Russian Journal of Plant Physiology

, Volume 62, Issue 1, pp 14–22 | Cite as

Can efficient insecticidal plants be created or the evolution of phytophage resistance to commercial transgenic Bt-plants

  • A. G. Viktorov


During 17 years when Bt-crops were used on an industrial scale, eight species of pests (seven species of lepidopterans from the order Lepidoptera belonging to four families and one species of coleopterous insects from the order Coleoptera) developed resistance to them. In five cases, the mutation of resistance was so widespread that it caused an economic damage. The rate of evolution of resistance to the so-called insecticidal plants (containing δ-endotoxins or Cry-proteins causing the lysis of intestines in the larvae of insects from different orders) is comparable to the rate of evolution of resistance to chemical insecticides, which suggests that the production of pesticidal plants with a view to protect agricultural crops from the pests has no future. Plausible reasons are the following: first, it is impossible to produce transgenic plants, where expression of Cry-proteins in all tissues throughout the entire life cycle would be at the level lethal for the pests; second, in spite of the assumptions based on a low probability of the event, there arise not only dominant mutations of resistance but also recessive mutations that are not associated with the fitness costs; third, in spite of expectations there arises cross-resistance between Cry-proteins from different families.


transgenic Bt-plants Cry-proteins phytophages evolution of resistance refuge 



δ-endotoxins (Bt-toxins), order-specific protein toxins produced by the bacterium Bacillus thuringiensis


genetically modified crops


resistance ratio


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Georghiou, G.P., The magnitude of the resistance problem, Pesticide resistance: strategies and tactics for management, Committee on strategies for the management of pesticide resistant pest populations, Washington, D.C.: National Academy Press, 1986, pp. 14–43.Google Scholar
  2. 2.
    Tabashnik, B.E., Mota-Sanchez, D., Whalon, M.E., Hollingworth, R.M., and Carrière, Y., Defining terms for proactive management of resistance to Bt crops and pesticides, J. Econ. Entomol., 2014, vol. 107, pp. 496–507.PubMedCrossRefGoogle Scholar
  3. 3.
    Tabashnik, B.E., Evolution of resistance to Bacillus thuringiensis, Annu. Rev. Entomol., 1994, vol. 39, pp. 47–79.CrossRefGoogle Scholar
  4. 4.
    Ferre, J. and van Rie, J., Biochemistry and genetics of insect resistance to Bacillus thuringiensis, Annu. Rev. Entomol., 2002, vol. 47, pp. 501–533.PubMedCrossRefGoogle Scholar
  5. 5.
    Georghiou, G.P. and Taylor, C.E., Factors influencing the evolution of resistance, Pesticide resistance: strategies and tactics for management, Committee on strategies for the management of pesticide resistant pest populations, Washington, D.C.: National Academy Press, 1986, pp. 157–169.Google Scholar
  6. 6.
    Downes, S.J., Mahon, R., Rossiter, L., Kauter, G., Leven, T., Fitt, G., and Baker, G., Adaptive management of pest resistance by Helicoverpa species (Noctuidae) in Australia to the Cry2Ab Bt toxin in Bollgard II cotton, Evol. Appl., 2010, vol. 3, pp. 574–584.PubMedCentralCrossRefGoogle Scholar
  7. 7.
    Liu, Y.B. and Tabashnik, B.E., Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis, Proc. R. Soc. Biol. Sci., 1997, vol. 264, pp. 605–610.CrossRefGoogle Scholar
  8. 8.
    Gould, F., Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology, Annu. Rev. Entomol., 1998, vol. 43, pp. 701–726.PubMedCrossRefGoogle Scholar
  9. 9.
    Bt Plant-Incorporated Protectants Biopesticides Registration Action Document, D, Insect Resistance Management, US Environmental Protection Agency (EPA), October 15, 2001,
  10. 10.
    Carrière, Y., Crowder, D.W., and Tabashnik, B.E., Evolutionary ecology of adaptation to Bt crops, Evol. Appl., 2010, vol. 3, pp. 561–573.PubMedCentralCrossRefGoogle Scholar
  11. 11.
    Jaffe, G., Complancency on the Farm. Significant Noncompliance with EPA’s Refuge Requirements Threatens the Future Effectiveness of Genetically Engineered Pest-Protected Corn, Washington, D.C.: Center for Science in the Public Interest, 2009.Google Scholar
  12. 12.
    A Set of Scientific Issues Being Considered by the Environmental Protection Agency Regarding Scientific Uncertainties Associated with Corn Rootworm Resistance Monitoring for Bt Corn Plant Incorporated Protectants (PIPs), US Environmental Protection Agency (EPA), December 4–5, 2013,
  13. 13.
    Kruger, M., van Rensburg, J.B.J., and Berg, J., Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa, Crop Protect., 2009, vol. 28, pp. 684–689.CrossRefGoogle Scholar
  14. 14.
    Kruger, M., van Rensburg, J.B.J., and Berg, J., No fitness costs associated with resistance of Busseola fusca (Lepidoptera: Noctuidae) to genetically modified Bt maize, Crop Protect., 2014, vol. 55, pp. 1–6.CrossRefGoogle Scholar
  15. 15.
    Viktorov, A.G., Influence of Bt-plants on soil biota and pleiotropic effect of δ-endotoxin-encoding genes, Russ. J. Plant Physiol., 2008, vol. 55, pp. 738–747.CrossRefGoogle Scholar
  16. 16.
    Bird, L.J. and Akhurst, R.J., Relative fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera, Noctuidae) on conventional and transgenic cotton, J. Econ. Entomol., 2004, vol. 97, pp. 1699–1709.PubMedCrossRefGoogle Scholar
  17. 17.
    Bird, L.J. and Akhurst, R.J., Fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera, Noctuidae) on transgenic cotton with reduced levels of Cry1Ac, J. Econ. Entomol., 2005, vol. 98, pp. 1311–1319.PubMedCrossRefGoogle Scholar
  18. 18.
    Pettigrew, W.T. and Adamczyk, J.J., Nitrogen fertility and planting date effects on lint yield and Cry1Ac (Bt) endotoxin production, Agron. J., 2006, vol. 98, pp. 691–697.CrossRefGoogle Scholar
  19. 19.
    Downes, S.J., Parker, T., and Mahon, R., Incipient resistance of Helicoverpa punctigera to the Cry2Ab Bt toxin in Bollgard II-cotton, PLoS ONE, 2010, vol. 5: e12567, PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Gould, F., Kennedy, G.G., and Johnson, M.T., Effects of natural enemies on the rate of herbivore adaptation to resistant host plants, Entomol. Exp. Appl., 1991, vol. 58, pp. 1–14.CrossRefGoogle Scholar
  21. 21.
    Johnson, M.T., Gould, F., and Kennedy, G.G., Effect of an entomopathogen on adaptation of Heliothis virescens populations to transgenic host plants, Entomol. Exp. Appl., 1997, vol. 83, pp. 121–135.CrossRefGoogle Scholar
  22. 22.
    Parker, C.D. and Luttrell, R.G., Interplant movement of Heliothis virescens (Lepidoptera: Noctuidae) larvae in pure and mixed plantings of cotton with and without expression of the Cry1Ac delta endotoxin protein of Bacillus thuringiensis Berliner, J. Econ. Entomol., 1999, vol. 92, pp. 837–845.PubMedGoogle Scholar
  23. 23.
    Gore, J., Leonard, B.R., Church, G.E., and Cook, D.R., Behavior of bollworm (Lepidoptera: Noctuidae) larvae on genetically engineered cotton, J. Econ. Entomol., 2002, vol. 95, pp. 763–769.PubMedCrossRefGoogle Scholar
  24. 24.
    Tabashnik, B.E., Gassmann, A.J., Crowder, D.W., and Carriere, Y., Insect resistance to Bt crops: evidence versus theory, Nat. Biotechnol., 2008, vol. 26, pp. 199–202.PubMedCrossRefGoogle Scholar
  25. 25.
    Monnerat, R., Martins, E., Queiroz, P., Orduz, S., Jaramillo, G., Benintende, G., Cozzi, J., Real, M.D., Martinez-Ramirez, A., Rausell, C., Cerón, J., Ibarra, J.E., del Rincon-Castro, M.C., Espinoza, A.M., Meza-Basso, L., Cabrera, L., Sánchez, J., Soberon, M., and Bravo, A., Genetic variability of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) populations from Latin America is associated with variations in susceptibility to Bacillus thuringiensis Cry toxins, Appl. Environ. Microbiol., 2006, vol. 72, pp. 7029–7035.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Tabashnik, B.E., Gassmann, A.J., Crowder, D.W., and Carriere, Y., Field-evolved resistance to Bt toxins, Nat. Biotechnol., 2008, vol. 26, pp. 1074–1076.CrossRefGoogle Scholar
  27. 27.
    Vélez, A.M., Spencer, T.A., Alves, A.P., Crespo, A.L.B., and Siegfried, B.D., Fitness costs of Cry1F resistance in fall armyworm, Spodoptera frugiperda, J. Appl. Entomol., 2014, vol. 138, pp. 315–325.CrossRefGoogle Scholar
  28. 28.
    US Environmental Protection Agency (EPA). Current & Previously Registered, Section 3, PIP Registrations, 2014,
  29. 29.
    Haldane, J.B.S., The cost of natural selection, J. Genet., 1957, vol. 55, pp. 511–524.CrossRefGoogle Scholar
  30. 30.
    Lu, B., Thresholds and mechanisms of survival for Bt-susceptible Helicoverpa spp. living on Bollgard II® cotton, Ph.D. Thesis, New England: University of New England, School of Environmental and Rural Sciences, 2010.Google Scholar
  31. 31.
    Brévault, T., Heuberger, S., Zhang, M., Ellers-Kirk, C., Masson, X., Ni, L., Li, X., Tabashnik, B.E., and Carriere, Y., Potential shortfall of pyramided Bt cotton for resistance management, Proc. Natl. Acad. Sci. USA, 2013, vol. 110, pp. 5806–5811.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Whitburn, G. and Downes, S., Surviving Helicoverpa larvae in Bollgard II: survey results, Aust. Cottongrower Mag., 2009, vol. 30, pp. 12–16.Google Scholar
  33. 33.
    Caccia, S., Hernandez-Rodrιguez, C., Mahon, R., Downes, S., James, W., Bautsoens, N., Rie, V.J., and Ferré, J., Target site alteration is responsible for field derived resistance to Bacillus thuringiensis Cry2A insecticidal proteins in Helicoverpa spp., PLoS ONE, 2010, vol. 5: e9975, http://10.1371/journal.pone.0009975PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Mahon, R. and Olsen, K., Limited survival of a Cry2Ab-resistant strain of Helicoverpa armigera (Lepidoptera: Noctuidae) on Bollgard II, J. Econ. Entomol., 2009, vol. 102, pp. 708–716.PubMedCrossRefGoogle Scholar
  35. 35.
    Mahon, R. and Young, S., Selection experiments to assess fitness costs associated with Cry2Ab resistance in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae), J. Econ. Entomol., 2010, vol. 103, pp. 835–842.PubMedCrossRefGoogle Scholar
  36. 36.
    Tabashnik, B.E., Unnithan, G.C., Masson, L., Crowder, D.W., Li, X., and Carrière, Y., Asymmetrical crossresistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 11 889–11 984.CrossRefGoogle Scholar
  37. 37.
    Downes, S.J. and Mahon, R., Evolution, ecology and management of resistance in Helicoverpa spp. to Bt cotton in Australia, J. Invertebrate Pathol., 2012, vol. 110, pp. 281–286.CrossRefGoogle Scholar
  38. 38.
    Jin, L., Wei, Y., Zhang, L., Yang, Y., Tabashnik, B.E., and Wu, Y., Dominant resistance to Bt cotton and minor cross resistance to Bt toxin Cry2Ab in cotton bollworm from China, Evol. Appl., 2013, vol. 6, pp. 1222–1235.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Gassmann, A.J., Petzold-Maxwell, J.L., Clifton, E.H., Dunbar, M.W., Hoffmann, A.M., Ingber, D.A., and Keweshan, R.S., Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize, Proc. Natl. Acad. Sci. USA, 2014, vol. 111, pp. 5141–5146.PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Van den Berg, J., Hilbeck, A., and Bohn, T., Pest resistance to Cry1Ab Bt maize: yield resistance, contributing factors and lessons from South Africa, Crop Protect., 2013, vol. 54, pp. 154–160.CrossRefGoogle Scholar
  41. 41.
    Zhang, H., Yin, W., Zhao, J., Jin, L., Yang, Y., Wu, S., Tabashnik, B.E., and Wu, Y., Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China, PLoS ONE, 2011, vol. 6: e22874, doi 10.1371/journal.pone.0022874PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Zhang, H., Wen, T., Zhao, J., Jin, L., Yang, J., Liu, C., Yang, Y., Wu, S., Wu, K., Cui, J., Tabashnik, B.E., and Wu, Y., Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China, Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 10275–10280.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Storer, N.P., Babcock, J.M., Schlenz, M., Meade, T., Thompson, G.D., Bing, J.W., and Huckaba, R.M., Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico, J. Econ. Entomol., 2010, vol. 103, pp. 1031–1038.PubMedCrossRefGoogle Scholar
  44. 44.
    Storer, N.P., Kubiszak, M.E., King, J.E., Thompson, G.D., and Santos, A.C., Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico, J. Invertebrate Pathol., 2012, vol. 110, pp. 294–300.CrossRefGoogle Scholar
  45. 45.
    Huang, F., Ghimire, M.N., Leonard, B.R., Davies, C., Levy, R., and Baldwin, J., Extended monitoring of resistance to Bacillus thuringiensis Cry1Ab maize in Diatraea saccharalis (Lepidoptera: Crambidae), GM Crops Food, 2012, vol. 3, pp. 245–254.PubMedCrossRefGoogle Scholar
  46. 46.
    Alcantara, E., Estrada, A., Alpuerto, V., and Head, G., Monitoring Cry1Ab susceptibility in Asian corn borer (Lepidoptera: Crambidae) on Bt corn in the Philippines, Crop Protect., 2011, vol. 30, pp. 554–559.CrossRefGoogle Scholar
  47. 47.
    Wan, P., Huang, Y., Wu, H., Huang, M., Cong, S., Tabashnik, B.E., and Wu, K., Increased frequency of pink bollworm resistance to Bt toxin Cry1Ac in China, PLoS ONE, 2012, vol. 7: e29975, doi 10.1371/journal.pone.0029975PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Dhurua, S. and Gujar, G.T., Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India, Pest Manag. Sci., 2011, vol. 67, pp. 898–903.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  1. 1.Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia

Personalised recommendations