Binding site alteration is responsible for field-isolated resistance to bacillus thuringiensis Cry2A insecticidal proteins in two Helicoverpa species

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Caccia, Silvia ^a   Hernández Rodríguez, Carmen Sara ^a   Mahon, Rod J ^b   Downes, Sharon ^b   William, James ^b   Bautsoens, Nadine ^c   van Rie, Jeroen ^c   Ferré, Juan ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b CSIRO   (Australia)

^c Bayer sa nv Belgium   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

INSECT PROTEIN; PROTEIN CRY2A; PROTEIN CRY2B; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; INSECTICIDE;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIUM ISOLATE; BINDING AFFINITY; BINDING SITE; BIOASSAY; CONTROLLED STUDY; CROSS RESISTANCE; HELICOVERPA ARMIGERA; HELICOVERPA PUNCTIGERA; INSECTICIDE RESISTANCE; LEPIDOPTERA; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; CROP; DRUG EFFECT; GENETICS; PARASITOLOGY; PATHOGENICITY; PROTEIN BINDING;

BACILLUS THURINGIENSIS; GOSSYPIUM HIRSUTUM; HELICOVERPA; HELICOVERPA ARMIGERA; HELICOVERPA PUNCTIGERA; HEXAPODA;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BINDING SITES; CROPS, AGRICULTURAL; INSECTICIDE RESISTANCE; INSECTICIDES; LEPIDOPTERA; PROTEIN BINDING;

EID: 77956301012     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009975     Document Type: Article

References (56)

1. Nester EW, Thomashow LS, Metz M, Gordon M (2002) 100 years of Bacillus thuringiensis: a critical scientific assessment. American Academy of Microbiology (Washington DC).
2. James C (2009) Global status of commercialized Biotech/GM crops: 2009. ISAAA Briefs 41-2009 (International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY).
3. Tabashnik BE, Van Rensburg JBJ, Carrière Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102: 2011-2025.
4. Roush RT (1998) Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil Trans R Soc Lond B 353: 1777-1786.
5. Ferré J, Van Rie J (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47: 501-533.
6. Ferré J, Van Rie J, MacIntosh SC (2008) Insecticidal genetically modified crops and insect resistance management (IRM). In: Romeis J, Shelton AM, Kennedy GG, eds. Integration of insect resistant genetically modified crops within IPM programs. New York: Springer. pp 41-85.
7. English L, Robbins HL, Von Tersch MA, Kulesza CA, Ave D, et al. (1994) Mode of action of CryIIA: a Bacillus thuringiensis delta-endotoxin. Insect Biochem Mol Biol 24: 1025-1035.
8. Luo S, Wu K, Tian Y, Liang G, Feng X, et al. (2007) Cross-resistance studies of Cry1Ac-resistant strains of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry2Ab. J Econ Entomol 100: 909-915.
9. Hernández-Rodríguez CS, Van Vliet A, Bautsoens N, Van Rie J, Ferré J (2008) Specific binding of Bacillus thuringiensis Cry2A insecticidal proteins to a common site in the midgut of Helicoverpa species. Appl Environ Microbiol 74: 7654-7659.
10. Van Rensburg JBJ (2007) First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S African J Plant Soil 24: 147-151.
11. Matten SR, Head GP, Quemada HD (2008) How governmental regulation can help or hinder the integration of Bt crops within IPM programs. In: Romeis J, Shelton AM, Kennedy GG, eds. Integration of insect resistant genetically modified crops within IPM programs. New York: Springer. Pp 27-39.
12. Ali MI, Lutrell RG (2007) Susceptibility of bollworm and tobacco budworm (Lepidoptera: Noctuidae) to Cry2Ab2 insecticidal protein. J Econ Entomol 100: 921-931.
13. Tabashnik BE, Gassmann AJ, Crowder DW, Carrier Y (2008) Insect resistance to Bt crops: evidence versus theory. Nature Biotechnol 26: 199-202.
14. Moar W, Roush R, Anthony S, Ferré J, MacIntosh S, et al. (2008) Field-evolved resistance to Bt toxins. Nature Biotechnol 26: 1072-1074.
15. Tabashnik BE, Gassmann AJ, Crowder DW, Carrier Y (2008) Field-evolved resistance to Bt toxins. Nature Biotechnol 26: 1074-1076.
16. Mahon RJ, Olsen KM, Downes S, Addison S (2007) Frequency of alleles conferring resistance to the Bt toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 100: 1844-1853.
17. Downes S, Parker TL, Mahon RJ (2009) Frequency alleles conferring resistance to the Bacillus thuringiensis toxin Cry1Ac and Cry2Ab in Australian populations of Helicoverpa punctigera (Lepidoptera: Noctuidae) from 2002 to 2006. J Econ Entomol 100: 1844-1853.
18. Ferré J, Real DM, Van Rie J, Jansens S, Peferoen M (1991) Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in a midgut membrane receptor. Proc Natl Acad Sci USA 88: 5119-5123.
19. Sayyed AH, Haward R, Herrero S, Ferré J, Wright DJ (2000) Genetic and biochemical approach for characterization of resistance to Bacillus thuringiensis toxin Cry1Ac in a field population of the diamondback moth, Plutella xylostella. Appl Environ Microbiol 66: 1509-1516.
20. Sayyed AH, Raymond B, Ibiza-Palacios MS, Escriche B, Wright DJ (2004) Genetic and biochemical characterization of field evolved resistance to Bacillus thuringiensis toxin Cry1Ac in diamondback moth, Plutella xylostella. Appl Environ Microbiol 70: 1710-1717.
21. Sayyed AH, Gatsi R, Ibiza-Palacios MS, Escriche B, Wright DJ, et al. (2005) Common, but complex, mode of resistance of Plutella xylostella to Bacillus thuringiensis toxins Cry1Ab and Cry1Ac. Appl Environ Microbiol 71: 6863-6869.
22. Tabashnik BE, Finson N, Groeters FR, Moar WJ, Johnson MW, et al. (1994) Reversal of resistance to Bacillus thuringiensis in Plutella xylostella. Proc Natl Acad Sci USA 10: 4120-4124.
23. Tabashnik BE, Liu YB, 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.
24. Wang P, Zhao JZ, Rodrigo-Simón A, Kain W, Janmaat AF, et al. (2007) Mechanism of resistance to Bacillus thuringiensis toxin Cry1Ac in a greenhouse population of cabbage looper, Trichoplusia ni. Appl Environ Microbiol 73: 1199-1207.
25. Wright DJ, Iqbal M, Granero F, Ferré J (1997) A change in a single midgut receptor in Plutella xylostella is only in part responsible for field resistance to Bacillus thuringiensis subspp. kurstaki and aizawai. Appl Environ Microbiol 63: 1814-1997.
26. Mahon RJ, Olsen KM, Garsia KA, Young SR (2007) Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. J Econ Entomol 100: 894-902.
27. Downes S, Parker TL, Mahon RJ (2009) Characteristics of resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa punctigera (Wallengren) (Lepidoptera: Noctuidae) isolated from a field population. J Econ Entomol, In press.
28. Bird LJ, Akhurst RJ (2007) Effects of host plant species on fitness costs of Bt resistance in Helicoverpa armigera (Lepidoptera: Noctuidae). Biol Control 40: 196-203.
29. Mahon RJ, Olsen KM, Downes S (2008) Isolations of Cry2Ab resistance in Australian populations of Helicoverpa armigera (Lepidoptera, Noctuidae) are allelic. J Econ Entomol 101: 909-914.
30. Gould F, Martínez-Ramírez A, Anderson A, Ferré J, Silva FJ, et al. (1992) Broad-spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens. Proc Natl Acad Sci USA 89: 7986-7990.
31. Jurat-Fuentes JL, Gould FL, Adang MJ (2003) Dual resistance to Bacillus thuringiensis Cry1Ac and Cry2Aa toxins in Heliothis virescens suggests multiple mechanisms of resistance. Appl Environ Microbiol 69: 5898-5906.
32. Gao Y, Wu K, Gould F, Shen Z (2009) Cry2Ab tolerance response of Helicoverpa armigera (Lepidoptera, noctuidae) populations from Cry1Ac cotton planting region. J Econ Entomol 102: 1217-1223.
33. Gonzàlez-Cabrera J, Escriche B, Tabashnik BE, Ferrè J(2003) Binding of Bacillus thuringiensis toxins in resistant and susceptible strains of pink bollworm (Pectinophora gossypiella). Insect Biochem Mol Biol 33: 929-935.
34. 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.
35. Van Rie J, Jansens S, Höfte H, Degheele D, Van Mellaert H (1990) Receptors on the brush border membrane of the insect midgut as determinants of the specificity of Bacillus thuringiensis delta-endotoxins. Appl Environ Microbiol 56: 1378-1385.
36. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, et al. (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62: 775-806.
37. Van Rie J, McGaughey WH, Johnson DE, Barnett BD, Van Mellaert H (1990) Mechanism of insect resistance to the microbial insecticide Bacillus thuringiensis. Science 247: 72-74.
38. Herrero S, Oppert B, Ferré J (2001) Different mechanisms of resistance to Bacillus thuringiensis toxins in the Indianmeal moth. Appl Environ Microbiol 67: 1085-1089.
39. Lee MK, Rajamohan F, Gould F, Dean DH (1995) Resistance to Bacillus thuringiensis CryIA d-endotoxins in a laboratory-selected Heliothis virescens strain is related to receptor alteration. Appl Environ Microbiol 61: 3836-3842.
40. Akhurst RJ, James W, Bird LJ, Beard C (2003) Resistance to the Cry1Ac deltaendotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 96: 1290-1299.
41. Granero F, Ballester V, Ferré J (1996) Bacillus thuringiensis crystal proteins Cry1Ab and Cry1Fa share a high affinity binding site in Plutella xylostella (L.). Biochem Biophys Res Commun 224: 779-783.
42. Jurat-Fuentes JL, Adang MJ (2001) Importance of Cry1 d-endotoxin domain II loops for binding specificity in Heliothis virescens (L.). Appl Environ Microbiol 67: 323-329.
43. Gahan LJ, Gould F, Heckel DG (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293: 857-860.
44. 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.
45. Baxter SW, Zhao J-Z, Gahan LJ, Shelton AM, Tabashnik BE, et al. (2005) Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol Biol 14: 327-334.
46. Baxter SW, Zhao J-Z, Gahan LJ, Shelton AM, Vogel H, et al. (2008) Genetic mapping of Bt-toxin binding proteins in a Cry1A-toxin resistant strain of diamondback moth Plutella xylostella. Insect Biochem Mol Biol 38: 125-135.
47. Yang Y, Chen H, Wu S, Yang Y, Xu X, et al. (2006) Identification and molecular detection of a deletion mutation responsible for a truncated cadherin of Helicoverpa armigera. Insect Biochem Mol Biol 36: 735-740.
48. 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.
49. LeOra Software (2008) POLO-PC. LeOra software, Berkeley, CA.
50. Convents D, Houssier C, Lasters I, Lauwereys M (1990) The Bacillus thuringiensis δ-endotoxin: evidence for a two domain structure of the minimal toxic fragment. J Biol Chem 265: 1369-1375.
51. Crickmore N, Ellar DJ (1992) Involvement of a possible chaperonin in the efficient expression of a cloned CryIIA d-endotoxin gene in Bacillus thuringiensis. Mol Microbiol 6: 1533-1537.
52. Hernández CS, Rodrigo A, Ferré J (2004) Lyophilization of lepidopteran midguts: a preserving method for Bacillus thuringiensis toxin binding studies. J Invertebr Pathol 85: 182-187.
53. Wolfersberger MG, Lüthy P, Maurer P, Parenti P, Sacchi VF, et al. (1987) Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comp Biochem Physiol 86: 301-308.
54. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem J 72: 248-254.
55. Van Rie J, Jansens S, Höfte H, Degheele D, Van Mellaert H (1989) Specificity of Bacillus thuringiensis d-endotoxins: importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur J Biochem 186: 239-247.
56. Munson P, Rodbard D (1980) LIGAND: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem 107: 220-239.