Abstract
Bacillus thuringiensis, known as Bt, is a spore-forming bacterium that occurs naturally in soil and that produces highly specific insecticidal proteins called Cry proteins. These proteins are stomach poisons that specifically affect insects. Today, Bt preparations are considered as the most effective, specific and environmentally-friendly bioinsecticides; they have been used as biological pesticides in agriculture, forestry and in human health for the elimination of vectors of diseases for more than 60 years and their implementation far exceeds other microbial agents such as fungi, protozoa or viruses. This review on the use of this entomopathogenic bacterium in crop protection is not intended to be a compilation of the results of all the investigations made in this field. Instead, it is an attempt to provide an overview of the major trends and developments of Bt for the control of agricultural insect pests and to describe the main approaches that have been used to improve this natural bioinsecticide. Bt-based insecticides are considered safe for mammals and birds, and are safer for non-target insects than conventional insecticides; they have become the most widely used microbial insecticides. However, Bt products have several limitations, such as a narrow activity spectrum, instability in rain and sunlight, and inefficiency against pest feeding on internal tissues of the plants. The first step towards improving Bt has involved the isolation of new strains with higher and broader insecticidal activity against targeted insect pests and the cloning of cry genes encoding new insecticidal crystal proteins. A second strategy was to increase the persistence of its toxins in the field by encapsulation in recombinant asporogenic Bt strains or other heterologous recombinant microbial hosts; this protected the toxins against UV degradation and had the advantage that the transgenic microorganisms released into the environment were non-viable. Bt has also become a key source of genes for transgenic expression to provide pest resistance in plants and in so-called genetically modified plants. The engineering of plants to express Bt cry genes has been especially helpful against pests that attack parts of the plant that are usually not well protected by conventional insecticide application. The potential effects on human health and the environment of the large-scale use of these Bt crops are also in the scope of this review.
Similar content being viewed by others
References
Addison J.A. (1993) Persistence and nontarget effects of Bacillus thuringiensis in soil: a review, Can. J. For. Res. 23, 2329–2342.
Angus T.A. (1954) A bacterial toxin paralyzing silkworm larvae, Nature 173, 545–546.
Aoki K., Chigasaki Y. (1915) Mber die Pathogenitat des sog. Bacillus sotto (Ishiwata) bei Seidenraupen, Mitt. Med. Fak. Kais. Univ., Tokyo 13, 419–440.
Aoki K., Chigasaki Y. (1916) Ueber atoxogene Sotto-Bacillen, Bull. Imp. Ser. Exp. Stat. Nakano, Tokyo 1, 141.
Audoin V. (1837) Nouvelles experiences sur la nature de la maladie contagieuse qui attaque les vers à soie, et qu’on désigne sous le nom de Muscardine, C.R. Acad. Sci. Paris 5, 712–717.
Barton K.A., Whiteley H.R., Yang N.S. (1987) Bacillus thuringiensis δ-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to lepidopteran insects, Plant Physiol. 85, 1103–1109.
Bassi A. (1835) Del mal del segno, calcinaccio o moscardino, malattia che affigge i bachi da seta, e sul modo di liberarne le bigattaje anche le piui infestate, Parte prima: della teoria, Tipografia Orcesi, Lodi.
Bassi A. (1836) Del mal del segno e di altre malattie dei bachi da seta. Parte seconda: Practica, Tipografia Orcesi, Lodi.
Baum J.A. (1998) Transgenic Bacillus thuringiensis, Phytoprotection 79, 127–130.
Berliner E. (1911) Uber die Schlaffsucht der Mehlmottenraupe, Z. Ges. Getreidew. 3, 63–70.
Berliner E. (1915) Uber die Schlaffsucht der Mehlmottenraupe (Ephestia Kuhniella, Zell.) und ihren Erreger Bacillus thuringiensis, n. sp., Z. Angew. Entomol. 2, 29–56.
Bourguet D. (2004) Resistance to Bacillus thuringiensis toxins in the European corn borer: what chance for Bt maize? Physiol. Entomol. 29, 251–256.
Choma C.T., Surewicz W.K., Kaplan H. (1991) The toxic moeity of the Bacillus thuringiensis protoxin undergoes a conformational change upon activation, Biochem. Biophys. Res. Commun. 179, 933–938.
Chorine V. (1931) Sur l’utilisation des microbes dans la lutte contre la pyrale du mais, Ann. lnst. Pasteur, Paris 46, 326–336.
Crickmore N., Zeigler D.R., Feitelson J., Schnepf E., Lereclus D., Baum J., Van Rie J., Dean D.H. (1998) Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins, Microbiol. Mol. Biol. Rev. 63, 807–813.
de Barjac H., Frachon E. (1990) Classification of Bacillus thuringiensis strains, Entomophaga 35, 233–240.
de Barjac H., Lemille F. (1970) Presence of Flagellar antigenic subfactors in Serotype 3 of Bacillus thuringiensis, J. Invertebr. Pathol. 15, 139–140.
d’Herelle F. (1911) Sur une épizootie de nature bactérienne sévissant sur les sauterelles auMexique, C.R. Acad. Sci. Paris, Ser. D 152, 1413–1415.
d’Herelle F. (1912) Sur la propagation, dans la République Argentine, de l’épizootie des sauterelles du Mexique, C.R. Acad. Sci. Paris, Ser. D 154, 623–625.
d’Herelle F. (1914) Le coccobacille des sauterelles, Ann. Inst. Pasteur, Paris 28, 280–328.
Down R.E., Gatehouse A.M.R., Hamilton W.D.O., Gatehouse J.A. (1996) Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulacorthum solani) when administred in vitro and via transgenic plants in laboratory and glasshouse trials, J. Insect Physiol. 42, 1035–1045.
Dulmage H.D. (1970) Insecticidal activity of HD1, a new isolate of Bacillus thuringiensis var. alesti, J. Invertebr. Pathol. 15, 232–239.
Dulmage H.D. (1981) Insecticidal activity of isolates of Bacillus thuringiensis and their potential for pest control, in: Burges H.D. (Ed.), Microbial Control of Pests and Diseases 1970–1980, Academic Press, London, pp. 193–222.
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.
Ely S. (1993) The engineering of plants to express Bacillus thuringiensis δ-endotoxins, in: Entwistle P.F., Cory J.S., Bailey M.J., Higgs S. (Eds.), Bacillus thuringiensis, An Environmental Biopesticide: Theory and Practice, John Wiley & Sons, Chichester, UK, pp. 105–124.
English L., Slatin S.L. (1990) Mode of action of delta-endotoxins from Bacillus thuringiensis: A comparison with other bacterial toxins, Insect. Biochem. Mol. Biol. 22, 1–7.
Entwistle P.F., Cory J.S., Bailey M.J., Higgs S. (1993) Bacillus thuringiensis, An Environmental Biopesticide: Theory and Practice, John Wiley & Sons, Chichester, UK.
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.
Fischhoff D.A., Bowdish K.S., Perlak F.J., Marrone P.G., McCormick S.H., Neidermeyer J.G., Dean D.A., Kusano-Kretzmer R.T., Mayer E.J., Rochester D.E., Rogers S.G., Fraley R.T. (1987) Insect tolerant tomato plants, Nat. Biotechnol. 5, 807–813.
Gaertner F.H., Quick T.C., Thompson M.A. (1993) CellCap: an encapsulation system for insecticidal biotoxin proteins, in: Kim L. (Ed.), Advanced engineered pesticides, Marcel Dekker, Inc., New York, pp. 73–83.
Goldberg L.J., Margalit J. (1977) A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univittatus, Aedes aegypti and Culex pipiens, Mosq. News 37, 355–358.
Gonzales J.M., Dulmage H.T., Carlton B.C. (1981) Correlation between specific plasmids and delta-endotoxin production in Bacillus thuringiensis, Plasmid. 5, 351–365.
Gonzáles J.M.J., Brown B.J., Carlton B.C. (1982) Transfer of Bacillus thuringiensis plasmids coding for delta-endotoxin among strains of B. thuringiensis and B. cereus, Proc. Natl. Acad. Sci. USA 79, 6951–6955.
Henle J. (1840) Von den Miasmen und Kontagien, Pathologische Untersuchungen, Berlin.
Hergula B. (1930) On the Mortality of Pyrausta nubilalis Hb, Int. Corn Borer Invest. Sci. Repts. 3, 142–147.
Hilbeck A. (2002) Transgenic host plant resistance and non-target effects, in: Letourneau D.K., Burrows B.E. (Eds.), Genetically Engineered Organisms: Assessing Environmental and Human Health Effects, CRC Press, Boca Raton, Fla., pp. 167–185.
Hilder V.A., Gatehouse A.M.R., Sheerman S.E., Barker R.F., Boulter D. (1987) A novel mechanism of insect resistance engineered into tobacco, Nature 333, 160–163.
Hofmann C., Vanderbruggen H., Hofte H., Van Rie J., Jansens S., Van Mellaert H. (1988) Specificity of Bacillus thuringiensis δ-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts, Proc. Natl. Acad. Sci. USA 85, 7844–7848.
Hofte H., Whiteley H.R. (1989) Insecticidal crystal proteins of Bacillus thuringiensis, Microbiol. Rev. 53, 242–255.
Huang D.-F., Zhang J., Song F.-P., Lang Z.-H. (2007) Microbial control and biotechnology research on Bacillus thuringiensis in China, J. Invertebr. Pathol. 95, 175–180.
Husz B. (1930) Field experiments on the application of Bacillus thuringiensis against the corn borer, Int. Corn Borer Invest. Sci. Repts. 3, 91–98.
Ishiwata S. (1901) On a kind of severe flacherie (sotto disease) (No. 1), Dainihon Sanshi Kaiho. 114, 1–5 (original in japanese).
Ishiwata S. (1905) About “sotokin”, a bacillus of a disease of the silkworm, Dainihon Sanshi Kaiho. 160, 1–8 (original in japanese).
Jacobs S.E. (1950) Bacteriological control of the flour moth (Ephestia kuehniella), Proc. Soc. Appl. Bacteriol. 13, 83–91.
James C. (2010) Global status of commercialized transgenic crops, ISAAA Briefs 43 (http://www.isaaa.org).
Johnston K.A., Lee M.J., Brough C., Hilder V.A., Gatehouse A.M.R., Gatehouse J.A. (1995) Protease activities in the larval midgut of Heliotis virescens: Evidence for trypsin and chymotrypsin-like enzymes, Insect. Biochem. Mol. Biol. 25, 375–383.
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.
Knowles B.H. (1994) Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins, Adv. Insect Physiol. 24, 273–308.
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, Nat. Biotechnol. 11, 194–200.
Krassilstschik J.M. (1888) La production industrielle des parasites vegetaux pour la destruction des insectes nuisibles, Bull. Sci. Fr. Belg. 19, 461–472
Krieg A., Huger A.M., Langenbruch G.A., Schnetter W. (1983) Bacillus thuringiensis var. tenebrionis: a new pathotype effective against larvae of Coleoptera, Z. Angew. Entomol. 96, 500–508.
Lampel J.S., Canter G.L., Dimock M.B., Kelly J.L., Anderson J.J., Uratani B.B., Foulke J.S. Jr., Turner J.T. (1994) Integrative cloning, expression, and stability of the cry1A(c) gene from Bacillus thuringiensis subsp. kurstaki in a recombinant strain of Clavibacter xyli subsp. Cynodontis, Appl. Environ. Microbiol. 60, 501–508.
Lecadet M.-M., Dedonder R. (1967) Enzymatic hydrolysis of the crystals of Bacillus thuringiensis by the proteases of Pieris brassicae I. Preparation and fractionation of the lysates, J. Invertebr. Pathol. 9, 310–321.
Lereclus D., Delécluse A., Lecadet M.-M. (1993) Diversity of Bacillus thuringiensis toxins and genes, in: Entwistle P.F., Cory J.S., Bailey M.J., Higgs S. (Eds.), Bacillus thuringiensis, An Environmental Biopesticide: Theory and Practice, John Wiley & Sons Ltd, Chichester, UK, pp. 37–69.
Liu Y.B., Tabashnik B.E. (1997) Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis, Proc. R. Soc. Lond. B 264, 605–610.
Lorenz M.G., Wackernagel W. (1996) Mechanism and consequences of horizontal gene transfer in natural bacterial populations, in: Tomiuk J., Wöhrmann K., Sentker A. (Eds.), Transgenic organisms: Biological and Social implications, Birkhauser Verlag, Basel, Boston Berlin, pp. 45–57.
Martin P.A., Travers R.S. (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates, Appl. Environ. Microbiol. 55, 2437–2442.
Mattes O. (1927) Parasitare Krankheiten der Mehlmottenlarven und Versuche uber ihre Verwendbarkeit als biologisches Bekiampfungsmittel, Sitzber. Ges. Beforder. Ges. Naturw. Marburg. 62, 381–417.
McBride K.E., Svab Z., Schaaf D.J., Hogan P.S., Stalker D.M., Maliga P. (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco, Nat. Biotechnol. 13, 362–365.
McGaughey W.H. (1985) Insect Resistance to the Biological Insecticide Bacillus thuringiensis, Sci. 229, 193–195.
Metalnikov S., Chorine V. (1929) On the Infection of the Gypsy Moth and certain other Insects with Bacterium thuringiensis, Int. Corn. Borer Invest. Sci. Repts. 2, 60–61.
Metalnikov S., Hergula B., Strail D.M. (1930) Experiments on the Application of Bacteria against the Corn Borer, Int. Corn. Borer Invest. Sci. Repts. 3, 148–151.
Metchnikoff E. (1879) Diseases of the larvae of the grain weevil, Insects harmful to agriculture (series), Issue III, Published by the commission attached to the Odessa Zemstvo Office.
Nysten P.H. (1808) Recherches sur les maladies des vers à soie et les moyens de les prévenir, Imprimerie Impériale, Paris.
Ohba M., Mizuki E., Uemori A. (2009) Parasporin, a new anticancer protein group from Bacillus thuringiensis, Anticancer Res. 29, 427–434.
Pasteur L. (1870) Études sur la maladie des vers à soie. Tomes I and II, Gauthier-Villars, Paris.
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.
Pigott C., Ellar D.J. (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity, Microbiol. Mol. Biol. Rev. 71, 255–281.
Richards A.G., Richards P.A. (1977) The peritrophic membranes of insects. Annu. Rev. Entomol. 22, 219–240.
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.
Sanchis V., Bourguet D. (2008) Bacillus thuringiensis: applications in agriculture and insect resistance management. A review, Agron. Sustain. Dev. 28, 11–20.
Schnepf H.E., Whiteley H.R. (1981) Cloning and expression of the Bacillus thuringiensis crystal protein gene in Escherichia coli, Proc. Natl. Acad. Sci. USA 78, 2893–2897.
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.
Shade R.E., Schroeder H.E., Pueyo J.J., Tabe L.M., Murdock L.L., Higgins T.J.V., Chrispeels M.J. (1994) Transgenic pea seeds expressing the alpha-amylase inhibitor of the common bean are resistant to bruchid beetles, Nat. Biotechnol. 12, 793–796.
Smith R.A., Couche G.A. (1991) The phylloplane as a source of Bacillus thuringiensis variants, Appl. Environ. Microbiol. 57, 311–315.
Steinhaus E.A. (1949) Principles of Insect pathology, McGraw-Hill, New-York, USA.
Steinhaus E.A. (1951) Possible use of Bacillus thuringiensis Berliner as an aid in the biological control of the alfalfa caterpillar, Hilgardia 20, 359–381.
Steinhaus E.A. (1956) Microbial control-the emergence of an idea: A brief history of insect pathology through the nineteenth century, Hilgardia 26, 107–160.
Stotzky G. (2000) Persistence and biological activity in soil of insecticidal proteins from Bacillus thuringiensis and of bacterial DNA bound on clays and humic acids, J. Environ. Qual. 29, 691–705.
Tabashnik B.E. (1994) Evolution of resistance to Bacillus thuringiensis, Annu. Rev. Entomol. 39, 47–79.
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.
Tabashnik B.E., Gassmann A.J., Crowder D.W., Carrière Y. (2008) Insect resistance to Bt crops: evidence versus theory, Nat. Biotechnol. 26, 199–202.
Tanada Y., Kaya H.K. (1993) Insect pathology, Academic Press, Inc, San Diego, California, USA.
Thuriaux P. (1996). Les flux de gènes, in: Kahn A. (Ed.), Les plantes transgéniques en agriculture, John Libbey Eurotext. Montrouge, France, pp. 99–110.
Toumanoff C. (1952) A propos d’un bacille pathogène pour les vers A soie au Japon (Bacillus sotto Ishiwata) et ses affinités avec d’autres bacilles entomophytes. Ann. Inst. Pasteur Paris 82, 512–516.
Toumanoff C., Vago C. (1951) L’agent pathogène de la flacherie des vers a soie endémique dans la région des Cevennes: Bacillus cereus var. alesti var. nov., C.R. Hebd. Seances Acad. Sci. 233, 1504–1506.
Vadlamudi R.K., Weber E., Ji I., Ji T.H., Bulla L.A. Jr. (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis, J. Biol. Chem. 270, 5490–5494.
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.
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.
Van Raamsdonk L.W.D., Schouten H.J. (1997) Gene flow and establishment of transgenes in natural plant populations, Acta Botanica Neerlandica 46, 69–84.
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.
Vouk V. (1930) The fight against the Corn Borer in Jugoslavia, Corn Borer Invest. Sci. Repts. 3, 113–115.
Wei J.-Z., Hale K., Carta L., Platzer E., Wong C., Fang S.-C., Aroian R.V. (2003) Bacillus thuringiensis crystal proteins that target nematodes, Proc. Natl. Acad. Sci. USA 100, 2760–2765.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Sanchis, V. From microbial sprays to insect-resistant transgenic plants: history of the biospesticide Bacillus thuringiensis. A review. Agronomy Sust. Developm. 31, 217–231 (2011). https://doi.org/10.1051/agro/2010027
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1051/agro/2010027