Insect resistance to transgenic Bt crops: Lessons from the laboratory and field

Journal of Economic Entomology

Volumn 96, Issue 4, 2003, Pages 1031-1038

  Tabashnik, Bruce E ^a,b   Carrière, Yves ^a   Dennehy, Timothy J ^a   Morin, Shai ^a   Sisterson, Mark S ^a   Roush, Richard T ^a,b   Shelton, Anthony M ^a,c   Zhao, Jian Zhou ^a,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c New York State Agricultural Experiment Station   (United States)

Author keywords

Bacillus thuringiensis; Bt crops; Genetically modified crops; Refuge; Resistance

Indexed keywords

BACTERIAL TOXIN;

ARTICLE; BACILLUS THURINGIENSIS; GENETICS; INSECTICIDE RESISTANCE; TRANSGENIC PLANT;

BACILLUS THURINGIENSIS; BACTERIAL TOXINS; INSECTICIDE RESISTANCE; PLANTS, GENETICALLY MODIFIED;

EID: 0041422690     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1093/jee/96.4.1031     Document Type: Article

References (62)

1. Abbott Laboratories. 1992. B. t. products manual. Abbott, North Chicago, IL.
2. Akhurst, R. J., W. James, L. Bird, and C. Beard. 2003. Resistance to the CrylAe δ-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicocerpa arnigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 96: 1290-1299
3. Andow, D. A., D. M. Olson, R. L. Hellmich, D. N. Alstad, and W. D. Hutchison. 2000. Frequency of resistance to Bacillus thuringicnsis toxin Cryl Ab in an Iowa population of European com borer (Lepidoptera: Crambidae). J. Econ. Entomol. 93: 26-30.
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 com borer (Lepidoptera: Crambidae). J. Econ. Entomol. 91: 572-578.
5. Bourguet, D., J. Chaufaux, M. Sequin, C. Buisson, J. L. Hinton, T. J. Stodola, P. Porter, G. Cronholm, L. L. Buschman, and D. A. Andow. 2003. Frequency of alleles conferring resistance to Bt maize in French and US com belt populations of the European corn borer, Ostrinia mubilalis. Theor. Appl. Genet. 106: 1225-1233.
6. Burd, A. D., F. Gould, J. R. Bradley, J. W. Van Duyn, and W.J. Moar. 2003. Estimated frequency of nonrecessive Bt resistance genes in bollworm, Helicocerpa zea (Boddie) (Lepidoptera: Noctuidae) in eastern North Carolina. J. Econ. Entomol. 96: 137-142.
7. Cao, J., J. D. Tang, N. Strizhov, A. M. Shelton, and E. D. Earle. 1999. Transgenic broccoli with high levels of Bacillus thuringiensis CrylC protein control diamondback moth larvae resistant to CrylA or CrylC. Mol. Breed. 5: 131-141.
8. Caprio, M. A. 2001. Source-sink dynamics between transgenic and nontransgenic habitats and their role in the evolution of resistance. J. Econ. Entomol. 94: 698-705.
9. Carriere, Y., and B. E. Tahashnik. 2001. Reversing insect adaptation to transgenic insecticidal plants. Proc. R. Soc. London Ser. B 268: 1475-1480.
10. Carriere, Y., T. J. Dennehy, B. Pedersen, S. Hallcr, C. Ellers-Kirk, L. Antilla, S. Haller, Y. B. Liu, E. Willott, and B. E. Tabashnik. 2001a. Large-scale management of insect resistance to transgenic cotton in Arizona: can transgenic insecticidal crops be sustained? J. Econ. Entomol. 94: 315-325.
11. Carriere, Y., C. Ellers-Kirk, A. L. Patin, M. A. Sims, S. Meyer, Y.-B. Liu, T. J. Dennehy, and B. E. Tabashnik. 2001b. Overwintering costs associated with resistance to transgenic cotton in the pink bollwomi. J. Econ. Entomol. 94: 935-941.
12. Carriere, Y., C. Ellers-Kirk, Y.-B. Liu, M. A. Sims, A. L. Patin, T.J. Dennehy, and B. E. Tabashnik. 2001c. Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm. J. Econ. Entomol. 94: 1571-1576.
13. Carriere, Y.,T. Dennehy, C. Ellers-Kirk, D. Holley, Y.-B. Liu, M. Simms, and B. Tabashnik. 2002. Fitness costs, incom plete resistance, and management of resistance to Bt crops, pp. 82-91. In R. J. Akhurst, C. E. Beard, and P. Hughes (eds.), Biotechnology of Bacillus thuringiensis and its environmental impact: Proceedings of the 4th Pacific Rim Conference, Canberra. CSIRO, Canberra, Australia.
14. Carriere, Y., C. Ellers-Kirk, M. Sisterson, L. Antilla, M. Whitlow, T. J. Dennehy, and B. E. Tabashnik. 2003. Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc. Natl. Acad. Sci. USA 100:1519-1523.
15. Fan, X., J.-Z. Zhao, Y. Fan, and X. Shi. 2000. Inhibition of transgenic Bt plants to the growth of cotton bollworm. Plant Protection 26(2): 3-5.
16. Ferre, J., and J. Van Rie. 2002. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47: 501-533.
17. Fitt, G. P., and L. J. Wilson. 2000. Genetic engineering in IPM: a case study, pp. 108-125. In G. G. Kennedy andT. B. Sutton (eds.), Emerging technologies in integrated pest management: concepts, research and implementation. APS Press, St. Paul, MN.
18. Gahan, L. J., F. Gould, and D. G. Heckel. 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293: 857-860.
19. Gcorghiou, G. P., and C. E. Taylor. 1977. Operational influences in the evolution of insecticide resistance. J. Econ. Entomol. 70: 653-658.
20. Gcorghiou, G. P., and A. Lagunes-Tcjeda. 1991. The occurrence of resistance to pesticides in arthropods. FAO, United Nations, Rome.
21. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43: 701-726.
22. Gould, F., A. Anderson, A. Reynolds, L. Bumgarner, and W. Moar. 1995. Selection and genetic analysis of a Hcliothis virescens (Lepidoptera: N'octuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. J. Econ. Entomol. 88: 1545-1559.
23. Gould, F., A. Anderson, A. Jones, D. Sumerford, D. G. Heckel, J. Lopez, S. Micinski, R. Leonard, and M. Laster. 1997. Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proc. Natl. Acad. Sci. USA 94: 3519-3523.
24. Gould, F., N. Blair, M. Reid, T. L. Rennie, J. Lopez, and S. Micinski. 2002. Bacillus thuringiensis-toxin resistance management: stable isotope assessment of alternate host use by Helicocerpa zea. Proc. Natl. Acad. Sci. USA 99: 16581-16586.
25. Heckel, D. G., B. E. Tabashnik, Y. B. Liu, L. J. Gahan, A. M. Shelton, J. Z. Zhao, and S. W. Baxter. 2003. Diamondback moth resistance to Bt: relevance of genetics and molecular biology to detection and management. In N. M. Endersby and P. M. Ridland (eds.), The management of diamondback moth and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Victoria, Australia, 26-29 November 2001. Department of Primary Industries, Victoria, Australia, (in press).
26. Huang, F., R. A. Higgins, and L. L. Buschman. 1999. Heritability and stability of resistance to Bacillus thuringiensis in Ostrinia nubilalis (Lepidoptera: Crambidae). Bull. Entomol. Res. 89: 449-454.
27. Huang, F., L. L. Busclunan, R. A. Higgins, and H. Li. 2002. Survival of Kansas Dipel-resistant European corn borer (Lepidoptera: Crambidae) on Bt and non-Bt corn hybrids. J. Econ. Entomol. 95: 614-621.
28. Jackson, R.E.,J.R. Bradley, Jr., F.Gould, and J. W.Van Duyn. 2002. Genetic variation for resistance to CrylAc and Cry2Ab in bollworm, Helicocerpa zea, in North Carolina. 2002 Beltwide Cotton Conferences, (www.cotton.org/ beltwide/proceedings/getPDF.cfm?year=2002&paper=H017.pdf.)
29. James, C. 2001. Global status of commercialized transgenic crops: 2001. IS AAA briefs no. 24. International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY.
30. James, C. 2002. Global status of commercialized transgenic crops: 2002. ISAAA briefs no. 27: preview. International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY.
31. Liu, Y. B., and B. E. Tabashnik. 1997. Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis toxin CrylC in diamondback moth. Appl. Environ. Microbiol. 63: 2218-2223.
32. Liu, Y. B., B. E. Tabashnik, T. J. Dennehy, A. L. Patin, and A. C. Bartlett. 1999. Development time and resistance to Bt crops. Nature 400: 519.
33. Liu, Y. B., B. E. Tabashnik, T. J. Dennehy, A. L. Patin, M. A. Sims, S. K. Meyer, and Y. Carriere. 2001a. Effects of Bt cotton and CrylAc toxin on survival and development of pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94: 1237-1242.
34. Liu, Y. B., B. E. Tabashnik, S. K. Meyer, Y. Carriere, and A. C. Bartlett. 2001b. Genetics of pink bollworm resistance to Bacillus thuringiensis toxin CrylAc. J. Econ. Entomol. 94: 248-252.
35. Metz, T. D., R. T. Roush, J. D. Tang, A. M. Shelton, and E. D. Earle. 1995. Transgenic broccoli expressing a Bacillus thuringiensis insecticidal crystal protein: implications for pest resistance management strategies. Mol. Breed. 1: 309-317.
36. Morin, S., R. W. Biggs, M. S. Sisterson, L. Shriver, C. Ellers-Kirk, D. Higginson, D. Holley, J. J. Gahan, D. G. Heckel, Y. Carriere, T. J. Dennehy, J. K. Brown, and B. E. Tabashnik. 2003. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. USA 100: 5004-5009.
37. Onstad, D. W., C. A. Guse, P. Porter, L. L. Busclunan, R. A. Higgins, P. E. Sloderbeck, F. B. Peairs, and G. B. Cronholm. 2002. Modeling the development of resistance by stalk-boring Lepidopteran insects (Crambidae) in areas with transgenic corn and frequent insecticide use. J. Econ. Entomol. 95: 1033-1043.
38. Patin, A. L., T. J. Dennehy, M. A. Sims, B. E. Tabashnik, Y. B. Liu, L. Antilla, D. Gouge,T.J. Henneberry,and R.Staten. 1999. Status of pink bollworm susceptibility to Bt in Arizona, vol.2, pp. 991-996. In Proceedings of Beltwide Cotton Conferences 1999. National Cotton Council of America, Memphis, TN.
39. Peck, S., F. Gould, and S. P. Ellner. 1999. Spread of resistance in spatially extended regions of transgenic cotton: implications for management of Heliothis virescens (Lepidoptera: Noctuidae). J. Econ. Entomol. 92: 1-16.
40. Pcrcz, C.J., J.D. Tang, and A.M. Shclton. 1997. Comparison of leaf-dip and diet bioassays for monitoring Bacillus thuringiensis resistance in field populations of diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 90: 94-101.
41. Ramachandran, S., G. D. Buntin, J. N. All, B. E. Tabashnik, P. L. Raymer, M. J. Adang, D. A. Pulliam, and C. N. Stewart, Jr. 1998. Survival, development, and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola producing a Bacillus thuringiensis toxin. J. Econ. Entomol. 91: 1239-1244.
42. Roush, R. T. 1994. Managing pests and their resistance to Bacillus thuringiensis: can transgenics be better than sprays? Biocontrol Sci. Technol. 4: 501-516.
43. Schnepf, E., N. Crickmore, J. van Rie, D. Lereclus, J. Baum, J. Feitelson, D. R. Zeigler, and D. H. Dean. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62: 775-806.
44. Shelton, A. M, J. D. Tang, R. T. Roush, T. D. Metz, and E. D. Earle. 2000. Field tests on managing resistance to Bt- engineered plants. Nat. Biotechnol. 18: 339-342.
45. Shelton, A.M., J.-Z. Zhao,and R.T. Roush. 2002. Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47: 845-881.
46. Sims, M. A., T.J. Dennehy, L. Shriver, D. Holley, Y. Carriere, and B. E. Tabashnik. 2002. Susceptibility of Arizona pink bollworm to CrylAc: 2002 Beltwide Cotton Conferences, (www.cotton.org/beltwide/proceedings/getPDF.cfm? year=2002&paper=H069.pdf.)
47. Tabashnik, B. E. 1994. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39: 47-79.
48. Tabashnik, B. E., and B. A. Croft. 1982. Managing pesticide resistance in crop-arthropod complexes: interactions between, biological and operational factors. Environ. Entomol. 11: 1137-1144.
49. Tabashnik, B. E., N. L. Cushing, N. Finson, and M. W. Johnson. 1990. Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 83: 1671-1676.
50. Tabashnik, B. E., N. Finson, M. W. Johnson, and W. J. Moar. 1993. Resistance to toxins from Bacillus thuringiensis subsp. kurstaki causes minimal cross-resistance to B. thuringiensis subsp. aizawai in diamondback moth (Lepidoptera: Plutellidae). Appl. Environ. Microbiol. 59: 1332-1335.
51. Tabashnik, B. E., Y. B. Liu, T. Malvar, D. G. Heckel, L. Masson, and J. Ferre. 1998. Insect resistance to Bacillus thuringiensis: uniform or diverse? Phil. Trans. R. Soc. London B 353: 1751-1756.
52. Tabashnik, B. E., A. L. Patin, T. J. Dennchy, Y. B. Liu, Y. Carriere, M. A. Sims, and L. Antilla. 2000a. Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proc. Natl. Acad. Sci. USA 97: 12980-12984.
53. Tabashnik, B. E., R. T. Roush, E. D. Earle, and A. M. Shelton. 2000b. Resistance to Bt toxins. Science 287: 42.
54. Tabashnik, B. E., Y. B. Liu, T. J. Dennehy, M. A. Sims, M. S. Sistcrson, R. W. Biggs, and Y. Carrière. 2002a. Inheritance of resistance to Bt toxin CrylAc in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 95: 1018-1026.
55. Tabashnik, B. E., T. J. Dennehy, M. A. Sims, K. Larkin, G. P. Head, W. J. Moar, and Y. Carriere. 2002b. Control of resistant pink bollworm by transgenic cotton with Bacillus thuringiensis toxin Cry2Ab. Appl. Environ. Microbiol. 68: 3790-3794.
56. Tang, J. D., S. Gilboa, R. T. Roush, and A. M. Shelton. 1997. Inheritance, stability, and lack-of-fitness costs of field- selected resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae) from Florida. J. Econ. Entomol. 90: 732-741.
57. Tang, J. D, H. L. Collins, R. T. Roush, T. D. Mctz, E. D. Earle, and A. M. Shelton. 1999. Survival, weight gain, and opposition of resistant and susceptible Plutella xylostella (L.) on broccoli expressing CrylAc toxin of Bacillus thuringiensis. J. Econ. Entomol. 92: 47-55.
58. Tang, J. D., H. L. Collins, T. D. Metz, E. D. Earle, J. Z. Zhao, R. T. Roush, and A. M. Shelton. 2001. Greenhouse tests on resistance management of Bt transgenic plants using refuge strategies. J. Econ. Entomol. 94: 240-247.
59. Wierenga, J.M.D., L. Norris,andM.E. Whalon. 1996. Stage- specific mortality of Colorado potato beetle (Coleoptera: Chrysomelidae) feeding on transgenic potatoes. J. Econ. Entomol. 89: 1047-1052.
60. Wu, K., Y. Guo, N. Lv,J. T. Greenplate, and R. Deaton. 2002. Resistance monitoring of Helicocerpa arinigera to Bacillus thuringiensis insecticidal protein in China. J. Econ. Entomol. 95: 826-831.
61. Zhao, J. Z., H. L. Collins, J. D. Tang, J. Cao, E. D. Earle, R. T. Roush, S. Herrero, B. Escriche, J. Ferre, and A. M. Shelton. 2000. Development and characterization of diamondback moth resistance to transgenic broccoli expressing high levels of CrylC. Appl. Environ. Microbiol. 66: 3784-3789.
62. Zhao, J. Z., Y. X. Li, H. L. Collins, and A. M. Shelton. 2002. Examination of the 2 screen for rare resistance alleles to Bacillus thuringiensis toxins in the diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 95: 14-21.