Development of Resistance to Bacillus thuringiensis (Bt) Toxin by Insect Pests

Main Article Content

Girma Gashu Kebede

Abstract

Insect pests are the primary scourge of agriculture down the ages. It is estimated that 14% of crop productivity is misplaced to insect pests on a global scale. To decrease reliance on insecticide sprays, scientists have genetically engineered plants to make insecticidal proteins encoded through genes from the common bacterium Bacillus thuringiensis (Bt). Currently, due to their importance, more than 70 kinds of Cry genes are described (cry1 up to cry70). These endotoxins have been categorized as Cry1–Cry69 and Cyt1–Cyt3 and specific subgroups relying on their amino acid sequence. Of these, some Bt genes such as cry1Ab, cry1Ac, cry2Ab and cry9C are already being commercially used in GMP. The crystalline proteins get solubilized in midgut at high pH, releasing d-endotoxin proteins. The exquisite capability of insects to adapt to Bt-toxin and different manage systems helps the conclusion that evolution of resistance by means of pests is the important hazard to the persevered success of transgenic Bt crop. This paper ambitions to overview the resistance improvement of insect pests towards Bt toxin. Insect populations regularly have herbal genetic variant affecting response to a toxin, with some alleles conferring susceptibility and others conferring resistance. Many laboratory and field researches showed, resistance improvement of insects in opposition to Bt toxin. Field-evolved resistance happens when exposure of a discipline populace to a toxin increases the frequency of alleles conferring resistance in subsequent generations. The chance insect resistance poses to the future use of Bt plant-incorporated protectants haveled into emergence of insect resistance management concept. IRM is of received with the aid of actions taken to prolong the improvement of insect resistance to pest control measures in goal pest populations or by way of practices aimed at decreasing the achievable for insect pests to grow to be resistant to a gene. The danger insect resistance poses to the future use of Bt plant-incorporated protectants have led into emergence of insect resistance management concept.

Keywords:
Bt-crops, resistance development, Bacillus thuringiensis (Bt), resistance management.

Article Details

How to Cite
Kebede, G. G. (2020). Development of Resistance to Bacillus thuringiensis (Bt) Toxin by Insect Pests. Asian Journal of Research in Biosciences, 2(1), 9-28. Retrieved from https://globalpresshub.com/index.php/AJORIB/article/view/840
Section
Review Papers

References

Devine GJ, Furlong MJ. Insecticide use: Contexts and ecological consequences. Agriculture and Human Values. 2007;24(3):281-306.

Hurst MR, Jones SM, Tan B, Jackson TA. Induced expression of the Serratia entomophila Sep proteins shows activity towards the larvae of the New Zealand grass grub Costelytra zealandica. FEMS Microbiology Letters. 2007;275(1):160-167.

Charles JF, Nielsen-LeRoux C. Mosquitocidal bacterial toxins: Diversity, mode of action and resistance phenomena. Memorias Do Instituto Oswaldo Cruz. 2000;95:201-206.

Bowen DJ. Novel insecticidal toxins from nematode-symbiotic bacteria. Cellular and Molecular Life Sciences CMLS. 2000;57(5):828-833.

Bravo A, Gill SS, Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon. 2007;49(4):423-435.

Crickmore N.. Beyond the spore–past and future developments of Bacillus thuringiensis as a biopesticide. Journal of Applied Microbiology. 2011;101(3):616-619.

James C. Global status of commercialized biotech/GM crops, Ithaca, NY: ISAAA. 2010;44.

Ferré J, Van Rie J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology. 2002;47(1):501-533.

Janmaat AF, Myers J.Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusiani. Proceedings of the Royal Society of London. Series B: Biological Sciences. 2003;270(1530):2263-2270.

Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y. Insect resistance to Bt crops: Evidence versus theory. Nature biotechnology. 2008;26(2):199.

Kruger M, Van Rensburg JBJ, Van den 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 Protection. 2009;28(8):684-689.

Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology. 2010;103(4):1031-1038.

Dhurua S, Gujar GT. Field‐evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest management science. 2011;67(8):898-903.

Gahan LJ, Pauchet Y, Vogel H, Heckel DG. An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS genetics. 2010;6(12), .e1001248.

Baxter SW, Badenes-Pérez FR, Morrison A, Vogel H, Crickmore N, Kain W, Wang P, Heckel DG, Jiggins CD. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics, 2011;189(2):675-679.

Tabashnik BE, Huang F, Ghimire MN, Leonard BR, Siegfried BD, Rangasamy M, Yang Y, Wu Y, Gahan LJ, Heckel DG, Bravo A. Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nature biotechnology, 2011;29(12), p.1128.

Andrews RE, Faust RM, Wabiko H, Raymond KC, Bulla LA. The biotechnology of Bacillus thuringiensis. Critical reviews in biotechnology, 1987;6(2), pp.163-232.

Stahly DP, Andrews RE, Yousten AA. The genus Bacillus—insect pathogens. The Prokaryotes: Volume 4: Bacteria: Firmicutes, Cyanobacteria, 1991;pp.563-608.

Hansen BM, Damgaard PH, Eilenberg J, Pedersen JC. Bacillus thuringensis: Ecology and Environmental Effects of Its Use for Microbial Pest Control; 1996.

Ohba M, Aizawa K. Distribution of Bacillus thuringiensis in soils of Japan. Journal of Invertebrate Pathology, 1986;47(3), pp.277-282.

Damgaard PH, Hansen BM, Pedersen JC, Eilenberg J. Natural occurrence of Bacillus thuringiensis on cabbage foliage and in insects associated with cabbage crops. Journal of Applied Microbiology, 1997;82(2):253-258.

Gordon RE. Some taxonomic observations on the genus Bacillus. Biological Regulation of Vectors: The saprophytic and aerobic bacteria and fungi. US DEW pub. no. NIH-77-1180. Washington, DC: Govt Printing Office, 1977;67-82.

Klier A, Lecadet MM. Arguments based on hybridization-competition experiments in favor of the in vitro synthesis of sporulation-specific mRNAs by the RNA polymerase of B. thuringiensis. Biochemical and biophysical research communications, 1976;73(2):263-270.

Kim H, Lee DW, Woo SD, Yu YM, Kang SK. Seasonal distribution and characterization of Bacillus thuringiensis isolated from Seri cultural environments in Korea. The Journal of General and Applied Microbiology. 1998;44(2):133-138.

Goldberg LJ, Margalit J. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegypti and Culex pipiens. Mosq. News. 1977;37(3);355-358.

Prasertphon S, Areekul P, Tanada Y. Sporulation of Bacillus thuringiensis in host cadavers. Journal of Invertebrate Pathology, 1973;21(2):205-207.

Akiba Y. Microbial ecology of Bacillus thuringiensis VI. Germination of Bacillus thuringiensis spores in the soil. Applied Entomology and Zoology. 1986;21(1):76-80.

DeLucca II AJ, Simonson JG, Larson AD. Bacillus thuringiensis distribution in soils of the United States. Canadian Journal of Microbiology, 1981;27(9):865-870.

Travers RS, Martin PA, Reichelderfer CF. Selective process for efficient isolation of soil Bacillus spp. Appl. Environ. Microbiol. 1987;53(6):1263-1266.

Martin PA, Travers RS. Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl. Environ. Microbiol. 1989;55(10):2437-2442.

Smith RA, Couche GA. The phylloplane as a source of Bacillus thuringiensis variants. Appl. Environ. Microbiol. 1991;57(1):311-315.

Meadows MP, Ellis DJ, Butt J, Jarrett P, Burges HD. Distribution, frequency, and diversity of Bacillus thuringiensis in an animal feed mill. Appl. Environ. Microbiol. 1992;58(4):1344-1350.

Meadows MP. Bacillus thuringiensis in the environment: Ecology and risk assessment. Bacillus thuringiensis, An environmental biopesticide: Theory and Practice. 1993;193-220.

De Barjac H, Bonnefoi A. Essai de classification biochimique et sérologique de 24 souchesdeBacillus du typeB. thuringiensis. Entomophaga. 1962;7(1);5-31.

Krieg A, Huger AM, Langenbruch GA, Schnetter W. Bacillus thuringiensis var. tenebrionis, a new pathotype effective against larvae of Coleoptera. Zeitschrift für angewandte Entomologie; 1983.

Narva KE, Payne JM, Schwab GE, Hickle LA, Galasan T, Sick AJ. Novel Bacillus thuringiensis microbes active against nematodes and genes encoding novel nematode-active toxins cloned from Bacillus thuringiensis isolates. European Patent Office, EP0462721; 1991.

Crickmore N, Zeigler DR, Feitelson J, Schnep f. E.S.C.H.E.R.I.C.H.I.A., Van Rie J, Lereclus D, Baum J, Dean DH. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998;62(3):807-813.

Schnepf HE, Whiteley HR. Cloning and expression of the Bacillus thuringiensis crystal protein gene in Escherichia coli. Proceedings of the National Academy of Sciences. 1981;78(5):2893-2897.

Höfte H, Whiteley HR. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiology and Molecular Biology Reviews. 1989;53(2):242-255.

Donovan WP, Engleman JT, Donovan JC, Baum JA, Bunkers GJ, Chi DJ, Clinton WP, English L, Heck GR, Ilagan OM, Krasomil-Osterfeld KC. Discovery and characterization of Sip1A: A novel secreted protein from Bacillus thuringiensis with activity against coleopteran larvae. Applied microbiology and biotechnology, 2006;72(4):713-719.

Ibrahim MA, Griko N, Junker M, Bulla LA. Bacillus thuringiensis: A genomics and proteomics perspective. Bioengineered Bugs, 2010;1(1):31-50.

De Maagd RA, Weemen-Hendriks M, Stiekema W, Bosch D. Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in Different, but Not All, Cry1-Cry1C Hybrids. Appl. Environ. Microbiol. 2000;66(4):1559-1563.

Shelton AM, Tang JD, Roush RT, Metz TD, Earle ED. Field tests on managing resistance to Bt-engineered plants. Nature Biotechnology. 2000;18(3):339.

Crickmore N, Zeigler DR, Feitelson J, Schnepf ESCHERICHIA, Van Rie J, Lereclus D, Baum J, Dean DH. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998;62(3):807-813.

James C. Global status of commercialized biotech/GM crops. Ithaca, NY: ISAAA; 2010.

James C. Global status of commercialized biotech/GM crops, 2010. Ithaca, NY: ISAAA; 2011.

McGaughey WH. Insect resistance to the biological insecticide Bacillus thuringiensis. Science. 1985;229(4709):193-195.

Liu YB, Tabashnik BE. Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis. Proceedings of the Royal Society of London. Series B: Biological Sciences. 1997;264(1381):605-610.

Tabashnik BE, Dennehy TJ, Carrière Y. Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences, 2005a;102(43):15389-15393.

Tabashnik BE, Gassman AJ, Crowder DW, Carriere Y. Erratum: Reply to Field-evolved resistance to Bt toxins. Nature Biotechnology. 2008b;26(12):1383.

Bourguet D. Resistance to Bacillus thuringiensis toxins in the European corn borer: what chance for Bt maize? Physiological Entomology, 2004;29(3), pp.251-256.

Sanchis V, Bourguet D. Bacillus thuringiensis: Applications in agriculture and insect resistance management. A review. Agronomy for sustainable development. 2008;28(1):11-20.

Brookes G, Barfoot P. GM crops: Global socio-economic and environmental impacts 1996-2008. Dorchester, UK: PG Economics Ltd; 2010.

Subramanian A, Qaim M. The impact of Bt cotton on poor households in rural India. The Journal of Development Studies. 2010;46(2):295-311.

Reed GL, Jensen AS, Riebe J, Head G, Duan JJ. Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: Comparative efficacy and non‐target impacts. Entomologia experimentalis et Applicata. 2001;100(1):89-100.

Dutton A, Klein H, Romeis J, Bigler F. Uptake of Bt‐toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecological Entomology, 2002;27 (4):441-447.

Faria CA, Wäckers FL, Pritchard J, Barrett DA, Turlings TC. High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS One. 2007;2(7): e600.

Lawo NC, Wäckers FL, Romeis J. Indian Bt cotton varieties do not affect the performance of cotton aphids. PLoS One. 2009;4(3):e4804.

Lu Y, Wu K, Jiang Y, Xia B, Li P, Feng H, Wyckhuys KA, Guo Y. Mired bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science. 2010;328 (5982):1151-1154.

Pray CE, Huang J, Hu R, Rozelle S. Five years of Bt cotton in China–the benefits continue. The Plant Journal. 2002;31(4):423-430.

Zeilinger AR, Andow DA, Zwahlen C, Stotzky G. Earthworm populations in a northern US Cornbelt soil are not affected by long-term cultivation of Bt maize expressing Cry1Ab and Cry3Bb1 proteins. Soil Biology and Biochemistry. 2010;42(8):1284-1292.

Bravo A, Gill SS, Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon. 2007;49(4):423-435.

Grochulski P, Masson L, Borisova S, Pusztai-Carey M, Schwartz JL, Brousseau R, Cygler M. Bacillus thuringiensis CrylA (a) Insecticidal toxin: Crystal structure and channel formation. Journal of Molecular Biology. 1995;254(3):447-464.

Zhang H, Tian W, Zhao J, Jin L, Yang J, Liu C, Yang Y, Wu S, Wu K, Cui J, Tabashnik BE. Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proceedings of the National Academy of Sciences. 2012;109(26):10275-10280.

Groot AT, Dicke M. Transgenic crops in an agro-ecological context: Multitrophic effects of insect-resistant plants. Wageningen Univ., Lab. of Entomology; 2001.

Ferré J, Van Rie J, MacIntosh SC. Insecticidal genetically modified crops and insect resistance management (IRM). In Integration of insect-resistant genetically modified crops within IPM programs (pp. 41-85). Springer, Dordrecht; 2003.

Tabashnik BE. Delaying insect resistance to transgenic crops. Proceedings of the National Academy of Sciences. 2008c105(49):19029-19030.

Downes S, Parker TL, Mahon RJ. Frequency of alleles conferring resistance to the Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa punctigera (Lepidoptera: Noctuidae) from 2002 to 2006. Journal of Economic Entomology. 2009;102(2): 733-742.

Tabashnik BE, Patin AL, Dennehy TJ, Liu YB, Carrière Y, Sims MA, Antilla L. Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proceedings of the National Academy of Sciences. 2000d;97(24):12980-12984.

Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology. 2010;103(4):1031-1038.

Bagla P. Hardy cotton-munching pests are latest blow to GM crops; 2010.

Xin S, Gu L, Zhao NH, Yin YX, Zhou LJ, Guo YG, Wan LJ. Smaller sulfur molecules promise better lithium–sulfur batteries. Journal of the American Chemical Society. 2012;134(45):18510-18513.

Downes S, Parker TL, Mahon RJ. Characteristics of resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa punctigera (Lepidoptera: Noctuidae) isolated from a field population. Journal of Economic Entomology. 2010;103(6):2147-2154.

Jensen MN. First documented case of pest resistance to biotech cotton. UA entomologists have published a report on their discovery of Bt-resistant bollworms in Mississippi and Arkansas; 2008.

Available:http://uanews. org/node/18178

Dennehy TJ, Unnithan G, Brink SA, Wood BD, Carrière Y, Tabashnik B, Antilla L, Whitlow M. Update on pink bollworm resistance to Bt cotton in the Southwest; 2004.

Tabashnik BE, Liu YB, Dennehy TJ, Sims MA, Sisterson MS, Biggs RW, Carrière Y. Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology. 2002k;95(5):1018-1026.

Zhang H, Tian W, Zhao J, Jin L, Yang J, Liu C, Yang Y, Wu S, Wu K, Cui J, Tabashnik BE. Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proceedings of the National Academy of Sciences. 2012;109(26):10275-10280.

Downes S, Parker TL, Mahon RJ. Characteristics of resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa punctigera (Lepidoptera: Noctuidae) isolated from a field population. Journal of Economic Entomology, 2010;103(6):2147-2154.

Santos-Amaya OF, Tavares CS, Monteiro HM, Teixeira TP, Guedes RN, Alves AP, Pereira EJ. Genetic basis of Cry1F resistance in two Brazilian populations of fall armyworm, Spodoptera frugiperda. Crop Protection. 2016;81:154-162.

Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW. Field-evolved resistance to Bt maize by western corn rootworm. PloS one. 2011;6(7):e22629.

Farias JR, Andow DA, Horikoshi RJ, Sorgatto RJ, Santos ACD, Omoto C. Dominance of Cry1F resistance in Spodoptera frugiperda (Lepidoptera: Noctuidae) on TC1507 Bt maize in Brazil. Pest Management Science. 2016;72(5):974-979.

Jakka SR, Gong L, Hasler J, Banerjee R, Sheets JJ, Narva K, Blanco CA, Jurat-Fuentes JL. Field-evolved Mode 1 fall armyworm resistance to Bt corn associated with reduced Cry1Fa toxin binding and midgut alkaline phosphatase expression. Applied and Environmental Microbiology, 2015;AEM-02871.

Monnerat R, Martins E, Macedo C, Queiroz P, Praça L, Soares CM, Moreira H, Grisi I, Silva J, Soberon M, Bravo A. Evidence of field-evolved resistance of Spodoptera frugiperda to Bt corn expressing Cry1F in Brazil that is still sensitive to modified Bt toxins. PLoS one. 2015;10(4): e0119544.

Gunning RV, Dang HT, Kemp FC, Nicholson IC, Moores GD. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 2005;71(5):2558-2563.

Gunning RV, Dang HT, Kemp FC, Nicholson IC, Moores GD. New resistance mechanism in Helicoverpaarmigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 2005;71(5):2558-2563.

Gunning RV, Dang HT, Kemp FC, Nicholson IC, Moores GD. New resistance mechanism in Helicoverpaarmigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 2005;71(5):2558-2563.

Tabashnik BE, Gassman AJ, Crowder DW, Carriere Y. Erratum: Reply to field-evolved resistance to Bt toxins. Nature Biotechnology. 2008;26(12):1383.

Onstad DW. Insect resistance management: Biology, economics and prediction. Academic Press; 2013.

Tabashnik BE, Patin AL, Dennehy TJ, Liu YB, Carrière Y, Sims MA, Antilla L. Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proceedings of the National Academy of Sciences. 2000;97(24):12980-12984.

Blanco CA, Chiaravalle W, Dalla-Rizza M, Farias JR, García-Degano MF, Gastaminza G, Mota-Sánchez D, Murúa MG, Omoto C, Pieralisi BK, Rodríguez J. Current situation of pests targeted by Bt crops in Latin America. Current Opinion in Insect Science. 2016;15:131-138.

Tabashnik BE, Patin AL, Dennehy TJ, Liu YB, Carrière Y, Sims MA, Antilla L. Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proceedings of the National Academy of Sciences. 2000;97(24):12980-12984.

Tabashnik BE. Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology. 1994;39(1):47-79.

Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y. Insect resistance to Bt crops: Evidence versus theory. Nature Biotechnology. 2008;26(2):199.

Tabashnik BE, Cushing NL, Johnson MW. Diamondback moth (Lepidoptera: Plutellidae) resistance to insecticides in Hawaii: Intra-island variation and cross-resistance. Journal of Economic Entomology. 1987;80(6):1091-1099.

Tabashnik BE. Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology. 1994;39(1):47-79.

Hutchison WD, Burkness EC, Mitchell PD, Moon RD, Leslie TW, Fleischer SJ, Abrahamson M, Hamilton KL, Steffey KL, Gray ME, Hellmich RL. Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science. 2010;330(6001):222-225.

Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology. 1998;43(1):701-726.

Tabashnik BE. Delaying insect resistance to transgenic crops. Proceedings of the National Academy of Sciences. 2008;105(49):19029-19030.

Georghiou GP, Taylor CE. Genetic and biological influences in the evolution of insecticide resistance. Journal of Economic Entomology. 1977;70(3):319-323.

Tabashnik BE, Croft BA. Managing pesticide resistance in crop-arthropod complexes: interactions between biological and operational factors. Environmental Entomology. 1982;11(6): 1137-1144.

EPA. The Environmental protection Agency's White Paper on Bt Plant‐Pesticide Resistance Management; 1998.

Tabashnik BE, Gould F, Carrière Y. Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. Journal of Evolutionary Biology. 2004;17(4):904-912.

Tabashnik BE, Van Rensburg JBJ, Carrière Y. Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology. 2009;102(6):2011-2025.

Yu SE. Insecticide resistance. The Toxicology and Biochemistry of Insecticides. 2008;201:230.

Tabashnik BE, Dennehy TJ, Carrière Y. Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences. 2005;102(43):15389-15393.

Tabashnik BE, Gassman AJ, Crowder DW, Carriere Y. Erratum: Reply to field-evolved resistance to Bt toxins. Nature Biotechnology. 2008;26(12):1383.

Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology. 1998;43(1):701-726.

Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology. 1998;43(1):701-726.

Tabashnik BE, Gould F, Carrière Y. Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. Journal of Evolutionary Biology. 2004;17(4);904-912.

Shelton AM, Tang JD, Roush RT, Metz TD, Earle ED. Field tests on managing resistance to Bt-engineered plants. Nature Biotechnology. 2000;18(3):339.

Krattiger AF. Insect resistance in crops: A case study of Bacillus thuringiensis (Bt) and its transfer to developing countries. ISAAA Briefs no. 2; 1997.

Briefs ISAAA. Global status of commercialized biotech/GM Crops in 2017: Biotech crop adoption surges as economic benefits accumulate in 22 years; 2017.

Wu K. Monitoring and management strategy for Helicoverpa armigera resistance to Bt cotton in China. Journal of Invertebrate Pathology. 2007;95(3):220-223.

Li Y, Gao Y, Wu K. Function and effectiveness of natural refuge in IRM strategies for Bt crops. Current Opinion in Insect Science. 2017; 21:1-6.

Jin L, Zhang H, Lu Y, Yang Y, Wu K, Tabashnik BE, Wu Y. Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nature Biotechnology. 2015;33(2): 169.

Blanco CA, Chiaravalle W, Dalla-Rizza M, Farias JR, García-Degano MF, Gastaminza G, Mota-Sánchez D, Murúa MG, Omoto C, Pieralisi BK, Rodríguez J. Current situation of pests targeted by Bt crops in Latin America. Current Opinion in Insect Science. 2016;15:131-138.

Fatoretto JC, Michel AP, Silva Filho MC, Silva N. Adaptive potential of fall armyworm (Lepidoptera: Noctuidae) limits Bt trait durability in Brazil. Journal of Integrated Pest Management. 2017;8(1): 17.