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Structure, Biological Activity and Environmental Fate of Insecticidal Bt (Bacillus thuringiensis) Cry Proteins of Bacterial and Genetically Modified Plant Origin

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Molecular Environmental Soil Science

Part of the book series: Progress in Soil Science ((PROSOIL))

Abstract

The properties and environmental fate of insecticidal proteins produced by the bacterium Bacillus thuringiensis are reviewed. These proteins, either produced directly by the bacterium and prepared in formulations of biopesticides or synthesised by genetically modified plants, have important roles to play in the control of agricultural pests and insect vectors of disease. Each strain of the bacterium produces a distinctive cocktail of crystal proteins, known as Cry proteins. The insecticidal properties of each protein are highly target species-specific. The mechanism of action of the proteins and differences between the proteins produced by the bacterium and by GM plants are discussed. Protein nomenclature and structure are briefly reviewed. The published literature on the interactions of Cry proteins with soils, soil minerals and reference clay minerals is reviewed. There is currently no link between protein structure and the extent of interaction with soil components. Hydrophobic interactions may play some part in these interactions. Both field studies and controlled laboratory studies of the persistence of Cry proteins in soil are analysed. There is ongoing debate as to the soil properties that determine the persistence of the proteins. There is very little information available on the environmental relevance of ongoing detection of the toxins in soil, since studies usually assay the protein after chemical extraction with no check on the insecticidal properties of the protein. New research directions are suggested on the basis of both the existing information on the environmental fate of Cry proteins in soil and the knowledge gaps identified.

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References

  • Abbas HK, Accinelli C, Zablotowicz RM et al (2008) Dynamics of mycotoxin and Aspergillus flavus levels in aging Bt and non-Bt corn residues under Mississippi no-till conditions. J Agric Food Chem 56:7578–7585

    Google Scholar 

  • Accinelli C, Koskinen WC, Becker JM et al (2008) Mineralization of the Bacillus thuringiensis Cry1Ac endotoxin in soil. J Agric Food Chem 56:1025–1028

    Google Scholar 

  • Adang MJ, Brody MS, Cardineau G et al (1993) The reconstruction and expression of a Bacillus thuringiensis cryIIIA gene in protoplasts and potato plants. Plant Mol Biol 21:1131–1145

    Google Scholar 

  • Agaisse H, Lereclus D (1995) How does Bacillus thuringiensis produce so much insecticidal crystal protein. J Bacteriol 177:6027–6032

    Google Scholar 

  • Al-Deeb MA, Wilde GE (2003) Effect of Bt corn expressing the Cry3Bb1 toxin for corn rootworm control on aboveground nontarget arthropods. Environ Entomol 32:1164–1170

    Google Scholar 

  • Andersson HC, Arpaia S, Bartsch D et al (2010) Statistical considerations for the safety evaluation of GMOs. EFSA J 8:1250–1259

    Google Scholar 

  • Angsuthanasombat C, Crickmore N, Ellar DJ (1992) Comparison of Bacillus thuringiensis subsp. israelensis CryIVA and CryIVB cloned toxins reveals synergism in vivo. FEMS Microbiol Lett 73:63–68

    Google Scholar 

  • Aragón P, Baselga A, Lobo JM (2010) Global estimation of invasion risk zones for the western corn rootworm Diabrotica virgifera virgifera: integrating distribution models and physiological thresholds to assess climatic favourability. J Appl Ecol 47:1026–1035

    Google Scholar 

  • Barros G, Magnoli C, Reynoso MM et al (2009) Fungal and mycotoxin contamination in Bt maize and non-Bt maize grown in Argentina. World Mycotoxin J 2:53–60

    Google Scholar 

  • Barton KA, Whiteley HR, Yang NS (1987) Bacillus thuringiensis delta-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to Lepidopteran insects. Plant Physiol 85:1103–1109

    Google Scholar 

  • Bauce E, Carisey N, Dupont A et al (2004) Bacillus thuringiensis subsp. kurstaki aerial spray prescriptions for balsam fir stand protection against spruce budworm (Lepidoptera: Tortricidae). J Econ Entomol 97:1624–1634

    Google Scholar 

  • Baumgarte S, Tebbe CC (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Mol Ecol 14:2539–2551

    Google Scholar 

  • Benedict JH, Ring DR (2004) Transgenic crops expressing Bt proteins: current status, challenges and outlook. In: Koul O, Dhaliwal GS (eds) Transgenic crop protection: concepts and strategies. Science Publishers, Enfield, NH, pp 15–84

    Google Scholar 

  • Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516

    Google Scholar 

  • Betz FS, Hammond BG, Fuchs RL (2000) Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regul Toxicol Pharmacol 32:156–173

    Google Scholar 

  • Bietlot H, Carey PR, Choma C et al (1989) Facile preparation and characterization of the toxin from Bacillus thuringiensis var. kurstaki. Biochem J 260:87–91

    Google Scholar 

  • Blackwood CB, Buyer JS (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J Environ Qual 33:832–836

    Google Scholar 

  • Bourguet D (2004) Resistance to Bacillus thuringiensis toxins in the European corn borer: what chance for Bt maize? Physiol Entomol 29:251–256

    Google Scholar 

  • Brar SK, Verma M, Tyaci RD et al (2006) Recent advances in downstream processing and formulations of Bacillus thuringiensis based biopesticides. Process Biochem 41:323–342

    Google Scholar 

  • Bravo A, Gill SS, Soberon M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435

    Google Scholar 

  • Broadwell AH (1994) Molecular biology of Bacillus thuringiensis. Agric Ecosyst Environ 49:27–29

    Google Scholar 

  • Brusetti L, Francia P, Bertolini C et al (2004) Bacterial communities associated with the rhizosphere of transgenic Bt 176 maize (Zea mays) and its non transgenic counterpart. Plant Soil 266:11–21

    Google Scholar 

  • Bryant JE (1994) Application strategies for Bacillus thuringiensis. Agric Ecosyst Environ 49:65–75

    Google Scholar 

  • Burges HD, Hurst JA (1977) Ecology of Bacillus thuringiensis in storage moths. J Invertebr Pathol 30:131–139

    Google Scholar 

  • Carozzi NB, Kramer VC, Warren GW et al (1991) Prediction of insecticidal activity of Bacillus thuringiensis strains by polymerase phain reaction product profiles. Appl Environ Microbiol 57:3057–3061

    Google Scholar 

  • Castaldini M, Turrini A, Sbrana C et al (2005) Impact of Bt corn on rhizospheric and on beneficial mycorrhizal symbiosis and soil eubacterial communities iosis in experimental microcosms. Appl Environ Microbiol 71:6719–6729

    Google Scholar 

  • Cellini F, Chesson A, Colquhoun I et al (2004) Unintended effects and their detection in genetically modified crops. Food Chem Toxicol 42:1089–1125

    Google Scholar 

  • Chang C, Yu YM, Dai SM et al (1993) High level cryIVD and cytA gene expression in Bacillus thuringiensis does not require the 20-kilodalton protein, and the coexpressed gene products are synergistic in their toxicity to mosquitos. Appl Environ Microbiol 59:815–821

    Google Scholar 

  • Chevallier T, Muchaonyerwa P, Chenu C (2003) Microbial utilisation of two proteins adsorbed to a vertisol clay fraction: toxin from Bacillus thuringiensis subsp tenebrionis and bovine serum albumin. Soil Biol Biochem 35:1211–1218

    Google Scholar 

  • Ciosi M, Miller NJ, Kim KS et al (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    Google Scholar 

  • Clark BW, Coats JR (2006) Subacute effects of CrylAb Bt corn litter on the earthworm Eisenia fetida and the springtail Folsomia candida. Environ Entomol 35:1121–1129

    Google Scholar 

  • Clark BW, Phillips TA, Coats JR (2005) Environmental fate and effects of Bacillus thuringiensis (Bt) proteins from transgenic crops: a review. J Agric Food Chem 53:4643–4653

    Google Scholar 

  • Cökmüs C, Sayar AH, Sacilik SC et al (2000) Effects of UV-light on Bacillus sphaericus and its protection by chemicals. J Basic Microbiol 40:215–221

    Google Scholar 

  • Cortet J, Andersen MN, Caul S et al (2006) Decomposition processes under Bt (Bacillus thuringiensis) maize: results of a multi-site experiment. Soil Biol Biochem 38:195–199

    Google Scholar 

  • Crecchio C, Stotzky G (1998) Insecticidal activity and biodegradation of the toxin from Bacillus thuringiensis subsp. kurstaki bound to humic acids from soil. Soil Biol Biochem 30:463–470

    Google Scholar 

  • Crecchio C, Stotzky G (2001) Biodegradation and insecticidal activity of the toxin from Bacillus thuringiensis subsp. kurstaki bound on complexes of montmorillonite-humic acids-Al hydroxypolymers. Soil Biol Biochem 33:573–581

    Google Scholar 

  • Crickmore N (2005) Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol 13:347–350

    Google Scholar 

  • Crickmore N (2006) Beyond the spore – past and future developments of Bacillus thuringiensis as a biopesticide. J Appl Microbiol 101:616–619

    Google Scholar 

  • Crickmore N, Bone EJ, Williams JA et al (1995) Contribution of the individual components of the delta-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensis subsp. israelensis. FEMS Microbiol Lett 131:249–254

    Google Scholar 

  • Crickmore N, Zeigler DR, Feitelson J et al (1998) Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol Mol Biol Rev 62:807–813

    Google Scholar 

  • Crickmore N, Zeigler DR, Schnefp E et al (2010) Bacillus thuringiensis toxin nomenclature. http://www.lifesci.sussex.ac.uk/Home/Neil_Criclmore/Bt/

  • Dale PJ, Clarke B, Fontes EMG (2002) Potential for the environmental impact of transgenic crops. Nat Biotechnol 20:567–574

    Google Scholar 

  • 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

    Google Scholar 

  • de Maagd RA, Bravo A, Berry C et al (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu Rev Genet 37:409–433

    Google Scholar 

  • de Vaufleury A, Kramarz PE, Binet P et al (2007) Exposure and effects assessments of Bt-maize on non-target organisms (gastropods, microarthropods, mycorrhizal fungi) in microcosms. Pedobiologia 51:185–194

    Google Scholar 

  • Delecluse A, Poncet S, Klier A et al (1993) Expression of cryIVA and cryIVB genes, independently or in combination, in a crystal negative strain of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 59:3922–3927

    Google Scholar 

  • Delucca AJ, Simonson J, Larson A (1979) Two new serovars of Bacillus thuringiensis – serovars Dakota and Indiana (serovars 15 and 16). J Invertebr Pathol 34:323–324

    Google Scholar 

  • Devare MH, Jones CM, Thies JE (2004) Effect of Cry3Bb transgenic corn and tefluthrin on the soil microbial community: biomass, activity, and diversity. J Environ Qual 33:837–843

    Google Scholar 

  • Devare M, Londono-R LM, Thies JE (2007) Neither transgenic Bt maize (MON863) nor tefluthrin insecticide adversely affect soil microbial activity or biomass: a 3-year field analysis. Soil Biol Biochem 39:2038–2047

    Google Scholar 

  • Donegan KK, Palm CJ, Fieland VJ et al (1995) Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Appl Soil Ecol 2:111–124

    Google Scholar 

  • Doohan FM, Brennan J, Cooke BM (2003) Influence of climatic factors on Fusarium species pathogenic to cereals. Eur J Plant Pathol 109:755–768

    Google Scholar 

  • Douville M, Gagne F, Masson L et al (2005) Tracking the source of Bacillus thuringiensis Cry1Ab endotoxin in the environment. Biochem Syst Ecol 33:219–232

    Google Scholar 

  • Dubelman S, Ayden BR, Bader BM et al (2005) Cry1Ab protein does not persist in soil after 3 years of sustained Bt corn use. Environ Entomol 34:915–921

    Google Scholar 

  • Dubois NR, Dean DH (1995) Synergism between CryIA insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores, and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) larvae. Environ Entomol 24:1741–1747

    Google Scholar 

  • Einspanier R, Lutz B, Rief S et al (2004) Tracing residual recombinant feed molecules during digestion and rumen bacterial diversity in cattle fed transgene maize. Eur Food Res Technol 218:269–273

    Google Scholar 

  • Escher N, Kach B, Nentwig W (2000) Decomposition of transgenic Bacillus thuringiensis maize by microorganisms and woodlice Porcellio scaber (Crustacea: Isopoda). Basic Appl Ecol 1:161–169

    Google Scholar 

  • Fang M, Kremer RJ, Motavalli PP et al (2005) Bacterial diversity in rhizospheres of nontransgenic and transgenic corn. Appl Environ Microbiol 71:4132–4136

    Google Scholar 

  • Ferré J, Van Rie J (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47:501–533

    Google Scholar 

  • Ferré J, Escriche B, Bel Y et al (1995) Biochemistry and genetics of insect resistance to Bacillus thuringiensis insecticidal crystal proteins. FEMS Microbiol Lett 132:1–7

    Google Scholar 

  • Ferreira L, Molina JC, Brasil C et al (2003) Evaluation of Bacillus thuringiensis bioinsecticidal protein effects on soil microorganisms. Plant Soil 256:161–168

    Google Scholar 

  • Finer JJ, McMullen MD (1990) Transformation of cotton (Gossypium hirsutum L.) via particle bombardment. Plant Cell Rep 8:586–589

    Google Scholar 

  • Flores S, Saxena D, Stotzky G (2005) Transgenic Bt plants decompose less in soil than non-Bt plants. Soil Biol Biochem 37:1073–1082

    Google Scholar 

  • Fujimoto H, Itoh K, Yamamoto M et al (1993) Insect resistant rice generated by introduction of a modified delta-endotoxin gene of Bacillus thuringiensis. Bio/Technology 11:1151–1155

    Google Scholar 

  • Gatehouse AMR, Ferry N, Raemaekers RJM (2002) The case of the monarch butterfly: a verdict is returned. Trends Genet 18:249–251

    Google Scholar 

  • Gazit E, Shai Y (1995) The assembly and arganization of the alpha-5 and alpha-7 helices from the pore-forming domain of Bacillus thuringiensis delta-endotoxin – relevance to a functional model. J Biol Chem 270:2571–2578

    Google Scholar 

  • Giles CH, D’Silva AP, Easton IA (1974) A general treatment and classification of the solute adsorption isotherm: part: II. Experimental interpretation. J Colloid Interface Sci 47:766–778

    Google Scholar 

  • Gill SS, Cowles EA, Pietrantonio PV (1992) The mode of action of Bacillus thuringiensis endotoxins. Annu Rev Entomol 37:615–636

    Google Scholar 

  • Greenplate JT, Penn SR, Shappley Z et al (2000) Bollgard II efficacy: quantification of total lepidopteran activity in a 2-gene product. 2000 Proceedings beltwide cotton conferences, vol 2, pp 1041–1043, San Antonio, 4–8 January 2000

    Google Scholar 

  • Griffiths BS, Caul S, Thompson J et al (2005) A comparison of soil microbial community structure, protozoa and nematodes in field plots of conventional and genetically modified maize expressing the Bacillus thuringiens is CryIAb toxin. Plant Soil 275:135–146

    Google Scholar 

  • Griffiths BS, Caul S, Thompson J et al (2006) Soil microbial and faunal community responses to Bt maize and insecticide in two soils. J Environ Qual 35:734–741

    Google Scholar 

  • Hammond B, Campbell K, Cea J et al (2008) Opportunities for mycotoxin reduction in maize using biotechnology. In: Siantar DP et al (eds) Food contaminants: mycotoxins and food allergens, vol 1001. American Chemical Society, Washington, DC, pp 109–124

    Google Scholar 

  • Hastowo S, Lay BW, Ohba M (1992) Naturally occurring Bacillus thuringiensis in Indonesia. J Appl Bacteriol 73:108–113

    Google Scholar 

  • Haynes CA (1994) Globular proteins at solid/liquid interaces. Colloids Surf B Biointerfaces 2:517–566

    Google Scholar 

  • Helassa N (2008) Devenir de la protéine insecticide Cry1Aa issue de Bacillus thuringiensis (Bt) dans le sol. Thèse de doctorat, Montpellier SupAgro

    Google Scholar 

  • Helassa N, Daudin G, Quiquampoix H, Noinville S, Janot JM, Déjardin P & Staunton S (2010) Mobility of adsorbed Cry1Aa insecticidal toxin from Bacillus thuringiensis (Bt) on montmorillonite measured by Fluorescence Recovery After Photobleaching (FRAP). Phil Mag 90:2365–2371

    Google Scholar 

  • Helassa N, Revault M, Quiquampoix H, Dejardin P, Staunton S Noinville S (2011a) Adsorption on Montmorillonite prevents oligomerization of Bt Cry1Aa Toxin. J Coll Interface Sci 356: 718–725

    Google Scholar 

  • Helassa N, M'Charek A, Quiquampoix H, Noinville S, Dejardin P, Frutos R & Staunton S (2011b) Effects of physicochemical interactions and microbial activity on the persistence of Cry1Aa Bt (Bacillus thuringiensis) toxin in soil. Soil Biol Biochem 43:1089–1097

    Google Scholar 

  • Helassa N, Quiquampoix H, Noinville S et al (2009) Adsorption and desorption of monomeric Bt (Bacillus thuringiensis) Cry1Aa toxin on montmorillonite and kaolinite. Soil Biol Biochem 41:498–504

    Google Scholar 

  • Helgason E, Okstad OA, Caugant DA et al (2000) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis – one species on the basis of genetic evidence. Appl Environ Microbiol 66:2627–2630

    Google Scholar 

  • Herman RA, Wolt JD, Halliday WR (2002) Rapid degradation of the Cry1F insecticidal crystal protein in soil. J Agric Food Chem 50:7076–7078

    Google Scholar 

  • Höfte H, Whiteley HR (1989) Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev 53:242–255

    Google Scholar 

  • Hopkins DW, Gregorich EG (2003) Detection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize. Eur J Soil Sci 54:793–800

    Google Scholar 

  • Hossain F, Pray CE, Lu YM et al (2004) Genetically modified cotton and farmers ’ health in China. Int J Occup Environ Health 10:296–303

    Google Scholar 

  • Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586

    Google Scholar 

  • Ishiwata S (1901) On a kind of severe flacherie (sotto disease). Dainihon Sanshi Kaiho 114:1–5

    Google Scholar 

  • James C (2007) Global status of commercialized biotech/GM crops: 2007. ISAAA Briefs, Ithaca

    Google Scholar 

  • James C (2009) Global status of commercialized biotech/GM crops: 2009. ISAAA Briefs, Ithaca

    Google Scholar 

  • Janot JM, Boissiere M, Thami T et al (2010) Adsorption of alexa-labeled Bt toxin on mica, glass, and hydrophobized glass: study by normal scanning confocal fluorescence. Biomacromolecules 11:1661–1666

    Google Scholar 

  • Johnson DE, McGaughey WH (1996) Contribution of Bacillus thuringiensis spores to toxicity of purified cry proteins towards Indianmeal moth larvae. Curr Microbiol 33:54–59

    Google Scholar 

  • Kaelin P, Morel P, Gadani F (1994) Isolation of Bacillus thuringiensis from stored tobacco and Lasioderma serricorne (F). Appl Environ Microbiol 60:19–25

    Google Scholar 

  • Koskella J, Stotzky G (1997) Microbial utilization of free and clay-bound insecticidal toxins from Bacillus thuringiensis and their retention of insecticidal activity after incubation with microbes. Appl Environ Microbiol 63:3561–3568

    Google Scholar 

  • Koskella J, Stotzky G (2002) Larvicidal toxins from Bacillus thuringiensis subspp. kurstaki, morrisoni (strain tenebrionis), and israelensis have no microbicidal or microbiostatic activity against selected bacteria, fungi, and algae in vitro. Can J Microbiol 48:262–267

    Google Scholar 

  • Kowalchuk GA, Bruinsma M, van Veen JA (2003) Assessing responses of soil microorganisms to GM plants. Trends Ecol Evol 18:403–410

    Google Scholar 

  • Koziel MG, Beland GL, Bowman C et al (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Bio/Technology 11:194–200

    Google Scholar 

  • Kramarz PE, De Vaufleury A, Carey M (2007) Studying the effect of exposure of the snail Helix aspersa to the purified Bt toxin, Cry1Ab. Appl Soil Ecol 37:169–172

    Google Scholar 

  • Lacey LA, Frutos R, Kaya HK et al (2001) Insect pathogens as biological control agents: do they have a future? Biol Control 21:230–248

    Google Scholar 

  • Lee L, Saxena D, Stotzky G (2003) Activity of free and clay-bound insecticidal proteins from Bacillus thuringiensis subsp. israelensis against the mosquito Culex pipiens. Appl Environ Microbiol 69:4111–4115

    Google Scholar 

  • Li J, Derbyshire DJ, Promdonkoy B et al (2001) Structural implications for the transformation of the Bacillus thuringiensis delta-endotoxins from water-soluble to membrane-inserted forms. Biochem Soc Trans 29:571–577

    Google Scholar 

  • Lilley AK, Bailey MJ, Cartwright C et al (2006) Life in earth: the impact of GM plants on soil ecology? Trends Biotechnol 24:9–14

    Google Scholar 

  • Llewellyn D, Cousins Y, Mathews A et al (1994) Expression of Bacillus thuringiensis insecticidal protein genes in transgenic crop plants. Agric Ecosyst Environ 49:85–93

    Google Scholar 

  • Losey JE, Rayor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399:214–214

    Google Scholar 

  • Manachini B, Lozzia GC (2002) First investigations into the effects of Bt corn crop on Nematofauna. Bollettino di Zoologia Agraria e di Bachicoltura 34:85–96

    Google Scholar 

  • Martin PAW, Travers RS (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl Environ Microbiol 55:2437–2442

    Google Scholar 

  • Marvier M, McCreedy C, Regetz J et al (2007) A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–1477

    Google Scholar 

  • Masson L, Mazza A, Sangadala S et al (2002) Polydispersity of Bacillus thuringiensis Cry1 toxins in solution and its effect on receptor binding kinetics. Biochim Biophys Acta 1594:266–275

    Google Scholar 

  • McGaughey WH (1978) Response of Plodia interpunctella Lepidoptera-Pyralidae and Ephestia cautella Lepidoptera-Pyralidae larvae to spores and parasporal crystals of Bacillus thuringiensis. J Econ Entomol 71:687–688

    Google Scholar 

  • McGaughey WH (1985) Insect resistance to the biological insecticide Bacillus thuringiensis. Science 229:193–194

    Google Scholar 

  • McGaughey WH, Whalon ME (1992) Managing insect resistance to Bacillus thuringiensis toxins. Science 258:1451–1455

    Google Scholar 

  • McGuire MR, Shasha BS, Lewis LC et al (1990) Field evaluation of antigranulocytes starch formulations of Bacillus thuringiensis against Ostrinia nubilalis (Lepidoptera, Pyralidae). J Econ Entomol 83:2207–2210

    Google Scholar 

  • Meadows MP, Ellis DJ, Butt J et al (1992) Distribution, frequency, and diversity of Bacillus thuringiensis in an animal feed mill. Appl Environ Microbiol 58:1344–1350

    Google Scholar 

  • Miyasono M, Inagaki S, Yamamoto M et al (1994) Enhancement of delta-endotoxin activity by toxin-free spore of Bacillus thuringiensis against the diamondback moth, Plutella xylostella. J Invertebr Pathol 63:111–112

    Google Scholar 

  • Moar WJ (2003) Breathing new life into insect-resistant plants. Nat Biotechnol 21:1152–1154

    Google Scholar 

  • Moar WJ, Trumble JT, Federici BA (1989) Comparative toxicity of spores and crystals from the NRD-12 and HD-1 strains of Bacillus thuringiensis subsp. kurstaki to neonate beet armyworm (Lepidoptera, Noctuidae). J Econ Entomol 82:1593–1603

    Google Scholar 

  • Moar WJ, Pusztaicarey M, Vanfaassen H et al (1995) Development of Bacillus thuringiensis CryIC resistance by Spodoptera exigua (Hubner) (Lepidoptera, Noctuidae). Appl Environ Microbiol 61:2086–2092

    Google Scholar 

  • Muchaonyerwa P, Chenu C, Pantani OL et al (2002) Adsorption of the insecticidal toxin from Bacillus thuringiensis subspecies tenebrionis to clay fractions of tropical soils. In: Violante A, Huang PM, Bollag J-M (eds) Soil mineral-organic matter-microorganism interactions and ecosystem health 28B. Elsevier, Amsterdam, pp 59–68

    Google Scholar 

  • Muchaonyerwa P, Chevallier T, Pantani OL et al (2006) Adsorption of the pesticidal toxin from Bacillus thuringiensis subsp tenebrionis on tropical soils and their particle-size fractions. Geoderma 133:244–257

    Google Scholar 

  • Naef A, Zesiger T, Defago G (2006) Impact of transgenic Bt maize residues on the mycotoxigenic plant pathogen Fusarium graminearum and the biocontrol agent Trichodearma atroviride. J Environ Qual 35:1001–1009

    Google Scholar 

  • Nayak P, Basu D, Das S et al (1997) Transgenic elite indica rice plants expressing CryIAc delta-endotoxin of Bacillus thuringiensis are resistant against yellow stem borer (Scirpophaga incertulas). Proc Natl Acad Sci USA 94:2111–2116

    Google Scholar 

  • Obrycki JJ, Losey JE, Taylor OR et al (2001) Transgenic insecticidal corn: beyond insecticidal toxicity to ecological complexity. Bioscience 51:353–361

    Google Scholar 

  • O’Callaghan M, Glare TR, Burgess EPJ et al (2005) Effects of plants genetically modified for insect resistance on nontarget organisms. Annu Rev Entomol 50:271–292

    Google Scholar 

  • Ostry V, Ovesna J, Skarkova J et al (2010) A review on comparative data concerning Fusarium mycotoxins in Bt maize and non-Bt isogenic maize. Mycotoxin Res 26:141–145

    Google Scholar 

  • Pagel-Wieder S, Niemeyer J, Fischer WR et al (2007) Effects of physical and chemical properties of soils on adsorption of the insecticidal protein (Cry1Ab) from Bacillus thuringiensis at Cry1Ab protein concentrations relevant for experimental field sites. Soil Biol Biochem 39:3034–3042

    Google Scholar 

  • Palm CJ, Donegan K, Harris D et al (1994) Quantification in soil of Bacillus thuringiensis var. kurstaki delta-endotoxin from transgenic plants. Mol Ecol 3:145–151

    Google Scholar 

  • Palm CJ, Schaller DL, Donegan KK et al (1996) Persistence in soil of transgenic plant produced Bacillus thuringiensis var kurstaki delta-endotoxin. Can J Microbiol 42:1258–1262

    Google Scholar 

  • Parker MW, Feil SC (2005) Pore-forming protein toxins: from structure to function. Prog Biophys Mol Biol 88:91–142

    Google Scholar 

  • Peferoen M (1997) Progress and prospects for field use of Bt genes in crops. Trends Biotechnol 15:173–177

    Google Scholar 

  • Perlak FJ, Deaton RW, Armstrong TA et al (1990) Insect resistant cotton plants. Bio/Technology 8:939–943

    Google Scholar 

  • Perlak FJ, Stone TB, Muskopf YM et al (1993) Genetically improved potatoe – protection from damage by colorado potato beetles. Plant Mol Biol 22:313–321

    Google Scholar 

  • Poncet S, Delecluse A, Klier A et al (1995) Evaluation of synergistic interactions among the CryIVA, CryIVB, and CryIVD toxic components of Bacillus thuringiensis subsp israelensis crystals. J Invertebr Pathol 66:131–135

    Google Scholar 

  • Pont B, Nentwig W (2005) Quantification of Bt-protein digestion and excretion by the primary decomposer Porcellio scaber, fed with two Bt-corn varieties. Biocontrol Sci Technol 15:341–352

    Google Scholar 

  • Quiquampoix H (2008) Enzymes and proteins, interactions with soil-constituent surfaces. In: Chesworth W (ed) Encyclopedia of soil science. Springer, Dordrecht, pp 210–216

    Google Scholar 

  • Quiquampoix H, Ratcliffe RG (1992) A P-31 NMR-study of the adsorption of bovine serum albumin on montmorillonite using phosphate and the paramagnetic cation Mn2+ – modification of conformation with pH. J Colloid Interface Sci 148:343–352

    Google Scholar 

  • Quiquampoix H, Staunton S, Baron MH et al (1993) Interpretation of the pH-dependence of protein adsorption on clay mineral surfaces and its relevance to the understanding of extracellular enzyme activity in soil. Colloids Surf, A Physicochem Eng Asp 75:85–93

    Google Scholar 

  • Ramessar K, Capell T, Twyman RM et al (2009) Calling the tunes on transgenic crops: the case for regulatory harmony. Mol Breed 23:99–112

    Google Scholar 

  • Ramessar K, Capell T, Twyman RM et al (2010) Going to ridiculous lengths-European coexistence regulations for GM crops. Nat Biotechnol 28:133–136

    Google Scholar 

  • Ravoahangimalala O, Charles JF, Schoellerraccaud J (1993) Immunological localization of Bacillus thuringiensis serovar israelensis toxins in midgut cells of intoxicated Anopheles gambiae larvae (Diptera, Culicidae). Res Microbiol 144:271–278

    Google Scholar 

  • Romeis J, Meissle M, Bigler F (2006a) Ecological risk assessment for Bt crops – response. Nat Biotechnol 24:751–753

    Google Scholar 

  • Romeis J, Meissle M, Bigler F (2006b) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71

    Google Scholar 

  • Roush RT (1994) Managing pests and their resistance to Bacillus thuringiensis – can transgenic crops be better than sprays. Biocontrol Sci Technol 4:501–516

    Google Scholar 

  • 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

    Google Scholar 

  • Rui YK, Yi GX, Zhao J et al (2005) Changes of Bt toxin in the rhizosphere of transgenic Bt cotton and its influence on soil functional bacteria. World J Microbiol Biotechnol 21:1279–1284

    Google Scholar 

  • Sander M, Madliger M, Schwarzenbach RP (2010) Adsorption of transgenic insecticidal Cry1Ab protein to SiO2. 1. Forces driving adsorption. Environ Sci Technol 44:8870–8876

    Google Scholar 

  • Saxena D, Stotzky G (2000) Insecticidal toxin from Bacillus thuringiensis is released from roots of transgenic Bt corn in vitro and in situ. FEMS Microbiol Ecol 33:35–39

    Google Scholar 

  • Saxena D, Stotzky G (2001a) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol Biochem 33:1225–1230

    Google Scholar 

  • Saxena D, Stotzky G (2001b) Bt corn has a higher lignin content than non-Bt corn. Am J Bot 88:1704–1706

    Google Scholar 

  • Saxena D, Flores S, Stotzky G (1999) Transgenic plants – insecticidal toxin in root exudates from Bt corn. Nature 402:480–480

    Google Scholar 

  • Saxena D, Flores S, Stotzky G (2002) Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biol Biochem 34:133–137

    Google Scholar 

  • Saxena D, Stewart CN, Altosaar I et al (2004) Larvicidal Cry proteins from Bacillus thuringiensis are released in root exudates of transgenic B. thuringiensis corn, potato, and rice but not of B. thuringiensis canola, cotton, and tobacco. Plant Physiol Biochem 42:383–387

    Google Scholar 

  • Schnepf HE (1995) Bacillus thuringiensis toxins – regulation, activities and structural diversity. Curr Opin Biotechnol 6:305–312

    Google Scholar 

  • Schnepf E, Crickmore N, Van Rie J et al (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806

    Google Scholar 

  • Schrader S, Munchenberg T, Baumgarte S et al (2008) Earthworms of different functional groups affect the fate of the Bt-toxin Cry1Ab from transgenic maize in soil. Eur J Soil Biol 44:283–289

    Google Scholar 

  • Shan GM, Embrey SK, Herman RA et al (2005) Biomimetic extraction of Bacillus thuringiensis insecticidal crystal proteins from soil based on invertebrate gut fluid chemistry. J Agric Food Chem 53:6630–6634

    Google Scholar 

  • Shelton AM, Tang JD, Roush RT et al (2000) Field tests on managing resistance to Bt-engineered plants. Nat Biotechnol 18:339–342

    Google Scholar 

  • 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

    Google Scholar 

  • Shelton AM, Naranjo SE, Romeis J et al (2009) Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies. Transgenic Res 18:317–322

    Google Scholar 

  • Shen RF, Cai H, Gong WH (2006) Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil. Plant Soil 285:149–159

    Google Scholar 

  • Sims SR (1995) Bacillus thuringiensis var kurstaki CryIA(c) protein expressed in transgenic cotton: effects on beneficial and other non-target insects. Southwest Entomol 20:493–500

    Google Scholar 

  • Sims SR, Berberich SA (1996) Bacillus thuringiensis CryIA protein levels in raw and processed seed of transgenic cotton: determination using insect bioassay and ELISA. J Econ Entomol 89:247–251

    Google Scholar 

  • Sims SR, Holden LR (1996) Insect bioassay for determining soil degradation of Bacillus thuringiensis subsp. kurstaki CryIA(b) protein in corn tissue. Environ Entomol 25:659–664

    Google Scholar 

  • Sims SR, Ream JE (1997) Soil inactivation of the Bacillus thuringiensis subsp. kurstaki CryIIA insecticidal protein within transgenic cotton tissue: laboratory microcosm and field studies. J Agric Food Chem 45:1502–1505

    Google Scholar 

  • Sims SR, Berberich SA, Nida DL et al (1996) Analysis of expressed proteins in fiber fractions from insect-protected and glyphosate-tolerant cotton varieties. Crop Sci 36:1212–1216

    Google Scholar 

  • Smith RA, Couche GA (1991) The phylloplane as a source of Bacillus thuringiensis variants. Appl Environ Microbiol 57:311–315

    Google Scholar 

  • 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

    Google Scholar 

  • Stotzky G (2004) Persistence and biological activity in soil of the insecticidal proteins from Bacillus thuringiensis, especially from transgenic plants. Plant Soil 266:77–89

    Google Scholar 

  • Sun CX, Chen LJ, Wu ZJ et al (2007) Soil persistence of Bacillus thuringiensis (Bt) toxin from transgenic Bt cotton tissues and its effect on soil enzyme activities. Biol Fertil Soils 43:617–620

    Google Scholar 

  • Sundaram KMS (1996) Sorptive interactions and binding of delta-endotoxin protein from Bacillus thuringiensis subsp kurstaki in forest soils. J Environ Sci Health B 31:1321–1340

    Google Scholar 

  • Tabashnik BE (1994) Evolution of resistance to Bacillus thuringiensis. Annu Rev Entomol 39:47–79

    Google Scholar 

  • Tabashnik BE (2001) Breaking the code of resistance. Nat Biotechnol 19:922–924

    Google Scholar 

  • Tabashnik BE, Gould F, Carriere Y (2004) Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. J Evol Biol 17:904–912

    Google Scholar 

  • Tabashnik BE, Gassmann AJ, Crowder DW et al (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199–202

    Google Scholar 

  • Tang JD, Shelton AM, VanRie J et al (1996) Toxicity of Bacillus thuringiensis spore and crystal protein to resistant diamondback moth (Plutella xylostella). Appl Environ Microbiol 62:564–569

    Google Scholar 

  • Tapp H, Stotzky G (1995a) Dot-blot enzyme-linked-immunosorbent-assay for monitoring the fate of insecticidal toxins from Bacillus thuringiensis in soil. Appl Environ Microbiol 61:602–609

    Google Scholar 

  • Tapp H, Stotzky G (1995b) Insecticidal activity of the toxins from Bacillus thuringiensis subspecies kurstaki and tenebrionis adsorbed and bound on pure and soil clays. Appl Environ Microbiol 61:1786–1790

    Google Scholar 

  • Tapp H, Stotzky G (1997) Monitoring the insecticidal toxins from Bacillus thuringiensis in soil with flow cytometry. Can J Microbiol 43:1074–1078

    Google Scholar 

  • Tapp H, Stotzky G (1998) Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biol Biochem 30:471–476

    Google Scholar 

  • Tapp H, Calamai L, Stotzky G (1994) Adsorption and binding of the insecticidal proteins from Bacillus thuringiensis subsp. kurstaki and subsp. tenebrionis on clay minerals. Soil Biol Biochem 26:663–679

    Google Scholar 

  • Turrini A, Sbrana C, Nuti MP et al (2004) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266:69–75

    Google Scholar 

  • Vacher C, Bourguet D, Rousset F et al (2003) Modelling the spatial configuration of refuges for a sustainable control of pests: a case study of Bt cotton. J Evol Biol 16:378–387

    Google Scholar 

  • Vanfrankenhuyzen K, Gringorten JL, Milne RE et al (1991) Specificity of activated cryia proteins from bacillus-thuringiensis subsp kurstaki Hd-1 for defoliating forest Lepidoptera. Appl Environ Microbiol 57:1650–1655

    Google Scholar 

  • Venkateswerlu G, Stotzky G (1992) Binding of the protoxin and toxin proteins of Bacillus thuringiensis subsp. kurstaki on clay minerals. Curr Microbiol 25:225–233

    Google Scholar 

  • Vercesi ML, Krogh PH, Holmstrup M (2006) Can Bacillus thuringiensis (Bt) corn residues and Bt-corn plants affect life-history traits in the earthworm Aporrectodea caliginosa? Appl Soil Ecol 32:180–187

    Google Scholar 

  • Vettori C, Paffetti D, Saxena D et al (2003) Persistence of toxins and cells of Bacillus thuringiensis subsp. kurstaki introduced in sprays to Sardinia soils. Soil Biol Biochem 35:1635–1642

    Google Scholar 

  • Wang HY, Ye QF, Wang W et al (2006) Cry1Ab protein from Bt transgenic rice does not residue in rhizosphere soil. Environ Pollut 143:449–455

    Google Scholar 

  • Watkinson I (1994) Global view of present and future markets for Bt products. Agric Ecosyst Environ 49:3–7

    Google Scholar 

  • West AW, Burges HD, White RJ et al (1984) Persistence of Bacillus thuringiensis parasporal crystal insecticidal activity in soil. J Invertebr Pathol 44:128–133

    Google Scholar 

  • Whalon ME, Wingerd BA (2003) Bt: mode of action and use. Arch Insect Biochem Physiol 54:200–211

    Google Scholar 

  • Wu D, Johnson JJ, Federici BA (1994) Synergism of mosquitocidal toxicity between CytA and CryIVD proteins using inclusions produced from cloned genes of Bacillus thuringiensis. Mol Microbiol 13:965–972

    Google Scholar 

  • Wu WX, Ye QF, Min H (2004a) Effect of straws from Bt-transgenic rice on selected biological activities in water-flooded soil. Eur J Soil Biol 40:15–22

    Google Scholar 

  • Wu WX, Ye QF, Min H et al (2004b) Bt-transgenic rice straw affects the culturable microbiota and dehydrogenase and phosphatase activities in a flooded paddy soil. Soil Biol Biochem 36:289–295

    Google Scholar 

  • Xue K, Luo HF, Qi HY et al (2005) Changes in soil microbial community structure associated with two types of genetically engineered plants analyzing by PLFA. J Environ Sci (China) 17:130–134

    Google Scholar 

  • Yanni SF, Whalen JK, Ma JK (2010) Crop residue chemistry, decomposition rates, and CO2 evolution in Bt and non-Bt corn agroecosystems in North America: a review. Nutr Cycl Agroecosyst 87:277–293

    Google Scholar 

  • Yu L, Berry RE, Croft BA (1997) Effects of Bacillus thuringiensis toxins in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Orbatidae). J Econ Entomol 90:113–118

    Google Scholar 

  • Zambryski P, Joos H, Genetello C et al (1983) Ti-plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity. EMBO J 2:2143–2150

    Google Scholar 

  • Zhao JZ, Fan YL, Fan XL et al (1999) Evaluation of transgenic tobacco expressing two insecticidal genes to delay resistance development of Helicoverpa armigera. Chin Sci Bull 44:1871–1874

    Google Scholar 

  • Zhao J, Rui C, Lu M et al (2000) Monitoring and management of Helicoverpa armigera resistance to transgenic Bt cotton in Northern China. Resist Pest Manage 11:28–31

    Google Scholar 

  • Zhou XY, Huang QY, Chen SW et al (2005) Adsorption of the insecticidal protein of Bacillus thuringiensis on montmorillonite, kaolinite, silica, goethite and Red soil. Appl Clay Sci 30:87–93

    Google Scholar 

  • Zhou XY, Huang QY, Cai P et al (2007) Adsorption and insecticidal activity of toxin from Bacillus thuringiensis on rectorite. Pedosphere 17:513–521

    Google Scholar 

  • Zwahlen C, Hilbeck A, Gugerli P et al (2003a) Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Mol Ecol 12:765–775

    Google Scholar 

  • Zwahlen C, Hilbeck A, Howald R et al (2003b) Effects of transgenic Bt corn litter on the earthworm Lumbricus terrestris. Mol Ecol 12:1077–1086

    Google Scholar 

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  1. INRA-Eco&Sols (Ecologie Fonctionnelle et Biogéochimie des Sols et des Agrosystémes), place Viala, 34060, Montpellier, France

    Nordine Helassa, Hervé Quiquampoix & Siobhán Staunton

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  1. Nordine Helassa
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  2. Hervé Quiquampoix
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  3. Siobhán Staunton
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Correspondence to Siobhán Staunton .

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  1. Institute of Soil and Water Resources, Zhejiang University, Hangzhou, China, People's Republic

    Jianming Xu

  2. Delaware Environmental Institute, University of Delaware, Newark, Delaware, USA

    Donald L. Sparks

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Helassa, N., Quiquampoix, H., Staunton, S. (2013). Structure, Biological Activity and Environmental Fate of Insecticidal Bt (Bacillus thuringiensis) Cry Proteins of Bacterial and Genetically Modified Plant Origin. In: Xu, J., Sparks, D. (eds) Molecular Environmental Soil Science. Progress in Soil Science. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4177-5_3

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