Frequency of alleles conferring resistance to the Bt toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa armigera (Lepidoptera: Noctuidae)

Journal of Economic Entomology

Volumn 100, Issue 6, 2007, Pages 1844-1853

  Mahon, R J ^a   Olsen, K M ^a   Downes, S ^a   Addison, S ^b  

^a CSIRO   (Australia)

^b Monsanto Company Australia   (Australia)

Author keywords

Allele frequency; Bt resistance; Cry1Ac; F2 screen; Helicoverpa armigera

Indexed keywords

BACILLUS THURINGIENSIS; GOSSYPIUM; GOSSYPIUM HIRSUTUM; HELICOVERPA ARMIGERA; LEPIDOPTERA; NOCTUIDAE;

EID: 38049119702     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1603/0022-0493(2007)100[1844:foacrt]2.0.co;2     Document Type: Article

References (63)

1. Akhurst, R. J., W. James, L. J. Bird, and C. Beard. 2003. Resistance to the Cry1Ac delta-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigere (Lepidoptera: Noctuidae). J. Econ. Entomol. 96: 1290-1299.
2. 2 screen for rare resistance alleles. J. Econ. Entomol. 91: 572-578.
3. Andow, D. A., and A. R. Ives. 2002. Monitoring and adaptive resistance management. Ecol. Appl. 12: 1378-1390.
4. Andow, D. A., D. N. Alstad, Y.-H. Pang, P. C. Bolin, and W. D. Hutchison. 1998. Using an F2 screen to search for resistance alleles to Bacillus thuringiensis toxin in European corn borer (Lepidoptera: Crambidae). J. Econ. Entomol. 91: 579-584.
5. [APVMA] Australian Pesticides and Veterinary Medicines Authority. 2003. Evaluation of the new active Bacillus thuringiensis var. kerstaki delta-endotoxins as produced by the Cry1Ac and Cry2Ab genes and their controlling sequences in the new product Bollgard II cotton event 15985. Australian Pesticides and Veterinary Medicines Authority, Canberra, Australia, (http://www.apvma.gov. au/publications/prsbollgard2.pdf).
6. Arrieta, G., and A. M. Espinoza. 2006. Characterization of a Bacillus thuringiensis strain collection from diverse Costa Rican natural ecosystems. Rev. Biol. Trop. 54: 13-27.
7. Armengol, G., M. C. Escobar, M. E. Maldonado, and S. Orduz. 2006. Diversity of Columbian strains of Bacilltis thuringiensia with insecticidal activity against dipteran and lepidopteran insects. J. Appl. Microbiol. 102: 77-88.
8. Augustin, S., C. Courtin, A. Rejasse, P. Lorme, A. Genissel, and D. Bourguet. 2004. Genetics of resistance to transgenic Bacillus thuringiensis poplars in Clirysomela tremutae (Coleopteru: Chrysomelidae). J. Econ. Entomol. 97: 1058-1064.
9. Bates, S. L., J.-Z. Zhao, R. T. Roush, and A. M. Shelton. 2005. Insect resistance management in GM crops: past, present and future. Nature (Lond.) 23: 57-62.
10. Bird, L. L., and R. J. Akhurst. 2004. The relative fitness of fitness of Cry1A-resistant and -susceptible Helicoverpa (armigera (Lepidoptera: Noctuidae) on conventional and transgenic cotton. J. Econ. Entomol. 97: 1699-1709.
11. Bird, L. L., and R. J. Akhurst. 2005. Fitness of Cry1A-resistant and -susceptible Helcoverpa armigera (Lepidoptera: Noctuidae) on transgenic cotton with reduced levels of Cry1Ac. J. Econ. Entomol. 98: 1311-1319.
12. Bravo, A., S. Sarahia, L. Lopez, H. Ontiveros, C. Abarca, A. Ortiz, M. Ortiz, L. Lina, F. J. Villalobos, G. Pena, et al. 1998. Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection. Appl. Environ. Microbiol. 64: 4965-4972.
13. Brunk, H. D. 1975. An introduction to mathematical statistics. Xerox College Publishing, Lexington, KY.
14. Carrière, Y., C. Ellers-Kirk, Y.-B. Liu, M. A. Sims, A. L. Patin, T. J. Dennehy, and B. E. Tabashnik. 2001a. Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94: 1571-1576.
15. Carrière, Y., C. Ellers-Kirk, A. L. Patin, M. A. Sims, S. Meyer, Y.-B. Liu, T. J. Dennehy, and B. E. Tabashnik. 2001b. Overwintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94: 935-941.
16. Daly, J., and K. Olsen. 2000. Genetics of Bt resistance pp185-188. In Proceedings of the 10th Australian Cotton Conference, 16-18 August 2000, Brisbane, Australia. Australian Cotton Growers Research Association, Narrabri, Australia.
17. Dang, H. T., and R. Gunning. 2002. Evidence of the shift in susceptibility to Bacillus thuringiensis delta-endotoxin Cry1Ac in Australian Helicoverpa armigera (Lepidoptera: Noctuidae). Resistant Pest Manag. Newsl. 11: 44-48.
18. Downes, S. J., R. Mahon, and K. Olsen. 2007. Adaptive resistance management in Australia for Bt-cotton: current status and future challenges. J. Invertebr. Pathol. 95:208-213.
19. English, L., H. Loidl Robbins, M. A. von Tersch, C. A. Kulesza, D. Ave, D. Coyle, C. S. Jany, and S. L. Slatin. 1994. Mode of action of CryIIA a Bacillus thuringiensis delta-endotoxin. Insect Biochem. Mol. Biol. 24: 1025-1035.
20. Falconer. D. S. 1964. Introduction to quantitative genetics. Oliver and Boyd, Glasgow, Scotland.
21. Fan, X., J.-Z. Zhao, Y. Fan, and X. Shi. 2000. Inhibition of transgenic Bt plants to the growth of cotton bollworm. Plant Protect. 26: 3-5.
22. Farrell, T. 2006. Cotton pest management guide 2006/07. NSW Department of Primary Industries, Orange, NSW, Australia.
23. Fitt, G. P. 2004. Implementation and impact of transgenic Bt cottons in Australia. In Proceedings of the World Cotton Research Conference-3, Cape Town, 9-13 March 2003. Agricultural Research Council, Institute for Industrial Crops, Pretoria, Republic of South Africa.
24. Fitt, G. P., J. C. Daly, C. L. Mares, and K. Olsen. 1998. Changing efficacy of transgenic Bt Cotton - patterns and consequences, pp. 189 -196. In M. P. Zalucki, R.A.I. Drew, and G. G. White [eds.], Pest management-future consequences, vol. 1. University of Queensland Printery, Brisbane, Australia.
25. Forrester, N. W., M. Cahill, L. Bird, and J. K. Layland. 1993. Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Bull. Entomol. Suppl. Ser. No. 1. 1-132.
26. Fox, J. L. 2003. Resistance to Bt toxin surprisingly absent from pests. Nat. Biotechnol. 21: 958-959.
27. Génissel, A., S. Augustin, C. Courtin, G. Pilate, P. Lorme, and D. Bourguet. 2003. Initial frequency of alleles conferring resistance to Bacillus thuringiensis poplar in a field population of Chrysomela tremulae, Proc. R. Soc. Lond. B 270: 791-797.
28. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43: 701-726.
29. Greenplate, J. T., J. W. Mullins, S. R. Penn, A. Dahm, B. J. Reich, J. A. Osborn, P. R. Rahn, L. Ruschke, and Z. W. Shappley. 2003. Partial characterization of cotton plants expressing two toxin proteins from Bacillus thuringiensis: relative toxin contribution, toxin interaction, and resistance management. J. Appl. Entomol. 127: 340-347.
30. Groeters, F. R., and B. E. Tabashnik. 2000. Roles of selection intensity, major genes, and minor genes in evolution of insecticidal resistance. J. Econ. Entomol. 93: 1580-1587.
31. Gunning, R. V., H. T. Dang, F. C. Kemp, I. C. Nicholson, and G. D. Moores. 2005. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 71: 2558-2563.
32. Higginson, D. M., S. Morin, M. E. Nyboer, R. W. Biggs, B. E. Tabashnik, and Y. Carriere. 2005. Evolutionary trade-offs in insect resistance to Bacillus thuringiensis crops: fitness cost affecting paternity. Evolution 59: 915-920.
33. Holt, H. E., C. Mares, and R. Akhurst. 2002. Determination of the Cry protein content of Bt transgenic cotton. CSIRO Technical Report No. 92. Commonwealth Scientific and Industrial Research Organisation, Canberra, Australia.
34. Höfte, H., and H. R. Whiteley. 1989. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53: 242-255.
35. Kerkpatrick, T. H. 1962. Methods of rearing Heliothis species and attempted crossbreeding. Qld. J. Agric. Sci. 19: 565-566.
36. Kim, H.-S. 2000. Comparative study of the frequency, flagellar serotype, crystal shape, toxicity and cry gene contents of Bacillus thuringiensis from three environments. Curr. Microbiol. 41: 250-256.
37. Kranthi, K. R., S. Kranthi, S. Ali, and S. K. Banerjee. 2000. Resistance to Cry1Ac 6-endotoxin of Bacillus thuringiensis in a laboratory selected strain of Helicoverpa armigera (Hubner). Curr. Sci. 78: 1001-1004.
38. Kvedaras, O. L., P. C. Gregg, and A.P.D. Socorro. 2000. Techniques used to determine the mating behaviour of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) in relation to host plants. Aust. J. Entomol. 39: 188-194.
39. Laster, M. L., and D. D. Hardee. 1995. Intermating compatibility between North American Helicoverpa zea and Heliothis armigera (Lepidoptera, Noctuidae) from Russia. J. Econ. Entomol. 88: 77-80.
40. Laster, M. L., and C. F. Sheng. 1995. Search for hybrid sterility for Helicoverpa zea in crosses between the North-American Heliothis zea and Helicoverpa armigera (Lepidoptera, Noctuidae) from China. J. Econ. Entomol. 88: 1288-1291.
41. Li, G., K. Wu, F. Gould, H. Feng, Y. He, and Y. Guo. 2004. Frequency of Bt resistance genes in Helicoverpa armigera populations from the Yellow River cotton-farming region of China. Entomol. Exp. Appl. 112: 135-143.
42. Liao, C., L. Brooks, S. C. Trowell, and R. J. Akhurst. 2005. Binding of Cry δ-endotoxins to brush border membrane vesicles of Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae). Insect Sci. 12: 231-240.
43. Liao, C., D. G. Heckel, and R. Akhurst. 2002. Toxicity of Bacillus thuringiensis insecticidal proteins for Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae), major pests of cotton. J. Invertebr. Pathol. 80: 55-63.
44. Liang, G., W. Tan, and Y. Guo. 2000. Study on screening and inheritance mode of resistance to Bt transgenic cotton in H. armigera. Acta Entomol. Sin. 43 (Suppl.): 57-62.
45. Mahon, R. J., K. M. Olsen, K. A. Garsia, and S. R. Young. 2007. Resistance to the Bt toxin Cry2Ab in a strain of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Australia. J. Econ. Entomol. 100: 894-902.
46. Martinez, C., J. E. Ibarra, and P. Caballero. 2005. Association between serotype, cry gene content, and toxicity to Helicoverpa armigera larvae among Bacillus thuringiensis isolates native to Spain. J. Invertebr. Pathol. 90: 91-97.
47. McGaughey, W. H., and M. E. Whalon. 1992. Managing insect resistance to Bacillus thuringiensis toxins. Science (Wash., D.C.) 258: 1451-1455.
48. McKenzie, J. A., A. G. Parker, and J. L. Yen. 1992. Polygenic and single gene responses to selection for resistance to diazinon in Lucilia cuprina. Genetics 130: 613-620.
49. Olsen, K. M., J. C. Daly, H. E. Holt, and E. J. Finnegan. 2005. Season-long variation in expression of the cry1Ac gene and efficacy of Bacillus thuringiensis toxin in transgenic cotton against Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 98: 1007-1017.
50. Prague, M. G. 2004. A new synonym of Helicoverpa zea (Boddie) and differentiation of adult males of H. zea and H. armigera (Hubner) (Lepidoptera: Noctuidae: Heliothinae). Ann. Entomol. Soc. Am. 97: 1222-1226.
51. Roush, R. T. 1998. Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil. Trans. R. Soc. Lond. B 353: 1777-1786.
52. Roush, R. T., and J. A. McKenzie. 1987. Ecological genetics of insecticide and acaricide resistance. Annu. Rev. Entomol. 32: 361-380.
53. Sokal, R. R., and F. J. Rohlf. 1969. Biometry. Freeman and Co., San Francisco, CA.
54. 2 screen variations and associated statistics. J. Econ. Entomol. 97: 1756-1764.
55. Stodola, T. J., D. A. Andow, A. R. Hyden, J. L. Hinton, J. J. Roark, L. L. Buschman, P. Porter, and G. B. Cronholm. 2006. Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in southern United States corn belt population of European corn borer (Lepidoptera: Crambidae). J. Econ. Entomol. 99: 502-507.
56. Tabashnik, B. E. 1994. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39: 47-79.
57. Tabashnik, B.E.T., J. Dennehy, and Y. Carrière. 2005. Delayed resistance to transgenic cotton in pink bollworm. Proc. Natl. Acad. Sci. U.S.A. 102: 15389-15393.
58. Teakle, R. E., and J. M. Jensen. 1985. Heliothis punctiger, pp. 312-322. In R. Singh and R. F. Moore [eds.], Handbook of insect rearing, vol. 2. Elsevier, Amsterdam, The Netherlands.
59. Wang, J., A. Boets, J. Van Rie, and G. Ren. 2003. Characterization of cry1, cry2, and cry9 genes in Bacillus thuringiensi isolates from China. J. Invertebr. Pathol. 82: 63-71.
60. Wenes, A.-L., D. Bourguet, D. A. Andow, C. Courtin, G. Carre, P. Lorme, L. Sanchez, and S. Augustin. 2006. Frequency and fitness cost of resistance to Bacillus thuringiensis in Chrysomela tremulae (Coleoptera: Chrysomelidae). Heredity 97: 127-134.
61. Wu, K. M., and Y. Y. Guo. 2005. The evolution of cotton pest management in China. Annu. Rev. Entomol. 50: 31-52.
62. Wu, K. M., Y. Y. Guo, and G. Head. 2006. Resistance monitoring of Helicoverpa armigera (Lepidoptera: Noctuidiae) to Bt insecticidal protein during 2001-2004 in China. J. Econ. Entomol. 99: 893-898.
63. Zimowska, G. J., and A. M. Handler. 2006. Highly conserved piggyBack elements in noctuid species of Lepidoptera. Insect Biochem. Mol. Biol. 36: 421-428.