Advertisement

Journal of Pest Science

, Volume 93, Issue 1, pp 127–134 | Cite as

A CAPS marker for determination of strong phosphine resistance in Tribolium castaneum from Brazil

  • Zhaorigetu Hubhachen
  • Hongbo Jiang
  • David Schlipalius
  • Yoonseong Park
  • Raul N. C. Guedes
  • Brenda Oppert
  • George Opit
  • Thomas W. PhillipsEmail author
Original Paper
  • 661 Downloads

Abstract

Strong phosphine resistance in Tribolium castaneum is due to point mutations in DNA that code for amino acid changes of P45S and/or G131S in the enzyme dihydrolipoamide dehydrogenase (DLD). One allele coding for P45S is the most common in all phosphine-resistant US populations and in one strain from Brazil (TCBR), whereas another allele, G131S, occurs only in Australian beetles. Dose-mortality studies found that the TCBR strain was more resistant to phosphine than US populations. To investigate strong resistance mutations in TCBR, we sequenced cDNA for DLD in TCBR and compared results with a US population from Kansas. The common P45S mutation was detected in both populations, but two additional mutations G131D and V167A were identified only from TCBR. We used a CAPS marker (Cleaved Amplified Polymorphic Sequence) for P45S, herein designated M1, to survey this resistance allele in TCBR. We also developed a marker for the G131D mutation, designated M2. Only two genotypes, R1R1S2S2 (homozygous for resistance at M1, but homozygous susceptible at the M2 site) and R1S1R2S2 (heterozygous for resistance at M1 and M2) existed in TCBR. However, phosphine resistance levels were similar between individuals with the two genotypes. Beetles with strong resistance in TCBR may be homozygous for either the presence of the common P45S allele, or heterozygous for two resistance alleles at a second locus, G131D. The strong resistance phenotype in TCBR may be expressed differently based on previously unknown mutations at the DLD locus, but this will require further research to resolve.

Keywords

Fumigation Insecticide resistance Molecular marker analysis Resistance ratio Resistance genotype 

Notes

Acknowledgements

The authors appreciate suggestions and technical advice on genetics and molecular biology from Drs. Jeremy Marshall and Kun Yan Zhu. The authors also acknowledge the financial support of the Plant Biosecurity Cooperative Research Centre (Project No: PBCRC3035) established and supported under the Australian Government’s Cooperative Research Centre Program (http://www.crcplantbiosecurity.com.au). This paper is contribution number 19-176-J of the Kansas Agricultural Experiment Station.

Funding

This study was funded by the Australian Plant Biosecurity Center for Cooperative Research.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest with this agency, among themselves, or with other funding sources or institutions in regard to this article.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Since no human was involved in this study, there was no need to obtain informed consent from any individual participants included in the study.

Supplementary material

10340_2019_1134_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 11 kb)

References

  1. Afful E, Elliott B, Nayak MK, Phillips TW (2018) Phosphine resistance in North American field populations of the lesser grain borer Rhyzopertha dominica (Coleoptera: Bostrichidae). J Econ Entomol 111(1):463–469.  https://doi.org/10.1093/jee/tox284 CrossRefPubMedGoogle Scholar
  2. Ahmad A, Ahmed M, Nourullah Ali GM, Abbas M, Arif S (2013) Monitoring of resistance against phosphine in stored grain insect pests in Sindh. Middle-East J Sci Res 16:1501–1507Google Scholar
  3. Benhalima H, Chaudhry MQ, Mills KA, Price NR (2004) Phosphine resistance in stored-product insects collected from various grain storage facilities in Morocco. J Stored Prod Res 40:241–249CrossRefGoogle Scholar
  4. Cao Y, Son Y, Sun GY (2003) A survey of psocid species infesting stored grain in China and. Res. resistance to phosphine in field populations of Liposcelis entomophila (Enderlein) (Psocoptera: Liposcelididae), pp 662–667. In: Credland PF, Armitage DM, Bell CH, Cogan PM, Highley E (eds) Proceedings of the 8th international working conference on stored product protection, 22–26 July 2002, York, UK. CAB International, Wallingford, United Kingdom (ISBN 0851996914)Google Scholar
  5. Cato A, Elliott B, Nayak MK, Phillips TW (2017) Geographic variation in phosphine resistance among North american populations of the red flour beetle (Coleoptera: Tenebrionidae). J Econ Entomol 110(3):1359–1365CrossRefGoogle Scholar
  6. Champ BR, Dyte CE (1976) Report of the FAO global survey of pesticide susceptibility of stored grain pests. FAO Plant Production and Series, 5, FAO, RomeGoogle Scholar
  7. Chen Z, Schliaplius DI, Opit GP, Subramanyam B, Phillips TW (2015) Diagnostic molecular markers for phosphine resistance. PLoS ONE 10(3):0121343Google Scholar
  8. Collins PJ, Daglish GJ, Nayak MK, Ebert PR, Schlipalius DI, Chen W, Pavic H, Lambkin TM, Kopittke R, Bridgeman BW (2001) Combating resistance to phosphine in Australia, pp 593–607. In: Donahaye EJ, Navarro S, Leesch JG (eds) International conference controlled atmosphere and fumigation in stored products, 29 October–3 November 2000, Fresno, CA. Executive Printing Services, Clovis, CAGoogle Scholar
  9. Daglish GJ, Collins PJ (1999) Improving the relevance of assays for phosphine resistance. In: Zuxun J, Quan L, Yongsheng L, Xianchang T, Langhua G (eds) Proceedings of the 7th international working conference of stored product protection. Sichuan Publishing House of Science and Technology, Chengdu, Sichuan, People’s Republic of China, pp 584–593Google Scholar
  10. Emery RN, Nayak MK, Holloway JC (2011) Lessons learned from phosphine resistance monitoring in Australia. Stewart Postharvest Rev 7:1–8Google Scholar
  11. Food and Agriculture Organization (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 Prot Bull 23:12–25Google Scholar
  12. Hagstrum DW, Phillips TW, Cuperus GW (2012) Stored product protection. Kansas State University. KSRE Publ. S-156. Manhattan, KS. 352 pGoogle Scholar
  13. Jagadeesan R, Fotheringham A, Ebert PR, Schlipalius DI (2013) Rapid genome wide mapping of phosphine resistance loci by a simple regional averaging analysis in the red flour beetle, Tribolium castaneum. BMC Genom 14:650.  https://doi.org/10.1186/1471-2164-14-650 CrossRefGoogle Scholar
  14. Jagadeesan R, Collins PJ, Nayak MK, Schlipalius DI, Ebert PR (2016) Genetic characterization of field-evolved resistance to phosphine in the rusty grain beetle, Cryptolestes ferrugineus (Laemophloeidae: Coleoptera). Pestic Biochem Physiol 127:67–75.  https://doi.org/10.1016/j.pestbp.2015.09.008Epub 2015 Sep 25 CrossRefPubMedGoogle Scholar
  15. Jittanun C, Chongrattanameteekul W (2014) Phosphine resistance in Thai local strains of Tribolium castaneum (Herbst) and their response to synthetic pheromone. Kasetsart J Nat Sci 48:9–16Google Scholar
  16. Katoh KK, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066CrossRefGoogle Scholar
  17. Kaur R, Daniels EV, Nayak MJ, Ebert PR, Schlipalius DI (2013) Determining changes in the distribution and abundance of a Rhyzopertha dominica phosphine resistance allele in farm grain storage using a DNA marker. Pest Man Sci 69:685–688CrossRefGoogle Scholar
  18. Kaur R, Subbarayalu M, Jagadeesan R, Daglish GJ, Nayak MK, Naik HR et al (2015) Phosphine resistance in India is characterized by a dihydrolipoamide dehydrogenase variant that is otherwise unobserved in eukaryotes. Heredity 115:188–194CrossRefGoogle Scholar
  19. Koçak E, Schlipalius DI, Kaur R, Tuck A, Ebert PR, Collins PJ, Yilmaz A (2015) Determining phosphine resistance in rust red flour beetle, Tribolium castaneum (Herbst.) (Coleoptera: Tenebrionidae) populations from Turkey. Türk Entomol Derg 39:129–136CrossRefGoogle Scholar
  20. Konemann CE, Hubhachen Z, Opit GP, Gautam S, Bajracharya NS (2017) Phosphine resistance in Cryptolestes ferrugineus (Coleoptera: Laemophloeidae) collected from grain storage facilities in Oklahoma, USA. J Econ Entomol 110(3):1377–1383CrossRefGoogle Scholar
  21. LeOra Software. (2005). PoloPlus user’s manual, version 2.0. LeOra Software, Petaluma, CAGoogle Scholar
  22. Lorini I, Collins PG, Daglish GJ, Nayak MK, Pavic H (2007) Detection and characterization of strong resistance to phosphine in Brazilian Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae). Pest Manag Sci 63:358–364CrossRefGoogle Scholar
  23. Lu Y, Zhang C, Wang Z, Yan X, Emery RN (2018) Rapid detection of phosphine resistance in the lesser grain borer, Rhyzopertha dominica (Coleoptera: Bostrychidae) from China using ARMS-PCR, pp 1043–1045. In: Adler C, Opit G, et al. (Eds) Proceedings of the 12th International working conference on stored product protection. Berlin, Germany October 7–11. Julius Kühn-Institut, BerlinGoogle Scholar
  24. Nayak MK, Holloway JC, Emery RN, Pavic H, Bartlet J, Collins PJ (2013) Strong resistance to phosphine in the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae): its characterization, a rapid assay for diagnosis and its distribution in Australia. Pest Manag Sci 69:48–53CrossRefGoogle Scholar
  25. Nguyen TT, Collins PJ, Duong TM, Schlipalius DI, Ebert PR (2016) Genetic conservation of phosphine resistance in the rice weevil Sitophilus oryzae. J Hered 107(3):228–237.  https://doi.org/10.1093/jhered/esw001 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Opit GP, Phillips TW, Aikins MJ, Hasan MM (2012) Phosphine resistance in Tribolium castaneum and Rhyzopertha dominica from Stored Wheat in Oklahoma. J Econ Entomol 105:1107–1114CrossRefGoogle Scholar
  27. Oppert B, Guedes RNC, Aikins MJ, Perkin L, Chen Z, Phillips TW, Zhu KY, Opit GP, Hoon K, Sun Y, Meredith G, Bramlett K, Supunpong Hernandez N, Sanderson B, Taylor M, Dhingra D, Blakey B, Lorenzen M, Adedipe F, Arthur F (2015) Genes related to mitochondrial functions are differentially expressed in phosphine-resistant and -susceptible Tribolium castaneum. BMC Genom 16:968CrossRefGoogle Scholar
  28. Pimentel MA, Faroni LR, Tótola MR, Guedes RN (2007) Phosphine resistance, respiration rate and fitness consequences in stored-product insects. Pest Manag Sci 63(9):876–881CrossRefGoogle Scholar
  29. Pimentel MA, Faroni LR, Silva FH, Batista MD, Guedes RN (2010) Spread of phosphine resistance among Brazilian populations of three species of stored product insects. Neotrop Entomol 39(1):101–107CrossRefGoogle Scholar
  30. Rajendran S (1999) Phosphine resistance in stored grain insect pests in India, pp 635–641. In: Jin Z, Liang Q, Liang Y, Tan X, Guan L (Eds) Proceedings of the 7th international working conference on stored-product protection, 14–19 October 1998, Beijing, China. Sichuan Publishing House of Science and Technology, Chengdu, ChinaGoogle Scholar
  31. Ren YL, O’Brien LG, Whittle GP (1994) Studies on the effect of carbon dioxide in insect treatment with phosphine. In: Highley E, Wright EJ, Banks H, Champ BR (eds) Stored products protection. Proceedings of the 6th international conference on stored product protection, CAB Press, Wallingford, Oxon, UK, pp 173–177Google Scholar
  32. Sağlam O, Edde PA, Phillips TW (2015) Resistance of Lasioderma serricorne (Coleoptera: Anobiidae) to fumigation with phosphine. J Econ Entomol 108:2489–2495CrossRefGoogle Scholar
  33. Schlipalius DI, Valmas N, Tuck AG, Jagadeesan R, Ma L, Kaur R, Goldinger A, Anderson C, Kuang K, Zuryn K, Mau YS, Cheng Q, Collins PJ, Nayak MK, Schirra HJ, Hilliard MA, Ebert PR (2012) A core metabolic enzyme mediates resistance to phosphine gas. Science 338:807–810CrossRefGoogle Scholar
  34. Schlipalius DI, Tuck AG, Jagadeesan R, Nguyen T, Kaur R, Subramanian S, Barrero R, Nayak MK, Ebert PR (2018) Variant linkage analysis using de Novo transcriptome sequencing identifies a conserved phosphine resistance gene in insects. Genetics 209:281–290CrossRefGoogle Scholar
  35. Tyler PS, Taylor RW, Rees DP (1983) Insect resistance to phosphine fumigation in food warehouses in Bangladesh. Internat Pest Cont 25:10–13Google Scholar
  36. Yeam I, Kang BC, Lindeman W, Frantz JD, Faber N, Jahn N (2005) Allele-specific CAPS markers based on point mutations in resistance alleles at the pvr1 locus encoding eIF4E in Capsicum. Theor Appl Gen 112:178–186CrossRefGoogle Scholar
  37. Zettler JL, Cuperus GW (1990) Pesticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae) and Rhyzopertha dominica (Coleoptera: Bostrichidae) in wheat. J Econ Entomol 83:1677–1681CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zhaorigetu Hubhachen
    • 1
    • 2
  • Hongbo Jiang
    • 1
    • 3
  • David Schlipalius
    • 4
  • Yoonseong Park
    • 1
  • Raul N. C. Guedes
    • 5
  • Brenda Oppert
    • 6
  • George Opit
    • 2
  • Thomas W. Phillips
    • 1
    Email author
  1. 1.Department of Entomology, 123 Waters HallKansas State UniversityManhattanUSA
  2. 2.Department of Entomology and Plant PathologyOklahoma State UniversityStillwaterUSA
  3. 3.Key Laboratory of Entomology and Pest Control Engineering, College of Plant ProtectionSouthwest UniversityChongqingPeople’s Republic of China
  4. 4.Department of Agriculture and Fisheries, Brisbane, QueenslandBrisbaneAustralia
  5. 5.Departamento de EntomologiaUniversidade Federal de VicosaVicosaBrazil
  6. 6.Center for Grain and Animal Health ResearchUSDA Agricultural Research ServiceManhattanUSA

Personalised recommendations