Insecticidal Proteins of Bacillus Thuringiensis and Their Application in Agriculture

  • P. Ananda Kumar
  • O. M. Bambawale


The insecticidal bacterium Bacillus thuringiensis (Bt) is the most commercially successful biological control agent of insect pests (Glare and O’Callaghan, 2000). Bt is a ubiquitous soil bacterium isolated from soil, stored grain, insect cadavers and the phylloplane (plant surface) (Martin and Travers, 1989). Thus, three prevailing niches of Bt can be envisaged viz., as an entomopathogen, as a phylloplane inhabitant and as a soil microorganism. Bt is a gram-positive, aerobic, endosporeforming bacterium belonging to morphological group I along with Bacillus cereus, Bacillus anthracis, and Bacillus laterosporus (Parry et al., 1983). All these bacteria have endospores. Bt, however, is recognized by its parasporal body (known as the crystal) that is proteinaceous in nature and possesses insecticidal properties. The parasporal body comprises of crystals varying in size, shape and morphology (Figure 1). Bt does not have a significant history of mammalian pathogenicity, and research has concentrated on the insecticidal nature of the crystal proteins, especially Sendotoxins. Considerable amount of information with respect to various aspects of Bt such as fermentation (Bryant, 1994), biology and genetics (Aronson et al., 1986), molecular biology (Hofte and Whiteley, 1989; Kumar et al., 1996; Schnepf et al., 1998), mechanism of action (Knowles, 1994), application as biopesticide (Federici, 1999), and Bt transgenic plants (Schuler et al., 1998; de Maagd et al., 1999) is available. The classification and nomenclature of Bt toxins has been recently described (Crickmore et al., 1998). To date, more than 100 different genes encoding crystal proteins have been cloned from Bt and two other species (Schnepf et al., 1998). Recent information about Bt proteins/genes can be obtained from


Transgenic Plant Bacillus Thuringiensis Crystal Protein Transgenic Crop Diamondback Moth 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alstad, D. N., and Andow, D. A., 1995, Managing the evolution of insect resistance to transgenic plants, Science 268: 1894–1896.PubMedCrossRefGoogle Scholar
  2. Aronson, A.I, Beckman, W., and Dunn. P., 1986, Bacillus thuringiensis and related insect pathogens, Microbiol. Rev. 50: 1–24.Google Scholar
  3. Arpaia, S., Chiriatti, K., and Gioro, G., 1998, Predicting the adaptation of Colorado potato beetle to transgenic eggplants expressing CryIll toxin: the role of gene dominance, migration and fitness cost, J. Econ. Entomol. 91: 21–29.Google Scholar
  4. Bar, E., Lieman-Hurwitz, J., Rahamim, E., Keynan, E., and Sandler, N., 1991, Cloning and expression of Bacillus thuringiensis israelensis S-endotoxin in B.sphaericus, J. Invertebr. Pathol. 57: 149–158.PubMedCrossRefGoogle Scholar
  5. Barton, K. A., Whiteley H. R., and Yang N. S., 1987, Bacillus thuringiensis 5-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to lepidopteran insects, Plant Physiol. 85: 1103–1109.Google Scholar
  6. Baum, J. A., Coyle, D.M., Gilbert, M.P., Jany, C.S., and Gawron -Burke, C., 1990, Novel cloning vectors for Bacillus thuringiensis, Appl. Environ. Microbiol. 56: 3420–3428.PubMedGoogle Scholar
  7. Baum, J.A., Johnson, T.B., and Carlton, B.C, 1998, Natural and recombinant bioinsecticide products. in: Biopesticides: Use and Delivery, F. R. Hall and J. J. Menn, ed., Humana Press, Totowa, pp. 189–209.CrossRefGoogle Scholar
  8. Becker, N., and Margalit, J., 1993, Use of Bacillus thuringiensis israelensis against mosquitoes and blackflies, in: Bacillus thuringiensis, An Environmental Biopesticide: Theory and Practice, Entwistle, P. F., Cory, P. F., Margalit, M. J. and Higgs, S., eds, John. Wiley & Sons, New York, pp. 145–170.Google Scholar
  9. Berliner, E.,1915, Uber die Schaffsucht der Mehimottenraupe, Z. Angew. Entomol.2: 29–56.Google Scholar
  10. Bezdicek, D. F., Quinn, M. A., Forse, L., Heron, D., and Kahn, M. L., 1994, Insecticidal activity and competitiveness of Rhizobium spp containing the Bacillus thuringiensis subsp tenebrionis 8-endotoxin gene (cry III) in legume nodules, Soil Biol. Biochem. 26: 1637–1646.CrossRefGoogle Scholar
  11. Bora, R. S., Murthy, M. G., Shenbagarathai, R., and Sekar, V., 1994, Introduction of a lepidopteran-specific insecticidal crystal protein gene of Bacillus thuringiensis subsp kurstaki by conjugal transfer into a Bacillus megaterium strain that persists in the cotton phyllosphere, Appl. Environ. Microbiol. 60: 214–222.PubMedGoogle Scholar
  12. Boucias, D.G., and Pendiand, J.C., 1998, Principles oflnsect Pathology, Kluwer, Norwell, Massachusetts.Google Scholar
  13. Bravo, A., Jansens, S., and Peferoen, M., 1992, Immunocytochemical localization of Bacillus thuringiensis crystal proteins intoxicated insects, J. Invert. Pathol. 60: 237–246.CrossRefGoogle Scholar
  14. Bryant, J.E., 1994, Commercial production and formulation of Bacillus thuringiensis, Agric. Eco. Environ. 49: 31–35CrossRefGoogle Scholar
  15. Cao, J., Tang, J. D., Strizhov, N., Shelton, A. M., and Earle, E. D., 1999, Transgenic broccoli with high levels of Bacillus thuringiensis CrylA or Cry 1C protein control diamondback moth larvae resistant to Cry IA or Cry1C, Mol. Breed. 5: 131–141.CrossRefGoogle Scholar
  16. Caprio, M. A., 1998, Evaluating resistance management strategies for multiple toxins in the presence of external refuges, J. Econ. Entomol. 91: 1021–1031.Google Scholar
  17. Carlson, C. R., and Kolsto, A.B., 1993, A complete physical map of a Bacillus thuringiensis chromosome, J. Bacteriol. 175: 1053–1060.PubMedGoogle Scholar
  18. Carozzi, N. B., Kramer, V. C., Warren G. W., Evola, S., and Koziel, M. G., 1991, Prediction of insecticidal activity of Bacillus thuringiensis strains by polymerase chain reaction product profiles, Appl. Environ. Microbiol. 57: 3057–3061.PubMedGoogle Scholar
  19. Carozzi, N. B., Warren, G. W., Desai, N., Jayne, S. M., Lotstein, R., Rice, D. A., Evola, S., and Koziel, M. G., 1992, Expression of a chimeric CaMV 35S Bacillus thuringiensis insecticidal protein gene in transgenic tobacco, Plant. Mol. Biol. 20: 538–539.CrossRefGoogle Scholar
  20. Chakrabarti, S.K., Mandaokar, A., Pattanayak, D., Shukla, A., Naik, P.S., Sharma, R.P., and Kumar, P.A., 2000, Bacillus thuringiensis crylAb gene confers resistance to potato against Helicoverpa armigera Hubner, Potato Res. 42: 227–23 8.Google Scholar
  21. Cheng, X., Sardana, R., Kaplan, H., and Altosaar, I., 1998, Agrobacterium-transformed rice plants expressing synthetic cry 1A(b) and crylA(c) genes are highly toxic to striped stem borer and yellow stem borer, Proc. Natl. Acad. Sci. USA. 95: 2767–2772.PubMedCrossRefGoogle Scholar
  22. Crickmore, N., Zeigler, D.R., Feitelson, J., Schnepf, E., Van Rie, J., Lereclus, D., Baum, J., and Dean, D.H., 1998, Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins, Microbiol. Mol. Biol. Rev. 62: 807–813.PubMedGoogle Scholar
  23. Curtis, C. F., 1985, Theoretical models of the use of insecticide mixtures for the management of resistance, Bull. Entomol. Res. 75: 259–265.CrossRefGoogle Scholar
  24. De Barjac, H., and Bonnefoi, A., 1962, Essai de classification biochimique et serologique de 24 sources de bacillus du type B. thuringiensis, Entomophaga 7: 5–31.CrossRefGoogle Scholar
  25. De Cosa, B., Moar, W., Lee, S. B., Miller, M., and Daniell, H., 2001, Over expression of the Bt ciy2Aa2 operan in chloroplasts leads to formation of insecticidal crystals, Nature Biotechnol. 19: 71–74.CrossRefGoogle Scholar
  26. Delecluse, A., Bourgouin, A., Klier, A., and Rapoport, G., 1989, Nucleotide sequence and characterization of a new insertion element IS 240 from Bacillus thuringiensis israelensis, Plasmid 21: 71–78.PubMedCrossRefGoogle Scholar
  27. Delecluse, A., Rosso, M. L., and Ragni, A., 1995, Cloning and expression of a novel toxin gene from Bacillus thuringiensis subsp. Jegathesan encoding a highly mosquitocidal protein, Appl. Environ. Microbiol.61: 4230–4235.Google Scholar
  28. de Maagd, R.A., Bravo, A., and Crickmore, N., 2001, How Bacillus thuringiensis has evolved specific toxins to colonize the insect world, Trends Genet.17: 193–199.Google Scholar
  29. de Maagd, R. A., Bosch, D., and Stiekema, W., 1999, Bacillus thuringensis toxin-mediated insect resistance in plants, Trends Plant Sci. 4: 9–13.Google Scholar
  30. Dulmage, H.T., 1970, Insecticidal activity of HD-1, a new isolate of Bacillus thuringiensis var alesti, J. Invertebr. Pathol. 15: 232–239.CrossRefGoogle Scholar
  31. English, L., Robbins, H.L., Von Tersch, M., Kulesza, C.A., Ave, D., Coule, D., Jany, C.S., and Slatin,S.L., 1994, Mode of action of CryIIA: a Bacillus thuringiensis delta endotoxin, Insect Biochem. Molec. Biol. 24: 1025–1035.CrossRefGoogle Scholar
  32. Federici, B.A., 1999, Bacillus thuringiensis in biological control, in: Handbook of Biological Control, Academic Press, New York, pp. 575–593.Google Scholar
  33. Federici, B. A. and Bauer, L. S., 1998, CytlAa protein of Bacillus thuringiensis is toxic to the cotton-wood leaf beetle, Chrysomela scripta, and suppresses high levels of resistance to Cry3Aa, Appl. Environ. Microbiol. 64: 4368–4371.PubMedGoogle Scholar
  34. Feitelson, J. S., Payne, J., and Kim, L., 1992, Bacillus thuringiensis: insects and beyond, Bio/Technol. 10: 271–275.Google Scholar
  35. Ferre, J., Real, M. D., van Rie, J., Jansens, S., and Peferoen, M., 1991, Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in midgut membrane receptor, Proc. Natl. Acad. Sci. USA 88: 5119–5123.PubMedCrossRefGoogle Scholar
  36. Fischhof, D. A., Bowdisch, K.S., Perlak, F. J., Marrone, P.G., McCormick, S. H., Niedermeyer, J. G., Dean, D. A., Kusano-Kretzmer, K., Mayer, E. J., Rochester, D. E., Rogers, S. G., and Fraley, R. T., 1987, Insect tolerant transgenic tomato plants, Bio/Technol. 5: 807–813.CrossRefGoogle Scholar
  37. Forcada, C., Alacer, E., Garcera, M. D., and Martinez, R., 1996, Differences in the midgut proteolytic activity of two Heliothis virescens strains, one susceptible and one resistant to Bacillus thuringiensis toxins, Arch. Insect Biochem. Physiol. 31: 257–272.CrossRefGoogle Scholar
  38. Fox, J.L., 1998, Science panel urges EPA to mandate Bt resistance management, ASMNews 64: 379–380.Google Scholar
  39. Frutos, R., Rang, C., and Royer, M., 1999, Managing Insect resistance to plants producing Bacillus thuringiensis toxins, Grit. Rev. Biotech. 19: 227–276.CrossRefGoogle Scholar
  40. Gaertner, F. H., Quick T. C., and Thompson M. A., 1993, CelICap: an encapsulation system for insecticidal biotoxin proteins, in: Advanced Engineered Pesticides, L. Kim, ed., Marcel Dekker, New York, pp. 73–83.Google Scholar
  41. Gamel, P. H., and Piot, J. C., 1992, Characterization and properties of a novel plasmid vector for Bacillus thuringiensis displaying compatibility with host plasmids, Gene 120: 17–26.PubMedCrossRefGoogle Scholar
  42. Garczynski, S.F., and Adang, M.J., 1995, Cry l Ac delta endotoxin-binding aminopeptidase N in the Manduca sexta midgut has glycosyl-phosphotidylinositol anchor, Insect Biochem. Molec. Biol. 25: 409–415.CrossRefGoogle Scholar
  43. Gawron-Burke, C., and Baum, J. A., 1991, Genetic manipulation of Bacillus thuringiensis insecticidal crystal protein genes in bacteria, in: Genetic Engineering: Principles and Methods, Vol. 13, J. K. Setlow, ed., Plenum Press, New York, pp. 237–263.Google Scholar
  44. Gill, S. S., Cowels, E. A., and Pietrantonio, E. A., 1992, The mode of action of Bacillus thuringiensis endotoxins, Annu. Rev. Entomol. 37: 615–636.PubMedCrossRefGoogle Scholar
  45. Glare, T. R., and O’Callaghan. M., 2000, Bacillus thuringiensis: Biology, Ecology and Safety. John Wiley and Sons, Chichester, 350 p.Google Scholar
  46. Gonzalez, J.M. Jr., Brown, B. J., and Carlton, B.C., 1982, Transfer of Bacillus thuringiensis plasmids coding for delta endotoxins among strains of B. thuringiensis and B. cereus, Proc. Natl. Acad. Sci. USA 79: 6951–6955.PubMedCrossRefGoogle Scholar
  47. Gould, F., 1994, Potential and problems with high-dose strategies for pesticidal engineered crops, Biocontrol Sci. Technol. 4: 451–461.CrossRefGoogle Scholar
  48. Gould, F., 1998, Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology, Annu. Rev. Entomol. 43: 701–726.PubMedCrossRefGoogle Scholar
  49. Gould, F., Martinez-Ramirez, A., Anderson, A., Ferre, J., Silva, F. J., and Moar, W. J.,1992, Broad spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens, Proc. Natl. Acad. Sci. USA 89: 7986–7990.Google Scholar
  50. Grochulski, P., Masson, L., Borisova, S., Pusztai-Carey, M., Schwartz, J.L., Brousseau, R., and Cygler, M., 1995, Bacillus thuringiensis CrylAa insecticidal toxin: crystal structure and channel formation, J. Mol. Biol. 254: 447–464.Google Scholar
  51. Hassan, S.A., 1992, Testing methodology and the concept of the IOBC/WPRS working group. Pesticides and Non-target Invertebrates, Jepson. P, C., ed., Intercept, Wimborne, Dorset, pp 1–18.Google Scholar
  52. Hassan, S.A., Bigler, F, Bogenschutz, H., Brown, J.U., Firth, S.I., Huang, P., Ledieu, M.S., Naton, E., Oomen, P.A., Overmeer, W.P.J., Rieckmann, W., Peterson, W.S., Viggiani, G., and van Zon, A.Q., 1983, Results of the joint pesticide testing programme by the IOBC/WPRS-Working group “Pesticides and Beneficial Arthropods”, Z. Angew. Entomol. 95: 151–158.CrossRefGoogle Scholar
  53. Hernandez, J.L.L., 1988, Evaluation of toxicity of Bacillus thuringiensis to Spodopterafrugiperda, Entomophaga 33: 163–171.CrossRefGoogle Scholar
  54. Hofte, H., and Whiteley, H. R., 1989, Insecticidal crystal proteins ofBacillus thuringiensis, Microbiol. Rev. 53: 242–255.PubMedGoogle Scholar
  55. Hoy, M. A., 1998, Myths: models and mitigation of resistance to pesticides, Phil. Trans. R. soc. Lond. 353: 1787–1795.CrossRefGoogle Scholar
  56. Husz, B., 1928, On the use of Bacillus thuringiensis in the fight against the corn borer, Int. Corn Borer Invest. Sci. Rep. 2: 99–110.Google Scholar
  57. Ishiwata, S., 1901, On a type of severe flacherie (sotto disease), Dainihan Sanbshi Kaiho 9: 1–5.Google Scholar
  58. Ives, A. R., 1996, Evolution of insect resistance to Bacillus thuringiensis-transformed plants, Science 273: 1412–1413.CrossRefGoogle Scholar
  59. Jansens, S., van Vliet, A., Dickburt, C., Buysse, L., Piens, C., Saey, B., De Wulf, A., Gossele, V., Paez, A., Gobel, E., and Peferoen, M., 1997, Transgenic corn expressing a Cry9C insecticidal protein from Bacillus thuringiensis protected from European corn borer damage, Crop Sci.37: 1616–1624.Google Scholar
  60. Kalman, S., Kiehne, K. L., Cooper, N., Reynoso, M. S., and Yamamoto, T., 1995, Enhanced production of insecticidal proteins in Bacillus thuringiensis strains carrying an additional crystal protein gene in their chromosomes, Appl. Environ. Microbiol. 61: 3063–3068.PubMedGoogle Scholar
  61. Kennedy, G.G., and Whalon, M.E., 1995, Managing pest resistance to Bacillus thuringiensis endotoxins: constraints and incentives to implementation, J. Econ. Entomol. 88: 454–460.Google Scholar
  62. Knowles, B. H., 1994, Mechanism of action of Bacillus thuringiensis insecticidal 5-endotoxins, Adv. Insect Physiol. 24: 275–308.CrossRefGoogle Scholar
  63. Koziel, M. G., Beland, G. L., Bowman, C., Carozzi, N. B., Crenshaw, R., Crossland, L., Dawson, J., Desai, N., Hill, M., Kadwell, S., Launis, K., Lewis, K., Maddox, D., McPherson, K., Meghji, M. R., Merlin, E., Rhodes, R., Warren, G. W., Wright, M., and Evola, S. V., 1993, Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis, Bio/Technol. 11: 194–200.CrossRefGoogle Scholar
  64. Kronstad, J. W., and Whiteley, H. R., 1986, Three classes of homologous Bacillus thuringiensis crystal protein genes, Gene 43: 29–40.PubMedCrossRefGoogle Scholar
  65. Kumar, P.A., Sharma, R.P., and Malik, V.S., 1996, Insecticidal proteins of Bacillus thuringiensis, Adv Appl Microbiol. 42: 1–43.PubMedCrossRefGoogle Scholar
  66. Kumar, P.A., Mandaokar, A., Sreenivasu, K., Chakrabarti, S.K., Sharma, S.R., Bisaria, S., Kaur, S., and Sharma, R.P., 1998, Insect resistant transgenic brinjal plants, Mol. Breed. 4: 33–37CrossRefGoogle Scholar
  67. Lambert, B., and Peferoen, M., 1992, Insecticidal promise of Bacillus thuringiensis: facts and mysteries about a successful biopesticide, BioSci. 42: 112–122.CrossRefGoogle Scholar
  68. Lampel, J. S., Canter, G. L., Dimock, M. B., Kelly, J. L., Anderson, J. J., Uratani, B. B., Foulke, J. S. Jr., and Turner, J. T., 1994, Integrative cloning, expression, and stability of the cryla(c) gene from Bacillus thuringiensis subsp. Kurstaki in a recombinant strain of Clavibacter xyli subsp. Cynodontis, Appl. Environ. Microbiol. 60: 501–508.PubMedGoogle Scholar
  69. Lereclus, D., Bourgouin, C., Lecadet, M. M., Klier, A., and Rapoport, G., 1989, Role, structure, and molecular organization of the genes coding for parasporal S-endotoxins of Bacillus thuringiensis, in: Regulation of Prokaryotic Development: Structural and Functional Analysis of Bacterial Sporulation and Germination, Smith, I., Slepecky, R. A. and Setlow, P., eds., American Society for Microbiology, Washington, D.C.Google Scholar
  70. Lereclus, D., Vallade, M., Chaufaux, J., Arantes, O., and Rambaud, S., 1992, Expansion of insecticidal host range of Bacillus thuringiensis by in vivo genetic recombination, Bio/ Technol. 10: 418–421.Google Scholar
  71. Lereclus, D., Agaisse, H., Gominet, M., and Chaufaux, J., 1995, Overproduction of encapsulated insecticidal crystal proteins in a Bacillus thuringiensis spOA mutant, Bio/ Technol. 13: 67–71.Google Scholar
  72. Leroy, T., Henry, A. M., Royer, M., Altosaar, I., Frutos, R., Duris, D. and Philippe, R., 2000, Genetically modified coffee plants expressing the Bacillus thuringiensis crylAc gene for resistance to leaf miner, Plant Cell Rep. 19: 382–389.CrossRefGoogle Scholar
  73. Li, J., Carroll, J., and Ellar, D. J., 1991, Crystal structure of insecticidal ä-endotoxin from Bacillus thuringiensis at 2.5 A° resolution, Nature 353: 815–821.PubMedCrossRefGoogle Scholar
  74. Liu, Y. B., and Tabashnik, B. E., 1997, Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis, Proc. R. Soc. Lond. 264: 605–610.Google Scholar
  75. Liu, Y. B., Tabashnik, B. E., and Pusztai-Carey, M., 1996, Field-evolved resistance to Bacillus thuringiensis toxin Cry1C in diamondback moth ( Lepidoptera: Plutellidae),J. Econ. Entomol. 89: 798–804.Google Scholar
  76. Luthy, P., Cordier, J., and Fischer, J., 1982, Bacillus thuringiensis as a bacterial insecticide, in: Microbial and Viral Pesticides, E. Kurstak, ed., Marcel and Decker, New York, pp. 35–74.Google Scholar
  77. Macintosh, S. C., Kishore, G. M., Perlak, F. J., Marron, P. G., Stone, T. B., Sims, S. R., and Fuchs, R. L., 1990, Potentiation of Bacillus thuringiensis insecticidal activity by serine protease inhibitors, J. Agric. Food Chem. 38: 1145–1152.Google Scholar
  78. Mandaokar, A., Goyal, R.K., Shukla, A., Bhalla, R., Chaurasia, A., Reddy, V.S., Altosaar, I., Sharma, R.P., and Kumar, P.A., 2000, Transgenic tomato plants resistant to fruitborer (Helicoverpa armigera Hubner), Crop Protect. 19: 307–312.CrossRefGoogle Scholar
  79. Martin, P. A. W., and Travers, R. S., 1989, Worldwide abundance and distribution of Bacillus thuringiensis isolates, Appl. Environ. Microbiol. 55: 2437–2442.PubMedGoogle Scholar
  80. Maqbool, S.B., Husnain, T., Riazuddin, S., Massom, L., and Chritou, P., 1998, Effective control of yellow stem borer and rice leaf folder in transgenic rice indica varieties Basmati 370 and M 7 using the novel S-endotoxin cry2A Bacillus thuringiensis gene, Mol. Breed. 4: 501–507.CrossRefGoogle Scholar
  81. McBride, K.E., Svab, Z., Schaaf, D.J., Hogan, P.S., Stalker, D.M., and Maliga, P., 1995, Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein tobacco, Biotechnol. 13: 362–365.CrossRefGoogle Scholar
  82. Meade, T. and Hare, J. D., 1995, Integration of host plant resistance and Bacillus thuringiensis insecticides in the management of lepidopterous pests of celery, J. Econ. Entomol. 88: 1787–1794.Google Scholar
  83. Metz, T. D., Roush, R. T., Tang, J. D., Shelton, A. M., and Earle, E. D., 1995, Transgenic broccoli expressing a Bacillus thuringiensis insecticidal crystal protein: implications for pest resistance management strategies, Mol. Breed]: 309–317.Google Scholar
  84. Moellenbeck, D. J., Peters, M. L., Bing, J. W., Rouse, J. R., Higgins, L. S., Sims, L., Nevshemal, T., Marshall, L., Ellis, R. T., Bystrak, P. G., Lang, B. A., Stewart, J. L., Kouba, K., Sondag, V., Gustafson, V., Nour, K., Xu, D., Swenson, J., Zhang, J., Czapla, T., Schwab, G., Jayne, S., Stockhoff, B. A., Narva, K., Schnepf, H. E., Stelman, S. J., Poutre, C., Koziel, M., and Duck, N., 2001, Insecticidal proteins from Bacillus thuringiensis protect corn from corn root worms, Nature Biotechnol. 19: 668–672.CrossRefGoogle Scholar
  85. Nambiar, P. T. C., Ma, S. W., and Iyer, V. N., 1990, Limiting an insect infestation of Nitrogen-fixing root nodules of the Pigeonpea (Cajanu Cajan) by engineering the expression of an entomocidal gene in its root nodules, Appl. Environ. Microbiol. 56: 2866–2869.Google Scholar
  86. Nayak, P., Basu, D., Das, S., Basu, A., Ghosh, D., Ramakrishnan, N.A., Ghosh, M., and Sen, S.K., 1997, Transgenic elite indica rice plants expressing Cry 1Ac delta-endotoxin of Bacillus thuringiensis are resistant against yellow stemborer, Proc Natl Acad Sci USA 94: 2111–2116PubMedCrossRefGoogle Scholar
  87. Obukowicz, M. G., Perlak, F. J., Kusano-Kretzmer, K., Mayer, E. J., Bolten, S. L., and Watrud, L.S., 1986, Tn5mediated integration of the S-endotoxin gene from Bacillus thuringiensis into the chromosome of root-colonising pseudomonads, J. Bacteriol. 168: 982–989.PubMedGoogle Scholar
  88. Onstad, D. W., and Gould, F., 1998, Do dynamics of crop maturation and herbivorous insect life cycle influence the risk of adaptation to toxins in transgenic host plants?, Environ. Entomol. 27: 517–522.Google Scholar
  89. Oppert, B., Kramer, K. J., Johnson, D. E., Maclnstosh, S. C., and McGaughey, W. H., 1994, Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpunctella, Biochem. Biophys. Res. Commun. 198: 940–947.Google Scholar
  90. Oppert, B., Kramer, K. J., Beeman, R. W., Johnson, D., and McGaughey, W. H., 1997, Proteinase-mediated insect resistance to Bacillus thuringiensis toxins, J. Biol. Chem. 272: 23473–23476.Google Scholar
  91. Parry, J.M., Turnbull, P.C.B., and Gibson, J.R., 1983, A Colour Atlas of Bacillus Species, Wolfe Medical, London, 99 p.Google Scholar
  92. Pattanayak, D., and Kumar, P. A., 2000, Plant biotechnology: Current advances and future perspectives, Proc. Indian Natl. Sci. Acad. B6: 265–310.Google Scholar
  93. Pattanayak, D., Srinivasan, K., Mandaokar, A., Shukla, A., Bhalla, R., Kumar, P. A., 2000, AFLP fingerprinting and genetic characterization of Bacillus thuringiensis subspecies, World J. Microbiol. Biotechnol. 16: 667–672.CrossRefGoogle Scholar
  94. Peferoen, M., 1997, Progress and prospects for field use of Bt genes in crops, Trends Biotechnol. 15: 173–177.CrossRefGoogle Scholar
  95. Perlak, F. J., Deaton, R. W., Armstrong, T. A., Fuchs, R. L., Sims, S. R., Greenplate, J. T., and Fischhoff, D. A., 1990, Insect resistant cotton plants, Bio/Technol. 8: 939–943.CrossRefGoogle Scholar
  96. Perlak, F.J., Fuchs, R.L., Dean, D.A., McPherson, S., Fischhoff, D.A. 1991, Modification of the coding sequence enhances plant expression of insect control genes, Proc. Natl. Acad. Sci. USA. 88: 3324–3328.PubMedCrossRefGoogle Scholar
  97. Perlak, F. J., Stone, T. B., Muskopf, Y. M., Petersen, L. J., Parker, G. B., McPherson, S. A., Wyman, J., Love, S., Reed, G., Biever, D., and Fishhoff, D. A., 1993, Genetically improved potatoes: protection from damage by Colorado potato beetles, Plant Mol. Biol. 22: 313–321.PubMedCrossRefGoogle Scholar
  98. Raina, S.K., and Khanna, H., 2001, Elite indica transgenic rice plants expressing CrylAc endotoxin of Bacillus thuringiensis show enhanced resistance to yellow stem borer, Transgenic Res. (In press).Google Scholar
  99. Roush, R. T., 1989, Designing resistance management programs: how can you choose? Pestic. Sci. 26: 423–441.CrossRefGoogle Scholar
  100. Roush, R. T., 1997, Managing risk of resistance in pests to insect-tolerant transgenic crops, in: Commercialization of transgenic crops: Risks, Benefits and Trade Considerations, P.M., Evans, G., and Gibbs, M.J., eds., Waterhouse, Cooperative Research Center for Plant science and Bureau of Statistics, Canberra, Australia, pp. 259–271.Google Scholar
  101. Roush, R. T., 1998, Two-toxin strategies for management of insecticidal transgenic crops; can pyramiding succeed where pesticide mixtures have not?, Phil. Trans. R. Soc. Lond. 353: 1777–1786.CrossRefGoogle Scholar
  102. Schnepf, H. E., 1995, Bacillus thuringiensis toxins: regulation, activities and structural diversity, Curr.Opinion Biotech.6: 305–312.Google Scholar
  103. Schnepf, E., Crickmore, N:, Van Rie, J., Lereclus, D., Baum, J., Feitelson, J., Zeigler, D.R., and Dean, D.H., 1998, Bacillus thuringiensis and its pesticidal crystal proteins, Microbiol. Mol. Biol. Rev. 62: 775–806.Google Scholar
  104. Schuler, T.H., Poppy, G.M., and Denholm, I., 1998, Insect-resistant transgenic plants, Trends Biotech. 16: 168–175.CrossRefGoogle Scholar
  105. Shelton, A.M., Juliet, D., Tang, J.D., Roush, R.T., Metz, T.D., and Earle, E.D., 2000, Field tests on managing resistance to Bt-engineered plants, Nature Biotech. 18: 339–342.CrossRefGoogle Scholar
  106. Shu, Q., Ye, G., Cui, H., Cheng, X., Xiang, Y., Wu, D., Gao, M., Xia, Y., Hu, C., Sardana, R., and Altosaar, I., 2000, Transgenic rice plants with a synthetic cry 1Ab gene from Bacillus thuringiensis were highly resistant to eight lepidopteran pests, Mol. Breed. 6: 433–439.CrossRefGoogle Scholar
  107. Singsit, C., Adang, M. J., Lynch, R. E., Anderson, W. F., Wang, A., Cardineau, G., and Ozias-Akins, P., 1997, Expression of a Bacillus thuringiensis crylA (c) gene in transgenic peanut plants and its efficacy against lesser cornstalk borer, Transgenic Res. 6 (2): 169–176.PubMedCrossRefGoogle Scholar
  108. Smith, R. A., and Couche, G. A., 1991, The phylloplane as a source of Bacillus thuringiensis variants, Appl. Environ. Microbiol. 57: 311–315.PubMedGoogle Scholar
  109. Soltes-Rak, Kushner, E. D. J., Williams, D. D., and Coleman J. R., 1993, Effects of promoter modification on mosquitocidal crylVB gene expression in Synechococcus sp. strain 7942, Appl. Environ. Microbiol. 59: 2404–2410.PubMedGoogle Scholar
  110. Stewart, C. N., Jr., Adang, M. J., All, J. N., Raymer, P. L., Ramachandran, S., and Parrott, W. A., 1996, Insect control and dosage effects in transgenic Canola containing a synthetic Bacillus thuringiensis crylAc gene, Plant Physiof. 112: 115–120.Google Scholar
  111. Steinhaus, E.A., 1951, Possible use of Bacillus thuringiensis as an aid in the biological control of the alfalfa caterpillar, Hilgardia 20: 359–381.Google Scholar
  112. Strizhov, N., Keller, M., Mathur, J., Koncz-Kalman, Z., Bosch, D., Prudovsky, E., Schell, J., Sneh, B., Koncz, C., and Zilberstein, A., 1996, A synthetic cry1C gene, encoding a Bacillus thuringiensis 8-endotoxin, confersGoogle Scholar
  113. Spodoptera resistance in alfalafa and tobacco, Proc. Natl. Acad. Sci. USA 93: 15012–15017.Google Scholar
  114. Tabashnik, B.E., 1994, Evolution of resistance to Bacillus thuringiensis, Annu. Rev. Entomol. 39: 47–79.Google Scholar
  115. Tabashnik, B. E., 1998, Transgenic crops for the pacific basin: prospects and problems, in: Proceedings of the Australian Applied Entomology Research Conference, Vol. 1, University of Queensland, Australia, pp. 161–161.Google Scholar
  116. Tang, J. D., Shelton, A. M, van Rie, J., de Roeck, S., Moar, W. J., Roush, R. T., and Peferoen, M., 1996, Toxicity of Bacillus thuringiensis spore and crystal protein to resistant diamondback moth (Plutella xylostella), Appl. Environ. Microbiol. 62: 564–569.PubMedGoogle Scholar
  117. Udayasuriyan, V., Nakamura, A., Masaki, H., and Uozumi, T., 1995, Transfer of an insecticidal protein gene of Bacillus thuringiensis into plant-colonisingAzospirillum, World J. Microbiol. Biotechnol. 11: 163–167.CrossRefGoogle Scholar
  118. Vaeck, M., Reynaerts, A., Hofte, H., Jansens, S., De Beukeleer, M., Dean, C., Zabeau, M., Van Montagu, M., and Leemans, J., 1987 Transgenic plants protected from insect attack, Nature 328: 33–37.CrossRefGoogle Scholar
  119. van der Salm, T., Bosch, D., Honee, G., Feng, L., Munsterman, E., Bakker, P., Stiekema, W. J., and Visser, B., 1994, Insect resistance of transgenic plants that express modified Bacillus thuringiensis cry 1A(b) and cry 1C genes: a resistance management strategy, Plant Mol. Biol. 26: 51–59.PubMedCrossRefGoogle Scholar
  120. Van Frankenhuyzen, K., 1990, Development and current status of Bacillus thuringiensis for control of defoliating forest insects, For. Chron. 66: 498–507.Google Scholar
  121. Wirth, M. C., Georghiou, G. P., and Federici, B. A. 1997, CytA enables CryIV endotoxins of Bacillus thuringiensis to overcome high levels of Cry IV resistance in the mosquito, Culex quinquefasciatus, Proc. Natl. Acad Sci. USA. 94: 10536–10540.PubMedCrossRefGoogle Scholar
  122. Wong, E. Y., Hironaka, C. M., and Fischhoff, D. A., 1992, Arabidopsis thaliana small subunit leader and transit peptide enhance the expression of Bacillus thuringiensis proteins in transgenic plants, Plant Mol. Biol. 20: 81–93.Google Scholar
  123. Zeigler, D.R., 1999, Bacillus thuringiensis and Bacillus cereus Catalog of Strains, Bacillus Genetic Stock Center, Columbus, p. 56.Google Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • P. Ananda Kumar
    • 1
  • O. M. Bambawale
    • 2
  1. 1.National Research Centre for Plant BiotechnologyNew DelhiIndia
  2. 2.National Centre for Integrated Pest Management Indian Agricultural Research InstituteNew DelhiIndia

Personalised recommendations