Shared Midgut Binding Sites for Cry1A.105, Cry1Aa, Cry1Ab, Cry1Ac and Cry1Fa Proteins from Bacillus thuringiensis in Two Important Corn Pests, Ostrinia nubilalis and Spodoptera frugiperda

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Hernández Rodríguez, Carmen Sara ^a   Hernández Martínez, Patricia ^a   Van Rie, Jeroen ^b   Escriche, Baltasar ^a   Ferré, Juan ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b Bayer Cropscience Belgium   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CRY1AB TOXIN; CRY1AC TOXIN; IODINE 125; PROTEIN CRY1A 105; PROTEIN CRY1AA; PROTEIN CRY1FA; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS THURINGIENSIS; BINDING AFFINITY; BINDING COMPETITION; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ISOTOPE LABELING; LARVA; MAIZE; MEMBRANE VESICLE; MIDGUT; NONHUMAN; OSTRINIA NUBILALIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SPODOPTERA FRUGIPERDA; TRANSGENIC PLANT;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BINDING, COMPETITIVE; COATED VESICLES; DISEASE SUSCEPTIBILITY; GASTROINTESTINAL TRACT; KINETICS; LARVA; MICROVILLI; MOTHS; PROTEIN BINDING; RECOMBINANT PROTEINS; SPODOPTERA; ZEA MAYS;

BACILLUS THURINGIENSIS; HEXAPODA; OSTRINIA NUBILALIS; SPODOPTERA FRUGIPERDA; ZEA MAYS;

EID: 84879803152     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068164     Document Type: Article

References (65)

1. Shelton AM, Zhao JZ, Roush RT, (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu Rev Entomol 47: 845-881.
2. Ferré J, Van Rie J, MacIntosh SC (2008) Insecticidal genetically modified crops and insect resistance management (IRM). In: Romeis J, Shelton AM, Kennedy GG, editors. Integration of Insect-Resistant Genetically Modified Crops within IPM Programs. Dordrecht: Springer. 41-85.
3. James C (2012) Global status of commercialized biotech/GM crops: 2012. ISAAA Brief No. 44. ISAAA: Ithaca, New York.
4. Roush RT, (1998) Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos Trans R Soc Lond B Biol Sci 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. Zhao JZ, Cao J, Li Y, Collins HL, Roush RT, et al. (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat Biotechnol 21: 1493-1497.
7. Storer NP, Thompson GD, Head GP, (2012) Application of pyramided traits against Lepidoptera in insect resistance management for Bt crops. GM Crops Food 3: 3-9.
8. Environmental Protection Agency (2010) Bacillus thuringiensis Cry1A.105 and Cry2Ab2 insecticidal proteins and the genetic material necessary for their production in corn. Biopesticide Registration Action Document. Available: http://www.epa.gov/oppbppd1/biopesticides/pips/mon-89034-brad.pdf. Accessed 2013 Jun.
9. de Maagd RA, Bravo A, Crickmore N, (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17: 193-199.
10. Environmental Protection Agency (2009) MON 89034 x TC1507 x MON 88017 x DAS-59122-7. Available: http://www.epa.gov/oppbppd1/biopesticides/pips/smartstax-factsheet.pdf. Accessed 2013 Jun.
11. Vaeck M, Reynaerts A, Höfte H, Jansens S, de Beuckeleer M, et al. (1987) Transgenic plants protected from insect attack. Nature 327: 33-37.
12. Bates SL, Zhao JZ, Roush RT, Shelton AM, (2005) Insect resistance management in GM crops: past, present and future. Nat Biotechnol 23: 57-62.
13. Ballester V, Granero F, Tabashnik BE, Malvar T, Ferré J, (1999) Integrative model for binding of Bacillus thuringiensis toxins in susceptible and resistant larvae of the diamondback moth (Plutella xylostella). Appl Environ Microbiol 65: 1413-1419.
14. González-Cabrera J, Escriche B, Tabashnik BE, Ferré J, (2003) Binding of Bacillus thuringiensis toxins in resistant and susceptible strains of pink bollworm (Pectinophora gossypiella). Insect Biochem Mol Biol 33: 929-935.
15. Lee MK, Rajamohan F, Gould F, Dean DH, (1995) Resistance to Bacillus thuringiensis CryIA δ-endotoxins in a laboratory-selected Heliothis virescens strain is related to receptor alteration. Appl Environ Microbiol 61: 3836-3842.
16. Caccia S, Hernández-Rodríguez CS, Mahon RJ, Downes S, James W, et al. (2010) Target site alteration is responsible for field-derived resistance to Bacillus thuringiensis Cry2A insecticidal proteins in Helicoverpa spp. PLoS ONE 5: e9975.
17. Hernández-Martínez P, Hernández-Rodríguez CS, Krishnan V, Crickmore N, Escriche B, et al. (2012) Lack of Cry1Fa binding to the midgut brush border membrane in a resistant colony of Plutella xylostella with a mutation in the ABCC2 locus. Appl Environ Microbiol 78: 6759-6761.
18. 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.
19. Gouffon C, Van Vliet A, Van Rie J, Jansens S, Jurat-Fuentes JL, (2011) Binding sites for Bacillus thuringiensis Cry2Ae toxin on heliothine brush border membrane vesicles are not shared with Cry1A, Cry1F, or Vip3A toxin. Appl Environ Microbiol 77: 3182-3188.
20. Gould F, Anderson A, Reynolds A, Bumgarner L, Moar WJ, (1995) Selection and genetic analysis of Heliothis virescens (Lepidoptera: Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. J Econ Entomol 88: 1545-1559.
21. Oppert B, Ellis RT, Babcock J, (2010) Effects of Cry1F and Cry34Ab1/35Ab1 on storage pests. J Stored Prod Res 46: 143-148.
22. Tabashnik BE, Finson N, Johnson MW, Heckel DG, (1994) Cross-resistance to Bacillus thuringiensis toxin CryIF in the diamondback moth (Plutella xylostella). Appl Environ Microbiol 60: 4627-4629.
23. 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.
24. Jurat-Fuentes JL, Adang MJ, (2001) Importance of Cry1 δ-endotoxin domain II loops for binding specificity in Heliothis virescens (L.). Appl Environ Microbiol 67: 323-329.
25. Hernández CS, Ferré J, (2005) Common receptor for Bacillus thuringiensis toxins Cry1Ac, Cry1Fa, and Cry1Ja in Helicoverpa armigera, Helicoverpa zea, and Spodoptera exigua. Appl Environ Microbiol 71: 5627-5629.
26. Luo K, Banks D, Adang MJ, (1999) Toxicity, binding, and permeability analyses of four Bacillus thuringiensis Cry1 delta-endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Appl Environ Microbiol 65: 457-464.
27. Wyniger R (1974) Insektenzucht. Methoden der Zucht und Haltung von Insektenund Milben im Laboratorium, Stuttgart: Verlag Eugen Ulmer.
28. Bell RA, Joachim FG, (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Amer 69: 365-373.
29. Herrero S, González-Cabrera J, Ferré J, Bakker PL, de Maagd R, (2004) Mutations in the Bacillus thuringiensis Cry1Ca toxin demonstrate the role of domains II and III in specificity towards Spodoptera exigua larvae. Biochem J 384: 507-513.
30. Ferré J, Real MD, Van Rie J, Jansens J, Peferoen SM, (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.
31. Finney DJ (1971) Probit analysis. London: Cambridge University Press.
32. Van Rie J, Jansens S, Höfte H, Degheele D, Van Mellaert H, (1989) Specificity of Bacillus thuringiensis δ-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur J Biochem 186: 239-247.
33. Hernández-Rodríguez CS, Hernández-Martínez P, Van Rie J, Escriche B, Ferré J, (2012) Specific binding of radiolabeled Cry1Fa insecticidal protein from Bacillus thuringiensis to midgut sites in lepidopteran species. Appl Environ Microbiol 78: 4048-4050.
34. Wolfersberger MG, Luethy 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 86A: 301-308.
35. 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 72: 248-254.
36. Munson P, Rodbard D, (1980) LIGAND: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem 107: 220-239.
37. Bravo A, (1997) Phylogenetic relationships of Bacillus thuringiensis δ-endotoxin family proteins and their functional domains. J Bacteriol 179: 2793-2801.
38. Herrero S, Borja M, Ferré J, (2002) Extent of variation of the Bacillus thuringiensis toxin reservoir: the case of the geranium bronze, Cacyreus marshalli Butler (Lepidoptera: Lycaenidae). Appl Environ Microbiol 68: 4090-4094.
39. Bosch DR, Schipper B, van der Kleij H, de Maagd R, WStiekema WJ, (1994) Recombinant Bacillus thuringiensis crystal proteins with new properties: Possibilities for resistance management. Bio/Technol 12: 915-918.
40. de Maagd RA, Kwa MSG, van der Klei H, Yamamoto T, Schipper B, et al. (1996) Domain III substitution in Bacillus thuringiensis delta-endotoxin CryIA(b) results in superior toxicity for Spodoptera exigua and altered membrane protein recognition. Appl Environ Microbiol 62: 1537-1543.
41. Vachon V, Laprade R, Schwartz JL, (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: A critical review. J Invertebr Pathol 111: 1-12.
42. 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.
43. de Maagd RA, Bakker PL, Masson L, Adang MJ, Sangadala S, et al. (1999) Domain III of the Bacillus thuringiensis delta-endotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and to its purified aminopeptidase N. Molec Microbiol. 31: 463-471.
44. Lee MK, Young BA, Dean DH, (1995) Domain III exchanges of Bacillus thuringiensis CryIA toxins affect binding to different gypsy moth midgut receptors. Biochem Biophys Res Commun 216: 306-312.
45. Gómez I, Arenas I, Benitez I, Miranda-Ríos J, Becerril B, et al. (2006) Specific epitopes of domains II and III of Bacillus thuringiensis Cry1Ab toxin involved in the sequential interaction with cadherin and aminopeptidase-N receptors in Manduca sexta. J Biol Chem 281: 34032-34039.
46. González-Cabrera J, Farinós GP, Caccia S, Díaz-Mendoza M, Castañera P, et al. (2006) Toxicity and mode of action of Bacillus thuringiensis Cry proteins in the Mediterranean corn borer, Sesamia nonagrioides (Lefebvre). Appl Environ Microbiol 59: 1828-1837.
47. Sena JA, Hernández-Rodríguez CS, Ferré J, (2009) Interaction of Bacillus thuringiresis Cry1 and Vip3A proteins with Spodoptera frugiperda midgut binding sites. Appl Environ Microbiol 75: 2236-2237.
48. 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: 12780-85.
49. Jurat-Fuentes JL, Gould F, Adang MJ, (2002) Altered glycosylation of 63- and 68-kilodalton microvillar proteins in Heliothis virescens correlates with reduced Cry1 toxin binding, decreased pore formation, and increased resistance to Bacillus thuringiensis Cry1 toxins. Appl Environ Microbiol. 68: 5711-5717.
50. Tabashnik BE, Liu YB, Finson N, Masson L, Heckel DG, (1997) One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proc Natl Acad Sci USA 94: 1640-1644.
51. Thompson MA, Schnepf HE, Feitelson JS, (1995) Structure, function and engineering of Bacillus thuringiensis toxins. Genet Eng. 17: 99-117.
52. Denolf P, Jansens S, Peferoen M, Degheele D, Van Rie J, (1993) Two different Bacillus thuringiensis Delta-endotoxin receptors in the midgut brush border membrane of the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae). Appl Environ Microbiol 59: 1828-1837.
53. Li H, González-Cabrera J, Oppert B, Ferré J, Higgins RA, et al. (2004) Binding analyses of Cry1Ab and Cry1Ac with membrane vesicles from Bacillus thuringiensis-resistant and-susceptible Ostrinia nubilalis. Biochem Biophys Res Commun 323: 52-57.
54. Hua G, Masson L, Jurat-Fuentes JL, Schwab G, Adang MJ, (2001) Binding analyses of Bacillus thuringiensis Cry δ-endotoxins using brush border membrane vesicles of Ostrinia nubilalis. Appl Environ Microbiol 67: 872-879.
55. Rang C, Bergvingson D, Bohorova N, Hoisington D, Frutos R, (2004) Competition of Bacillus thuringiensis Cry1 toxins for midgut binding sites: a basis for the development and management of transgenic tropical maize resistant to several stemborers. Curr Microbiol 49: 22-27.
56. Siqueira HAA, González-Cabrera J, Ferré J, Flannagan R, Siegfried BD, (2006) Analyses of Cry1Ab binding in resistant and susceptible strains of the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae). Appl Environ Microbiol 72: 5318-5324.
57. Crespo ALB, Rodrigo-Simón A, Siqueira HAA, Pereira EJG, Ferré J, et al. (2011) Cross-resistance and mechanism of resistance to Cry1Ab toxin from Bacillus thuringiensis in a field-derived strain of European corn borer, Ostrinia nubilalis. J Invertebr Pathol 107: 185-192.
58. Pereira EJG, Lang BA, Storer NP, Siegfried BD, (2008) Selection for Cry1F resistance in the European corn borer and cross-resistance to other Cry toxins. Entomol Exper Appl 126: 115-121.
59. Siqueira HAA, Moellenbeck D, Spencer T, Siegfried BD, (2004) Cross-resistance of Cry1Ab-selected Ostrinia nubilalis (Lepidoptera: Crambidae) to Bacillus thuringiensis δ-endotoxins. J Econ Entomol 97: 1049-1057.
60. Pereira EJG, Siqueira HAA, Zhuang M, Storer NP, Siegfried BD, (2010) Measurements of Cry1F binding and activity of luminal proteases in susceptible and Cry1F resistant Ostrinia nubilalis larvae (Lepidoptera: Crambidae). J Invertebr Pathol 103: 1-7.
61. Coates BS, Sumerford DV, Lopez MD, Wang H, Fraser LM, et al. (2011) A single major QTL controls expression of larval Cry1F resistance trait in Ostrinia nubilalis (Lepidoptera: Crambidae) and is independent of midgut receptor genes. Genetica 139: 961-972.
62. Wu X, Leonard BR, Zhu YC, Abel CA, Head GP, et al. (2009) Susceptibility of Cry1Ab-resistant and-susceptible sugarcane borer (Lepidoptera: Crambidae) to four Bacillus thuirngiensis toxins. J Invertebr Pathol 100: 29-34.
63. Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, et al. (2010) Discovery and characterization of field resistance to Bt maize: in Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103: 1031-1038.
64. Storer NP, Kubiszak ME, King JE, Thompson GD, Santos AC, (2012) Status of Resistance to Bt maize in Spodoptera frugiperda: Lessons from Puerto Rico. J Invertebr Pathol 110: 294-300.
65. Jakka SRK, Oppert C, Blanco C, Portilla M, Jurat-Fuentes JL (2011) Characterization of field-evolved resistance to transgenic Bt corn in Spodoptera frugiperda. Proceedings of the 2011 International Congress on Invertebrate Pathology and Microbial Control, OCDE Symposium on Disease in Aquatic Crustaceans and 44th Annual Meeting of the Society for Invertebrate Pathology. August 7-11, Halifax, Nova Scotia, Canada.