A general approach to test for interaction among mixtures of insecticidal proteins which target different orders of insect pests
Open accessAbstract
A shift toward transgenic crops which produce combinations of insecticidal proteins has increased the interest (Syngenta Seeds, Inc., Minnetonka, MN) in studying the potential for interactions amongst those proteins. We present a general testing method which accommodates proteins with nonoverlapping spectrums of activity. Our sequential testing approach first investigates groups of the proteins with overlapping activity; e.g., proteins active against Lepidoptera or Coleoptera, respectively. The Colby method is used to test for interactions within each respective group. Subsequently, the mixture of proteins within each group is regarded as a single entity and tests for interactions between the groups (when combined) is conducted using analysis of variance. We illustrate the method using Cry1Ab, Vip3Aa20, and Cry1F (a mixture of proteins active against Lepidoptera), and mCry3A and eCry3.1Ab (a mixture of proteins active against Coleoptera). These insecticidal proteins are produced by Bt11 × MIR162 × TC1507 × MIR604 × 5307 maize. We detected no interactions between Cry1Ab, Vip3Aa20, and Cry1F in tests using larvae of two different lepidopteran species, and possible slight antagonism between mCry3A and eCry3.1Ab with a coleopteran test species. We detected no effect of (eCry3.1Ab + mCry3A) on the potency of (Cry1Ab + Vip3Aa20 + Cry1F) to lepidopteran larvae, and no effect of (Cry1Ab + Vip3Aa20 + Cry1F) on the potency of (mCry3A + eCry3.1Ab) to coleopteran larvae. We discuss implications of these results for characterization of Bt11 × MIR162 × TC1507 × MIR604 × 5307 maize, and the value of the method for characterizing other transgenic crops that produce several insecticidal proteins.
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Pyramided insecticidal proteins typically act additively in sensitive species and cause no unexpected effects in species not sensitive to individual toxins.
“The available data indicate that these pyramided insecticidal proteins typically act additively in sensitive species and cause no unexpected effects in species that are not sensitive to the individual toxins (Graser et al., 2017;Guo et al., 2016;Haller et al. 2017;Kumar et al., 2014;Levine et al., 2016;Raybould et al., 2012;Shu et al., 2018;Su et al., 2015;Svobodová et al., 2017;Tian et al., 2014T”
From Genetically engineered crops help support conservation biological control (2019) · cites this paper as Graser et al., 2017
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A Method of Computing the Effectiveness of an Insecticide
Abbott, W. S. (1925) · Journal of Economic Entomology · doi:10.1093/jee/18.2.265a · Cited by 16,204 · 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
Bacillus thuringiensis: A story of a successful bioinsecticide
Bravo, A., Likitvivatanavong, S., Gill, S. S., & Soberón, M. (2011) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2011.02.006 · Cited by 1,163 · see citing works
Analysis of drug combinations: current methodological landscape
Foucquier, J., & Guedj, M. (2015) · Pharmacology Research & Perspectives · doi:10.1002/prp2.149 · Cited by 1,115 · see citing works
Koziel, M. G., Beland, G. L., Bowman, C., Carozzi, N. B., Crenshaw, R. W., Crossland, L. D., Dawson, J., Desai, N., Hill, M., Kadwell, S. H., et al. (1993) · Nature Biotechnology · doi:10.1038/nbt0293-194 · Cited by 851 · see citing works
Bacillus thuringiensis Toxins: An Overview of Their Biocidal Activity
Palma, L., Muñoz, D., Berry, C., Murillo, J., & Caballero, P. (2014) · Toxins · doi:10.3390/toxins6123296 · Cited by 834 · see citing works
Estruch, J., Warren, G. W., Mullins, M. A., Nye, G., Craig, J. A., & Koziel, M. G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.11.5389 · Cited by 707 · see citing works
Calculating Synergistic and Antagonistic Responses of Herbicide Combinations
Colby, S. R. (1967) · Weeds · doi:10.2307/4041058 · Cited by 650 · see citing works
Optimizing pyramided transgenic Bt crops for sustainable pest management
Carrière, Y., Crickmore, N., & Tabashnik, B. E. (2015) · Nature Biotechnology · doi:10.1038/nbt.3099 · Cited by 388 · 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
Self-citationYu, C.-G., Mullins, M. A., Warren, G. W., Koziel, M. G., & Estruch, J. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.2.532-536.1997 · Cited by 271 · see citing works
Insecticidal proteins from Bacillus thuringiensis protect corn from corn rootworms
Moellenbeck, D. J., Peters, M. L., Bing, J., Rouse, J. R., Higgins, L. S., Sims, L., Nevshemal, T., Marshall, L., Ellis, R. T., Bystrak, P. G., et al. (2001) · Nature Biotechnology · doi:10.1038/90282 · Cited by 202 · see citing works
Wirth, M. C., Georghiou, G. P., & Federici, B. A. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10536 · Cited by 192 · see citing works
Trait stacking in transgenic crops: Challenges and opportunities
Que, Q., Chilton, M.-D. M., de Fontes, C. M., He, C., Nuccio, M., Zhu, T., Wu, Y., Chen, J. S., & Shi, L. (2010) · GM Crops · doi:10.4161/gmcr.1.4.13439 · Cited by 191 · see citing works
Hernández‐Rodríguez, C. S., Hernández‐Martínez, P., Rie, J. V., Escriche, B., & Ferré, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068164 · Cited by 142 · see citing works
Synergistic interactions of fungicides with different modes of action
Gisi, U., Binder, H., & Rimbach, E. (1985) · Transactions of the British Mycological Society · doi:10.1016/s0007-1536(85)80192-3 · Cited by 120 · see citing works
Walters, F. S., Stacy, C. M., Lee, M. K., Palekar, N., & Chen, J. S. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02165-07 · Cited by 107 · see citing works
Self-citationSiegfried, B. D., Spencer, T. A., Crespo, A. L. B., Storer, N. P., Head, G., Owens, E. D., & Guyer, D. (2007) · American Entomologist · doi:10.1093/ae/53.4.208 · Cited by 106 · see citing works
Some Comments on the Assessment of Joint Action in Herbicide Mixtures
Morse, P. M. (1978) · Weed Science · doi:10.1017/s0043174500032690 · Cited by 106 · see citing works
Role of Proteolysis in Determining Potency of Bacillus thuringiensis Cry1Ac δ-Endotoxin
Lightwood, D. J., Ellar, D. J., & Jarrett, P. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.12.5174-5181.2000 · Cited by 100 · see citing works
Walters, F. S., deFontes, C. M., Hart, H., Warren, G. W., & Chen, J. S. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00155-10 · Cited by 94 · see citing works
Self-citationThe main features of Bacillus thuringiensis ?-endotoxin molecular structure
Chestukhina, G. G., Kostina, L. I., Mikhailova, A. L., et al. (1982) · Archives of Microbiology · doi:10.1007/bf00508723 · Cited by 76 · see citing works
Siebert, M. W., Babock, J. M., Nolting, S. P., dos Santos, A. C., Adamczyk, J. J., Neese, P. A., King, J. E., Jenkins, J. N., McCarty, J. C., Lorenz, G. M., et al. (2008) · Florida Entomologist · doi:10.1653/0015-4040-91.4.555 · Cited by 72 · see citing works
Niu, Y., Yang, F., Dangal, V., & Huang, F. (2014) · Crop Protection · doi:10.1016/j.cropro.2014.01.005 · Cited by 61 · see citing works
Hibbard, B. E., Frank, D. L., Kurtz, R. W., Boudreau, E., Ellersieck, M. R., & Odhiambo, J. F. (2011) · Journal of Economic Entomology · doi:10.1603/ec11186 · Cited by 58 · see citing works
Herman, R. A., Scherer, P. N., Young, D. L., et al. (2002) · Journal of Economic Entomology · doi:10.1603/0022-0493-95.3.635 · Cited by 57 · see citing works
Bt resistance: characterization and strategies for GM crops producing Bacillus thuringiensis toxins
(2015) · CABI eBooks · doi:10.1079/9781780644370.0000 · Cited by 55 · see citing works
Siegfried, B. D., Rangasamy, M., Wang, H., Spencer, T. A., Haridas, C. V., Tenhumberg, B., Sumerford, D. V., & Storer, N. P. (2013) · Pest Management Science · doi:10.1002/ps.3662 · Cited by 49 · see citing works
An ecological risk assessment of Cry1F maize pollen impact to pale grass blue butterfly
Wolt, J. D., Conlan, C. A., & Majima, K. (2005) · Environmental Biosafety Research · doi:10.1051/ebr:2006005 · Cited by 48 · see citing works
Compositional Equivalency of Cry1F Corn Event TC6275 and Conventional Corn (Zea mays L.)
Herman, R. A., Phillips, A. M., Collins, R. A., Tagliani, L. A., Claussen, F. A., Graham, C. D., Bickers, B. L., Harris, T. A., & Prochaska, L. M. (2004) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf049969n · Cited by 43 · see citing works
Molecular Approaches to Improve the Insecticidal Activity of Bacillus thuringiensis Cry Toxins
Lucena, W. A., Pelegrini, P. B., Martins-de-Sa, D., et al. (2014) · Toxins · doi:10.3390/toxins6082393 · Cited by 34 · see citing works
Raybould, A. F., Graser, G., Hill, K., & Ward, K. (2010) · Journal of Applied Entomology · doi:10.1111/j.1439-0418.2010.01601.x · Cited by 27 · see citing works
Self-citationTimmermann, S. E., Zangerl, A. R., & Berenbaum, M. R. (1999) · Archives of Insect Biochemistry and Physiology · doi:10.1002/(sici)1520-6327(199909)42:1 · Cited by 23 · see citing works
Frank, D. L., Kurtz, R. W., Tinsley, N. A., et al. (2015) · Journal of Economic Entomology · doi:10.1093/jee/tov081 · Cited by 14 · see citing works
Huang, F. (2015) · CABI eBooks · doi:10.1079/9781780644370.0173 · Cited by 9 · see citing works
Graser, G., & Walters, F. S. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-3289-4_18 · Cited by 6 · see citing works
Self-citation
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Research works printed but not linked: 1
- Nespeca M. 1997. Interactive Effects of Imazapyr plus Triclopyr ester and Imazapyr plus Glyphosate Mixtures on Woody Weed Seedlings. M.S. thesis, Virginia Tech. University
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Genetically engineered crops help support conservation biological control
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M. (2019) · Biological Control · doi:10.1016/j.biocontrol.2018.10.001 · Cited by 231 · see citing works
- Authors
- Graser, G., Walters, F. S., Burns, A., Sauve, A., & Raybould, A.
- Affiliations
- Syngenta (United States) (US)
- Syngenta Crop Protection, Product Safety, LLC, Durham, NC, USA
- Syngenta (Switzerland) (CH)
- Corresponding author
- Graser, Gerson
- Venue
- Journal of Insect Science
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-03-01
- Volume
- 17
- Issue
- 2
- ISSN
- 1536-2442 (ISSN-L)
- PMC
- PMC5416900
- OpenAlex
- W2591711989
- Cited by
- 16
- References
- 36
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 3 · 2017: 1
- FWCI
- 0.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Journal of Insect Science (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (publishedVersion, other-oa)
- 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 › Plant Science › Insect Pest Control Strategies
- Keywords
- insecticidal proteins, protein-protein interaction, Bt maize, Cry1Ab, Cry1F, Lepidoptera, Coleoptera, antagonism, synergistic effect, genetically modified crops, insect resistance
- MeSH terms
- Animals, Bacillus thuringiensis, Bacterial Proteins, Coleoptera, Biological Assay, Zea mays, Insecticide Resistance, Insecticides, Larva, Lepidoptera, Pest Control, Biological, Plants, Genetically Modified, Biological Control Agents
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