Insect resistance management in GM crops: Past, present and future

Nature Biotechnology

Volumn 23, Issue 1, 2005, Pages 57-62

  Bates, Sarah L ^a   Zhao, Jian Zhou ^a   Roush, Richard T ^b   Shelton, Anthony M ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CROPS; GENETIC ENGINEERING; INSECTICIDES; PLANTS (BOTANY); PROTEINS;

ENVIRONMENTALISTS; INSECT PESTS;

INSECT CONTROL;

BACILLUS THURINGIENSIS TOXIN; BACTERIAL TOXIN;

BACILLUS THURINGIENSIS; GENETIC PEST CONTROL; GENETICALLY MODIFIED CROP; INSECT RESISTANCE; NONHUMAN; PEST MANAGEMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SURVIVAL; TOXIN SYNTHESIS; TRANSGENIC PLANT; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CROP; GENETICS; HETEROZYGOTE; INSECT; INSECTICIDE RESISTANCE; METABOLISM; TIME; TRANSGENE;

BACTERIA; FARM CROPS; GENETIC ENGINEERING; INSECT CONTROL; INSECTICIDES; PLANTS; PROTEINS;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); GOSSYPIUM HIRSUTUM; INSECTA; ZEA MAYS;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL TOXINS; CROPS, AGRICULTURAL; HETEROZYGOTE; INSECTICIDE RESISTANCE; INSECTS; MODELS, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; TIME FACTORS; TRANSGENES;

EID: 19644400147     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt1056     Document Type: Review

References (71)

1. McCaffrey, A.R. Resistance to insecticides in heliothine Lepidoptera: a global view. Phil. Trans. R. Soc. Lond. B 353, 1735-1750 (1998).
2. Tabashnik, B.E. et al. Insect resistance to transgenic Bt crops: lessons from the laboratory and the field. J. Econ. Entomol. 96, 1031-1038 (2003).
3. US Environmental Protection Agency. Biopesticides registration action document -Bacillus thuringiensis plant-incorporated protectants (EPA, Washington, DC, USA 2001). http://www.epa.gov/pesticides/biopesticides/pips/ bt_brad.htm
4. Fox, J.L. Resistance to Bt toxin surprisingly absent from pests. Nat. Biotechnol. 21, 958-959 (2003).
5. Tabashnik, B.E., Gushing, N.L., Finson, N. & Johnson, M.W. Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 83, 1671-1676 (1990).
6. Janmaat, A.F. & Meyers, J. Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc. R. Soc. Lond. B Biol.Sci. 270, 2263-2270 (2003).
7. Frutos, R., Rang, C. & Royer, M. Managing resistance to plants producing Bacillus thuringiensis toxins. Crit. Rev. Biotechnol. 19, 227-276 (1999).
8. Oppert, B., Hammel, R., Throne, J.E. & Kramer, K.J. Fitness costs of resistance to Bacillus thuringiensis in the Indianmeal moth, Plodia interpunctella. Entomol. Exp. Appl. 96, 281-287 (2000).
9. Carrière, Y. et al. Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94, 1571-1576 (2001).
10. Liu, Y.B. et al. Effects of Bt cotton and Cry1Ac toxin on survival and development of pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 94, 1237-1242 (2001).
11. Carrière, Y. et al. Overwintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae;. J. Econ. Entomol. 94, 935-941 (2001).
12. Groeters, F.R., Tabashnik, B.E., Finson, N. & Johnson, M.W. Fitness costs of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution 48, 197-201 (1994).
13. Trisyono, A. & Whalon, M.E. Fitness costs of resistance to Bacillus thuringiensis in Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 90, 267-271 (1997).
14. Alyokhin, A. & Ferro, D.N. Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. J. Econ. Entomol. 92, 510-515 (1999).
15. Akhurst, R.J., James, W., Bird, L.J. & Beard, C. Resistance to the Cry1Ac δ-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 96, 1290-1299 (2003).
16. Tang, J.D., Gilboa, S., Roush, R.T. & Shelton, A.M. 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 (1997).
17. Ramachandran, S. et al. Survival, development, and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola producing a Bacillus thuringiensis toxin. J. Econ. Entomol. 91, 1239-1244 (1998).
18. Sayyed, A.M. & Wright, D.J. Fitness costs and stability of resistance to Bacillus thuringiensis in a field population of the diamondback moth, Plutella xylostella. Ecol. Entomol. 26, 502-508 (2001).
19. Tabashnik, B.E. Groeters, F.R., Finson, N. & Johnson, M.W. Instability of resistance to Bacillus thuringiensis. Biocont. Sci. Technol. 4, 419-426 (1994).
20. Tabashnik, B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39, 47-79 (1994).
21. Roush, R.T. Bt-transgenic crops: just another pretty insecticide or a chance for a new start in resistance management? Pestic. Sci. 51, 328-334 (1997).
22. Roush, R.T. 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(1998).
23. Roush, R.T. Managing resistance to transgenic crops, in Advances in Insect Control (eds. Carozzi, N. & Koziel, M.) 271-294 (Taylor and Francis, London, UK, 1997).
24. Roush, R.T. Designing resistance management programs: how can you choose? Pestic. Sci. 26, 423-441 (1989).
25. Zhao, J-Z. et al. Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21, 1493-1497 (2003).
26. Huang, F., Higgins, R.A. & Buschman, L.L. Heritability and stability of resistance to Bacillus thuringiensis in Ostrinia nubilalis (Lepidoptera: Pyralidae). Bull. Entomol. Res. 89, 449-454 (1999).
27. Jackson, R.E., Bradley, J.R. & Van Duyn, J.W. Performance of feral and Cry1Ac-selected Helicoverpa zea (Lepidoptera: Noctuidae) strains on transgenic cottons expressing one or two Bacillus thuringiensis ssp. kurstaki proteins under greenhouse conditions. J. Entomol. Sci. 39, 46-55 (2004).
28. Tabashnik, B.E. Delaying insect adaptation to transgenic plants: seed mixtures and refugia reconsidered. Proc. R. Soc. Lond. B 255, 7-12 (1994).
29. Mallet, J. & Porter, P. Preventing insect adaptation to insect-resistant crops: are seed mixtures or refugia the best strategy? Proc. R. Soc. Lond. B. 250, 165-169.
30. Tang, J.D. et al. Greenhouse tests on resistance management of Bt transgenic plants using refuge strategies. J. Econ. Entomol. 94, 240-247 (2001).
31. Shelton, A.M.,Tang, J.D., Roush, R.T., Metz, T.D. & Earle, E.D. Field tests on managing resistance to Bt-engineered plants. Nat. Biotechnol. 18, 339-342 (2000).
32. Burd, A.D., Gould, F., Bradly, J.R., Van Duyn, J.W. & Moar, W.J. Estimated frequency of nonrecessive f resistance genes in bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in eastern North Carolina. J. Econ. Entomol. 96, 137-142 (2003).
33. Gould, F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43, 701-726 (1998).
34. Chilcutt, C.F. & Tabashnik, B.E. Contamination of refuges by Bacillus thuringiensis toxin genes from transgenic maize. Proc. Natl. Acad. Sci. USA 101, 7526-7529 (2004).
35. Gould, F. Potential and problems with high-dose strategies for pesticide engineered crops. Biocont. Sci. Technol 4, 451-461 (1994).
36. Hargrove, T.R. Wrangling over refuge. Am. Sci. 87, 24-25 (1999).
37. Dove, A. Bt resistance plan appraised. Nat. Biotechnol. 17, 531-532 (1999).
38. Glaser, J.A. & Matten, S.R. Sustainability of insect resistance management strategies for transgenic Bt corn. Biotechnol. Adv. 22, 45-69 (2003).
39. Caprio, M.A. Source-sink dynamics between transgenic and non-transgenic habitats and their role in the evolution of resistance. J. Econ. Entomol. 94, 698-705 (2001).
40. Ives, A.R. & Andow, D.A. Evolution of resistance to Bt-crops: directional selection in structured environments, Ecol. Lett. 5, 792-801 (2002).
41. Gould, F. et al. Bacillus thuringiensis-toxin resistance management: stable isotope assessment of alternate host use by Helicoverpa zea. Proc. Natl. Acad. Sci. USA 99, 16581-16586.
42. Jaffe, G. Planting Trouble Update. (Center for Science in the Public Interest, Washington, DC, USA, 2003). http://www.cspinet.org/new/pdf/ planting_trouble_updatel.pdf
43. Hurley, T.M. & Secchi, S., Babcok, B.A. & Hellmich, R.L. Managing the risk of European corn borer resistance to Bt corn. Environ. Resour. Econ. 22, 537-558 (2002).
44. James, C. Global status of commercialized transgenic crops: 2003. ISAAA Brief No. 30. (International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY, USA, 2003).
45. Zhao, J.-Z., Zhao, K., Lu, M., Fan, X. & Guo, S. Interactions between Helicoverpa armigera and transgenic cotton in North China. Sci. Agr. Sinica 31, 1-6 (1998).
46. Zhao, J.-Z. & Rui, C. Insect resistance management (IRM) for transgenic Bt cotton. In Transgenic Cotton, (eds. Jia, S.R. et. al.), 165-180, (China Science Press, Beijing, 2001).
47. Gould, F. Testing Bt refuge strategies in the field. Nat. Biotechnol. 18, 266-276 (2000).
48. http://vww.dowagro.com/usag/resource/20030423a.htm
49. Cao, J., Shelton, A.M. & Earle, E.D. Gene expression and insect resistance in transgenic broccoli containing a Bacillus thuringiensis cry1Ab gene with the chemically inducible PR-1a promoter. Mol. Breed. 8, 207-216 (2001).
50. Schnepf, E. et al. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 775-806 (1998).
51. Lee, M.K., Walters, F.S., Hart, H., Palekar, N. & Chen, J.-S. The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab δ-endotoxin. Appl. Environ. Microbiol. 69, 4648-4657 (2003).
52. Warren, G.W. Vegetative insecticidal proteins: novel proteins for control of corn pests, in Advances in Insect Control (eds. Carozzi, N. & Koziel, M.) 109-121 (Taylor and Francis, London, UK, 1997).
53. Liu, D. et al. Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat. Biotechnol. 21, 1222-1228 (2003).
54. Williamson, V.M. & Kaya, H.K. Sequence of a symbiont. Nat. Biotechnol. 21, 1294-1295 (2003).
55. Fitt, G.P. An Australian approach to IPM in cotton: integrating new technologies to minimize insecticide dependence. Crop Prof. 19, 793-800 (2000).
56. Sequeira, R.V. & Playford, C.L. Abundance of Helicoverpa (Lepidoptera: Noctuidae) pupae under cotton and other crops in central Queensland: implications for resistance management. Aust. J. Entomol. 40, 264-269 (2001).
57. Smith, M. Public sector plant breeding and pest resistance management, in Online Proceedings of CAST Pest Resistance Management Symposium, Indianapolis, IN, USA, April 10-11, 2003. (The Council for Agricultural Science and Technology, Washington, DC, USA, 2003). http://www.pestmanagement.info/ rmworkshop/
58. Alstad, D.N. & Andow, D.A. Managing the evolution of insect resistance to transgenic plants. Science 266, 1894-1896 (1995).
59. Gould, F. Potential and problems with high-dose strategies for pesticide engineered crops. Biocont. Sci. Technol 4, 451-461 (1994).
60. Arpaia, S., Gould, F. & Kennedy, G. Potential impact of Coleomegilla maculata predation on adaptation of Leptinotarsa decemlineatato Bt-transgenic potatoes. Entomol. Exp. Appl. 82, 91-100 (1997).
61. James, C. Global status of commercialized transgenic crops: 2002. ISAA Brief NO. 27 (International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY, USA, 2002).
62. Shelton, A.M., Zhao, J-Z. & Roush, R.T. Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47, 845-881 (2002).
63. Andow, D.A. & Ives, R.A. Monitoring and adaptive resistance management, Ecol. Appl. 12, 1378-1390 (2002).
64. Carrière, Y. et al. Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc. Natl. Acad. Sci. USA 100, 1519-1523 (2003).
65. Hawthorne, D., Sigfried, B., Shelton, A.M. & Hellmich, R. Monitoring for Resistance Alleles: a Report from an Advisory Panel on Insect Resistance Monitoring Methods for Bt corn. Agricultural Biotechnology Stewardship Committee Report (Agricultural Biotechnology Stewardship Technical Committee, Washington, DC, 2002).
66. Andow, D.A. & Alstad, D.N. F2 screen for rare resistance alleles. J. Econ. Entomol. 91, 572-578 (1998).
67. Zhao, J-Z., Li, Y., Collins, H.L. & Shelton, A.M. Examination of the F2 screen for rare resistance alleles to Bacillus thuringiensis toxins in the diamondback moth. J. Econ. Entomol. 95, 14-21 (2002).
68. Nagamatsu, Y., Koike, T., Sasaki, K., Yoshimoto, A. & Furukawa, Y. The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal Cry1Aa toxin. FEBS Lett. 460, 385-390 (1999).
69. Vadlamudi, R.K., Weber, E., Ji, I., Ji, T.H. & Bulla Lee, A. Jr. Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J. Biol. Chem. 270, 5490-5494 (1995).
70. Gahan, L.J., Gould, F. & Heckel, D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293, 857-860 (2001).
71. Morin, S. et al. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. USA 100, 5004-5009 (2003).