Insect resistance management in GM crops: past present and future
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.
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Tissue-specific and inducible promoters may help limit exposure to natural enemies and can be used for resistance management.
“Other examples of nonconstitutive promoters include tissue-specific and inducible promoters that may help not only limit exposure to natural enemies but can be used for resistance management (Bates et al., 2005).”
From Genetically engineered crops help support conservation biological control (2019) · cites this paper as Bates et al., 2005
Cites
US Environmental Protection Agency
Liu, X. (1998) · Choice Reviews Online · doi:10.5860/choice.35-4455 · Cited by 5,887 · see citing works
Bacillus thuringiensis and Its Pesticidal Crystal Proteins
Schnepf, E., Crickmore, N., Rie, J. V., Lereclus, D., Baum, J. A., Feitelson, J. S., Zeigler, D. R., & Dean, D. H. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.3.775-806.1998 · Cited by 3,062 · see citing works
Sustainability of Transgenic Insecticidal Cultivars: Integrating Pest Genetics and Ecology
Gould, F. (1998) · Annual Review of Entomology · doi:10.1146/annurev.ento.43.1.701 · Cited by 1,392 · see citing works
Evolution of Resistance to Bacillus thuringiensis
Tabashnik, B. E. (1994) · Annual Review of Entomology · doi:10.1146/annurev.ento.39.1.47 · Cited by 981 · see citing works
Evolution of Resistance to Bacillus Thuringiensis
Tabashnik, B. E. (1994) · Annual Review of Entomology · doi:10.1146/annurev.en.39.010194.000403 · Cited by 906 · see citing works
Economic, Ecological, Food Safety, and Social Consequences of the Deployment of Bt Transgenic Plants
Shelton, A. M., Zhao, J.-Z., & Roush, R. T. (2002) · Annual Review of Entomology · doi:10.1146/annurev.ento.47.091201.145309 · Cited by 794 · see citing works
Self-citationTabashnik, B. E., Cushing, N. L., Finson, N., et al. (1990) · Journal of Economic Entomology · doi:10.1093/jee/83.5.1671 · Cited by 787 · see citing works
Identification of a Gene Associated with Bt Resistance in Heliothis virescens
Gahan, L. J., Gould, F. L., & Heckel, D. G. (2001) · Science · doi:10.1126/science.1060949 · Cited by 622 · see citing works
Insect Resistance to Transgenic Bt Crops: Lessons from the Laboratory and Field
Tabashnik, B. E., Carrière, Y., Dennehy, T. J., Morin, S., Sisterson, M. S., Roush, R. T., Shelton, A. M., & Zhao, Y. (2003) · Journal of Economic Entomology · doi:10.1093/jee/96.4.1031 · Cited by 525 · see citing works
Self-citationRoush, R. T. (1998) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1998.0330 · Cited by 445 · see citing works
Self-citationTransgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution
Zhao, Y., Cao, J. W., Li, Y., Collins, H. L., Roush, R. T., Earle, E. D., & Shelton, A. M. (2003) · Nature Biotechnology · doi:10.1038/nbt907 · Cited by 435 · see citing works
Self-citationThree cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm
Morin, S., Biggs, R. W., Sisterson, M. S., Shriver, L. C., Ellers‐Kirk, C., Higginson, D. M., Holley, D., Gahan, L. J., Heckel, D. G., Carrière, Y., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0831036100 · Cited by 435 · see citing works
Managing the Evolution of Insect Resistance to Transgenic Plants
Alstad, D. N., & Andow, D. A. (1995) · Science · doi:10.1126/science.268.5219.1894 · Cited by 395 · see citing works
Cloning and Expression of a Receptor for an Insecticidal Toxin of Bacillus thuringiensis
Vadlamudi, R. K., Weber, E., Ji, I., et al. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.10.5490 · Cited by 345 · see citing works
Long-term regional suppression of pink bollworm by <i>Bacillus thuringiensis</i> cotton
Carrière, Y., Ellers-Kirk, C., Sisterson, M., Antilla, L., Whitlow, M., Dennehy, T. J., & Tabashnik, B. E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0436708100 · Cited by 320 · see citing works
Lee, M. K., Walters, F. S., Hart, H., Palekar, N., & Chen, J.-S. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.8.4648-4657.2003 · Cited by 315 · see citing works
F2 Screen for Rare Resistance Alleles
Andow, D. A., & Alstad, D. N. (1998) · Journal of Economic Entomology · doi:10.1093/jee/91.3.572 · Cited by 308 · see citing works
Designing resistance management programs: How can you choose?
Roush, R. T. (1989) · Pesticide Science · doi:10.1002/ps.2780260409 · Cited by 294 · see citing works
Self-citationJanmaat, A. F., & Myers, J. H. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2497 · Cited by 291 · see citing works
Mallet, J., & Porter, P. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0145 · Cited by 284 · see citing works
Field tests on managing resistance to Bt-engineered plants
Shelton, A. M., Tang, J. D., Roush, R. T., et al. (2000) · Nature Biotechnology · doi:10.1038/73804 · Cited by 254 · see citing works
Self-citationResistance to insecticides in Heliothine Lepidoptera: a global view
McCaffery, A. R. (1998) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1998.0326 · Cited by 243 · see citing works
Akhurst, R. J., James, W., Bird, L. J., & Beard, C. E. (2003) · Journal of Economic Entomology · doi:10.1603/0022-0493-96.4.1290 · Cited by 223 · see citing works
Managing Insect Resistance to Plants ProducingBacillus thuringiensisToxins
Frutos, R., Rang, C., & Royer, M. (1999) · Critical Reviews in Biotechnology · doi:10.1080/0738-859991229251 · Cited by 185 · see citing works
Caprio, M. A. (2001) · Journal of Economic Entomology · doi:10.1603/0022-0493-94.3.698 · Cited by 166 · see citing works
Delaying insect adaptation to transgenic plants: seed mixtures and refugia reconsidered
Tabashnik, B. E. (1994) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1994.0002 · Cited by 164 · see citing works
Tang, J. D., Gilboa, S., Roush, R. T., et al. (1997) · Journal of Economic Entomology · doi:10.1093/jee/90.3.732 · Cited by 151 · see citing works
Self-citationContamination of refuges by Bacillus thuringiensis toxin genes from transgenic maize
Chilcutt, C. F., & Tabashnik, B. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400546101 · Cited by 143 · see citing works
Potential and problems with high‐dose strategies for pesticidal engineered crops
Gould, F. L. (1994) · Biocontrol Science and Technology · doi:10.1080/09583159409355357 · Cited by 142 · see citing works
Gould, F. L., Blair, N. E., Reid, M., Rennie, T. L., López, J. D., & Micinski, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242382499 · Cited by 137 · see citing works
Groeters, F. R., Tabashnik, B. E., Finson, N., et al. (1994) · Evolution · doi:10.1111/j.1558-5646.1994.tb01306.x · Cited by 137 · see citing works
Carrière, Y., Ellers‐Kirk, C., Patin, A. L., et al. (2001) · Journal of Economic Entomology · doi:10.1603/0022-0493-94.4.935 · Cited by 136 · see citing works
Nagamatsu, Y., Koike, T., Sasaki, K., et al. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01327-7 · Cited by 130 · see citing works
Fitt, G. P. (2000) · Crop Protection · doi:10.1016/s0261-2194(00)00106-x · Cited by 129 · see citing works
Liu, Y., Tabashnik, B. E., Dennehy, T. J., Patin, A. L., Sims, M. A., Meyer, S. K., & Carrière, Y. (2001) · Journal of Economic Entomology · doi:10.1603/0022-0493-94.5.1237 · Cited by 121 · see citing works
Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana
Liu, D., Burton, S., Glancy, T. P., et al. (2003) · Nature Biotechnology · doi:10.1038/nbt866 · Cited by 114 · see citing works
Greenhouse Tests on Resistance Management of Bt Transgenic Plants Using Refuge Strategies
Tang, J. D., Collins, H. L., Metz, T. D., Earle, E. D., Zhao, Y., Roush, R., & Shelton, A. M. (2001) · Journal of Economic Entomology · doi:10.1603/0022-0493-94.1.240 · Cited by 113 · see citing works
Self-citationBurd, A. D., Gould, F. L., Bradley, J. R., Duyn, J. W. V., & Moar, W. J. (2003) · Journal of Economic Entomology · doi:10.1093/jee/96.1.137 · Cited by 111 · see citing works
Evolution of resistance to Bt crops: directional selection in structured environments
Ives, A. R., & Andow, D. A. (2002) · Ecology Letters · doi:10.1046/j.1461-0248.2002.00392.x · Cited by 109 · see citing works
Carrière, Y., Ellers‐Kirk, C., Liu, Y. B., et al. (2001) · Journal of Economic Entomology · doi:10.1603/0022-0493-94.6.1571 · Cited by 108 · see citing works
Alyokhin, A., & Ferro, D. N. (1999) · Journal of Economic Entomology · doi:10.1093/jee/92.3.510 · Cited by 107 · see citing works
Sustainability of insect resistance management strategies for transgenic Bt corn
Glaser, J. A., & Matten, S. R. (2003) · Biotechnology Advances · doi:10.1016/j.biotechadv.2003.08.016 · Cited by 103 · see citing works
Managing Resistance to Transgenic Crops
Roush, R. (2010) · Taylor & Francis eBooks · doi:10.4324/9780203211731_chapter_15 · Cited by 95 · see citing works
Self-citationSayyed, A. H., & Wright, D. J. (2001) · Ecological Entomology · doi:10.1046/j.1365-2311.2001.00358.x · Cited by 93 · see citing works
Ramachandran, S., Buntin, G. D., All, J. N., et al. (1998) · Journal of Economic Entomology · doi:10.1093/jee/91.6.1239 · Cited by 85 · see citing works
MONITORING AND ADAPTIVE RESISTANCE MANAGEMENT
Andow, D. A., & Ives, A. R. (2002) · Ecological Applications · doi:10.1890/1051-0761(2002)012[1378:maarm]2.0.co;2 · Cited by 84 · see citing works
Vegetative Insecticidal Proteins
Warren, G. W. (2010) · Taylor & Francis eBooks · doi:10.4324/9780203211731_chapter_7 · Cited by 78 · see citing works
Testing Bt refuge strategies in the field
Gould, F. L. (2000) · Nature Biotechnology · doi:10.1038/73693 · Cited by 77 · see citing works
Zhao, Y., Li, Y., Collins, H. L., et al. (2002) · Journal of Economic Entomology · doi:10.1603/0022-0493-95.1.14 · Cited by 64 · see citing works
Burd, A. D., Gould, F. L., Bradley, J. R., et al. (2003) · Journal of Economic Entomology · doi:10.1603/0022-0493-96.1.137 · Cited by 61 · see citing works
Fitness costs of resistance to Bacillus thuringiensis in the Indianmeal moth, Plodia interpunctella
Oppert, B., Hammel, R., Throne, J. E., et al. (2000) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2000.00707.x · Cited by 58 · see citing works
Cao, J. W., Shelton, A. M., & Earle, E. D. (2001) · Molecular Breeding · doi:10.1023/a:1013734923291 · Cited by 47 · see citing works
Self-citationTrisyono, Y. A., & Whalon, M. E. (1997) · Journal of Economic Entomology · doi:10.1093/jee/90.2.267 · Cited by 46 · see citing works
Arpaia, S., Gould, F. L., & Kennedy, G. G. (1997) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.1997.00117.x · Cited by 45 · see citing works
Managing the Risk of European Corn Borer Resistance to Bt Corn
Hurley, T. M., Secchi, S., Babcock, B. A., et al. (2002) · Environmental and Resource Economics · doi:10.1023/a:1019858732103 · Cited by 43 · see citing works
Jackson, R. E., Bradley, J. R., & Duyn, J. W. V. (2004) · Journal of Entomological Science · doi:10.18474/0749-8004-39.1.46 · Cited by 34 · see citing works
Instability of resistance toBacillus thuringiensis
Tabashnik, B. E., Groeters, F. R., Finson, N., et al. (1994) · Biocontrol Science and Technology · doi:10.1080/09583159409355352 · Cited by 32 · see citing works
Resistance to Bt toxin surprisingly absent from pests
Fox, J. L. (2003) · Nature Biotechnology · doi:10.1038/nbt0903-958b · Cited by 32 · see citing works
Sequeira, R. V., & Playford, C. L. (2001) · Australian Journal of Entomology · doi:10.1046/j.1440-6055.2001.00234.x · Cited by 30 · see citing works
Huang, F., Higgins, R. A., & Buschman, L. L. (1999) · Bulletin of Entomological Research · doi:10.1017/s0007485399000589 · Cited by 25 · see citing works
Interactions between Helicoverpa armigera and transgenic Bt cotton in North China.
Zhao, J. Z., Zhao, K., LU, M.-X., et al. (1998) · Cited by 22 · see citing works
Self-citationCarozzi, N. B. (1997) · CRC Press eBooks · doi:10.1201/9780203211731 · Cited by 21 · see citing works
Williamson, V. M., & Kaya, H. K. (2003) · Nature Biotechnology · doi:10.1038/nbt1103-1294 · Cited by 14 · see citing works
Dove, A. (1999) · Nature Biotechnology · doi:10.1038/9830 · Cited by 6 · see citing works
Hemingway, J., Penilla, R. P., Rodriguez, A. D., James, B. M., Edge, W., Rogers, H., & Rodriguez, M. H. (1997) · Pesticide Science · doi:10.1002/(sici)1096-9063(199711)51:3
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- Authors
- Bates, S. L., Zhao, J.-Z., Roush, R. T., & Shelton, A. M.
- Affiliations
- Cornell University (US)
- University of California, Davis (US)
- Corresponding author
- Shelton, Anthony M
- ORCID
- Shelton, Anthony M
- Venue
- Nature Biotechnology
- Published
- 2005-01
- Volume
- 23
- Issue
- 1
- Pages
- 57-62
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- OpenAlex
- W2120395741
- Cited by
- 577
- References
- 65
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 10 · 2023: 17 · 2022: 14 · 2021: 18 · 2020: 21 · 2019: 25 · 2018: 23 · 2017: 25 · 2016: 41 · 2015: 35 · 2014: 33 · 2013: 33 · 2012: 37
- FWCI
- 16.33
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Biotechnology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Keywords
- insect resistance management, Bt crops, Bacillus thuringiensis, transgenic plants, insecticidal proteins, insect resistance, Bt maize, Bt cotton, resistance risk assessment
- MeSH terms
- Animals, Bacillus thuringiensis, Bacterial Toxins, Heterozygote, Insecticide Resistance, Insecta, Models, Biological, Time Factors, Crops, Agricultural, Transgenes, Plants, Genetically Modified
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