxylesterase in both deltamethrin resistant and susceptible strains of the cotton aphid, Aphis gossypii. Insect Science, 15 (3): 209-216.
• Carletto, J., T. Martin, F. Vanlerberghe-Masutti & T. Brévault, 2010. Insecticide resistance traits differ among and within host races in Aphis gossypii. Pest Management Science, 66 (3): 301-307.
• Chen, Y., F. Vanlerberghe‐Masutti, L. J. Wilson, I. Barchia, M. O. McLoon, T. Smith & G. A. Herron, 2013. Evidence of superclones in Australian cotton aphid Aphis gossypii Glover (Aphididae: Hemiptera). Pest Management Science, 69 (8): 938-948.
• Cheng, S., R. Li, Z. Chen, J. Ni, N. Lv, P. Liang, T. Guo, C. Zhen, P. Liang & X. Gao, 2023. Comparative susceptibility of Aphis gossypii Glover (Hemiptera: Aphididae) on cotton crops to imidacloprid and a novel insecticide cyproflanilide in China. Industrial Crops and Products, 192: 116053.
• Devonshire, A. L. & G. D. Moores, 1982. A carboxylesterase with broad substrate specificity causes organ- ophosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae). Pesticide Biochemistry and Physiology, 18 (2): 235-246.
• Erdogan, C., A. Ozdem, Y. N. Alpkent & D. Demiroz, 2023. Resistance to common insecticides and mechanisms of resistance in Aphis pomi de Geer (Hemiptera: Aphididae), in apple orchards in Turkey. Phytoparasitica, 51 (2): 323-335.
• Field, L. M. & A. L. Devonshire, 1998. Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family. Biochemical Journal 330 (1): 169-173.
• Field, L. M., 2000. Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). Biochemical Journal, 349 (3): 863-868.
• Fontaine, S., L. Caddoux & B. Barrès, 2023. First report of the kdr pyrethroid resistance mutation in a French population of the English grain aphid, Sitobion avenae. Crop Protection, 165: 106153.
• Habig, W. H., M. J. Pabst & W. B. Jakoby, 1974. Glutathione S- transferases. Journal of Biological Chemistry, 249 (22): 7130-7139.
• Hansen, L. & G. E. Hodgson, 1971. Biochemical characteristics of insect microsomes N-and O-demethylation. Biochemical Pharmacology, 20 (7): 1569-1573.
• Hawkes, N. J. & J. Hemingway, 2002. Analysis of the promoters for the β-esterase genes associated with insecticide resistance in the mosquito Culex quinquefasciatus. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1574 (1): 51-62.
• Herron, G. A, K. Powis & J. Rophail, 2001. Insecticide resistance in Aphis gossypii Glover (Hemiptera: Aphididae), a serious threat to Australian cotton. Australian Journal Entomology, 40 (1): 85-89.
• Herron, G. A., G. C. Gullick & K. J. Powis, 2003. Cross-resistance studies in cotton aphid Aphis gossypii Glover from Australian cotton. General and Applied Entomology: The Journal of the Entomological Society of New South Wales, 32: 13-19.
• Hlaoui, A., O. Chiesa, C. C. Figueroa, R. Souissi, E. Mazzoni & S. Boukhris‐Bouhachem, 2022. Target site mutations underlying insecticide resistance in Tunisian populations of Myzus persicae (Sulzer) on peach orchards and potato crops. Pest Management Science, 78 (4): 1594-1604.
• IRAC, 2023. Cotton Aphid (Aphis gossypii). (Web page: https://irac-online.org/test-methods/test-method-library/) (Date accessed: 21.09.2023).
• Karunker, I, J. Benting, B. Lueke, T. Ponge, R. Nauen, E. Roditakis, J. Vontas, K. Gorman, I. Denholm & S. Morin, 2008. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochemistry and Molecular Biology, 38 (6): 634-644.
• Kersting, U., S. Satar & N. Uygun, 1999. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Hom., Aphididae) reared on Gossypium hirsutum L.. Journal of Applied Entomology, 123 (1): 23-27.
• Kranthi, K. R., 2005. Insecticide resistance-monitoring, mechanisms and management manual. Central Institute for Cotton Research, Nagpur, 153: 75-77.
• Lee, S. H., T. J. Smith, D. C. Knipple & D. M. Soderlund, 1999. Mutations in the house fly Vssc1 sodium channel gene associated with super-kdr resistance abolish the pyrethroid sensitivity of Vssc1/tipE sodium channels expressed in Xenopus oocytes. Insect Biochemistry Molecular Biology, 29 (2): 185-194.
• LeOra, 1987. POLO-PC: a user’s guide to probit or logit analysis. LeOra Software Berkeley, CA.
• Li, F. & Z. Han, 2004. Mutations in acetylcholinesterase associated with insecticide resistance in the Cotton Aphid, Aphis gossypii Glover. Insect Biochemistry and Molecular Biology, 34 (4): 397-405.
• Liu, N., F. Zhu, Q. Xu, J. W. Pridgeon & X. Gao, 2006. Behavioral change, physiological modification, and metabolic detoxification: mechanisms of insecticide resistance. Acta Entomologica Sinica, 49 (4): 671-679.
• Livak, K. J & T. D. Schmittgen, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Δ Δ C[T]] method]. Methods, 25: 402-408.
• Lokeshwari, D., N.K.K. Kumar, H. Manjunatha & S. Shivashankar, 2016. Biochemical characterization of detoxifying enzymes in dimethoate-resistant strains of melon aphid, Aphis gossypii (Hemiptera: Aphididae). Advances in Entomology, 4 (3): 167-182.
• Ma, M. L., H. L. Jia, X. P. Cui, N. Zhai, H. F. Wang, X. Q. Guo & B. H. Xu, 2018. Isolation of carboxylesterase (esterase FE4) from Apis cerana and its role in oxidative resistance during adverse environmental stress. Biochimie, 144: 85-97.
• Marshall, K. L., C. Moran, Y. Chen & G. A. Herron, 2012. Detection of kdr pyrethroid resistance in the cotton aphid, Aphis gossypii (Hemiptera: Aphididae), using a PCR-RFLP assay. Journal of Pesticide Science, 37 (2): 169-172.
• McLoon, M. O. & G. A. Herron, 2009. PCR detection of pirimicarb resistance in Australian field isolates of Aphis gossypii Glover (Aphididae: Hemiptera). Australian Journal of Entomology, 48 (1): 65-72.
• Moran, N. A., 1992. The Evolution of Aphid Life Cycles. Annual Review of Entomology, 37 (1): 321-348.
• Nam, H. Y., S. Kim, S. H. Lee, J. H. Lee & J. Kim, 2022. Insecticide resistance in pepper greenhouse populations of Aphis gossypii (Hemiptera: Aphididae) in Korea. Pesticide Biochemistry and Physiology, 182: 105033.
• O’Brien, P. J. & J. B. Graves, 1992. Insecticide resistance and reproductive biology of Aphis gossypii Glover. Southwestern Entomologist, 17 (12): 115-122.
• Pan, Y, H. Guo & X. Gao, 2009. Carboxylesterase Activity, cDNA Sequence, and Gene Expression between Malathion Susceptible and Resistant Strains of the Cotton Aphid, Aphis gossypii. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 152 (3): 266-270.
• Pan, Y, Q. Shang, K. Fang, J. Zhang & J. Xi, 2010. Down-regulated transcriptional level of Ace1 combined with mutations in Ace1 and Ace2 of Aphis gossypii are related with omethoate resistance. Chemico-Biological Interactions, 188 (3): 553-557.
• Puinean, A. M., S. P. Foster, L. Oliphant, I. Denholm, L. M. Field, N. S. Millar, M. S. Williamson & C. Bass, 2010. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the Aphid, Myzus persicae. PLoS Genetics, 6 (6): e1000999.
• Roush, R. T. & J. A. McKenzie, 1987. Ecological genetics of insecticide and acaricide resistance. Annual Review of Entomology, 32 (1): 361-380.
• Scott, J. G., 1999. Cytochrome P450 and insecticide resistance. Insect Biochemistry and Molecular Biology, 29 (9): 757-777.
• Seyedebrahimi, S. S., K. T. Jahromi, S. Imani, V. S. Naveh & S. Hesami, 2015. Characterization of imidaclropid resistance in Aphis gossypii (Glover) (Hemiptera: Aphididae) in Southern Iran. Turkish Journal of Entomology, 39 (4): 413-423.
• Shang, Q., Y. Pan, K. Fang, J. Xi & J. A. Brennan, 2012. Biochemical characterization of acetylcholinesterase, cytochrome P450 and cross-resistance in an omethoate-resistant strain of Aphis gossypii Glover. Crop Protection, 31 (1): 15-20.
• Shen, B., H. Dong, H. Tian, L. Ma, X. Li, G. Wu & C. Zhu, 2003. Cytochrome P450 genes expressed in the deltamethrin-susceptible and resistant strains of Culex pipiens pallens. Pesticide Biochemistry and Physiology, 75 (1-2): 19-26.
• Sial, M. U., Z. Zhao, L. Zhang, Y. Zhang, L. Mao & H. Jiang, 2018. Evaluation of insecticides induced hormesis on the demographic parameters of Myzus persicae and expression changes of metabolic resistance detoxification genes. Scientific Reports, 8 (1): 16601.
• Sun, L., X. Zhou, J. Zhang & X. Gao, 2005. Polymorphisms in a carboxylesterase gene between organophosphate-resistant and susceptible Aphis gossypii (Homoptera: Aphididae). Journal of Economic Entomology, 98 (4): 1325-1332.
• Toda, S., S. Komazaki, T. Tomita & Y. Kono, 2004. Two amino acid substitutions in acetylcholinesterase associated with pirimicarb and organophosphorous insecticide resistance in the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae). Insect Molecular Biology, 13 (5): 549-53.
• Ullah, F., H. Gul, K. Tariq, N. Desneux, X. W. Gao & D. L. Song, 2020. Thiamethoxam induces transgenerational hormesis effects and alteration of genes expression in Aphis gossypii. Pesticide Biochemistry and Physiology, 165: 104-557.
• Ulusoy, S., E. Atakan & S. Dinçer, 2018. Neonicotinoid resistance of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) in cotton fields of Cukurova Region, Türkiye. Turkish Journal of Entomology, 42 (1): 23-31.
• Valmorbida, I., J. D. Hohenstein, B. S. Coates, J. G. Bevilaqua, J. Menger, E. W. Hodgson, K. L. Robert & E. O. Matthew, 2022. Association of voltage-gated sodium channel mutations with field-evolved pyrethroid resistant phenotypes in soybean aphid and genetic markers for their detection. Scientific Reports, 12 (1): 1-14.
• Wang, Z. J., C. R. Liang, Z.Y. Shang, Q.T. Yu & C. B. Xue, 2021. Insecticide resistance and resistance mechanisms in the melon aphid, Aphis gossypii, in Shandong, China. Pesticide Biochemistry and Physiology, 172: 104768.
• WHO, 1980. WHO Status of Resistance in Houseflies, Musca domestica, Document VBC/EC/80.7, World Health Organization, Geneva. (Web page: https://iris.who.int/handle/10665/58637?locale-attribute=pt&mode=simple) (Date accessed: 23.10.2023).
• Williamson, M. S., D. Martinez-Torres, C. A. Hick & A. L. Devonshire, 1996. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molecular and General Genetics MGG, 252: 51-60.
• Yorulmaz, S. & R. Ay, 2010. Akar ve böceklerde pestisitlerin detoksifikasyonunda rol oynayan enzimler. Uludağ Üniversitesi Ziraat Fakültesi Dergisi, 24 (2): 137-148 (in Turkish with abstract in English).