Detection of the S431F mutation associated with resistance to organophosphate/carbamate insecticides in Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae) distributed in Türkiye

Öz

The green peach aphid Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae) is a globally significant agricultural pest responsible for extensive crop damage through direct feeding and virus transmission. Long-term exposure to organophosphate (OP) and carbamate (CB) insecticides has led to the evolution of resistance mechanisms, particularly mutations in the acetylcholinesterase gene (ace-2). Among these, the S431F substitution, known as the Modified Acetylcholinesterase (MACE) mutation, confers reduced sensitivity to dimethylcarbamate insecticides, such as pirimicarb. This study, conducted between April 2024 and July 2025, aimed to detect and quantify the frequency of the S431F mutation in M. persicae populations collected from nine major peach-growing provinces of Türkiye using the PCR-RFLP technique. A total of 360 individuals were genotyped, revealing 15 homozygous resistant (RR), 131 heterozygous resistant (RS), and 214 homozygous susceptible (SS) individuals. The overall resistant allele frequency was 22.36%, with the highest rates observed in Niğde (17%), İzmir (15%), and Aydın (5%). Regionally, the Mediterranean, Aegean, and Marmara Regions exhibited similar resistance frequencies (22.8%, 22.5%, and 21.3%, respectively). These results indicate that resistance to OP/CB insecticides may be in its early stage of development, or that previously high resistance levels may have decreased. Continued molecular surveillance and region-specific IPM programs should be applied to delay the spread of resistance.

Anahtar Kelimeler

• ace-2
• chemical control
• insecticide resistance
• Myzus persicae
• PCR-RFLP

Proje Numarası

FMT 2024/2-BAGEP

Teşekkür

This study was financially supported by the Coordination Unit for Scientific Research Projects of Niğde Ömer Halisdemir University, grant number FMT2024/2-BAGEP.

Türkiye'de yayılış gösteren Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)’nin organofosfat/karbamat insektisitlere dirençle ilişkili S431F mutasyonunun tespiti

Öz

Öz Yeşil şeftali yaprak biti Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae), doğrudan beslenme ve virüs taşıma yoluyla geniş ölçekli mahsul hasarına neden olan, küresel öneme sahip bir tarım zararlısıdır. Organofosfat (OP) ve karbamat (CB) böcek ilaçlarına uzun süre maruz kalmak, direnç mekanizmalarının, özellikle de asetilkolinesteraz geninde (ace-2) mutasyonların ortaya çıkmasına neden olmaktadır. Bunlar arasında, Modifiye Asetilkolinesteraz (MACE) mutasyonu olarak bilinen S431F mutasyonu, pirimikarb gibi dimetilkarbamat insektisitlere karşı duyarlılığı azaltır. Bu çalışma Nisan 2024 ile Temmuz 2025 ayları arasında, PCR-RFLP tekniği kullanılarak Türkiye'nin dokuz önemli şeftali üreticisi illerinden toplanan M. persicae popülasyonlarında S431F mutasyonunun sıklığını tespit etmek ve ölçmek amacıyla yapılmıştır. Toplam 360 bireyin genotipi belirlenmiş ve 15 homozigot dirençli (RR), 131 heterozigot dirençli (RS) ve 214 homozigot duyarlı (SS) birey tespit edilmiştir. Toplam dirençli alel sıklığı %22,36 olup, en yüksek oranlar Niğde (%17), İzmir (%15) ve Aydın (%5) illerinde gözlemlenmiştir. Bölgesel olarak, Akdeniz, Ege ve Marmara bölgeleri benzer direnç sıklıkları göstermiştir (sırasıyla %22,8, %22,5 ve %21,3). Bu sonuçlar, OP/CB insektisitlere direncin, gelişimin erken aşamasında olabileceğini veya daha önce yüksek olan direnç seviyelerinin azalmış olabileceğini göstermektedir. Dirençliliğin yayılmasını geciktirmek için moleküler takip ve bölgeye özgü IPM programları uygulamaya devam edilmelidir.

Anahtar Kelimeler

• ace-2
• kimyasal kontrol
• insektisit direnci
• Myzus persicae
• PCR-RFLP

Destekleyen Kurum

Coordination Unit for Scientific Research Projects of Niğde Ömer Halisdemir University

Proje Numarası

FMT 2024/2-BAGEP

Kaynakça

1. Alptekin, S., 2009. İnsektisitlere Dirençli Myzus persicae (Sulzer) (Hemiptera: Aphididae) Populasyonlarında Asetilkolinesteraz Geni ve Sodyum Kanalı Geninde Meydana Gelen Mutasyonların İncelenmesi. (Unpublished) Yüksek Lisans Tezi, Ankara Üniversitesi, 45 pp. (in Turkish with abstract in English)
2. Anstead, J. A., M. S., Williamson & I. Denholm, 2008. New methods for the detection of insecticide-resistant Myzus persicae in the U.K. suction trap network. Agricultural and Forest Entomology, 10 (3): 291-295.
3. Bass, C., L. M. Field & M. S. Williamson, 2004. The insensitivity of insect acetylcholinesterase: mutation identification and structural comparisons. Insect Biochemistry and Molecular Biology, 34 (8): 845-853.
4. Bass, C., A. M. Puinean, C. T. Zimmer, I. Denholm, L. M. Field, S. P. Foster, O. Gutbrod, R. Nauen, R. Slater & M. S. Williamson, 2014. The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology, 51: 41-51.
5. Beekman, M. M., J. van den Heuvel, S. H. Donner, J. J. Litjens, M. Dicke, B. J. Zwaan & B. A. Pannebakker, 2024. Population genetic structure of the aphid pest Myzus persicae in organic and conventional greenhouses. bioRxiv, 2024 (7): 1-38.
6. Berber, G., B. Demirci, U. Toprak, E. İnak & Yorulmaz, S. 2022. Acetamiprid resistance in the Green peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae): selection, cross-resistance, biochemical and molecular resistance mechanisms. Journal of Agricultural Faculty of Gaziosmanpaşa University, 39 (3): 136-142.
7. Blackman, R. L. & V. F. Eastop, 2000. Aphids on the World's Crops: An Identification and Information Guide (2nd Ed.). John Wiley & Sons, Chichester, UK, 476 pp.
8. Blackman, R. & V. F. Eastop, 2025. Aphids on the World’s Plants: An online identification and information guide. (Web page: http://www.aphidsonworldsplants.info) (Date accessed: December 2025).

9. Cassanelli, S., B. Cerchiari, S. Giannini, D. Bizzaro, E. Mazzoni & G. C. Manicardi, 2005. Use of the RFLP-PCR diagnostic test for characterizing MACE and kdr insecticide resistance in the peach potato aphid Myzus persicae. Pest Management Science, 61 (1): 91-96.
10. Criniti, A., E. Mazzoni, S. Cassanelli, P. Cravedi, A. Tondelli & D. Bizzaro, 2008. Biochemical and molecular diagnosis of insecticide resistance conferred by esterase, MACE, kdr and super-kdr based mechanisms in Italian strains of the peach potato aphid, Myzus persicae (Sulzer). Pesticide Biochemistry and Physiology, 90 (3): 168-174.
11. Demiröz, D. & A. E. Atış, 2023. Resistance status in Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae) populations against single and mixture of neonicotinoid and synthetic pyrethroid insecticides. Turkish Journal of Entomology, 47 (2): 167-174.
12. Devonshire, A. L., L. M. Field, S. P. Foster, G. D. Moores, M. S. Williamson & R. L. Blackman, 1998. The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 353 (1376): 1677-1684.
13. Eleftherianos, I., S. P. Foster, M. S. Williamson & I. Denholm, 2008. Characterization of the M918T sodium channel gene mutation associated with strong resistance to pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer). Bulletin of Entomological Research. 98 (2): 183-191.
14. Fontaine, S., L. Caddoux, C. Brazier, C. Bertho, P. Bertolla, A. Micoud & L. Roy, 2011. Uncommon associations in target resistance among French populations of Myzus persicae from oilseed rape crops. Pest Management Science, 67 (8): 881-885.
15. Fournier, D., 2005. Mutations of acetylcholinesterase which confer insecticide resistance in insect populations. Chemico-Biological Interactions, 157-158: 257-261.
16. Kwon, D. H., B. R. Choi, S. W. Lee, J. M. Clark & S. H. Lee, 2009. Characterization of carboxylesterase-mediated pirimicarb resistance in Myzus persicae. Pesticide Biochemistry and Physiology, 93 (3): 120-126.
17. Liu, X., Q. Tang, Y. Li, M. Campos, P. Liang & X. Gao, 2017. Widespread resistance of the aphid Myzus persicae to pirimicarb across China, and insights on ace2 mutation frequency in this species. Entomologia Generalis, 36 (4): 285-299.
18. Margaritopoulos J. T., A. N. Kati, C. C. Voudouris, P. J. Skouras & J. A Tsitsipis, 2021. Long-term studies on the evolution of resistance of Myzus persicae (Hemiptera: Aphididae) to insecticides in Greece. Bulletin of Entomological Research, 111 (1): 1-16.
19. Menozzi, P., M. A. Shi, A. Lougarre, Z. H. Tang & D. Fournier, 2004. Mutations of acetylcholinesterase confer insecticide resistance in Drosophila melanogaster populations. BMC Evolutionary Biology, 4 (2007): 4 (1-7).
20. Mingeot, D., L. Hautier & J. P. Jansen, 2021. Structuration of multilocus genotypes associated with insecticide resistance of the peach potato aphid, Myzus persicae (Sulzer), in potato fields in southern Belgium. Pest Management Science, 77 (1): 482-491.
21. Moores, G. D., G. J. Devine & A. L. Devonshire, 1994. Insecticide-insensitive acetylcholinesterase can enhance esterase-based resistance in Myzus persicae and Myzus nicotianae. Pesticide Biochemistry and Physiology, 49 (2): 114-120.
22. Mutero, A., M. Pralavorio, J. M. Bride & D. Fournier, 1994. Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proceedings of the National Academy of Sciences, 91 (13): 5922-5926.
23. Nabeshima, T., A. Mori, T. Kozaki, Y. Iwata, O. Hidoh, S. Harada, S. Kasai & T. Tomita, 2003. An amino acid substitution on the second acetylcholinesterase gene in the pirimicarb-resistant strain of the peach-potato aphid, Myzus persicae. Biochemical and Biophysical Research Communications, 307 (1): 15-22.
24. Panini, M., D. Dradi, G. Marani, A. Butturini & E. Mazzoni, 2014. Detecting the presence of target-site resistance to neonicotinoids and pyrethroids in Italian populations of Myzus persicae. Pest Management Science, 70 (6): 931-938.
25. Roy, L., S. Fontaine, L. Caddoux, A. Micoud & J. C. Simon, 2013. Dramatic changes in the genotypic frequencies of target insecticide resistance in French populations of Myzus persicae (Hemiptera: Aphididae) over the last decade. Journal of Economic Entomology, 106 (4): 1838-1847.
26. Rubiano-Rodríguez, J. A., E. Fuentes-Contreras, C. C. Figueroa, J. T. Margaritopoulos, L. M. Briones & C. C. Ramírez, 2014. Genetic diversity and insecticide resistance during the growing season in the green peach aphid (Hemiptera: Aphididae) on primary and secondary hosts: a farm-scale study in Central Chile. Bulletin of Entomological Research, 104 (2):182-194.
27. Srigiriraju, L., P. J. Semtner, T. D. Anderson & J. R. Bloomquist, 2010. Monitoring for MACE resistance in the tobacco-adapted form of the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) in the eastern United States. Crop Protection, 29 (2): 197-202.
28. Stará, J., T. Hovorka, T. Horská, E. Zusková & Kocourek, F. 2024. Pyrethroid and carbamate resistance in Czech populations of Myzus persicae (Sulzer) from oilseed rape. Pest Management Science, 80 (1): 2342-2352.
29. Tang, Q. L., K. S. Ma, Y. M. Hou & X. W. Gao, 2017. Monitoring insecticide resistance and diagnostics of resistance mechanisms in the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) in China. Pesticide Biochemistry and Physiology, 143: 39-47.
30. Ulusoy, S., D. Kahya, M. Gökhan & O. Özgür, 2023. Insecticide resistance of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) in cotton fields in Çukurova Region (Türkiye). Turkish Journal of Entomology, 47 (4): 387-399.
31. Umina, P. A., O. Edwards, P. Carson, A. Van Rooyen & A. Anderson, 2014. High levels of resistance to carbamate and pyrethroid chemicals widespread in Australian Myzus persicae (Hemiptera: Aphididae) populations. Journal of Economic Entomology, 107 (4): 1626-1638.
32. Velioğlu, A. S. & S. Toros, 2002. Değişik bölgelerden toplanan Myzus persicae (Sulz.) (Hom.: Aphididae) popülasyonlarının bazı insektisitlere karşı dayanıklılık düzeylerinin araştırılması. Bitki Koruma Bülteni, 42 (1-4): 67-79. (in Turkish with abstract in English)
33. Velioğlu, S. A., S. Toros & A. L. Devonshire, 2008. Determination of the insecticide resistance mechanisms using biochemical methods in the Aphis gossypii Glover (Hemiptera: Aphididae) populations damaging cotton in Turkey. Journal of Agricultural Sciences (Turkey). 14 (2): 116-123.
34. Voudouris, C. C., A. N. Kati, E. Sadikoglou, M. Williamson, P. J. Skouras, O. Dimotsiou & J. T. Margaritopoulos, 2015. Insecticide resistance status of Myzus persicae in Greece: long-term surveys and new diagnostics for resistance mechanisms. Pest Management Science, 72 (4): 671-683.