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Article Number - 156B3C458824


Vol.11(1), pp. 1-5 , May 2016
DOI: 10.5897/BMBR2016.0256
ISSN: 1538-2273



Review

Resistance to Bt Crops; Influence, mechanisms and management strategies



Mohammed Esmail Abdalla Elzaki
  • Mohammed Esmail Abdalla Elzaki
  • Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Jiangsu/The Key Laboratory of Monitoring and Management of Plant Diseases and Insects, Ministry of Agriculture, Nanjing, 210095, Jiangsu, China.
  • Google Scholar







 Received: 19 March 2016  Accepted: 16 May 2016  Published: 31 May 2016

Copyright © 2016 Author(s) retain the copyright of this article.
This article is published under the terms of the Creative Commons Attribution License 4.0


The genetically engineered insect-resistant crops, Bt crops, were first commercially grown in 1996 and adopted in different countries. The economic benefits of Bt crops are reducing the use of insecticides and more safe to environment, however, development of resistance by insects might reduce their efficacy. Unfortunately, the field population evolved resistance to different Bt toxins and the number of resistant species is going to increase, which threat the continuous success of Bt crops. Thus, understanding the Bt resistance mechanisms, including the molecular basis of resistance is important for well-resistance control in Bt crops. This review paper displayed the mechanisms of insect pests resistance to Bt crops and appropriate strategies to delay and manage the resistance in Bt crops.

Key words: Field-evolved resistance, molecular mechanism, resistance to Bt toxins, resistance management strategies, transgenic crops. 

Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S, Sezutsu H, Kobayashi I, Uchino K, Tamura T, Mita K (2012). Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. 109: E1591-E1598.
Crossref

 

Bernardi D, Salmeron E, Horikoshi RJ, Bernardi O, Dourado PM, Carvalho RA, Martinelli S, Head GP, Omoto C (2015). Cross-resistance between Cry1 proteins in fall armyworm (Spodoptera frugiperda) may affect the durability of current pyramided Bt maize hybrids in Brazil. PLoS One 10: e0140130.
Crossref

 
 

Brévault T, Heuberger S, Zhang M, Ellers-Kirk C, Ni X, Masson L, Li X, Tabashnik BE, Carrière Y (2013). Potential shortfall of pyramided transgenic cotton for insect resistance management. Proc. Natl. Acad. Sci. 110:5806-5811.
Crossref

 
 

Brévault T, Tabashnik BE, Carrière Y (2015). A seed mixture increases dominance of resistance to Bt cotton in Helicoverpa zea. Sci. Rep. 5:9807.
Crossref

 
 

Carrière Y, Crickmore N, Tabashnik BE (2015). Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat. Biotechnol. 33:161-168.
Crossref

 
 

Carrière Y, Fabrick JA, Tabashnik BE (2016). Can Pyramids and Seed Mixtures Delay Resistance to Bt Crops? Trends Biotechnol. 34(4):291-302
Crossref

 
 

Coates BS, Siegfried BD (2015). Linkage of an ABCC transporter to a single QTL that controls Ostrinia nubilalis larval resistance to the Bacillus thuringiensis Cry1Fa toxin. Insect. Biochem. Mol. Biol. 63:86-96.
Crossref

 
 

Denholm I, Devine G, Williamson M (2002). Insecticide resistance on the move. Science 297:2222-2223.
Crossref

 
 

Dennehy TJ, Unnithan G, Brink SA, Wood BD, Carrière Y, Tabashnik B, Antilla L, Whitlow M (2004). Update on pink bollworm resistance to Bt cotton in the Southwest. Cotton: A College of Agriculture and Life Sciences Report.

 
 

Ding Z, Wen Y, Yang B, Zhang Y, Liu S, Liu Z, Han Z (2013). Biochemical mechanisms of imidacloprid resistance in Nilaparvata lugens: Over-expression of cytochrome P450 CYP6AY1. Insect Biochem. Mol. Biol. 43:1021-1027.
Crossref

 
 

Downes S, Parker T, Mahon R (2010). Characteristics of resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa punctigera (Lepidoptera: Noctuidae) isolated from a field population. J. Econ. Entomol. 103:2147-2154.
Crossref

 
 

Elzaki MEA, Zhang W, Han Z (2015). Cytochrome P450 CYP4DE1 and CYP6CW3v2 contribute to ethiprole resistance in Laodelphax striatellus (Fallén). Insect Mol. Biol. 24:368-376.
Crossref

 
 

Fabrick JA, Unnithan GC, Yelich AJ, DeGain B, Masson L, Zhang J, Carrière Y, Tabashnik BE (2015). Multi-toxin resistance enables pink bollworm survival on pyramided Bt cotton. Sci. Rep. 5:16554.
Crossref

 
 

Farias JR, Andow DA, Horikoshi RJ, Sorgatto RJ, dos Santos AC, Omoto C (2015). Dominance of Cry1F resistance in Spodoptera frugiperda (Lepidoptera: Noctuidae) on TC1507 Bt maize in Brazil. Pest Manage. Sci. 72(5):974-979.
Crossref

 
 

Ferré J, Van Rie J (2002). Biochemistry and Genetics of Insect Resistance to B acillus thuringiensis. Annu. Rev. Entomol. 47:501-533.
Crossref

 
 

Franklin MT, Nieman CL, Janmaat AF, Soberón M, Bravo A, Tabashnik BE, Myers JH (2009). Modified Bacillus thuringiensis toxins and a hybrid B. thuringiensis strain counter greenhouse-selected resistance in Trichoplusia ni. Appl. Environ. Microbiol. 75:5739-5741.
Crossref

 
 

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

 
 

Gould F (1998). Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43:701-726.
Crossref

 
 

Gould F, Schliekelman P (2004). Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 49:193-217.
Crossref

 
 

Griffitts JS, Whitacre JL, Stevens DE, Aroian RV (2001). Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 293:860-864.
Crossref

 
 

Harvey-Samuel T, Morrison NI, Walker AS, Marubbi T, Yao J, Collins HL, Gorman K, Davies TE, Alphey N, Warner S (2015). Pest control and resistance management through release of insects carrying a male-selecting transgene. BMC Biol. 13:1.
Crossref

 
 

Hutchison W, Burkness E, Mitchell P, Moon R, Leslie T, Fleischer SJ, Abrahamson M, Hamilton K, Steffey KL, Gray M (2010). Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330:222-225.
Crossref

 
 

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

 
 

James C (2010). Global status of commercialized biotech/GM crops: 2010. International Service for the Acquisition of Agri-biotech Applications (ISAAA) Ithaca, NY, USA.

 
 

Jensen MN (2008). First documented case of pest resistance to biotech cotton.< http://uanews. org/node/18178>. Acesso em 10.

 
 

Jin L, Zhang H, Lu Y, Yang Y, Wu K, Tabashnik BE, Wu Y (2015). Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nat. Biotechnol. 33:169-174.
Crossref

 
 

Krafsur E (1998). Sterile insect technique for suppressing and eradicating insect population: 55 years and counting. J. Agric. Entomol. 15:303-317.

 
 

Kruger M, Van Rensburg J, Van den Berg J (2011). Resistance to Bt maize in Busseola fusca (Lepidoptera: Noctuidae) from Vaalharts, South Africa. Environ. Entomol. 40:477-483.
Crossref

 
 

Liu C, Xiao Y, Li X, Oppert B, Tabashnik BE, Wu K (2014a). Cis-mediated down-regulation of a trypsin gene associated with Bt resistance in cotton bollworm. Sci. Rep. 4:7219.
Crossref

 
 

Liu X, Chen M, Collins HL, Onstad DW, Roush RT, Zhang Q, Earle ED, Shelton AM (2014b). Natural enemies delay insect resistance to Bt crops. PLoS One 9:e90366.
Crossref

 
 

Liu Y-B, Tabashnik BE, Dennehy TJ, Patin AL, Bartlett AC (1999). Development time and resistance to Bt crops. Nature 400:519-519.
Crossref

 
 

Mahon R, Olsen K, Garsia K, Young S (2007). Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. J. Econ. Entomol. 100:894-902.
Crossref

 
 

Mehlo L, Gahakwa D, Nghia PT, Loc NT, Capell T, Gatehouse JA, Gatehouse AM, Christou P (2005). An alternative strategy for sustainable pest resistance in genetically enhanced crops. Proc. Natl. Acad. Sci. 102:7812-7816.
Crossref

 
 

Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, Field SG, Hemingway J, Paine MJI, Ranson H, Donnelly MJ (2012). Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc. Natl. Acad. Sci. 109:6147-6152.
Crossref

 
 

Moar WJ, Anilkumar KJ (2007). Plant science. The power of the pyramid. Science 318(5856):1561-1562.
Crossref

 
 

Monnerat R, Martins E, Macedo C, Queiroz P, Praça L, Soares CM, Moreira H, Grisi I, Silva J, Soberon M (2015). 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 10:e0119544.
Crossref

 
 

Morin S, Biggs RW, Sisterson MS, Shriver L, Ellers-Kirk C, Higginson D, Holley D, Gahan LJ, Heckel DG, Carriere Y (2003). Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. 100:5004-5009.
Crossref

 
 

Ocelotl J, Sánchez J, Arroyo R, García-Gómez BI, Gómez I, Unnithan GC, Tabashnik BE, Bravo A, Soberón M (2015). Binding and Oligomerization of Modified and Native Bt Toxins in Resistant and Susceptible Pink Bollworm. PLoS One 10:e0144086.
Crossref

 
 

Qiu L, Hou L, Zhang B, Liu L, Li B, Deng P, Ma W, Wang X, Fabrick JA, Chen L (2015). Cadherin is involved in the action of Bacillus thuringiensis toxins Cry1Ac and Cry2Aa in the beet armyworm, Spodoptera exigua. J. Invertebr. Pathol. 127:47-53.
Crossref

 
 

Roush R (1998). Two–toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos. Trans. R. Soc. B Biol. Sci. 353:1777-1786.

 
 

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

 
 

Shelton AM, Tang JD, Roush RT, Metz TD, Earle ED (2000). Field tests on managing resistance to Bt-engineered plants. Nat. Biotechnol. 18:339-342.
Crossref

 
 

Soberón M, Pardo-López L, López I, Gómez I, Tabashnik BE, Bravo A (2007). Engineering modified Bt toxins to counter insect resistance. Science 318:1640-1642.
Crossref

 
 

Tabashnik BE (2001). Breaking the code of resistance. Nat. Biotechnol. 19:922-924.
Crossref

 
 

Tabashnik BE, Brévault T, Carrière Y (2013). Insect resistance to Bt crops: lessons from the first billion acres. Nat. Biotechnol. 31:510-521.
Crossref

 
 

Tabashnik BE, Carrière Y, Dennehy TJ, Morin S, Sisterson MS, Roush RT, Shelton AM, Zhao J-Z (2003). Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J. Econ. Entomol. 96:1031-1038.
Crossref

 
 

Tabashnik BE, Dennehy TJ, Carrière Y (2005). Delayed resistance to transgenic cotton in pink bollworm. Proc. Natl. Acad. Sci. 102:15389-15393.
Crossref

 
 

Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y (2008). Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 26:199-202.
Crossref

 
 

Tabashnik BE, Gould F (2012). Delaying corn rootworm resistance to Bt corn. J. Econ. Entomol. 105:767-776.
Crossref

 
 

Tabashnik BE, Huang F, Ghimire MN, Leonard BR, Siegfried BD, Rangasamy M, Yang Y, Wu Y, Gahan LJ, Heckel DG (2011). Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat. Biotechnol. 29:1128-1131.
Crossref

 
 

Tabashnik BE, Liu Y-B, Dennehy TJ, Sims MA, Sisterson MS, Biggs RW, Carrière Y (2002). Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 95:1018-1026.
Crossref

 
 

Tabashnik BE, Mota-Sanchez D, Whalon ME, Hollingworth RM, Carrière Y (2014). Defining terms for proactive management of resistance to Bt crops and pesticides. J. Econ. Entomol. 107:496-507.
Crossref

 
 

Tabashnik BE, Patin AL, Dennehy TJ, Liu Y-B, Carriere Y, Sims MA, Antilla L (2000). Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proc. Natl. Acad. Sci. 97:12980-12984.
Crossref

 
 

Tabashnik BE, Sisterson MS, Ellsworth PC, Dennehy TJ, Antilla L, Liesner L, Whitlow M, Staten RT, Fabrick JA, Unnithan GC (2010). Suppressing resistance to Bt cotton with sterile insect releases. Nat. Biotechnol. 28:1304-1307.
Crossref

 
 

Tabashnik BE, Zhang M, Fabrick JA, Wu Y, Gao M, Huang F, Wei J, Zhang J, Yelich A, Unnithan GC (2015). Dual mode of action of Bt proteins: protoxin efficacy against resistant insects. Sci. Rep. 5:15107.
Crossref

 
 

Tay WT, Mahon RJ, Heckel DG, Walsh TK, Downes S, James WJ, Lee S-F, Reineke A, Williams AK, Gordon KH (2015). Insect resistance to Bacillus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC transporter subfamily A protein. PLoS Genet. 11:e1005534.
Crossref

 
 

Tiewsiri K, Wang P (2011). Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. Proc. Natl. Acad. Sci. 108:14037-14042.
Crossref

 
 

Van Rensburg J (2007). First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S. Afr. J. Plant Soil 24:147-151.
Crossref

 
 

Wei J, Guo Y, Liang G, Wu K, Zhang J, Tabashnik BE, Li X (2015). Cross-resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against the cotton bollworm. Sci. Rep. 5:7714.
Crossref

 
 

Welch KL, Unnithan GC, Degain BA, Wei J, Zhang J, Li X, Tabashnik BE, Carrière Y (2015). Cross-resistance to toxins used in pyramided Bt crops and resistance to Bt sprays in Helicoverpa zea. J. Invertebr. Pathol. 132:149-156.
Crossref

 
 

Wu K-M, Lu Y-H, Feng H-Q, Jiang Y-Y, Zhao J-Z (2008). Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin–containing cotton. Science 321:1676-1678.
Crossref

 
 

Zhang H, Tian W, Zhao J, Jin L, Yang J, Liu C, Yang Y, Wu S, Wu K, Cui J (2012). Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proc. Natl. Acad. Sci. 109:10275-10280.
Crossref

 
 

Zhao J-Z, Cao J, Collins HL, Bates SL, Roush RT, Earle ED, Shelton AM (2005). Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc. Natl. Acad. Sci. USA 102:8426-8430.
Crossref

 
 

Zhao J-Z, Cao J, Li Y, Collins HL, Earle ED, Roush RT, Shelton AM (2002). Plants expressing two Bacillus thuringiensis toxins delay insect resistance compared to single toxins used sequentially or in a mosaic. In The 2002 ESA Annual Meeting and Exhibition.

 
 

Zhao J-Z, Cao J, Li Y, Collins HL, Roush RT, Earle ED, Shelton AM (2003). Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21:1493-1497.
Crossref

 

 


APA Elzaki, M. E. A. (2016). Resistance to Bt Crops; Influence, mechanisms and management strategies. Biotechnology and Molecular Biology Reviews, 11(1), 1-5.
Chicago Mohammed Esmail Abdalla Elzaki. "Resistance to Bt Crops; Influence, mechanisms and management strategies." Biotechnology and Molecular Biology Reviews 11, no. 1 (2016): 1-5.
MLA Mohammed Esmail Abdalla Elzaki. "Resistance to Bt Crops; Influence, mechanisms and management strategies." Biotechnology and Molecular Biology Reviews 11.1 (2016): 1-5.
   
DOI 10.5897/BMBR2016.0256
URL http://academicjournals.org/journal/BMBR/article-abstract/156B3C458824

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