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Bacillus thuringiensis : a century of research, development and commercial applications
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Sanahuja, Georgina, Banakar, Raviraj, Twyman, Richard M., Capell, Teresa and Christou, Paul. (2011) Bacillus thuringiensis : a century of research, development and commercial applications. Plant Biotechnology Journal, Vol.9 (No.3). pp. 283-300. ISSN 14677644
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Official URL: http://dx.doi.org/10.1111/j.1467-7652.2011.00595.x
Abstract
Bacillus thuringiensis (Bt) is a soil bacterium that forms spores during the stationary phase of its growth cycle. The spores contain crystals, predominantly comprising one or more Cry and/or Cyt proteins (also known as δ-endotoxins) that have potent and specific insecticidal activity. Different strains of Bt produce different types of toxin, each of which affects a narrow taxonomic group of insects. Therefore, Bt toxins have been used as topical pesticides to protect crops, and more recently the proteins have been expressed in transgenic plants to confer inherent pest resistance. Bt transgenic crops have been overwhelmingly successful and beneficial, leading to higher yields and reducing the use of chemical pesticides and fossil fuels. However, their deployment has attracted some criticism particularly with regard to the potential evolution of pest-resistant insect strains. Here, we review recent progress in the development of Bt technology and the countermeasures that have been introduced to prevent the evolution of resistant insect populations.
| Item Type: | Journal Article |
|---|---|
| Subjects: | Q Science > QR Microbiology S Agriculture > SB Plant culture |
| Divisions: | Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010) |
| Library of Congress Subject Headings (LCSH): | Bacillus thuringiensis, Pesticides, Transgenic plants, Plants -- Disease and pest resistance |
| Journal or Publication Title: | Plant Biotechnology Journal |
| Publisher: | Wiley-Blackwell Publishing Ltd. |
| ISSN: | 14677644 |
| Date: | 25 February 2011 |
| Volume: | Vol.9 |
| Number: | No.3 |
| Page Range: | pp. 283-300 |
| Identification Number: | 10.1111/j.1467-7652.2011.00595.x |
| Status: | Peer Reviewed |
| Publication Status: | Published |
| Access rights to Published version: | Restricted or Subscription Access |
| Funder: | European Research Council (ERC), Spain. Ministerio de Ciencia e Innovación (MICINN), COST Action FA0804, Associated Unit CAVA, Seventh Framework Programme (European Commission) (FP7/2007-2013) |
| Grant number: | BFU2007-61413 (MICINN) |
| References: | Akhurst, R.J., James, W., Bird, L.J. and Beard, C. (2003) Resistance to the Cry1Ac d-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 96, 1290–1299. Arantes, O. and Lereclus, D. (1991) Construction of cloning vectors for Bacillus thuringiensis. Gene, 108, 115–119. Aronson, A. (2002) Sporulation and delta-endotoxin synthesis by Bacillus thuringiensis. Cell. Mol. Life Sci. 59, 417–425. Baum, J.A., Johnson, T.B. and Carlton, B.C. (1999) Bacillus thuringiensis. Natural and recombinant bioinsecticide products. Methods Biotechnol. 5, 189–209. Berry, C., O’Neil, S., Ben-Dov, E., Jones, A.F., Murphy, L., Quail, M.A., Holden, M.T.G., Harris, D., Zaritsky, A. and Parkhill, J. (2002) Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl. Environ. Microbiol. 68, 5082–5095. Boonserm, P., Mo, M., Angsuthanasombat, C. and Lescar, J. (2006) Structure of the functional form of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8- angstrom resolution. J. Bacteriol. 188, 3391–3401. Bourguet, D. (2004) Resistance to Bacillus thuringiensis toxins in the European corn borer: what chance for Bt maize? Physiol. Entomol. 29, 251–256. Brookes, G. and Barfoot, P. (2010) GM Crops: Global Socioeconomic and Environmental Impacts 1996–2008. Dorchester, UK: PG Economics Ltd. Burges, H.D. (2001) Bacillus thuringiensis in pest control: now and the future. Pest Outlook, 12, 90–97. Burges, H.D. and Jones, K.A. (1998a) Formulation of bacteria, viruses and protozoa to control insects. In Formulation of Microbial Biopesticides, Beneficial Microorganisms. Nematodes and Seed Treatments (Burges, H.D., ed), pp. 33–127. Dordrecht: Kluwer Academic Publishers. Burges, H.D. and Jones, K.A. (1998b) Trends in formulation of microorganisms and future research requirements. In Formulation of Microbial Biopesticides, Beneficial Microorganisms, Nematodes and Seed Treatments (Burges, H.D., ed), pp. 311–332. Dordrecht: Kluwer Academic Publishers. Carlton, B.C. and Gawron-Burke, C. (1993) Genetic improvement of Bacillus thuringiensis for bioinsecticide development. In Advanced Engineered Biopesticides (Kim, L., ed), pp. 43–61. NY: Marcel Dekker Inc. Carlton, B.C. and Gonzalez, J.M. (1985) Plasmids and deltaendotoxin production in different subspecies of Bacillus thuringiensis. In Molecular Biology of Microbial Differentiation (Hoch, J.A. and Setlow, Q., eds), pp. 246–252. Washington DC: American Society for Microbiology. Chen, J., Hua, G., Jurat-Fuentes, J.L., Abdullah, M.A. and Adang, M.J. (2007) Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin. Proc. Natl Acad. Sci. U S A, 104, 13901–13906. Christou, P., Capell, T., Kohli, A., Gatehouse, J.A. and Gatehouse, A.M.R. (2006) Recent developments and future prospects in insect pest control in transgenic crops. Trends Plant Sci. 11, 302–308. Crickmore, N. (2006) Beyond the spore – past and future developments of Bacillus thuringiensis as a biopesticide. J. Appl. Microbiol. 101, 616–619. 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. Crickmore, N., Zeigler, D.R., Schnepf, E., Van Rie, J., Lereclus, D., Baum, J., Bravo, A. and Dean, D.H. (2010) Bacillus thuringiensis toxin nomenclature. http://www.lifesci.sussex.ac.uk/Home/ Neil_Crickmore/Bt/. Dutton, A., Klein, H., Romies, J. and Bigler, F. (2002) Uptake of Bt toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla cornea. Ecol. Entomol. 27, 441–447. Faria, C.A., Wa¨ ckers, F.L., Pritchard, J., Barrett, D.A. and Turlings, T.C. (2007) High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS ONE, 2, e600. Fillinger, U., Knols, B.G.J. and Becker, N. (2003) Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and Bacillus sphaericus formulations against Afrotropical anophelines in Western Kenya.Trop. Med. Int. Health, 8, 37–47. Fischhoff, D.A., Bowdish, K.S., Perlak, F.J., Marrone, P.G., McCormick, S.M., 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. Nature Biotechnol. 5, 807–813. Goldberg, L.H. and Margalit, J. (1977) A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex inivitattos, Aedes aegypti and Culexpipiens. Mosq. News, 37, 355–358. Gonza´ lez, J.M., Brown Jr, B.J. and 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. U S A, 79, 6951–6955. Gould, F. (1994) Potential and problems with high-dose strategies for pesticidal engineered crops. Biocontrol Sci. Technol. 4, 451– 461. Hilder, V.A. and Boulter, D. (1999) Genetic engineering of crop plants for insect resistance – a critical review. Crop Prot., 18, 177–191. Hoffmann, M.P., Zalom, F.G., Wilson, L.T., Smilanick, J.M., Malyj, L.D., Kiser, J., Hilder, V.A. and Barnes, W.M. (1992) Field evaluation of transgenic tobacco containing genes encoding Bacillus thuringiensis delta-endotoxin or cowpea trypsin inhibitor: efficacy against Helicoverpa zea (Lepidoptera: Noctuidae). J. Econ. Entomol. 85, 2516–2522. Huang, J., Pray, C. and Rozelle, S. (2002a) Enhancing the crops to feed the poor. Nature, 418, 678–684. Huang, J., Rozelle, S., Pray, C. and Wang, Q. (2002b) Plant biotechnology in China. Science, 295, 674–676. Huang, D.-F., Zhang, J., Song, F.-P. and 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. Rep. 3, 91–98. James, C. (2010) Global Status of Commercialized Biotech ⁄GM Crops: 2009. ISAAA Brief 41-2009. Ithaca, NY: ISAAA. Kaur, S. (2000) Molecular approaches towards development of novel Bacillus thuringiensis biopesticides. World J. Microbiol. Biotechnol. 16, 781–793. 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. Nature Biotechnol. 11, 194–200. Krattiger, A.F. (1996) Insect Resistance in Crops: A Case Study of Bacillus thuringiensis (Bt) and its Transfer to Developing Countries. ISAAA Briefs No. 2. Ithaca, NY: ISAAA. Kronstad, J.W., Schnepf, H.E. and Whiteley, H.R. (1983) Diversity of locations for Bacillus thuringiensis crystal protein genes. J. Bacteriol. 154, 419–428. Kuo, W.S. and Chak, K.F. (1996) Identification of novel cry-type genes from Bacillus thuringiensis strains on the basis of restriction fragment length polymorphism of the PCR-amplified DNA. Appl. Environ. Microbiol. 62, 1369–1377. Lampel, J.S., Canter, G.L., Dimock, M.B., Kelly, J.L., Anderson, J.J., Uratani, B.B., Foulke Jr, J.S. and 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. Lawo, N.C., Wa¨ ckers, F.L. and Romeis, J. (2009) Indian Bt cotton varieties do not affect the performance of cotton aphids. PLoS ONE, 4, e4804. Liao, C., Heckel, D.G. and Akhurst, R. (2002) Toxicity of Bacillus thuringiensis insecticidal proteins for Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae), major pests of cotton. J. Invertebr. Pathol. 80, 55–63. Liu, Y.B. and Tabashnik, B.E. (1997) Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis. Proc. R. Soc. Lond. B, 264, 605–610. Liu, J., Yan, G., Shu, C., Zhao, C., Liu, C., Song, F., Zhou, L., Ma, J., Zhang, J. and Huang, D. (2010) Construction of a Bacillus thuringiensis engineered strain with high toxicity and broad pesticidal spectrum against coleopteran insects. Appl. Microbiol. Biotechnol. 87, 243–249. Lu, Y., Wu, K., Jiang, Y., Xia, B., Li, P., Feng, H., Wyckhuys, K.A. and Guo, Y. (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science, 328, 1151–1154. de Maagd, R.A., Bravo, A. and Crickmore, N. (2001) Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. 17, 193–199. Margalith, Y. and Ben-Dov, E. (2000) Biological control by Bacillus thuringiensis subsp. israelensis. In Insect Pest Management: Techniques for Environmental Protection (Rechcigl, J.E. and Rechcigl, N.A., eds), pp. 243–301. Boca Raton FL: CRC Press. Marra, M.C., Piggott, N.E. and Goodwin, B.K. (2010) The anticipated value of SmartStax for US corn growers. AgBioForum, 13, 1. article 1. 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. and Maliga, P. (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Nature Biotechnol. 13, 362–365. McGaughey, W.H. (1985) Insect resistance to the biological insecticide Bacillus thuringiensis. Science, 229, 193–195. Mehlo, L., Gahakwa, D., Nghia, P.T., Loc, N.T., Capell, T., Gatehouse, J.A., Gatehouse, A.M. and Christou, P. (2005) An alternative strategy for sustainable pest resistance in genetically enhanced crops. Proc. Natl Acad. Sci. U S A, 102, 7812–7816. Monsanto, C. (2010) Press release, 5th March 2010. Available online at: http://www.monsanto.com/newsviews/Pages/india-pinkbollworm. aspx. Mun˜ o´ z-Garay, C., Portugal, L., Pardo-Lo´ pez, L., Jime´ nez-Jua´ rez, N., Arenas, I., Go´ mez, I., Sa´ nchez-Lo´ pez, R., Arroyo, R., Holzenburg, A., Savva, C.G., Sobero´ n, M. and Bravo, A. (2009) Characterization of the mechanism of action of the genetically modified Cry1AbMod toxin that is active against Cry1Ab-resistant insects. Biochim. Biophys. Acta, 1788, 2229– 2237. Naimov, S., Dukiandjiev, S. and de Maagd, R.A. (2003) A hybrid Bacillus thuringiensis delta-endotoxin gives resistance against a coleopteran and a lepidopteran pest in transgenic potato. Plant Biotechnol. J. 1, 51–57. Pardo-Lo´ pez, L., Mun˜ oz-Garay, C., Porta, H., Rodrı´guez-Almaza´ n, C., Sobero´ n, M. and Bravo, A. (2009) Strategies to improve the insecticidal activity of Cry toxins from Bacillus thuringiensis. Peptides, 30, 589–595. Perlak, F.J., Fuchs, R.L., Dean, D.A., McPherson, S.L. and Fischoff, D.A. (1991) Modification of the coding sequence enhances plant expression of insect control genes. Proc. Natl Acad. Sci. U S A, 88, 3324–3328. Perlak, F.J., Stone, T.B., Muskopf, Y.M., Petersen, L.J., Parker, G.B., McPherson, S.A., Wyman, J., Love, S., Reed, G. and Biever, D. (1993) Genetically improved potatoes: protection from damage by Colorado potato beetles. Plant Mol. Biol. 22, 313–321. Porcar, M. and Jua´ rez-Pe´ rez, V. (2003) PCR-based identification of Bacillus thuringiensis. FEMS Microbiol. Rev. 26, 419–432. Pray, C.E., Huang, J., Hu, R. and Rozelle, S. (2002) Five years of Bt cotton in China - the benefits continue. Plant J. 31, 423– 430. Rajamohan, F., Alzate, O., Cotrill, J.A., Curtiss, A. and Dean, D.H. (2006) Protein engineering of Bacillus thuringiensis deltaendotoxin: mutations at domain II of CryIAb enhance receptor affinity and toxicity toward gypsy moth larvae. Proc. Natl Acad. Sci. U S A, 93, 14338–14343. Reed, G.L., Jensen, A.S., Riebe, J.F., Head, G. and Duan, J.J. (2001) Transgenetic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts. Entomologia Experimentalis et Applicata, 100, 89–100. Rodrı´guez-Almaza´ n, C., Zavala, L.E., Mun˜ oz-Garay, C., Jime´ nez- Jua´ rez, N., Pacheco, S., Masson, L., Sobero´ n, M. and Bravo, A. (2009) Dominant negative mutants of Bacillus thuringiensis Cry1Ab toxin function as anti-toxins: demonstration of the role of oligomerization in toxicity. PLoS ONE, 4, e5545. Sanchis, V. and Bourguet, D. (2008) Bacillus thuringiensis: applications in agriculture and insect resistance management. A review. Agron. Sustain. Dev. 28, 11–20. Shelton, A.M., Zhao, J.Z. and Roush, R.T. (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Ann. Rev. Entomol. 47, 845–881. Siegel, J.P. (2000) Bacteria. In Field Manual of Techniques in Invertebrate Pathology (Lacey, L.L. and Kaya, H.K. eds), pp. 209–230. Dordrecht, Netherlands: Kluwer Scientific Publishers. Siegel, J.P. (2001) The mammalian safety of Bacillus thuringiensisbased insecticides. J. Invertebr. Pathol. 77, 13–21. Sobero´ n, M., Gill, S.S. and Bravo, A. (2009) Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cell. Mol. Life Sci. 66, 1337–1349. Subramanian, A. and Qaim, M. (2010) The Impact of Bt cotton on poor households in rural India. J. Dev. Sci. 46, 295–311. Sun, Y. and Park, H.W. (2010) Proteomic analysis of the crystal and spore mixture from Bacillus thuringiensis strains to search for novel mosquitocidal proteins. NCBI database, http:// www.ncbi.nlm.nih.gov/protein/292398077. Tabashnik, B.E., Dennehy, T.J. and Carrie` re, Y. (2005) Delayed resistance to transgenic cotton in pink bollworm. Proc. Natl Acad. Sci. U S A, 102, 15389–15393. Tabashnik, B.E., Gassmann, A.J., Crowder, D.W. and Carrie´ re, Y. (2008) Insect resistance to Bt crops: evidence versus theory. Nature Biotechnol. 26, 199–202. Vaeck, M., Reynaerts, A., Ho¨ fte, H., Jansens, S., De Beuckeleer, M., Dean, C., Zabeau, M., Van Montagu, M. and Leemans, J. (1987) Transgenic plants protected from insect attack. Nature, 328, 33–37. Walters, F.S., deFontes, C.M., Hart, H., Warren, G.W. and Chen, J.S. (2010) Lepidopteran-active variable-region sequence imparts coleopteran activity in eCry3.1Ab, an engineered Bacillus thuringiensis hybrid insecticidal protein. Appl. Environ. Microbiol. 76, 3082–3088. Wang, G., Zhang, J., Song, F., Gu, A., Uwais, A., Shao, T. and Huang, D. (2008) Recombinant Bacillus thuringiensis strain shows high insecticidal activity against Plutella xylostella and Leptinotarsa decemlineata without affecting nontarget species in the field. J. Appl. Microbiol. 105, 1536–1543. Zeilinger, A.R., Andow, D.A., Zwahlen, C. and Stotzky, G. (2010) Earthworm populations in a northern U.S. Cornbelt soil are not affected by long-term cultivation of Bt maize expressing Cry1Ab and Cry3Bb1 proteins. Soil Biol. Biochem. 42, 1284–1292. Zhang, X., Candas, M., Griko, N.B., Taissing, R. and Bulla Jr, L.A. (2006) A mechanism of cell death involving an adenylyl cyclase ⁄ PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc. Natl Acad. Sci. U S A, 103, 9897–9902. Zhang, L., Huang, E., Lin, J., Gelbic, I., Zhang, Q., Guan, Y., Huang, T. and Guan, X. (2010) A novel mosquitocidal Bacillus thuringiensis strain LLP29 isolated from the phylloplane of Magnolia denudata. Microbiol. Res. 165, 133–141. Zhao, J., Jin, L., Yang, Y. and Wu, Y. (2010) Diverse cadherin mutations conferring resistance to Bacillus thuringiensis toxin Cry1Ac in Helicoverpa armigera. Insect Biochem. Mol. Biol. 40, 113–118. |
| URI: | http://wrap.warwick.ac.uk/id/eprint/38371 |
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