Hostname: page-component-6bf8c574d5-vmclg Total loading time: 0 Render date: 2025-02-22T05:17:14.643Z Has data issue: false hasContentIssue false
  • English
  • Français

Inheritance of Cry1F resistance in laboratory-selected European corn borer and its survival on transgenic corn expressing the Cry1F toxin

Published online by Cambridge University Press:  17 July 2008

E.J.G. Pereira ,
N.P. Storer  and
B.D. Siegfried
E.J.G. Pereira
Affiliation:
Department of Entomology, University of Nebraska, Lincoln, NE 68583
N.P. Storer
Affiliation:
Dow AgroSciences LLC, 9330 Zionsville Rd., Indianapolis, IN 46268
B.D. Siegfried*
Affiliation:
Department of Entomology, University of Nebraska, Lincoln, NE 68583
*
*Author for correspondence Fax: 001 (402) 472-4687 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

A major assumption of the high-dose/refuge strategy proposed for insect resistance management strategies for transgenic crop plants that express toxins from Bacillus thuringiensis is that resistance traits that evolve in pest species will be recessive. The inheritance of Cry1F resistance and larval survival on commercially available Cry1F corn hybrids were determined in a laboratory-selected strain of European corn borer, Ostrinia nubilalis (Hübner), displaying more than 3000-fold resistance to Cry1F. Concentration-response bioassays of reciprocal parental crosses indicated that the resistance is autosomal and recessive. Bioassays of the backcross of the F1 generation with the selected strain were consistent with the hypothesis that a single locus, or a set of tightly linked loci, is responsible for the resistance. Greenhouse experiments with Cry1F-expressing corn hybrids indicated that some resistant larvae survived the high dose of toxin delivered by Cry1F-expressing plants although F1 progeny of susceptible by resistant crosses had fitness close to zero. These results provide the first direct evidence that the high dose/refuge strategy currently in place to manage resistance in Cry1F-expressing corn is appropriate.

Keywords

Bt cornOstrinia nubilalisgenetic crosseson-plant survivalhigh-dose refuge strategyresistance management
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 6 , December 2008 , pp. 621 - 629
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alves, A.P., Spencer, T.A., Tabashnik, B.E. & Siegfried, B.D. (2006) Inheritance of resistance to the Cry1Ab Bacillus thuringiensis toxin in Ostrinia nubilalis (Lepidoptera: Crambidae). Journal of Economic Entomology 99, 494–501.CrossRefGoogle Scholar
Andow, D.A. & Hutchison, W.D. (1998) Bt-corn resistance management. pp. 19–66 in Mellon, M. & Rissler, J. (Eds) Now or Never: Serious New Plans to Save a Natural Pest Control. Cambridge, MA, Union of Concerned Scientists.Google Scholar
Bates, S.L., Zhao, J.Z., Roush, R.T. & Shelton, A.M. (2005) Insect resistance management in GM crops: past, present and future. Nature Biotechnology 23, 57–62.CrossRefGoogle ScholarPubMed
Bolin, P.C., Hutchison, W.D. & Andow, D.A. (1999) Long-term selection for resistance to Bacillus thuringiensis Cry1Ac endotoxin in a Minnesota population of European corn borer (Lepidoptera: Crambidae). Journal of Economic Entomology 92, 1021–1030.CrossRefGoogle Scholar
Bourguet, D., Genissel, A. & Raymond, M. (2000) Insecticide resistance and dominance levels. Journal of Economic Entomology 93, 1588–1595.CrossRefGoogle ScholarPubMed
Carrière, Y. & Tabashnik, B.E. (2001) Reversing insect adaptation to transgenic insecticidal plants. Proceedings of the Royal Society of London, Series B: Biological Sciences 268, 1475–1480.CrossRefGoogle ScholarPubMed
Carrière, Y., Deland, J.P., Roff, D.A. & Vincent, C. (1994) Life-history costs associated with the evolution of insecticide resistance. Proceedings of the Royal Society of London, Series B: Biological Sciences 258, 35–40.Google Scholar
Chambers, J.A., Jelen, A., Gilbert, M.P., Jany, C.S., Johnson, T.B. & Gawronburke, C. (1991) Isolation and characterization of a novel insecticidal crystal protein gene from Bacillus thuringiensis subsp. aizawai. Journal of Bacteriology 173, 3966–3976.CrossRefGoogle ScholarPubMed
Chaufaux, J., Seguin, M., Swanson, J.J., Bourguet, D. & Siegfried, B.D. (2001) Chronic exposure of the European corn borer (Lepidoptera: Crambidae) to CrylAb Bacillus thuringiensis toxin. Journal of Economic Entomology 94, 1564–1570.CrossRefGoogle Scholar
Ferré, J. & Van Rie, J. (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology 47, 501–533.CrossRefGoogle ScholarPubMed
Gahan, L.J., Gould, F. & Heckel, D.G. (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293, 857–860.CrossRefGoogle ScholarPubMed
Glaser, J.A. & Matten, S.R. (2003) Sustainability of insect resistance management strategies for transgenic Bt corn. Biotechnology Advances 22, 45–69.CrossRefGoogle ScholarPubMed
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726.CrossRefGoogle ScholarPubMed
Hellmich, R.L., Siegfried, B.D., Sears, M.K., Stanley-Horn, D.E., Daniels, M.J., Mattila, H.R., Spencer, T., Bidne, K.G. & Lewis, L.C. (2001) Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proceedings of the National Academy of Sciences of the United States of America 98, 11925–11930.CrossRefGoogle ScholarPubMed
Huang, F.N., Higgins, R.A. & Buschman, L.L. (1997) Baseline susceptibility and changes in susceptibility to Bacillus thuringiensis subsp. kurstaki under selection pressure in European corn borer (Lepidoptera: Pyralidae). Journal of Economic Entomology 90, 1137–1143.CrossRefGoogle Scholar
Huang, F., Buschman, L.L., Higgins, R.A. & McGaughey, W.H. (1999) Inheritance of resistance to Bacillus thuringiensis toxin (Dipel ES) in the European corn borer. Science 284, 965–967.CrossRefGoogle ScholarPubMed
Huang, F.N., Buschman, L.L., Higgins, R.A. & Li, H. (2002) Survival of Kansas Dipel-resistant European corn borer (Lepidoptera: Crambidae) on Bt and non-Bt corn hybrids. Journal of Economic Entomology 95, 614–621.CrossRefGoogle ScholarPubMed
Hudon, M., LeRoux, E.J. & Harcourt, D.G. (1989) Seventy years of European corn borer (Ostrinia nubilalis) research in North America. Agricultural Zoology Reviews 3, 53–96.Google Scholar
ILSI – International Life Sciences Institute (1998) An Evaluation of Insect Resistance Management in Bt Field Corn: A Science-based Framework for Risk Assessment and Risk Management. 85 pp. Washington, DC, ILSI.Google Scholar
Koziel, M.G., Beland, G.L., Bowman, C., Carozzi, N.B., Crenshaw, R., Crossland, L., Dawson, J., Desai, N., Hill, M., Kadwell, S., Launis, K., Lewis, K., Maddox, D., Mcpherson, K., Meghji, M.R., Merlin, E., Rhodes, R., Warren, G.W., Wright, M. & Evola, S.V. (1993) Field Performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Nature Biotechnology 11, 194–200.CrossRefGoogle Scholar
LeOra Software (1987) POLO-PC: A User's Guide to Probit and Logit Analysis. 22 pp. Berkeley, CA.Google Scholar
Lewis, L.C. & Lynch, R.E. (1969) Rearing the European corn borer, Ostrinia nubilalis (Hübner), on diets containing corn leaf and wheat germ. Iowa State Journal of Science 44, 9–14.Google Scholar
Liu, Y.B. & Tabashnik, B.E. (1997) Inheritance of resistance to the Bacillus thuringiensis toxin Cry1C in the diamondback moth. Applied and Environmental Microbiology 63, 2218–2223.CrossRefGoogle Scholar
Liu, Y.B., Tabashnik, B.E., Dennehy, T.J., Patin, A.L. & Bartlett, A.C. (1999) Development time and resistance to Bt crops. Nature 400, 519.CrossRefGoogle ScholarPubMed
Marçon, P.C.R.G., Young, L.J., Steffey, K.L. & Siegfried, B.D. (1999) Baseline susceptibility of European corn borer (Lepidoptera: Crambidae) to Bacillus thuringiensis toxins. Journal of Economic Entomology 92, 279–285.CrossRefGoogle Scholar
Mason, C.E., Rice, M.E., Calvin, D.D., Van Duyn, J.W., Showers, W.B., Hutchison, W.D., Witkowski, J.F., Higgins, R.A., Onstad, D.W. & Dively, G.P. (1996) European Corn Borer – Ecology and Management. 57 pp. Ames, IA, Iowa State University.Google Scholar
Mendelsohn, M., Kough, J., Vaituzis, Z. & Matthews, K. (2003) Are Bt crops safe? Nature Biotechnology 21, 1003–1009.CrossRefGoogle ScholarPubMed
Metz, T.D., Roush, R.T., Tang, J.D., Shelton, A.M. & Earle, E.D. (1995) Transgenic broccoli expressing a Bacillus thuringiensis insecticidal crystal protein – implications for pest resistance management strategies. Molecular Breeding 1, 309–317.CrossRefGoogle Scholar
Moellenbeck, D.J., Peters, M.L., Bing, J.W., Rouse, J.R., Higgins, L.S., Sims, L., Nevshemal, T., Marshall, L., Ellis, R.T., Bystrak, P.G., Lang, B.A., Stewart, J.L., Kouba, K., Sondag, V., Gustafson, V., Nour, K., Xu, D.P., Swenson, J., Zhang, J., Czapla, T., Schwab, G., Jayne, S., Stockhoff, B.A., Narva, K., Schnepf, H.E., Stelman, S.J., Poutre, C., Koziel, M. & Duck, N. (2001) Insecticidal proteins from Bacillus thuringiensis protect corn from corn rootworms. Nature Biotechnology 19, 668–672.CrossRefGoogle ScholarPubMed
Morin, S., Biggs, R.W., Sisterson, M.S., Shriver, L., Ellers-Kirk, C., Higginson, D., Holley, D., Gahan, L.J., Heckel, D.G., Carriere, Y., Dennehy, T.J., Brown, J.K. & Tabashnik, B.E. (2003) Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proceedings of the National Academy of Sciences of the United States of America 100, 5004–5009.CrossRefGoogle ScholarPubMed
Morin, S., Henderson, S., Fabrick, J.A., Carrière, Y., Dennehy, T.J., Brown, J.K. & Tabashnik, B.E. (2004) DNA-based detection of Bt resistance alleles in pink bollworm. Insect Biochemistry and Molecular Biology 34, 1225–1233.CrossRefGoogle ScholarPubMed
Naranjo, S.E., Head, G. & Dively, G.P. (2005) Field studies assessing arthropod nontarget effects in Bt transgenic crops: introduction. Environmental Entomology 34, 1178–1180.Google Scholar
Pereira, E.J.G., Lang, B.A., Storer, N.P. & Siegfried, B.D. (2008) Selection for Cry1F resistance in the European corn borer and cross resistance to other Cry toxins. Entomologia Experimentalis et Applicata 126, 115–121.CrossRefGoogle Scholar
Preisler, H.K., Hoy, M.A. & Robertson, J.L. (1990) Statistical analysis of modes of inheritance for pesticide resistance. Journal of Economic Entomology 83, 1649–1655.CrossRefGoogle Scholar
Ritchie, S.W., Hanway, J.J. & Benson, G.O. (1992) How a Corn Plant Develops, Special Report. 48 pp. Ames, IA, Iowa State University.Google Scholar
Roush, R.T. (1997) Bt-transgenic crops: just another pretty insecticide or a chance for a new start in resistance management? Pesticide Science 51, 328–334.3.0.CO;2-B>CrossRefGoogle Scholar
Roush, R.T. (1998) Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 353, 1777–1786.CrossRefGoogle Scholar
Russell, R.M., Robertson, J.L. & Savin, N.E. (1977) POLO: a new computer program for probit analysis. Bulletin of the Entomological Society of America 23, 209–213.CrossRefGoogle Scholar
SAS Institute. (2002) SAS User's Manual. version 9.1 Cary, NC, SAS Institute.Google Scholar
Shelton, A.M., Tang, J.D., Roush, R.T., Metz, T.D. & Earle, E.D. (2000) Field tests on managing resistance to Bt-engineered plants. Nature Biotechnology 18, 339–342.CrossRefGoogle ScholarPubMed
Shelton, A.M., Zhao, J.Z. & Roush, R.T. (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annual Review of Entomology 47, 845–881.CrossRefGoogle ScholarPubMed
Siegfried, B.D., Zoerb, A.C. & Spencer, T. (2001) Development of European corn borer larvae on Event 176 Bt corn: influence on survival and fitness. Entomologia Experimentalis et Applicata 100, 15–20.CrossRefGoogle Scholar
Siqueira, H.A.A., Moellenbeck, D., Spencer, T. & Siegfried, B.D. (2004) Cross-resistance of Cry1Ab-selected Ostrinia nubilalis (Lepidoptera: Crambidae) to Bacillus thuringiensis delta-endotoxins. Journal of Economic Entomology 97, 1049–1057.CrossRefGoogle ScholarPubMed
Tabashnik, B.E. (1991) Determining the mode of inheritance of pesticide resistance with backcross experiments. Journal of Economic Entomology 84, 703–712.CrossRefGoogle ScholarPubMed
Tabashnik, B.E., Schwartz, J.M., Finson, N. & Johnson, M.W. (1992) Inheritance of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology 85, 1046–1055.CrossRefGoogle Scholar
Tabashnik, B.E., Liu, Y.B., Finson, N., Masson, L. & Heckel, D.G. (1997) One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proceedings of the National Academy of Sciences of the United States of America 94, 1640–1644.CrossRefGoogle ScholarPubMed
Tabashnik, B.E., Liu, Y.B., Malvar, T., Heckel, D.G., Masson, L. & Ferre, J. (1998) Insect resistance to Bacillus thuringiensis: uniform or diverse? Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 353, 1751–1756.CrossRefGoogle Scholar
Tang, J.D., Collins, H.L., Metz, T.D., Earle, E.D., Zhao, J.Z., Roush, R.T. & Shelton, A.M. (2001) Greenhouse tests on resistance management of Bt transgenic plants using refuge strategies. Journal of Economic Entomology 94, 240–247.CrossRefGoogle ScholarPubMed
Van Rie, J., Mcgaughey, W.H., Johnson, D.E., Barnett, B.D. & Vanmellaert, H. (1990) Mechanism of Insect resistance to the microbial insecticide Bacillus thuringiensis. Science 247, 72–74.CrossRefGoogle Scholar
Zhao, J.Z., Collins, H.L., Tang, J.D., Cao, J., Earle, E.D., Roush, R.T., Herrero, S., Escriche, B., Ferre, J. & Shelton, A.M. (2000) Development and characterization of diamondback moth resistance to transgenic broccoli expressing high levels of Cry1C. Applied and Environmental Microbiology 66, 3784–3789.CrossRefGoogle ScholarPubMed
Zhao, J.Z., Cao, J., Li, Y.X., Collins, H.L., Roush, R.T., Earle, E.D. & Shelton, A.M. (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nature Biotechnology 21, 1493–1497.CrossRefGoogle ScholarPubMed