Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

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

Nature Biotechnology volume 23, pages 57–62 (2005)Cite this article

Abstract

Transgenic plants expressing insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) were first commercialized in 1996 amid concern from some scientists, regulators and environmentalists that the widespread use of Bt crops would inevitably lead to resistance and the loss of a 'public good,' specifically, the susceptibility of insect pests to Bt proteins. Eight years later, Bt corn and cotton have been grown on a cumulative area >80 million ha worldwide. Despite dire predictions to the contrary, resistance to a Bt crop has yet to be documented, suggesting that resistance management strategies have been effective thus far. However, current strategies to delay resistance remain far from ideal. Eight years without resistance provides a timely opportunity for researchers, regulators and industry to reassess the risk of resistance and the most effective strategies to preserve Bt and other novel insect-resistant crops in development.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Bob Crimi

Figure 2

Bob Crimi

Similar content being viewed by others

References

  1. McCaffrey, A.R. Resistance to insecticides in heliothine Lepidoptera: a global view. Phil. Trans. R. Soc. Lond. B 353, 1735–1750 (1998).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  5. Tabashnik, B.E., Cushing, 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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  7. Frutos, R., Rang, C. & Royer, M. Managing resistance to plants producing Bacillus thuringiensis toxins. Crit. Rev. Biotechnol. 19, 227–276 (1999).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  18. Sayyed, A.H. & 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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  20. Tabashnik, B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39, 47–79 (1994).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Google Scholar 

  24. Roush, R.T. Designing resistance management programs: how can you choose? Pestic. Sci. 26, 423–441 (1989).

    Article  CAS  Google Scholar 

  25. Zhao, J-Z. et al. Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21, 1493–1497 (2003).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  28. Tabashnik, B.E. Delaying insect adaptation to transgenic plants: seed mixtures and refugia reconsidered. Proc. R. Soc. Lond. B 255, 7–12 (1994).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  32. Burd, A.D., Gould, F., Bradly, J.R., Van Duyn, J.W. & Moar, W.J. Estimated frequency of nonrecessive Bt resistance genes in bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in eastern North Carolina. J. Econ. Entomol. 96, 137–142 (2003).

    Article  CAS  PubMed  Google Scholar 

  33. Gould, F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43, 701–726 (1998).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  35. Gould, F. Potential and problems with high-dose strategies for pesticide engineered crops. Biocont. Sci. Technol 4, 451–461 (1994).

    Article  Google Scholar 

  36. Hargrove, T.R. Wrangling over refuge. Am. Sci. 87, 24–25 (1999).

    Google Scholar 

  37. Dove, A. Bt resistance plan appraised. Nat. Biotechnol. 17, 531–532 (1999).

    Article  CAS  PubMed  Google Scholar 

  38. Glaser, J.A. & Matten, S.R. Sustainability of insect resistance management strategies for transgenic Bt corn. Biotechnol. Adv. 22, 45–69 (2003).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  40. Ives, A.R. & Andow, D.A. Evolution of resistance to Bt-crops: directional selection in structured environments. Ecol. Lett. 5, 792–801 (2002).

    Article  Google Scholar 

  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_update1.pdf

    Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Google Scholar 

  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).

    Google Scholar 

  47. Gould, F. Testing Bt refuge strategies in the field. Nat. Biotechnol. 18, 266–276 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. http://www.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).

    Article  CAS  Google Scholar 

  50. Schnepf, E. et al. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 775–806 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Google Scholar 

  53. Liu, D. et al. Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat. Biotechnol. 21, 1222–1228 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Williamson, V.M. & Kaya, H.K. Sequence of a symbiont. Nat. Biotechnol. 21, 1294–1295 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Fitt, G.P. An Australian approach to IPM in cotton: integrating new technologies to minimize insecticide dependence. Crop Prot. 19, 793–800 (2000).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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/

    Google Scholar 

  58. Alstad, D.N. & Andow, D.A. Managing the evolution of insect resistance to transgenic plants. Science 268, 1894–1896 (1995).

    Article  CAS  PubMed  Google Scholar 

  59. Gould, F. Potential and problems with high-dose strategies for pesticide engineered crops. Biocont. Sci. Technol 4, 451–461 (1994).

    Article  Google Scholar 

  60. Arpaia, S., Gould, F. & Kennedy, G. Potential impact of Coleomegilla maculata predation on adaptation of Leptinotarsa decemlineata to Bt-transgenic potatoes. Entomol. Exp. Appl. 82, 91–100 (1997).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  63. Andow, D.A. & Ives, R.A. Monitoring and adaptive resistance management. Ecol. Appl. 12, 1378–1390 (2002).

    Article  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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 CryIAa toxin. FEBS Lett. 460, 385–390 (1999).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank N. Stewart and G. Head for their thoughtful reviews and helpful comments.

Author information

Authors and Affiliations

  1. Department of Entomology, Cornell University, NYSAES, 630 W. North Street, Geneva, 14456, New York, USA

    Sarah L Bates, Jian-Zhou Zhao & Anthony M Shelton

  2. Statewide IPM Program, University of California, 1 Shields Ave., Davis, 95616, California, USA

    Richard T Roush

Authors
  1. Sarah L Bates
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian-Zhou Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard T Roush
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anthony M Shelton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anthony M Shelton.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bates, S., Zhao, JZ., Roush, R. et al. Insect resistance management in GM crops: past, present and future. Nat Biotechnol 23, 57–62 (2005). https://doi.org/10.1038/nbt1056

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt1056

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing