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Inheritance of Cry1F resistance, cross-resistance and frequency of resistant alleles in Spodoptera frugiperda (Lepidoptera: Noctuidae)

  • A.M. Vélez (a1), T.A. Spencer (a1), A.P. Alves (a2), D. Moellenbeck (a3), R.L. Meagher (a4), H. Chirakkal (a5) and B.D. Siegfried (a1)...

Transgenic maize, Zea maize L., expressing the Cry1F protein from Bacillus thuringiensis has been registered for Spodoptera frugiperda (J. E. Smith) control since 2003. Unexpected damage to Cry1F maize was reported in 2006 in Puerto Rico and Cry1F resistance in S. frugiperda was documented. The inheritance of Cry1F resistance was characterized in a S. frugiperda resistant strain originating from Puerto Rico, which displayed >289-fold resistance to purified Cry1F. Concentration–response bioassays of reciprocal crosses of resistant and susceptible parental populations indicated that resistance is recessive and autosomal. Bioassays of the backcross of the F1 generation crossed with the resistant parental strain suggest that a single locus is responsible for resistance. In addition, cross-resistance to Cry1Aa, Cry1Ab, Cry1Ac, Cry1Ba, Cry2Aa and Vip3Aa was assessed in the Cry1F-resistant strain. There was no significant cross-resistance to Cry1Aa, Cry1Ba and Cry2Aa, although only limited effects were observed in the susceptible strain. Vip3Aa was highly effective against susceptible and resistant insects indicating no cross-resistance with Cry1F. In contrast, low levels of cross-resistance were observed for both Cry1Ab and Cry1Ac. Because the resistance is recessive and conferred by a single locus, an F1 screening assay was used to measure the frequency of Cry1F-resistant alleles from populations of Florida and Texas in 2010 and 2011. A total frequency of resistant alleles of 0.13 and 0.02 was found for Florida and Texas populations, respectively, indicating resistant alleles could be found in US populations, although there have been no reports of reduced efficacy of Cry1F-expressing plants.

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Adamczyk, J.J. & Mahaffey, J.S. (2008) Efficacy of Vip3A and Cry1Ab transgenic traits in cotton against various Lepidopteran pests. Florida Entomologist 91, 570574.
Andow, D.A. & Alstad, D.N. (1999) F2 screen for rare resistance alleles. Journal of Economic Entomology 91, 572578.
Bourguet, D., Genissel, A. & Raymond, M. (2000) Insecticide resistance and dominance levels. Journal of Economic Entomology 93, 15881595.
Buntin, G.D. (1986) A review of plant response to fall armyworm, Spodoptera frugiperda (J. E. Smith), injury in selected field and forage crops. Florida Entomologist 69, 549559.
Buntin, G.D. (2008) Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera: Noctuidae) management in field corn for grain production. Florida Entomologist 91, 523530.
Buntin, G.D., Lee, R.D., Wilson, D.M. & McPherson, M. (2000) Evaluation of Yieldgard transgenic resistance for control of fall armyworm and corn earworm (Lepidoptera: Noctuidae) on corn. Florida Entomologist 84, 3742.
Crespo, A.L.B., Spencer, T.A., Nekl, E. & Siegfried, B.D. (2008) Comparison and validation of methods to quantify Cry1Ab from Bacillus thuringiensis or standardization of insect bioassays. Applied Environmental Microbiology 73, 130135.
Crespo, A.L.B., Spencer, T.A., Tan, S.Y. & Siegfried, B.D. (2010) Fitness costs of Cry1Ab resistance in a field-derived strain of Ostrinia nubilalis (Lepidoptera: Crambidae). Journal of Economic Entomology 103, 13861393.
Dhurua, S. & Gujar, G.T. (2011) Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Management Science 67, 898903.
Falconer, D.S. & Mackay, T.F.C. (1996) Introduction to Quantitative Genetics. 4th edn. London, England, Pearson-Prentice Hall.
Ferré, J. & Van Rie, J. (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology 47, 501533.
Finney, D.J. (1971) Probit Analysis. 3rd edn. Cambridge, Cambridge University Press.
Gassmann, A.J., Petzold-Maxwell, J.L., Keweshan, R.S. & Dunbar, M.W. (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS One 6, e22629.
Georghiou, G.P. (1969) Parasitological review: genetics of resistance to insecticide in houseflies and mosquitoes. Experimental Parasitology 26, 224255.
Gould, F. (1988) Evolutionary biology and genetically engineered crops. Bioscience 38, 2633.
Gould, F. (1994) Potential and problems with high-dose strategies for pesticidal engineered crops. Biocontrol Science and Technology 4, 451461.
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701726.
Gould, F., Anderson, A., Jones, A., Summerford, D., Heckel, D.G., Lopez, J., Micinski, S., Leonard, R. & Laster, M. (1997) Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proceedings of the National Academy of Science 94, 35193523.
Hardke, J.T., Leonard, B.R., Huang, F. & Jackson, R.E. (2011) Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection 30, 168172.
Hernández-Martínez, P., Ferré, J. & Escriche, B. (2009) Broad spectrum cross-resistance in Spodoptera exigua from selection with a marginally toxic Cry protein. Pest Management Science 65, 645650.
Huang, F., Andow, D.A. & Buschman, L.L. (2011) Success of the high-dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomology Experimentalis et Applicata 140, 116.
James, C. (2009) Global Status of Commercialized Biotech/GM Crops: 2008. ISAAA Brief No. 39. Ithaca, NY, International Service for the Acquisition of Ag-biotech Applications.
Lee, M.K., Milne, R.E. & Dean, D.H. (1992) Location of Bombyx mori receptor binding region on a Bacillus thuringiensis delta-endotoxin. Journal of Biological Chemistry 267, 31153121.
LeOra Software (1987) POLO-PC: A user's Guide to Probit and Logit Analysis. Berkeley, CA, LeOra Software Company.
Levy, C.H., García-Maruniak, A. & Maruniak, J. (2002) Strain identification of Spodoptera frugiperda (Lepidoptera: Noctuidae) insects and cell line: PCR-RFLP of cytochrome oxidase c subunit I gene. Florida Entomology 85, 186190.
Lewis, L.C. & Lynch, R.E. (1969) Rearing the European corn borer on corn leaf and wheat germ diets. Iowa State Journal of Science 44, 914.
Luo, K., Banks, D. & Adang, M.J. (1999) Toxicity, binding, and permeability analyses of four Bacillus thuringiensis Cry1 δ-endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Applied Environmental Microbiology 65, 457464.
Mahon, R.J., Downes, S., James, W. & Parker, T. (2010) Why do F1 screens estimate higher frequencies of Cry2Ab resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) than do F2 screens? Journal of Economic Entomology 103, 472481.
Marçon, P.C.R.G., Young, L.J., Steffey, K.L. & Siefgried, B.D. (1999) Baseline susceptibility of European corn borer (Lepidoptera: Crambidae) to Bacillus thuringiensis toxins. Journal of Economic Entomology 92, 279285.
Marçon, P.C.R.G., Siegfried, B.D., Spencer, T. & Hutchison, W.D. (2000) Development of diagnostic concentrations for monitoring Bacillus thuringiensis resistance in European corn borer (Lepidoptera: Crambidae). Journal of Economic Entomology 93, 925930.
Matten, S.R., Head, G.P. & Quemada, H.D. (2008) How governmental regulation can help or hinder the integration of Bt crops into IPM programs. pp. 2739 in Romeis, J., Shelton, A.M. & Kennedy, G.G.S. (Eds) Integration of Insect-Resistant Genetically Modified Crops within IPM Programs. New York, Springer.
Mitchell, E.R., McNeil, J.N., Westbrook, J.K., Silvain, J.F., Lalanne-Cassou, B., Chalfant, R.B., Pair, S.D., Waddill, V.H., Sotomayor-Rios, A. & Proshold, F.I. (1991) Seasonal periodicity of fall armyworm (Lepidoptera: Noctuidae) in the Caribbean Basin and northward to Canada. Journal of Entomological Science 26, 3950.
Monnerat, R., Martins, E., Queiroz, P., Ordúz, S., Jaramillo, G., Benintende, G., Cozzi, J., Real, M.D., Martinez-Ramirez, A., Rausell, A., Cerón, J., Ibarra, J.E., del Rincón-Castro, M.C., Espinoza, A.M., Meza-Basso, L., Cabrera, L., Sánchez, J., Soberón, M. & Bravo, A. (2006) Genetic variability of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) populations from Latin America is associated with variations in susceptibility to Bacillus thuringiensis cry toxins. Applied and Environmental Microbiology 72, 70297035.
Nagoshi, R.D. & Meagher, R.L. (2004) Behavior and distribution of the two fall armyworm host strains in Florida. Florida Entomology 87, 440448.
Nagoshi, R.D., Silvie, P., Meagher, R.L., López, L. & Machado, V. (2007 a) Identification and comparison of fall armyworm (Lepidoptera: Noctuidae) host strains in Brazil, Texas, and Florida. Annals of the Entomological Society of America 100, 394402.
Nagoshi, R.N., Silvie, P. & Meagher, R.L. (2007 b) Comparison of haplotype frequencies differentiates fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Florida and Brazil. Journal of Economic Entomology 100, 954961.
Nagoshi, R.N., Meagher, R.L. & Jenkins, D.A. (2010) Puerto Rico Fall Armyworm has only limited interactions with those from Brazil or Texas but could have substantial exchanges with Florida populations. Journal of Economic Entomology 103, 360367.
Nagoshi, R.N., Meagher, R.L. & Hay-Roe, M. (2012) Inferring the annual migration patterns of fall armyworm (Lepidoptera: Noctuidae) in the United States from mitochondrial haplotypes. Ecology and Evolution 2, 14581467.
Pashley, D.P. (1986) Host-associated genetic differentiation in fall armyworm (Lepidoptera: Noctuidae) a sibling species complex? Annals of the Entomological Society of America 79, 898904.
Pashley, D.P. (1988) Current status of fall armyworm host strains. Florida Entomologist 71, 227234.
Pereira, E.J.G., Lang, B.A., Storer, N.P. & Siegfried, B.D. (2007) Selection for Cry1F resistance in the European corn borer and cross-resistance to other Cry toxins. Entomology Experimentalis et Applicata 126, 115121.
Pereira, E.J.G., Storer, N.P. & Siegfried, B.D. (2008) Inheritance of Cry1F resistance in laboratory-selected European corn borer and its survival on transgenic corn expressing the Cry1F toxin. Bulletin of Entomological Research 98, 621629.
Pereira, E.J.G., Storer, N.P. & Siegfried, B.D. (2009) Fitness costs of Cry1F resistance in laboratory-selected European corn borer (Lepidoptera: Crambidae). Journal of Applied Entomology 132, 18.
Perkins, W.D. (1979) Laboratory rearing of the fall armyworm. Florida Entomologist 62, 8790.
Preisler, H.K., Hoy, M.A. & Robertson, J.L. (1990) Statistical analysis of modes of inheritance for pesticide resistance. Journal of Economic Entomology 83, 16491655.
Quisenberry, S.S., & Whitford, F. (1988) Evaluation of bermudagrass resistance to fall armyworm (Lepidoptera: Noctuidae): influence of host strain and dietary conditioning. Journal of Economic Entomology 81, 14631468.
Robertson, J.L., Preisler, H.K., Ng, S.S., Hickle, L.A. & Gelernter, W.D. (1995) Natural variation – a complication factor in bioassays with chemical and microbial pesticides. Journal of Economic Entomology 88, 110.
Robertson, J.L., Russel, R.M., Preisler, H.K. & Savin, N.E. (2007) Bioassays with Arthropods. 2nd edn. Boca Raton, Florida, CRC Press.
Roush, R.T. (1994) Managing pests and their resistance to Bacillus thuringiensis: can transgenic crops do better than sprays? Biocontrol Science and Technology 4, 501516.
Roush, R.T. & Daly, J.C. (1990) The role of population genetics in resistance research and management. pp. 97152 in Roush, R.T. & Tabashnik, B.E. (Eds) Pesticide Resistance in Arthropods. New York, Chapman & Hall.
SAS Institute (2011) SAS User's Manual, Version 9.3. Cary, NC, SAS Institute.
Sena, J.D.A., Hernandez-Rodriguez, C.S. & Ferré, J. (2009) Interaction of Bacillus thuringiensis Cry1 and Vip3A proteins with Spodoptera frugiperda midgut binding sites. Applied Environmental Microbiology 75, 22362237.
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, 845881.
Siebert, M., Babock, J.M., Nolting, S., Santos, A.C., Adamczyk, J.J., Neese, P.A., King, J.E., Jenkins, J.N., McCarty, J., Lorenz, G.M., Fromme, D.D. & Lassiter, R.B. (2008 a) Efficacy of Cry1F insecticidal protein in maize and cotton for control of fall armyworm (Lepidoptera: Noctuidae). Florida Entomology 91, 555565.
Siebert, M.W., Tindall, K.V., Leonard, B.R., Van Duyn, J.W. & Babcock, J.M. (2008 b) Evaluation of corn hybrids expressing Cry1F (Herculex® I Insect Protection) against fall armyworm (Lepidoptera: Noctuidae) in Southern United States. Journal of Entomological Science 43, 4151.
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. Entomology Experimentalis et Applicata 100, 1520.
Siegfried, B.D., Spencer, T., Crespo, A.L., Storer, N.P., Head, G.P., Owens, E.D. & Guyer, D. (2007) Ten years of Bt resistance monitoring in the European corn borer. American Entomologist 53, 208214.
Sparks, A.N. (1979) A review of the biology of the fall armyworm. Florida Entomologist 62, 8287.
Stewart, S.D., Adamczyk, J.J. Jr., Knighten, K.S. & Davis, F.M. (2001) Impact of Bt cottons expressing one or two insecticidal proteins of Bacillus thuringiensis Berliner on growth and survival of noctuid (Lepidoptera) larvae. Journal of Economic Entomology 94, 752760.
Storer, N.P., Babcock, J.M., Schlenz, M., Meade, T., Thompson, G.D., Bing, J.W. & Huckaba, R.M. (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology 103, 10311038.
Storer, N.P., Kubiszak, M.E., King, E., Thompson, G.D. & Santos, A.C. (2012) Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico. Journal of Invertebrate Pathology 110, 294300.
Tabashnik, B.E. (1991) Determining the mode of inheritance of pesticide resistance with backcross experiments. Journal of Economic Entomology 84, 703712.
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, 10461055.
Tabashnik, B.E., Liu, Y.B., Dennehy, T.J., Sims, M.A., Sisterson, M.S., Biggs, R.W. & Carrière, Y. (2002) Inheritance of resistance to Bt toxin Cry1AC in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology 95, 10181026.
Tabashnik, B.E., Carrière, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., Shelton, A.M. & Zhao, J.Z. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology 96, 10311038.
Tabashnik, B.E., Van Rensburg, J.B.J. & Carrière, Y. (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology 102, 2112025.
Tan, S.Y., Cayabyab, B.F., Alcantara, E.P., Ibrahim, Y.B., Huang, F., Blankenship, E.E. & Siegfried, B.D. (2011) Comparative susceptibility of Ostrinia nubilalis and Diatraea saccharalis (Lepidoptera: Crambidae) to Bacillus thuringiensis Cry1 toxins. Crop Protection 30, 11841189.
United States Environmental Protection Agency (2001) Insect Resistance Management, in Biopesticides Registration Action Document-Bacillus thuringiensis Plant-Incorporated Protectants.
Van Rensburg, J.B.J. (2007) First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. South African Journal of Plant and Soil 24, 147151.
Van Rie, J. (1991) Insect control with transgenic plants: resistance proof? Trends in Biotechnology 9, 177179.
Waquil, J.M., Ferreira Villela, F.M. & Foster, J.E. (2002) Resistência do milho (Zea mays L.) transgênico (Bt) à lagarta-do-cartucho, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Revista Brasileira de Milho e Sorgo 1, 111.
Wenes, A.L., Bourguet, D., Andow, D.A., Courtin, C., Carré, G., Lorme, P., Sanchez, L. & Agustin, S. (2006) Frequency and fitness cost of resistance to Bacillus thuringiensis in Chrysomela tremulae (Coleoptera: Chrysomelidae). Heredity 97, 127134.
Whitford, F., Quisenberry, S.S., Riley, T.J. & Lee, W. (1988) Oviposition preference, mating compatibility, and development of two fall armyworm strains. Florida Entomologist 71, 234243.
Wiseman, B.R. & Davis, F.M. (1979) Plant resistance to the fall armyworm. Florida Entomologist 62, 123129.
Yue, B., Huang, F., Leonard, B.R., Moore, S., Parker, R., Andow, D.A., Cook, D., Emfinger, K. & Lee, D.R. (2008) Verifying an F1 screen for identification and quantification of rare Bacillus thuringiensis resistance alleles in field populations of the sugarcane borer, Diatraea saccharalis. Entomology Experimentalis et Applicata 129, 172180.
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