Agronomy for Sustainable Development

, Volume 28, Issue 1, pp 11–20 | Cite as

Bacillus thuringiensis: applications in agriculture and insect resistance management. A review

  • Vincent SanchisEmail author
  • Denis Bourguet
Review Article


Bacillus thuringiensis (Bt) is a sporulating, Gram-positive facultative-aerobic soil bacterium. Its principal characteristic is the synthesis, during sporulation, of a crystalline inclusion containing proteins known as δ-endotoxins or Cry proteins. These proteins have insecticidal properties. The considerable diversity of these toxins, their efficacy and their relatively cheap production have made Bt the most widely used biopesticide in the world. It is used in the fight against many agricultural crop pests — mostly lepidopteran and coleopteran larvae — notably in the creation of new plant varieties expressing Bt cry genes. For human health, Bt can be used for the effective control of populations of several dipteran disease vectors. The aim of this review is to provide an overview of the use of Bt for crop protection and to deal with the problem of the emergence of insects resistant to this biopesticide. We will begin by presenting various aspects of the biology of this entomopathogenic micro-organism, focusing on the diversity and mode of action of the insecticidal toxins it produces. We will then present several examples of utilization of commercially available Bt products used as sprays or as transgenic crops. Finally, we will describe the principal strategy for the use of Bt transgenic plants, developed so as to prevent or delay the emergence of resistance in target insect populations.

Bacillus thuringiensis biopesticide δ-endotoxin transgenic plants resistance management Cry protein 


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  1. Alstad D.N., Andow D.A. (1995) Managing the Evolution of Insect Resistance to Transgenic Plants, Science 268, 1894–1896.PubMedCrossRefGoogle Scholar
  2. Alves A.P., Spencer T.A., Tabashnik B.E., Siegfried B.D. (2006) Inheritance of resistance to the CrylAb Bacillus thuringiensis toxin in Ostrinia nubilalis (Lepidoptera: Crambidae), J. Econ. Entomol. 99, 494–501.PubMedCrossRefGoogle Scholar
  3. Angus T.A. (1954) A Bacterial toxin paralysing silkworm larvae, Nature 173, 54–56.CrossRefGoogle Scholar
  4. Becker N. (2000) Bacterial control of vector-mosquitoes and black flies, in: Charles J.F., Delécluse A., Nielsen-Leroux C. (Eds.), Entomopathogenic Bacteria: From Laboratory to Field Application, Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 383–398.Google Scholar
  5. Berliner E. (1915) Über die Schlaffsucht der Mehlmottenraupe (Ephestia kühniella Zell.) und ihren Erreger Bacillus thuringiensis, n.sp., Z. Angewandte Entomologie 2, 29–56.CrossRefGoogle Scholar
  6. Bourguet D., Génissel A., Raymond M. (2000) Insecticide resistance and dominance levels J. Econ. Entomol. 93, 1588–1595.PubMedCrossRefGoogle Scholar
  7. Bourguet D., Chaufaux J., Seguin M., Buisson C., Hinton L., Stodola T.J., Porter P., Cronholm G., Buschman L.L., Andow D.A. (2003) Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer, Ostrinia nubilalis, Theor. Appl. Genet. 106, 1225–1233.PubMedGoogle Scholar
  8. Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., Zhuang M., Gill S.S., Soberon M. (2004) Oligomerization triggers binding of a Bacillus thuringiensis CrylAb pore-formingtoxin to aminopeptidase N receptor leading to insertion into membrane microdomains, Biochim. Biophys. Acta 1667, 38–46.PubMedCrossRefGoogle Scholar
  9. Calamari D., Yameogo L., Hougard J.-M., Levêque C. (1998) Environmental assessment of larvicide use in the onchocerciasis programme, Parasitol. Today 14, 485–489.PubMedCrossRefGoogle Scholar
  10. Chaufaux J., Seguin M., Swanson J.J., Bourguet D., Siegfried B.D. (2001) Chronic exposure of the European corn borer (Lepidoptera: Crambidae) to Cry1Ab Bacillus thuringiensis toxin, J. Econ. Entomol. 94, 1564–1570.PubMedCrossRefGoogle Scholar
  11. Crickmore N., Zeigler D.R., Schnepf E., Van Rie J., Lereclus D., Baum J., Bravo A., Dean D.H. (2005) Bacillus thuringiensis Toxin Nomenclature (Homepage), Scholar
  12. Dalecky A., Ponsard S., Bailey R.I., Pélissier C., Bourguet D. (2006) Resistance evolution to Bt crops: predispersal mating of European corn borers, PLoS Biology 4, 1048–1057.CrossRefGoogle Scholar
  13. De la Riva G., Adang M.J. (1996) Expression of Bacillus thuringiensis δ-endotoxin genes in transgenic plants, Biotecnologia Aplicada 13, 251–260.Google Scholar
  14. Ellis R.T., Stockhoff B.A., Stamp L., Schnepf H.E., Schwab G.E., Knuth M., Russell J., Cardineau G.A., Narva K.E. (2002) Novel Bacillus thuringiensis binary insecticidal crystal proteins active on western corn rootworm, Diabrotica virgifera virgifera LeConte, Appl. Environ. Microbiol. 68, 1137–1145.PubMedCrossRefGoogle Scholar
  15. Estruch J.J., Warren G.W., Mullins M.A., Nye G.J., Craig J.A., Koziel M.G. (1996) Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects, Proc. Natl. Acad. Sci. (USA) 93, 5389–5394.CrossRefGoogle Scholar
  16. Farinés G.P., de la Poza M., Hernández-Crespo P., Ortego F., Castañera P. (2004) Resistance monitoring of field populations of the corn borers Sesamia nonagrioides and Ostrinia nubilalis after 5 years of Bt maize cultivation in Spain, Entomol. Exp. Appl. 110, 23–30.CrossRefGoogle Scholar
  17. Higginson D.M., Morin S., Nyboer M.E., Biggs R.W., Tabashnik B.E., Carrière Y. (2005) Evolutionary trade-offs of insect resistance to Bacillus thuringiensis crops: fitness cost affecting paternity, Evolution, 59, 915–920.PubMedGoogle Scholar
  18. Huang D.-F., Zhang J., Song F.-P., Lang Z.-H. (2007) Microbial control and biotechnology research on Bacillus thuringiensis in China, J. Invert. Pathol. 95, 175–180.CrossRefGoogle Scholar
  19. Ishiwata S. (1901) On a kind of severe flacherie (sotto disease), Dainihon Sanshi Kaiho 114, 1–5.Google Scholar
  20. James C. (2006) Preview, global status of commercialized transgenic crops, ISAAA Briefs No. 35 ( Scholar
  21. Knight P.J., Crickmore N., Ellar D.J. (1994) The receptor for Bacillus thuringiensis CryIA(c) delta-endotoxin the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N, Mol. Microbiol. 11, 429–436.PubMedCrossRefGoogle Scholar
  22. Knowles B.H. (1994) Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins, Adv. Insect Physiol. 24, 273–308.Google Scholar
  23. Koziel G.M., Beland G.L., Bowman C., Carozzi N.B., Crenshaw R., Crossland L., Dawson J., Desai N., Hill M., Kadwell S., Launis K., Maddox D., McPherson K., Heghji M., Merlin E., Rhodes R., Warren G., Wright M., Evola S. (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis, Biotechnology 11, 194–200.CrossRefGoogle Scholar
  24. Levêque C., Fairhust C.P., Abbau K., Pangy D., Curtis M.S., Traoré K. (1988) Onchocerciasis control programme in West Africa: ten years of monitoring fish populations, Chemosphere, 17, 421–440.CrossRefGoogle Scholar
  25. Li J., Carroll J., Ellar D.J. (1991) Crystal structure of insecticidal deltaendotoxin from Bacillus thuringiensis at 2.5 A resolution, Nature 353, 815–821.PubMedCrossRefGoogle Scholar
  26. Maagd R.A. de, Weemen-Hendriks M., Stiekema W., Bosch D. (2000) Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in different, but not all, Cry1-Cry1C hybrids, Appl. Environ. Microbiol. 66, 1559–1563.PubMedCrossRefGoogle Scholar
  27. Maagd R.A. de, Bravo A., Berry C., Crickmore N., Schnepf H.E. (2003) Structure, diversity, and evolution of protein toxins from sporeforming entomopathogenic bacteria, Annu. Rev. Genet. 37, 409–33.PubMedCrossRefGoogle Scholar
  28. Marvier M., McCreedy C., Regetz J., Kareiva P. (2007) Meta-analysis of effects of Bt cotton and maize on nontarget invertebrates, Science 316, 1475–1477.PubMedCrossRefGoogle Scholar
  29. McGaughey W.H. (1985) Insect resistance to the biological insecticide Bacillus thuringiensis, Science 229, 193–195.PubMedCrossRefGoogle Scholar
  30. Perlak F.J., Fuchs R.L., Dean D.A., McPherson S.L., Fishhoff D.A. (1991) Modification of the coding sequences enhances plant expression of insect control protein genes, Proc. Natl. Acad. Sci. (USA) 88, 3324–3328.CrossRefGoogle Scholar
  31. Perlak F.J., Stone T.B., Muskopf Y.M., Petersen L.J., Parker J.B., Mc Pherson S.A., Wyman J., Love S., Reed G., Biever D. (1993) Genetically improved potatoes: protection from damage by Colorado potato beetles, Plant. Mol. Biol. 22, 313–321.PubMedCrossRefGoogle Scholar
  32. Pigott C., Ellar D.J. (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity, Microbiol. Mol. Biol. Rev. 71, 255–281.PubMedCrossRefGoogle Scholar
  33. Riba G., Silvy C. (1989) Combattre les ravageurs des cultures enjeux et perspectives, INRA, Paris.Google Scholar
  34. Sanchis V. (2000) Biotechnological improvement of Bacillus thuringiensis for agricultural control of insect pests: benefits and ecological implications, in: Charles J.F., Delécluse A., Nielsen-Leroux C. (Eds.), Entomopathogenic Bacteria: From Laboratory to Field Application, Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 441–459.Google Scholar
  35. Schnepf H.E., Wong H.C., Whiteley H.R. (1985) The amino acid sequence of a crystal protein from Bacillus thuringiensis: deduced from the DNA base sequence, J. Biol. Chem. 260, 6264–6272.PubMedGoogle Scholar
  36. Singh-Ashk G.K. (2007) Bt cotton not pest resistant, The times of India, 24 August 2007.Google Scholar
  37. Smedley D.P., Ellar D.J. (1996) Mutagenesis of three surface-exposed loops of a Bacillus thuringiensis insecticidal toxin reveals residues important for toxicity, receptor recognition and possibly membrane insertion, Microbiol. 142, 1617–1624.CrossRefGoogle Scholar
  38. Stodola T.J., Andow D.A., Hyden A.R., Hinton J.L., Roark J.J., Buschman L.L., Porter P., Cronholm G.B. (2006) Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in southern United States Corn Belt population of European corn borer (Lepidoptera: Crambidae), J. Econ. Entomol. 99, 502–507.PubMedCrossRefGoogle Scholar
  39. Tabashnik B.E. (1994) Evolution of resistance to Bacillus thuringiensis, Ann. Rev. Entomol. 39, 47–79.CrossRefGoogle Scholar
  40. Tabashnik B.E., Carrière Y., Dennehy T.J., Morin S., Sisterson M.S., Roush R.T., Shelton A.M., Zhao J.Z. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field, J. Econ. Entomol. 96, 1031–1038.PubMedCrossRefGoogle Scholar
  41. Tabashnik B.E., Dennehy T.J., Carrière Y. (2005) Delayed resistance to transgenic cotton in pink bollworm, Proc. Natl. Acad. Sci. (USA) 102, 15389–15393.CrossRefGoogle Scholar
  42. Vadlamudi R.K., Weber E., Ji I., Ji T.H., Bulla Jr. L.A. (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thruingiensis, J. Biol. Chem. 270, 5490–5494.PubMedCrossRefGoogle Scholar
  43. Vaeck M., Reynaerts A., Höfte H., Jansens S., De Beukeleer M., Dean C., Zabeau M., Van Montagu M., Leemans J. (1987) Transgenic plants protected from insect attack, Nature 327, 33–37.CrossRefGoogle Scholar
  44. Van Frankenhuyzen K. (2000) Applications of Bacillus thuringiensis in forestry, in: Charles J.F., Delécluse A., Nielsen-Leroux C. (Eds.), Entomopathogenic Bacteria: From Laboratory to Field Application. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 371–382.Google Scholar
  45. Van Rie J., Jansens S., Hofte 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 deltaendotoxins, Appl. Environ. Microbiol. 56, 1378–1385.PubMedGoogle Scholar
  46. Walker K., Mendelsohn M., Matten S., Alphin M., Ave D. (2003) The role of microbial Bt products in US crop protection, in: Metz M. (Ed.), Bacillus thuringiensis: a cornerstone of modern agriculture, Food Products Press, Binghamton, USA, pp. 31–51.Google Scholar
  47. Wang G., Zhang J., Song F., Wu J., Feng S., Huang D. (2006) Engineered Bacillus thuringiensis GO33A with broad insecticidal activity against lepidopteran and coleopteran pests, Appl. Microbiol. Biotechnol. 72, 924–30.PubMedCrossRefGoogle Scholar
  48. Zhang X., Candas M., Griko N., Taussig R., Bulla Jr. L. (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the CrylAb toxin of Bacillus thuringiensis, Proc. Natl. Acad. Sci. (USA) 103, 9897–9902.CrossRefGoogle Scholar

Copyright information

© INRA, EDP Sciences 2008

Authors and Affiliations

  1. 1.Unité de Génétique Microbienne et EnvironnementINRA La MinièreGuyancourt CedexFrance
  2. 2.Centre de Biologie et de Gestion des PopulationsUMR INRA-IRD-Montpellier SupAgro-CIRADMontferrier sur LezFrance

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