Similar genetic basis of resistance to Bt toxin Cry1Ac in boll-selected and diet-selected strains of pink bollworm

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Fabrick, Jeffrey A ^a   Tabashnik, Bruce E ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CADHERIN; CRY1AC TOXIN;

ALLELISM; ARTICLE; CADHERIN GENE; CONTROLLED STUDY; COTTON; DIET; FEMALE; GENE; GENE DELETION; GENE LOCUS; GENETIC ANALYSIS; GENETIC IDENTIFICATION; GENETIC PEST CONTROL; GENETIC SIMILARITY; GENOTYPE; INSECTICIDE RESISTANCE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PGCAD1 GENE; PINK BOLLWORM; PLANT INSECT INTERACTION; PROGENY; UNITED STATES; WORM;

ALLELES; ANIMALS; BACTERIAL PROTEINS; CADHERINS; CROSSES, GENETIC; ENDOTOXINS; FEMALE; GENOTYPE; GOSSYPIUM; HEMOLYSIN PROTEINS; INSECTICIDE RESISTANCE; INSECTICIDES; MALE; MOTHS; PARASITIC SENSITIVITY TESTS; PEST CONTROL, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED;

EID: 84859939820     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035658     Document Type: Article

References (55)

1. Mendelsohn M, Kough J, Vaituzis Z, Matthews K, (2003) Are Bt crops safe? Nat Biotechnol 21: 1003-1009.
2. Bravo A, Likitvivatanavong S, Gill SS, Soberon M, (2011) Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem Mol Biol 41: 423-431.
3. Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P, (2011) Bacillus thuringiensis: A century of research, development and commercial applications. Plant Biotechnol J 9: 283-300.
4. James C, (2010) Global Status of Commercialized Biotech/GM Crops: 2010. ISAAA Brief No. 42. ISAAA: Ithaca, NY.
5. Carrière Y, Ellers-Kirk C, Sisterson M, Antilla L, Whitlow M, et al. (2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc Natl Acad Sci USA 100: 1519-1523.
6. Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao JZ, (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321: 1676-1678.
7. Hutchison WD, Burkness EC, Mitchell PD, Moon RD, Leslie TW, et al. (2010) Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330: 222-225.
8. National Research Council (2010) The impact of genetically engineered crops on farm sustainability in the United States National Academies Press.
9. Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y, (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotech 26: 199-202.
10. Kruger M, Van Rensburg JBJ, Van den Berg J, (2009) Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot 28: 684-689.
11. Tabashnik BE, Van Rensburg JB, Carrière Y, (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102: 2011-2025.
12. Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, et al. (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103: 1031-1038.
13. Bagla P, (2010) Hardy Cotton-Munching Pests Are Latest Blow to GM Crops. Science 327: 1439.
14. Dhurua S, Gujar GT, (2011) Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag Sci 67: 898-903.
15. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW, (2011) Field-evolved resistance to Bt maize by Western corn rootworm. PLoS ONE 6: e22629.
16. Tabashnik BE, (1994) Evolution of resistance to Bacillus thuringiensis. Annu Rev Entomol 39: 47-79.
17. Ferré J, Van Rie J, (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47: 501-533.
18. Tabashnik BE, Carrière Y, Dennehy TJ, Morin S, Sisterson M, et al. (2003) Insect resistance to transgenic Bacillus thuringiensis crops: Lessons from the laboratory and field. J Econ Entomol 96: 1031-1038.
19. Baxter SW, Badenes-Pérez FR, Morrison A, Vogel H, Crickmore N, et al. (2011) Parallel evolution of Bt toxin resistance in Lepidoptera. Genetics Genetics 189: 675-679.
20. Gahan LJ, Gould F, Heckel DG, (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293: 857-860.
21. Morin S, Biggs RW, Sisterson MS, Shriver L, Ellers-Kirk C, et al. (2003) Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc Natl Acad Sci USA 100: 5004-5009.
22. Xu X, Yu L, Wu Y, (2005) Disruption of a cadherin gene associated with resistance to Cry1Ac delta-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl Environ Microbiol 71: 948-954.
23. Jurat-Fuentes JL, Gahan LJ, Gould FL, Heckel DG, Adang MJ, (2004) The HevCaLP Protein Mediates Binding Specificity of the Cry1A Class of Bacillus thuringiensis Toxins in Heliothis virescens. Biochemistry 43: 14299-14305.
24. Herrero S, Gechev T, Bakker PL, Moar WJ, de Maagd RA, (2005) Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four Aminopeptidase N genes. BMC Genomics 6.
25. Zhang X, Candas M, Griko N, Taussig R, Bulla LA, (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci 103: 9897-9902.
26. Henneberry TJ, Naranjo SE, (1998) Integrated management approaches for pink bollworm in the Southwestern United States. Integr Pest Manage Rev 3: 31-52.
27. Wan P, Huang Y, Wu H, Huang M, Cong S, et al. (2012) Increased frequency of pink bollworm resistance to Bt toxin Cry1Ac in China. PLoS ONE 7: e29975.
28. Tabashnik BE, Fabrick JA, Henderson S, Biggs RW, Yafuso CM, et al. (2006) DNA screening reveals pink bollworm resistance to Bt cotton remains rare after a decade of exposure. J Econ Entomol 99: 1525-1530.
29. Tabashnik BE, Sisterson MS, Ellsworth PC, Dennehy TJ, Antilla L, et al. (2010) Suppressing resistance to Bt cotton with sterile insect releases. Nat Biotechnol 28: 1304-1307.
30. Liu Y-B, Tabashnik BE, Dennehy TJ, Patin AL, Bartlett AC, (1999) Development time and resistance to Bt crops. Nature 400: 519.
31. Tabashnik BE, Liu Y-B, de Maagd RA, Dennehy TJ, (2000b) Cross-resistance of pink bollworm (Pectinophora gossypiella) to Bacillus thuringiensis toxins. Appl Environ Microbiol 66: 4582-4584.
32. Tabashnik BE, Biggs RW, Higginson DM, Henderson S, Unnithan DC, et al. (2005) Association between resistance to Bt cotton and cadherin genotype in pink bollworm. J Econ Entomol 98: 635-644.
33. Tabashnik BE, Liu Y-B, Unnithan DC, Carrière Y, Dennehy TJ, et al. (2004) Shared genetic basis of resistance to Bt toxin Cry1Ac in independent strains of pink bollworm. J Econ Entomol 97: 721-726.
34. Fabrick JA, Tabashnik BE, (2007) Binding of Bacillus thuringiensis toxin Cry1Ac to multiple sites of cadherin in pink bollworm. Insect Biochem Mol Biol 37: 97-106.
35. Fabrick JA, Mathew LG, Tabashnik BE, Li X, (2011) Insertion of an intact CR1 retrotransposon in a cadherin gene linked with Bt resistance in the pink bollworm, Pectinophora gossypiella. Insect Mol Biol 20: 651-665.
36. Henneberry TJ, Forlow-Jech L, Maurer J, (2006) Effects of pink bollworm larval feeding on 'NuCOTN 33b' cotton bolls and pollen and tolerance to Cry1Ac toxin in artificial diet bioassays. Southwest Entomol 31: 169-185.
37. Fabrick JA, Forlow Jech L, Henneberry TJ, (2009) Novel pink bollworm resistance to the Bt toxin Cry1Ac: Effects on mating, oviposition, larval development and survival. J Insect Sci 9: 8.
38. Tabashnik BE, Patin AL, Dennehy TJ, Liu Y-B, Carrière Y, et al. (2000) Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proc Natl Acad Sci USA 97: 12980-12984.
39. Tabashnik BE, Liu Y-B, Dennehy TJ, Sims MA, Sisterson MS, et al. (2002) Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 95: 1018-1026.
40. Liu Y-B, Tabashnik BE, Dennehy TJ, Patin AL, Sims MA, et al. (2001) Effects of Bt cotton and Cry1Ac toxin on survival and development of pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 94: 1237-1242.
41. Carrière Y, Ellers-Kirk C, Biggs RW, Nyboer ME, Unnithan GC, et al. (2006) Cadherin-based resistance to Bt cotton in hybrid strains of pink bollworm: Fitness costs and incomplete resistance. J Econ Entomol 99: 1925-1935.
42. Tabashnik BE, Dennehy TJ, Carrière Y, (2005) Delayed resistance to transgenic cotton in pink bollworm. Proc Natl Acad Sci USA 102: 15389-15393.
43. Carrière Y, Ellers-Kirk C, Liu Y-B, Sims MA, Patin AL, et al. (2001) Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm. J Econ Entomol 94: 1571-1576.
44. Carrière Y, Ellers-Kirk C, Biggs RW, DeGain B, Holley D, et al. (2005) Effects of cotton cultivar on fitness costs associated with resistance of pink bollworm (Lepidoptera: Gelechiidae) to Bt cotton. J Econ Entomol 98: 947-954.
45. Williams JL, Ellers-Kirk C, Orth RG, Gassmann AJ, Head G, et al. (2011) Fitness cost of resistance to Bt cotton linked with increased gossypol content in pink bollworm larvae. PLoS ONE 6: e21863.
46. Gonzalez-Cabrera J, Escriche B, Tabashnik BE, Ferre J, (2003) Binding of Bacillus thuringiensis toxins in resistant and susceptible strains of pink bollworm (Pectinophora gossypiella). Insect Biochem Mol Biol 33: 929-935.
47. Zhao J, Jin L, Yang Y, Wu Y, (2010) Diverse cadherin mutations conferring resistance to Bacillus thuringiensis toxin Cry1Ac in Helicoverpa armigera. Insect Biochem Mol Biol 40: 113-118.
48. Liu Y-B, Tabashnik BE, Meyer SK, Carrière Y, Bartlett AC, (2001) Genetics of pink bollworm resistance to Bacillus thuringiensis toxin Cry1Ac. J Econ Entomol 94: 248-252.
49. Bartlett AC, (1995) Resistance of the pink bollworm to Bt transgenic cotton. pp. 766-768 In Proceedings, 1995 Beltwide Cotton Conferences. National Cotton Council of America, Memphis, TN.
50. Tabashnik BE, Unnithan GC, Masson L, Crowder DW, Li X, et al. (2009) Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc Natl Acad Sci USA 106: 11889-11894.
51. Bartlett AC, Wolf WW, (1985) Pectinophora gossypiella. In: Moore RF, Singh P, editors. Handbook of Insect Rearing Elsevier Scientific Publishing Co., Amsterdam pp. 415-430.
52. Liu Y-B, Tabashnik BE, (1997) Inheritance of resistance to the Bacillus thuringiensis toxin Cry1C in the diamondback moth. Appl Environ Microbiol 63: 2218-2223.
53. Tabashnik BE, Liu Y-B, Malvar T, Heckel DG, Masson L, et al. (1997) Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. Proc Natl Acad Sci USA 94: 12780-12785.
54. Morin S, Henderson S, Fabrick JA, Carrière Y, Dennehy TJ, et al. (2004) DNA-based detection of Bt resistance alleles in pink bollworm. Insect Biochem Mol Biol 34: 1225-1233.
55. Tabashnik BE, Dennehy TJ, Sims MA, Larkin K, Head GP, et al. (2002) Control of resistant pink bollworm by transgenic cotton with Bacillus thuringiensis toxin Cry2Ab. Appl Environ Microbiol 68: 3790-3794.