Comparing bioassay and diagnostic molecular marker for phosphine resistance in Turkish populations of Rhyzopertha dominica (F., 1792) (Coleoptera: Bostrichidae)

Öz

Phosphine gas is the major pesticide applied to stored cereal grains against insects across the world and has been used in Türkiye since the 1950s. Increasing resistance to this fumigant is a problem in stored grain pests worldwide. This study determined the phosphine resistance ratios of the lesser grain borer, Rhyzopertha dominica (F., 1792) (Coleoptera: Bostrichidae) in 18 populations from 12 provinces of Türkiye between 2013 and 2017. Discriminating dose studies showed 3 of 15 populations comprise phosphine-resistant specimens. Dose-response bioassays established that resistance ratios were between 96 and 533-fold. The current molecular resistance marker, which detects the amino acid mutation P49S in the DLD (dihydrolipoamide dehydrogenase) gene, were assayed in phosphine-resistant populations. The R allele occurred at a high frequency (83.7%) in 15 highly resistant populations and was absent in three susceptible populations. For 324 individuals from the resistant populations the average proportion of homozygous resistant, heterozygous resistant and homozygous susceptible alleles were 62.0, 18.9 and 19.1%, respectively. The genetic marker detection results were comparable to bioassay results in relation to the resistance status of Turkish populations of R. dominca. So, genetic testing for phosphine resistance will simplify resistance management in Türkiye.

Anahtar Kelimeler

• Bioassay
• DLD
• lesser grain borer
• P49S
• phosphine

Rhyzopertha dominica (F., 1792) (Coleoptera: Bostrichidae)’nın Türkiye popülasyonlarındaki fosfin direncinde bioassay ile moleküler markörün karşılaştırılması

Öz

Fosfin gazı depolanmış hububattaki böceklere karşı dünya genelinde kullanılan ana pestisittir. Türkiye’de de 1950’lerden itibaren kullanılmaktadır. Bu fumiganta karşı dünya genelinde böceklerde direnç artışı önemli bir problemdir. Bu çalışmada ekin kambur böceği, Rhyzoperta dominica (F., 1792) (Coleoptera: Bostrichidae)’nın ülkemizde 12 ilden 18 popülasyonundaki fosfin dirençleri 2013-2017 yılları arasında belirlenmiştir. Ayırıcı doz çalışmaları 15 popülasyonda fosfin direnci geliştiğini göstermiştir. Bu popülasyonlarda doz-yanıt bioassayleri, direnç oranlarının 96-533 kat arasında değiştiğini göstermiştir. Ayrıca, fosfin direncine sahip bu popülasyonlarda DLD (dihydrolipoamide dehydrogenase) geninde amino asit mutasyonunu gösteren mevcut moleküler direnç markörü P49S test edilmiştir. R direnç alleli bu 15 popülasyonda yüksek frekansta (%83.7) belirlenmişken hassas olan üç popülasyonda ise belirlenmemiştir. Dirençli popülasyonlardaki 324 bireyden elde edilen genetic sonuçlara göre homozigot direnç, heterozigot direnç ve homozigot hassas allel oranları sırasıyla %62.0, 18.9 ve 19.1 olarak belirlenmiştir. Türkiye R. dominica popülasyonlarında genetik markör ile fosfin direncini belirleme sonuçlarının bioassay sonuçlarıyla kıyaslanabilir olduğu görülmüştür. Sonuçta, fosfin direncinin genetik olarak testlenmesi Türkiye’de direnç yönetimini kolaylaştıracaktır.

Anahtar Kelimeler

• Bioassay
• DLD
• ekin kambur biti
• P49S
• fosfin

Kaynakça

1. Abbott, W. S., 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18 (2): 265-267.
2. Acda, M. A., M. Bengston & G. J. Daglish, 2000. Response to phosphine of susceptible and resistant strains of Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) from the Philippines. Asia Life Science, 9 (2): 103-113.
3. Afful, E., B. Elliot, M. K. Nayak & T. W. Phillips, 2018. Phosphine resistance in North American field populations of the lesser grain borer, Rhyzopertha dominica (Coleoptera: Bostrichidae). Journal of Economic Entomology, 111 (1): 463-469.
4. Agrafioti, P., C. G. Athanassiou & M. K. Nayak, 2019. Detection of phosphine resistance in major stored-product insects in Greece and evaluation of a field resistance test kit. Journal of Stored Products Research, 82: 40-47.
5. Ahmad, A., M. Ahmed, Q. Noorullah, M. Ali, M. Abbas & S. Arif, 2013. Monitoring of resistance against phosphine in stored grain insect pests in Sindh. Middle-East Journal of Scientific Research, 16 (11): 1501-1507.
6. Benhalima, H., M. Q. Chaudhry, K. A. Mills & N. R. Price, 2004. Phosphine resistance in stored-product insects collected from various grain storage facilities in Morocco. Journal of Stored Products Research, 40: 241-249.
7. Cao, Y., G. J. Daglish & X. Liu, 2004. “Characterization of response to phosphine in adults of representative strains of Sitophilus zeamais (MOTSCH.), Sitophilus oryzae (L.) and Rhyzopertha dominica (F.) from China, 301-310”. Proceedings, International Conference on Controlled Atmosphere and Fumigation in Stored Products (8-13 August 2004, Gold-Coast, Australia), Israel: FTIC Ltd. Publishing, 2007, 738 pp.
8. Cato, A. J., B. Elliot, M. K. Nayak & T. W. Phillips, 2017. Geographic variation in phosphine resistance among North American populations of the red flour beetle (Coleoptera: Tenebrionidae). Journal of Economic Entomology, 110 (3): 1359-1365.

9. Champ, B. R. & C. E. Dyte, 1977. Report on FAO global survey of pesticide susceptibility of stored grain pests. Rome, FAO Plant Production and Protection, Paper No. 25 (2): 49-67.
10. Chen, Z., D. Schlipalius, G. Opit, B. Subramanyam & T. W. Phillips, 2015. Diagnostic molecular markers for phosphine resistance in U.S. populations of Tribolium castaneum and Rhyzopertha dominica. PLoSOne, 10 (3): e0121343.
11. Collins, P. J., 1998. “Resistance to grain protectants and fumigants in insect pests of stored products in Australia, 55-57”. Proceedings of the Australian Post-harvest Technical Conference, Canberra, Australia. CSIRO, 366 pp.
12. Collins, P. J., G. J. Daglish, M. Bengston, T. M. Lambkin & H. Pavic, 2002. Genetics of resistance to phosphine in Rhyzopertha dominica (Coleoptera: Bostrichidae). Journal of Economic Entomology, 95 (4): 862-869.
13. Collins, P. J., G. J. Daglish, R. H. Pavic & A. Kopittke, 2005. Response of mixed-age cultures of phosphine-resistant and susceptible strains of lesser grain borer, Rhyzopertha dominica, to phosphine at a range of concentrations and exposure periods. Journal of Stored Products Research, 41 (4): 373-385.
14. Collins, P. J., M. G. Falk, M. K. Nayak, R. N. Emery & J. C. Holloway, 2016. Monitoring resistance to phosphine in the lesser grain borer, Rhyzopertha dominica, in Australia: A national analysis of trends, storage types and geography in relation to resistance detections. Journal of Stored Products Research, 70: 25-36.
15. FAO, 1975. Recommended methods for the detection and measurement of resistance of agricultural pests to pesticides. Tentative method for adults of some major pest species of stored cereals, with methyl bromide and phosphine-FAO Method No. 16. FAO Plant Protection Bulletin, No. 23: 12-25.
16. Finney, D. J., 1971. Probit Analysis, 3rd Edition. Cambridge University Press: Cambridge, 333 pp.
17. Hasan, M. M., C. Adler, C. Reichmuth & T. W. Phillips, 2018. “Phosphine resistance status in lesser grain borer Rhyzopertha dominica (Fab.) (Coleoptera: Bostrichidae) strains originating from the tropical countries, 628-635”. Proceedings of the 12th International Working Conference on Stored Product Protection (IWCSPP) (October 7-11, 2018, Berlin, Germany), Julius-Kühn-Archiv 2018, No.463, 1130 pp.
18. Işıkber, A. A., Ö. Sağlam, H. Bozkurt & I. Ş. Doğanay, 2017. “Determining phosphine resistance in Sitophilus oryzae (l.) (Rice weevil) populations from different geographical regions of Turkey, 60”. Abstracts of the Conference of the IOBC-WPRS (OILB-srop) Working Group on “Integrated Protection of Stored Products” (3-5 July 2017, Ljubljana, Slovenia), 126 pp.
19. Kaur, R., E. V. Daniels, M. J. Nayak, P. R. Ebert & D. I. Schlipalius, 2013. Determining changes in the distribution and abundance of a Rhyzopertha dominica phosphine resistance allele in farm grain storage using a DNA marker. Pest Management Science, 69 (6): 685-688.
20. Kaur, R., S. Mohankumar, R. Jagadeesan, G. J. Daglish & M. K. Nayak, 2015. Phosphine resistance in India is characterized by a dihydrolipoamide dehydrogenase variant that is otherwise unobserved in eukaryotes. Heredity, 115 (3): 188-194.
21. Koçak, E., D. Schlipalius, R. Kaur, A. Tuck & P. Ebert, 2015. Determining phosphine resistance in rust red flour beetle, Tribolium castaneum (Herbst.) (Coleoptera: Tenebrionidae) populations from Turkey. Turkish Journal of Entomology, 39 (2): 129-136.
22. Koçak, E., A. Yılmaz, Y. N. Alpkent & S. Bilginturan, 2018a. Phosphine resistance of rusty grain beetle Cryptolestes ferrugineus (Coleoptera: Laemophloeidae) populations in Turkey. Scientific Papers. Series A. Agronomy, 61 (1): 286-290.
23. Koçak, E., A. Yılmaz, Y. N. Alpkent & S. Ertürk, 2018b. Phosphine resistance to some coleopteran pests in stored grains across Turkey. IOBC-WPRS Bulletin, 130: 303-310.
24. Lorini, I. & P. J. Collins, 2006. “Resistance to phosphine in Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) collected from wheat storages in Brazil, 319-323”. 9th International Working Conference on Stored Product Protection, (15-18 October 2006, Brazil), 1359 pp.
25. Lorini, I., P. J. Collins, G. J. Daglish, M. K. Nayak & H. Pavic, 2007. Detection and characterization of strong resistance to phosphine in Brazilian Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae). Pest Management Science, 63 (4): 358-364.
26. Mason, L. J. & M. McDonough, 2012. “Biology, Behavior, and Ecology of Stored Grain Legume Insects, 7-32”. In: Stored Product Protection (Eds. D. W. Hagstrum, T. W. Phillips & G. Cuperus). Kansas State University, 358 pp.
27. Mau, Y. S., P. J. Collins, G. J. Daglish, M. K. Nayak & P. R. Ebert, 2012. The rph2 gene is responsible for high level resistance to phosphine in independent field strains of Rhyzopertha dominica. PLoS ONE 7(3): e34027.
28. Muralitharan, V., T. S. Rajan, S. Chandrasekaran & S. Mohankumar, 2016. Investigation on resistance to phosphine in lesser grain borer, Rhyzopertha dominica (Fabricius) (Coleoptera: Bostrichidae) collected from Tamil Nadu, India. Current Biotica, 10 (1): 5-12.
29. Nayak, M. K., G. J. Daglish & T. W. Phillips, 2015. Managing resistance to chemical treatments in stored products pests. Stewart Postharvest Review, 11 (3): 1-6.
30. Nayak, M. K., J. Holloway, H. Pavic, M. Head & R. Reid, 2010. Developing strategies to manage highly phosphine resistant populations of rusty grain beetles in large bulk storages in Australia. Julius-Kühn-Archiv, 425: 396-401.
31. Nayak, M. K., R. Jagadeesan, N. S. Nath, G. J. Daglish & S. Virgine, 2018. “Utility of biotechnology based decision making tools in postharvest grain pest management: an Australian case study, 991-995”. Proceedings of the 12th International Working Conference on Stored Product Protection (IWCSPP) (7-11 October, 2018, Berlin, Germany), 1130 pp.
32. Nayak, M. K., R. Jagadeesan, V. T. Singarayan, N. S. Nath & H. Pavic, 2021. First report of strong phosphine resistance in stored grain insects in a far northern tropical region of Australia, combining conventional and genetic diagnostics. Journal of Stored Products Research, Article 101813.
33. Opit, G. P., T. W. Phillips, M. J. Aikins & M. M. Hasan, 2012. Phosphine resistance in Tribolium castaneum and Rhyzopertha dominica from stored wheat in Oklahoma. Journal of Economic Entomology, 105 (4): 1107-1114.
34. Pimentel, M. A. G., L. R. D. A. Faroni, F. H. D. Silva, M. D. Batista & R. N. C. Guedes, 2010. Spread of phosphine resistance among Brazilian populations of three species of stored product insects. Neotropical Entomology, 39 (1): 101-107.
35. Schlipalius, D. I., W. Chen, P. J. Collins, T. Nguyen, P. E. B. Reilly & P. R. Ebert, 2008. Gene interactions constrain the course of evolution of phosphine resistance in the lesser grain borer, Rhyzopertha dominica. Heredity, 100 (51): 506-516.
36. Schlipalius, D. I., Q. Cheng, P. E. Reilly, P. J. Collins & P. R. Ebert, 2002. Genetic linkage analysis of the lesser grain borer Rhyzopertha dominica identifies two loci that confer high-level resistance to the fumigant phosphine. Genetics, 161 (2): 773-782.
37. Schlipalius, D. I., A. G. Tuck, H. Pavic, G. J. Daglish & M. K. Nayak, 2019. A high-throughput system used to determine frequency and distribution of phosphine resistance across large geographical regions. Pest Management Science, 75 (4): 1091-1098.
38. Schlipalius, D. I., N. Valmas, A. G. Tuck, R. Jagadeesan & L. Ma, 2012. A core metabolic enzyme mediates resistance to phosphine gas. Science, 338 (6108): 807-810.
39. Solomon, M. E., 1951. Control of humidity with potassium hydroxide, sulphuric acid, or other solutions. Bulletin of Entomological Research, 42 (3): 543-554.
40. Song, X. H., P. Wang & H. Y. Zhang, 2011. Phosphine resistance in Rhyzopertha dominica (Fabricius) (Coleoptera: Bostrichidae) from different geographical populations in China. African Journal of Biotechnology, 10 (72): 16367-16373.
41. Tyler, P. S., R. W. Taylor & D. P. Rees, 1983. Insect resistance to phosphine fumigation in food warehouses in Bangladesh. International Pest Control, 25 (1): 10-13.
42. Wakil, W., N. G. Kavallieratos, M. Usman, S. Gulzar & H. A. F. El-Shafie, 2021. Detection of phosphine resistance in field populations of four key stored-grain insect pests in Pakistan. Insects, 12 (4): 288-299.
43. Yılmaz, A. & E. Koçak, 2017. “Phosphine resistance in the lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) populations from Turkey, 62”. Books of the Abstracts of the Conference of the IOBC/WPRS (OILB/srop) Working Group on “Integrated Protection of Stored Products”, (3-5 July 2017, Ljubljana, Slovenia) 126 pp.