Comparative Aspects of Cry Toxin Usage in Insect Control

Chapter

Abstract

Crystalline (Cry) endotoxins from Bacillus thuringiensis (Bt) and related toxins are currently being used as active ingredients of bacterial insecticides and as expressed proteins in genetically modified plants. While both approaches take advantage of the specificity of Cry toxins against various insect orders, there are characteristic differences between these technologies in (i) form of application; (ii) compatibility with agrotechnologies; (iii) composition of the active ingredients; and (iv) their environmental fate. The technical advantage of Bt plants is that they eliminate labor- and energy-demanding field applications of insecticides against insect pests manageable with Cry toxins. In turn, however, Bt plants continuously produce Cry toxin during vegetation. As a result, these Bt plants do not comply with the principle of integrated pest management, as Cry toxin administration cannot be limited to the duration of the occurrence of the insect pest targeted. Bt insecticides and Bt plants may also differ in their active ingredients (bacterial protoxins and plant-expressed preactivated toxin), which in addition to pesticide registration issues, has pronounced effects on Cry toxin resistance and environmental persistence in stubble.

References

  1. Adamczyk JJ Jr, Adam LC, Hardee DD (2001) Field efficacy and seasonal expression profiles for terminal leaves of single and double Bacillus thuringiensis toxin cotton genotypes. J Econ Entomol 94:1589–1593PubMedCrossRefGoogle Scholar
  2. Anderson PL, Hellmich RL, Prasifka JR, Lewis LC (2005) Effects on fitness and behavior of monarch butterfly larvae exposed to a combination of Cry1Ab-expressing corn anthers and pollen. Environ Entomol 34:944–952CrossRefGoogle Scholar
  3. Andow DA, Lövei GL, Arpaia S (2006) Ecological risk assessment for Bt crops. Nat Biotechnol 24:749–751PubMedCrossRefGoogle Scholar
  4. Arvidson H, Dunn PE, Strnad S, Aronson AI (1989) Specificity of Bacillus thuringiensis for lepidopteran larvae: factors involved in vivo and in the structure of a purified protoxin. Mol Microbiol 3:1533–1543PubMedCrossRefGoogle Scholar
  5. Bagla P (2010) Hardy cotton-munching pests are latest blow to GM crops. Science 327:1439PubMedCrossRefGoogle Scholar
  6. Bakonyi G, Szira F, Kiss I, Villányi I, Seres A, Székács A (2006) Preference tests with collembolas on isogenic and Bt-maize. Eur J Soil Biol 42:S132–S135CrossRefGoogle Scholar
  7. Bakonyi G, Dolezsai A, Mátrai N, Székács A (2011) Long-term effects of Bt-maize (MON 810) consumption on the Collembolan Folsomia candida, over multiple generations: a laboratory study. Insects 2:243–252CrossRefGoogle Scholar
  8. Baum JA, Malvar T (1995) Regulation of insecticidal crystal protein production in Bacillus thuringiensis. Mol Microbiol 18:1–12PubMedCrossRefGoogle Scholar
  9. 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 14:2539–2551PubMedCrossRefGoogle Scholar
  10. Bernhard K, Utz R (1993) Production of Bacillus thuringiensis insecticides for experimental and commercial uses. In: Entwistle PF, Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringiensis, an environmental biopesticide: theory and practice. Wiley, New York, pp 255–267Google Scholar
  11. Betz FS, Hammond BG, Fuchs RL (2000) Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regul Toxicol Pharmacol 32:156–173PubMedCrossRefGoogle Scholar
  12. Bietlot HPL, Vishnubhatla I, Carey PR, Pozsgay M, Kaplan H (1990) Characterization of the cysteine residues and disulphide linkages in the protein crystal of B. thuringiensis. J Biochem 267:309–315Google Scholar
  13. Blackwood CB, Buyer JS (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J Environ Qual 33:832–836PubMedCrossRefGoogle Scholar
  14. Bøhn T, Primicerio R, Hessen DO, Traavik T (2008) Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch Environ Contam Toxicol 55:584–592PubMedCrossRefGoogle Scholar
  15. Bøhn T, Traavik T, Primicerio R (2010) Demographic responses of Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19:419–430PubMedCrossRefGoogle Scholar
  16. Bravo A, Soberón M (2008) How to cope with insect resistance to Bt toxins? Trends Biotechnol 26:573–579PubMedCrossRefGoogle Scholar
  17. Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435PubMedCrossRefGoogle Scholar
  18. Broderick NA, Raffa KF, Handelsman J (2006) Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci USA 103:15196–15199PubMedCrossRefGoogle Scholar
  19. Bruns HA, Abel CA (2003) Nitrogen fertility effects on Bt delta-endotoxin and nitrogen concentrations of maize during-early growth. Agron J 95:207–211CrossRefGoogle Scholar
  20. Bruns HA, Abel CA (2004) Effects of nitrogen fertility on Bt endotoxin levels in Bt hybrid maize. In: 4th proceedings of the international crop science congress. Poster 3.8. The Regional Institute Ltd, Gosford, Australia. (http://www.cropscience.org.au/icsc2004/poster/3/8/453_brunsha.htm)
  21. Calsamiglia S, Hernandez B, Hartnell GF, Phipps R (2007) Effects of corn silage derived from a genetically modified variety containing two transgenes on feed intake, milk production, and composition, and the absence of detectable transgenic deoxyribonucleic acid in milk in Holstein dairy cows. J Dairy Sci 90:4718–4723PubMedCrossRefGoogle Scholar
  22. Cannon RJC (2000) Bt transgenic crops: risks and benefits. Integr Pest Manag Rev 5:151–173CrossRefGoogle Scholar
  23. Castaldini M, Turrini A, Sbrana C, Benedetti A, Marchionni M, Mocali S, Fabiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovannetti M (2005) Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 71:6719–6729PubMedCrossRefGoogle Scholar
  24. Castle LA, Wu G, McElroy D (2006) Agricultural input traits: past, present and future. Curr Opin Biotechol 17:105–112CrossRefGoogle Scholar
  25. Chambers CP, Whiles MR, Rosi-Marshall EJ, Tank JL, Royer TV, Griffiths NA, Evans-White MA, Stojak AR (2010) Responses of stream macroinvertebrates to Bt maize leaf detritus. Ecol Appl 20:1949–1960PubMedCrossRefGoogle Scholar
  26. Chen M, Ye G, Liu Z, Fang Q, Hu C, Peng Y, Shelton AM (2009) Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology 18:230–238PubMedCrossRefGoogle Scholar
  27. Chestukhina GG, Kostina LI, Mikhailova AL, Tyurin SA, Klepikova FS, Stepanov VM (1982) Crystal-forming proteins of Bacillus thuringiensis. Arch Microbiol 132:159–162CrossRefGoogle Scholar
  28. Choma CT, Surewicz WK, Carey PR, Pozsgay M, Kaplan H (1990) Unusual proteolysis of the protoxin and toxin from Bacillus thuringiensis. J Protein Chem 9:87–94PubMedCrossRefGoogle Scholar
  29. 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 53:4643–4653PubMedCrossRefGoogle Scholar
  30. Clements MJ, Campbell KW, Maragos CM, Pilcher C, Headrick JM, Pataky JK, White DG (2003) Influence of Cry1Ab protein and hybrid genotype on fumonisin contamination and Fusarium ear rot of corn. Crop Sci 43:1283–1293CrossRefGoogle Scholar
  31. Cortet J, Griffiths BS, Bohanec M, Demsar D, Andersen MN, Caul S, Birch ANE, Pernin C, Tabone E, de Vaufleury A, Ke X, Krogh PH (2007) Evaluation of effects of transgenic Bt maize on microarthropods in a European multi-site experiment. Pedobiologia 51:207–250CrossRefGoogle Scholar
  32. Crespo ALB, Spencer TA, Nekl E, Pusztai-Carey M, Moar WJ, Siegfried BD (2008) Comparison and validation of methods to quantify Cry1Ab toxin from Bacillus thuringiensis for standardization of insect bioassays. Appl Environ Microbiol 74:130–135PubMedCrossRefGoogle Scholar
  33. Crespo ALB, Spencer TA, Alves AP, Hellmich RL, Blankenship EE, Magalhäesa LC, Siegfried BD (2009) On-plant survival and inheritance of resistance to Cry1Ab toxin from Bacillus thuringiensis in a field-derived strain of European corn borer, Ostrinia nubilalis. Pest Manag Sci 65:1071–1081PubMedCrossRefGoogle Scholar
  34. Crickmore N, Zeigler DR, Feitelson J, Schnepf E, Van Rie J, Lereclus D, Baum J, Dean DH (1998) Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol Mol Biol Rev 62:807–813PubMedGoogle Scholar
  35. Crickmore N, Zeigler DR, Schnepf E, Van Rie J, Lereclus D, Baum J, Bravo A, Dean DH (2009) Bacillus thuringiensis toxin nomenclature. (http://www.lifesci.sussex.ac.uk/home/Neil_Crickmore/Bt/)
  36. Darvas B (2011) GM plants and resistance – resistance-management. In: Darvas B, Székács A (eds) Hungarian background on views of 1st generation genetically modified plants. Agricultural Committee of the Hungarian Parliament, Budapest, Hungary, pp 140–141. (http://www.kormany.hu/download/2/9d/20000/GenetEM.pdf)
  37. Darvas B, Polgár LA (1998) Novel type insecticides: specificity and effects on non-target organisms. In: Ishaaya I, Degheele D (eds) Insecticides with novel modes of action, mechanism and application. Springer, Berlin, pp 188–259Google Scholar
  38. Darvas B, Csóti A, Gharib A, Peregovits L, Ronkay L, Lauber É, Polgár AL (2004) Some data to the risk analysis of Bt-corn pollen and protected Lepidoptera species in Hungary. Növényvédelem 40:441–449 (in Hungarian)Google Scholar
  39. Darvas B, Bánáti H, Takács E, Lauber É, Szécsi Á, Székács A (2011) Relationships of Helicoverpa armigera, Ostrinia nubilalis and Fusarium verticillioides on MON 810 maize. Insects 2:1–11CrossRefGoogle Scholar
  40. de Barjac H (1978) Une nouvelle variété de Bacillus thuringiensis très toxique pour les moustiques: Bacillus thuringiensis subsp. israelensis serotype 14. C R Acad Sci Paris D 286:797–800Google Scholar
  41. de Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu Rev Genet 37:409–433PubMedCrossRefGoogle Scholar
  42. de Vendômois JS, Roullier F, Cellier D, Séralini G-E (2009) A comparison of the effects of three GM corn varieties on mammalian health. Int J Biol Sci 5(7):706–726PubMedCrossRefGoogle Scholar
  43. de Vendômois JS, CellierD VC, Clair E, Mesnage R, Séralini G-E (2010) Debate on GMOs health risks after statistical findings in regulatory tests. Int J Biol Sci 6:590–598PubMedCrossRefGoogle Scholar
  44. Dively GP, Rose R, Sears MK, Hellmich RL, Stanley-Horn DE, Calvin DD, Russo JM, Anderson PL (2004) Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis. Environ Entomol 33:1116–1125CrossRefGoogle Scholar
  45. Donkin SS, Velez JC, Totten AK, Stanisiewski EP, Hartnell GF (2003) Effects of feeding silage and grain from glyphosate-tolerant or insect-protected corn hybrids on feed intake, ruminal digestion, and milk production in dairy cattle. J Dairy Sci 86:1780–1788PubMedCrossRefGoogle Scholar
  46. Doull J, Gaylor D, Greim HA, Lovell DP, Lynch B, Munro IC (2007) Report of an expert panel on the reanalysis by Séralini et al. (2007) of a 90-day study conducted by Monsanto in support of the safety of a genetically modified corn variety (MON 863). Food Chem Toxicol 45:2073–2085PubMedCrossRefGoogle Scholar
  47. Douville M, Gagné F, Masson L, McKay J, Blaise C (2001) Tracking the source of Bacillus thuringiensis Cry1Ab endotoxin in the environment. Biochem Syst Ecol 33:219–232CrossRefGoogle Scholar
  48. Ermolli M, Fantozzi A, Marini M, Scotti D, Balla B, Hoffmann S, Querci M, Paoletti C, Van den Eede G (2006a) Food safety: screening tests used to detect and quantify GMO proteins. Accredit Qual Assur 11:55–57CrossRefGoogle Scholar
  49. Ermolli M, Prospero A, Balla B, Querci M, Mazzeo A, Van Den Eede G (2006b) Development of an innovative immunoassay for CP4EPSPS and Cry1AB genetically modified protein detection and quantification. Food Addit Contam 23:876–882PubMedCrossRefGoogle Scholar
  50. European Council (1992) Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. OJ L 206, 22.7.1992, pp 1–7Google Scholar
  51. European Environment Agency (2002) Europe’s biodiversity – biogeographical regions and seas. In: Pinborg U, Larsson TJ (eds) European Environment Agency, Copenhagen, Denmark. (http://www.eea.europa.eu/publications/report_2002_0524_154909)
  52. European Food Safety Authority (2004) Opinion of the scientific panel on genetically modified organisms on a request from the Commission related to the notification for the placing on the market of insect protected genetically modified maize MON 863 and MON 863 x MON 810, for import and processing, under Part C of Directive 2001/18/EC from Monsanto. EFSA J 49:1–25Google Scholar
  53. European Food Safety Authority (2005) Opinion of the scientific panel on genetically modified organisms on an application (Reference EFSAGMO-DE-2004-03) for the placing on the market of insect-protected genetically modified maize MON 863 x MON 810, for food and feed use, under Regulation (EC) No 1829/2003 from Monsanto. EFSA J 252:1–23Google Scholar
  54. European Food Safety Authority (2007) Statement of the scientific panel on genetically modified organisms on the analysis of data from a 90-day rat feeding study with MON 863 maize. doi:10.2903/j.efsa.2007.753. (http://www.efsa.europa.eu/en/efsajournal/pub/753.htm)
  55. European Food Safety Authority (2009a) Technical meeting between EFSA GMO panel environmental experts and environmental experts from Member States (May 26, 2009). European Food Safety Authority, Parma, Italy. (http://www.efsa.europa.eu/en/events/event/gmo090526.htm)
  56. European Food Safety Authority (2009b) Applications (EFSA-GMO-RX-MON810) for renewal of authorisation for the continued marketing of (1) existing food and food ingredients produced from genetically modified insect resistant maize MON810; (2) feed consisting of and/or containing maize MON810, including the use of seed for cultivation; and of (3) food and feed additives, and feed materials produced from maize MON810, all under Regulation (EC) No 1829/2003 from Monsanto. EFSA J 1149:1–85Google Scholar
  57. Fantozzi A, Ermolli M, Marini M, Scotti D, Balla B, Querci M, Langrell SR, Van den Eede G (2007) First application of a microsphere-based immunoassay to the detection of genetically modified organisms (GMOs): quantification of Cry1Ab protein in genetically modified maize. J Agric Food Chem 55:1071–1076PubMedCrossRefGoogle Scholar
  58. Fearing PL, Brown D, Vlachos D, Meghji M, Privalle L (1997) Quantitative analysis of CryIA(b) expression in Bt maize plants, tissues, and silage and stability of expression over successive generations. Mol Breed 3(3):169–176CrossRefGoogle Scholar
  59. Federici BA, Lüthy P, Ibarra JE (1990) Parasporal body of Bacillus thuringiensis israelensis. Structure, protein composition, and toxicity. In: de Barjac H, Sutherland DJ (eds) Bacterial control of mosquitoes and black flies: biochemistry, genetics and applications of Bacillus thuringiensis israelensis. Rutgers University Press, New Brunswick, pp 16–44CrossRefGoogle Scholar
  60. Ferré J, Van Rie J (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47:501–533PubMedCrossRefGoogle Scholar
  61. Folcher L, Jarry M, Weissenberger A, Gérault F, Eychenne N, Delos M, Regnault-Roger C (2009) Comparative activity of agrochemical treatments on mycotoxin levels with regard to corn borers and Fusarium mycoflora in maize (Zea mays L.) fields. Crop Prot 28:302–308CrossRefGoogle Scholar
  62. Folcher L, Delos M, Marengue E, Jarry M, Weissenberger A, Eychenne N, Regnault-Roger C (2010) Lower mycotoxin levels in Bt maize grain. Agron Sustain Dev 30:711–719CrossRefGoogle Scholar
  63. Füsti Molnár G (2011) Results of the Hungarian variety evaluation of genetically modified varieties awaiting government authorization. In: Darvas B, Székács A (eds) Hungarian background on views of 1st generation genetically modified plants. Agricultural Committee of the Hungarian Parliament, Budapest, Hungary, pp 125–128. (http://www.kormany.hu/download/2/9d/20000/GenetEM.pdf)
  64. Gassmann A, Carrière Y, Tabashnik BE (2009) Fitness costs of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 54:147–163PubMedCrossRefGoogle Scholar
  65. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS One 6(7):e22629. doi:10.1371/journal.pone.0022629 PubMedCrossRefGoogle Scholar
  66. Gelernter W (2004) The rise and fall of Bacillus thuringiensis tenebrionis. Phytoparasitica 32:321–324CrossRefGoogle Scholar
  67. Gill SS, Cowles EA, Pietrantonio PV (1992) The mode of action of Bacillus thuringiensis endotoxins. Annu Rev Entomol 37:615–634PubMedCrossRefGoogle Scholar
  68. Goldberg LJ, Margalit J (1977) A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univittatus, Aedes aegypti and Culex pipiens. Mosq News 37:355–358Google Scholar
  69. Gómez I, Pardo-López L, Munoz-Garay C, Fernandez LE, Pérez C, Sánchez J, Soberón M, Bravo A (2007) Role of receptor interaction in the mode of action of insecticidal Cry and Cyt toxins produced by Bacillus thuringiensis. Peptides 28:169–173PubMedCrossRefGoogle Scholar
  70. Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol 43:701–726PubMedCrossRefGoogle Scholar
  71. Graf J (2011) Shifting paradigm on Bacillus thuringiensis toxin and a natural model for Enterococcus faecalis Septicemia. mBio 2. doi:10.1128/mBio.00161-11
  72. Griffiths BS, Caul S, Thompson J, Birch AN, Scrimgeour C, Cortet J, Foggo A, Hackett CA, Krogh PH (2006) Soil microbial and faunal community responses to Bt maize and insecticide in two soils. J Environ Qual 35:734–741PubMedCrossRefGoogle Scholar
  73. Grothaus GD, Bandla M, Currier T, Giroux R, Jenkins GR, Lipp M, Shan G, Stave JW, Pantella V (2006) Immunoassay as an analytical tool in agricultural biotechnology. J AOAC Int 89:913–928PubMedGoogle Scholar
  74. Hammock BD, Gee SJ, Harrison RO, Jung F, Goodrow M, Li Q-X, Lucas AD, Székács A, Sundaram KMS (1991) Immunochemical technology in environmental analysis: addressing critical problems. In: Van Emon J, Mumma RO (eds) Immunochemical methods for environmental analysis, vol 442, ACS Symp Ser. American Chemical Society, Washington, DC, pp 112–139CrossRefGoogle Scholar
  75. Hammond BG, Dudek R, Lemen JK, Nemeth MA (2006) Results of a 90-day safety assurance study with rats fed grain from corn borer-protected corn. Food Chem Toxicol 44:1092–1099PubMedCrossRefGoogle Scholar
  76. Harwood JD, Wallin WG, Obrycki JJ (2005) Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol Ecol 14:2815–2823PubMedCrossRefGoogle Scholar
  77. Heszky L (2011a) Scientific problems associated with the cultivation of transgenic (GM) crops. In: Darvas B, Székács A (eds) Hungarian background on views of 1st generation genetically modified plants). Agricultural Committee of the Hungarian Parliament, Budapest, Hungary, pp 130–135. (http://www.kormany.hu/download/2/9d/20000/GenetEM.pdf)
  78. Heszky L (2011b) Coexistence is professionally unacceptable, practically unaccomplishable. In: Darvas B, Székács A (eds) Hungarian background on views of 1st generation genetically modified plants). Agricultural Committee of the Hungarian Parliament, Budapest, Hungary, pp 119–122. (http://www.kormany.hu/download/2/9d/20000/GenetEM.pdf)
  79. Hickle LA, Fitch WL (1990) Analytical chemistry of Bacillus thuringiensis. An overview. In: Hickle LA, Fitch WL (eds) Analytical chemistry of Bacillus thuringiensis, vol 432, ACS Symp Ser. American Chemical Society, Washington, DC, pp 1–8Google Scholar
  80. Hilbeck A (2001) Implications of transgenic, insecticidal plants for insect and plant biodiversity. Perspect Plant Ecol Evol Syst 4:43–61CrossRefGoogle Scholar
  81. Hilbeck A, Schmidt JEU (2006) Another view on Bt proteins – How specific are they and what else might they do? Biopesticides Int 2:1–50Google Scholar
  82. 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 54:793–800CrossRefGoogle Scholar
  83. Huber HE, Luthy P, Rudolf H-R, Cordier J-L (1981) The subunits of the parasporal crystal of Bacillus thuringiensis: size linkage and toxicity. Arch Microbiol 129:14–18CrossRefGoogle Scholar
  84. Icoz I, Stotzky G (2008a) Cry3Bb1 protein from Bacillus thuringiensis in root exudates and biomass of transgenic corn does not persist in soil. Transgenic Res 17:609–620PubMedCrossRefGoogle Scholar
  85. Icoz I, Stotzky G (2008b) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586CrossRefGoogle Scholar
  86. Icoz I, Saxena D, Andow DA, Zwahlen C, Stotzky G (2008) Microbial populations and enzyme activities in soil in situ under transgenic corn expressing Cry proteins from Bacillus thuringiensis. J Environ Qual 37:647–662PubMedCrossRefGoogle Scholar
  87. Icoz I, Andow D, Zwahlen C, Stotzky G (2009) Is the Cry1Ab protein from Bacillus thuringiensis (Bt) taken up by plants from soils previously planted with Bt corn and by carrot from hydroponic culture? Bull Environ Contam Toxicol 83:48–58PubMedCrossRefGoogle Scholar
  88. Ives AR, Glaum PR, Ziebarth NL, Andow DA (2011) The evolution of resistance to two-toxin pyramid transgenic crops. Ecol Appl 21:503–515PubMedCrossRefGoogle Scholar
  89. Jesse LCH, Obrycki JJ (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125:241–248CrossRefGoogle Scholar
  90. Jurat-Fuentes JL, Gould FL, Adang MJ (2003) Dual resistance to Bacillus thuringiensis Cry1Ac and Cry2Aa toxins in Heliothis virescens suggests multiple mechanisms of resistance. Appl Environ Microbiol 69:5898–5906PubMedCrossRefGoogle Scholar
  91. Kamota A, Muchaonyerwa P, Mnkeni PNS (2011) Effects of ensiling of Bacillus thuringiensis (Bt) maize (MON810) on degradation of the crystal 1Ab (Cry1Ab) protein and compositional quality of silage. Afr J Biotechnol 10(76):17484–17489Google Scholar
  92. Kiliç A, Akay MT (2008) A three generation study with genetically modified Bt corn in rats: biochemical and histopathological investigation. Food Chem Toxicol 46:1164–1170PubMedCrossRefGoogle Scholar
  93. Knowles BH (1994) Mechanism of action of Bacillus thuringiensis insecticidal delta-endotoxins. Adv Insect Physiol 24:275–308CrossRefGoogle Scholar
  94. Knowles BH, Ellar DJ (1987) Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis δ-endotoxins with different insect specificity. Biochim Biophys Acta 924:509–518CrossRefGoogle Scholar
  95. Laboratories A (1992) Bt products manual. Abbott, North ChicagoGoogle Scholar
  96. Lambert B, Buysse L, Decock C, Jansens S, Piens C, Saey B, Seurinck J, van Audenhove K, van Rie J, van Vliet A, Peferoen M (1996) A Bacillus thuringiensis insecticidal crystal protein with a high activity against members of the family Noctuidae. Appl Environ Microbiol 62:80–86PubMedGoogle Scholar
  97. Lang A (2004) Monitoring the impact of Bt maize on butterflies in the field: estimation of required sample sizes. Environ Biosafety Res 3:55–66PubMedCrossRefGoogle Scholar
  98. Lang A, Vojtech E (2006) The effects of pollen consumption of transgenic Bt maize on the common swallowtail, Papilio machaon L. (Lepidoptera, Papilionidae). Basic Appl Ecol 7:296–306CrossRefGoogle Scholar
  99. Lang A, Lauber É, Darvas B (2007) Early tier tests are not sufficient for GMO risk assessment. Nat Biotechnol 25:35–36PubMedCrossRefGoogle Scholar
  100. Lang A, Brunzel S, Dolek M, Otto M, Theißen B (2011) Modelling in the light of uncertainty of key parameters: a call to exercise caution in field predictions of Bt-maize effects. Proc R Soc B 278:980–981PubMedCrossRefGoogle Scholar
  101. Lauber É (2011) The Cry1-toxin content of MON 810 and the affectivity of its pollen on Hungarian protected lepidopteran species (Supervisor: Darvas B.) PhD dissertation, Corvinus University of Budapest, Budapest, pp 1–102 (in Hungarian)Google Scholar
  102. Lauber É, Peregovits L, Ronkay L, Csóti A, Székács A, Darvas B (2010) Protected lepidopteran larvae and Cry1Ab toxin exposure by Bt maize pollen in the Pannonian Region. In: 9th European congress of entomology, programme and book of abstracts. Hungarian Entomological Society, Budapest, Hungary, p 205Google Scholar
  103. Lecadet MM, Frachon E, Dumanoir VC, Ripouteau H, Hamon S, Laurent P, Thiéry I (1999) Updating the H-antigen classification of Bacillus thuringiensis. J Appl Microbiol 86:660–672PubMedCrossRefGoogle Scholar
  104. Lemen JK, Hammond BG, Riordan SG, Jiang C, Nemeth M (2002) 13-Week dietary subchronic comparison study with MON 863 corn in rats preceded by a 1-week baseline food consumption determination with PMI certified rodent diet #5002. Monsanto Co. No: MSL-18175. (http://www.greenpeace.de/fileadmin/gpd/user_upload/themen/gentechnik/Monsanto_Rattenfuetterungsstudie.pdf)
  105. Li J, Koni PA, Ellar DJ (1996) Structure of the mosquitocidal δ-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. J Mol Biol 257:129–152PubMedCrossRefGoogle Scholar
  106. Li W, Wu K, Wang X, Wang G, Guo Y (2005) Impact of pollen grains from Bt transgenic corn on the growth and development of Chinese tussah silkworm, Antheraea pernyi (Lepidoptera: Saturniidae). Environ Entomol 34:922–928CrossRefGoogle Scholar
  107. Lilley M, Ruffell RN, Somerville HJ (1980) Purification of the insecticidal toxin in crystals of Bacillus thuringiensis. J Gen Microbiol 118:1–11PubMedGoogle Scholar
  108. Lisansky SG, Coombs J, Dale T, Frederick R (1997) Biopesticides – markets, technology, registration and IPR companies. CPL Scientific Information Services Ltd., NewburyGoogle Scholar
  109. Liu Y-B, Tabashnik B, Meyer SK, Crickmore N (2001) Cross-resistance and stability of resistance to Bacillus thuringiensis toxin Cry1C in diamondback moth. Appl Environ Microbiol 67:3216–3219PubMedCrossRefGoogle Scholar
  110. Losey JE, Rayor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399:214PubMedCrossRefGoogle Scholar
  111. Ma BL, Subedi KD (2005) Development, yield, grain moisture and nitrogen uptake of Bt corn hybrids and their conventional near-isolines. Field Crop Res 93:199–211CrossRefGoogle Scholar
  112. Margarit E, Reggiardo MI, Vallejos RH, Permingeat HR (2006) Detection of BT transgenic maize in foodstuffs. Food Res Int 39:250–255CrossRefGoogle Scholar
  113. Mason KL, Stepien TA, Blum JE, Holt JF, Labbe NH, Rush JS, Raffa KF, Handelsman J (2011) From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. mBio 2. doi:10.1128/mBio.00065-11
  114. Meihls LN, Higdon ML, Siegfried BD, Miller NJ, Sappington TW, Ellersieck MR, Spencer TA, Hibbard BA (2008) Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc Natl Acad Sci USA 105:19177–19182PubMedCrossRefGoogle Scholar
  115. Mesnage R, Clair E, Gress S, Then C, Székács A, Séralini G-E (2011) Cytotoxicity on human cells of Cry1Ab and Cry1Ac Bt insecticidal toxins alone or with a glyphosate-based herbicide. J Appl Toxicol. doi:10.1002/jat.2712
  116. Messean A, Angevin F, Gómez-Barbero M, Menrad K, Rodríguez-Cerezo E (2006) New case studies on the coexistence of GM and non-GM crops in European agriculture. European Commission Joint Research Centre Institute for Prospective Technological Studies. Technical Report EUR 22102 EN, pp 1–112Google Scholar
  117. Miranda R, Zamudio FZ, Bravo A (2001) Processing of Cry1Ab [delta]-endotoxin from Bacillus thuringiensis by Manduca sexta and Spodoptera frugiperda midgut proteases: role in protoxin activation and toxin inactivation. Insect Biochem Mol Biol 31:1155–1163PubMedCrossRefGoogle Scholar
  118. Mohan M, Gujar GT (2003) Characterization and comparison of midgut proteases of Bacillus thuringiensis susceptible and resistant diamondback moth (Plutellidae: Lepidoptera). J Invertebr Pathol 82:1–11PubMedCrossRefGoogle Scholar
  119. Monsanto (2010) Monsanto response: de Vendômois et al. 2009 (A comparison of the effects of three GM corn varieties on mammalian health) regarding: MON 863, MON 810 and NK603. Monsanto Scientific Affairs. (http://www.monsanto.com/newsviews/Documents/SpirouxdeVendimois.pdf)
  120. Munkvold GP (2003) Cultural and genetic approaches to managing mycotoxins in maize. Annu Rev Phytopathol 41:99–116PubMedCrossRefGoogle Scholar
  121. Nguyen TH, Jehle JA (2007) Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize MON 810. J Plant Dis Prot 114:82–87Google Scholar
  122. Okumura S, Akao T, Mizuki E, Ohba M, Inouye K (2001) Screening of the Bacillus thuringiensis Cry1Ac δ-endotoxin on the artificial phospholipid monolayer incorporated with brush border membrane vesicles of Plutella xylostella by optical biosensor technology. J Biochem Biophys Methods 47:177–188PubMedCrossRefGoogle Scholar
  123. Oliveira AP, Pampulha ME, Bennett JP (2008) A two-year field study with transgenic Bacillus thuringiensis maize: effects on soil microorganisms. Sci Total Environ 405:351–357PubMedCrossRefGoogle Scholar
  124. Oppert B (1999) Protease interactions with Bacillus thuringiensis insecticidal toxins. Arch Insect Biochem Physiol 42:1–12PubMedCrossRefGoogle Scholar
  125. Oppert BS, Morgan TD, Kramer KJ (2011) Efficacy of Bacillus thuringiensis Cry3Aa protoxin and protease inhibitors toward coleopteran storage pests. Pest Manag Sci 67:568–573PubMedCrossRefGoogle Scholar
  126. Pagel-Wieder S, Niemeyer J, Fischer WR, Gessler F (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 39:3034–3042CrossRefGoogle Scholar
  127. Palm CJ, Donegan K, Harris D, Seidler RJ (1994) Quantification in soil of Bacillus thuringiensis var. kurstaki δ-endotoxin from transgenic plants. Mol Ecol 3:145–151CrossRefGoogle Scholar
  128. Papst C, Utz HF, Melchinger AE, Eder J, Magg T, Klein D, Bohn M (2005) Mycotoxins produced by Fusarium spp. in isogenic, Bt vs. non-Bt maize hybrids under European corn borer pressure. Agron J 97:219–224Google Scholar
  129. Perry JN, Devos Y, Arpaia S, Bartsch D, Ehlert C, Gathmann A, Hails RS, Hendriksen NB, Kiss J, Messéan A, Mestdagh S, Neemann G, Nuti M, Sweet JB, Tebbe CC (2012) Estimating the effects of Cry1F Bt-maize on non-target Lepidoptera using a mathematical model of exposure. J Appl Ecol 49:29–37CrossRefGoogle Scholar
  130. Perry JN, Devos Y, Arpaia S, Bartsch D, Gathmann A, Hails RS, Kiss J, Lheureux K, Manachini B, Mestdagh S, Neemann G, Ortego F, Schiemann J, Sweet JB (2010) A mathematical model of exposure of nontarget Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe. Proc R Soc B 277:1417–1425PubMedCrossRefGoogle Scholar
  131. Pleasants JM, Hellmich RL, Dively GP, Sears MK, Stanley-Horn DE, Mattila HR, Foster JE, Clark P, Jones GD (2001) Corn pollen deposition on milkweeds in and near cornfields. Proc Natl Acad Sci USA 98:11919–11924PubMedCrossRefGoogle Scholar
  132. Promdonkoy B, Ellar DJ (2003) Investigation of the pore-forming mechanism of a cytolytic δ-endotoxin from Bacillus thuringiensis. Biochem J 374:255–259PubMedCrossRefGoogle Scholar
  133. Rauschen S, Schuphan I (2006) Fate of the Cry1Ab protein from Bt-maize MON810 silage in biogas production facilities. J Agric Food Chem 54(3):879–883PubMedCrossRefGoogle Scholar
  134. Ravensberg WJ (2011) Critical factors in the successful commercialization of microbial pest control products. Prog Biol Control 10:295–356Google Scholar
  135. Rodics K, Homoki H, Bakonyi G, Darvas B, Székács A (2011) The hereafter of Hungarian scientific lectures for EFSA GMO Panel (Parma, June 11, 2008). In: Darvas B, Székács A (eds) Hungarian background on views of 1st generation genetically modified plants. Agricultural Committee of the Hungarian Parliament, Budapest, Hungary, pp 155–169. (http://www.kormany.hu/download/2/9d/20000/GenetEM.pdf)
  136. Roh JY, Choi JY, Li MS, Jin BR, Je YH (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J Microbiol Biotechnol 17:547–559PubMedGoogle Scholar
  137. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71PubMedCrossRefGoogle Scholar
  138. Romeis J, Shelton A, Kennedy GG (eds) (2008) Integration of insect-resistant genetically modified crops within IPM programs. Springer, DordrechtGoogle Scholar
  139. Rosi-Marshall EJ, Tank JL, Royer TV, Whiles MR, Evans-White M, Chamber C, Griffiths NA, Pokelsek J, Stephen ML (2007) Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104:16204–16208PubMedCrossRefGoogle Scholar
  140. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806PubMedGoogle Scholar
  141. Sears MK, Hellmich RL, Stanley-Horn DE, Oberhauser KS, Pleasants JM, Mattila HR, Siegfried BD, Dively GP (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc Natl Acad Sci USA 98:11937–11942PubMedCrossRefGoogle Scholar
  142. Séralini G-E (2010) Ces OGM qui changent le monde. Flammarion, ParisGoogle Scholar
  143. Séralini G-E, Cellier D, de Vendômois JP (2007) New analysis of a rat feeding study with a genetically modified maize reveals signs of hepatorenal toxicity. Arch Environ Contam Toxicol 45:2073–2085Google Scholar
  144. Séralini G-E, de Vendômois JS, Cellier D, Sultan C, Buiatti M, GallagherL AM, Dronamraju KR (2009) How subchronic and chronic health effects can be neglected for GMOs, pesticides or chemicals. Int J Biol Sci 5:438–443PubMedCrossRefGoogle Scholar
  145. Séralini G-E, Mesnage R, Clair E, Gress S, de Vendômois JS, Cellier D (2011) Genetically modified crops safety assessments: present limits and possible improvements. Environ Sci Eur 23(10):1–10Google Scholar
  146. Shao Z, Cui Y, Liu X, Yi H, Ji J, Yu Z (1998) Processing of delta-endotoxin of Bacillus thuringiensis subsp. kurstaki HD-1 in Heliothis armigera midgut juice and the effects of protease inhibitors. J Invertebr Pathol 72:73–81PubMedCrossRefGoogle Scholar
  147. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85PubMedCrossRefGoogle Scholar
  148. Steinke K, Guertler P, Paul V, Wiedemann S, Ettle T, Albrecht C, Meyer HHD, Spiekers H, Schwarz FJ (2010) Effects of long-term feeding of genetically modified corn (event MON810) on the performance of lactating dairy cows. J Anim Physiol Anim Nutr 94(5):185–193CrossRefGoogle Scholar
  149. Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103:1031–1038PubMedCrossRefGoogle Scholar
  150. Székács A, Darvas B (2012) Forty years with glyphosate. In: Hasaneen MNAE-G (ed) Herbicides – properties, synthesis and control of weeds. InTech, Rijeka, Croatia. pp 247–284. (http://www.intechopen.com/articles/show/title/forty-years-with-glyphosate)
  151. Székács A, Juracsek J, Polgár LA, Darvas B (2005) Levels of expressed Cry1Ab toxin in genetically modified corn DK-440-BTY (YieldGard) and stubble. FEBS J 272(Suppl 1):508Google Scholar
  152. Székács A, Lauber É, Juracsek J, Darvas B (2010a) Cry1Ab toxin production of MON 810 transgenic maize. Environ Toxicol Chem 29:182–190PubMedCrossRefGoogle Scholar
  153. Székács A, Lauber É, Takács E, Darvas B (2010b) Detection of Cry1Ab toxin in the leaves of MON 810 transgenic maize. Anal Bioanal Chem 396:2203–2211PubMedCrossRefGoogle Scholar
  154. Székács A, Weiss G, Quist D, Takács E, Darvas B, Meier M, Swain T, Hilbeck A (2012) Inter-laboratory comparison of Cry1Ab toxin quantification in MON 810 maize by enzyme-immunoassay. Food Agric Immunol 23:99–121Google Scholar
  155. Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199–202PubMedCrossRefGoogle Scholar
  156. Tabashnik BE, van Rensburg JBJ, Carriére Y (2009a) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102:2011–2025PubMedCrossRefGoogle Scholar
  157. Tabashnik BE, Unnithan GC, Masson L, Crowder DW, Li X, Carrière Y (2009b) Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc Natl Acad Sci USA 106:11889–11894PubMedCrossRefGoogle Scholar
  158. Takács E, Fónagy A, Juracsek J, Kugler N, Székács A (2011) Characterisation of tritrophic effects of DAS-59122-7 maize on seven-spotted ladybird (Coccinella septempunctata) feeding on the bird cherry-oat aphid (Rhopalosiphum padi). IOBC/WPRS Bull 73:121–134Google Scholar
  159. Tan FX, Wang JW, Feng YJ, Chi GL, Kong HL, Qiu HF, Wei SL (2010) Bt corn plants and their straw have no apparent impact on soil microbial communities. Plant Soil 329:349–364CrossRefGoogle Scholar
  160. Tank JL, Rosi-Marshall EJ, Royer TV, Whiles MR, Griffiths NA, Frauendorf TC, Treering DJ (2010) Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape. Proc Natl Acad Sci USA 107:17645–17650PubMedCrossRefGoogle Scholar
  161. Tapp H, Stotzky G (1998) Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biol Biochem 30:471–476CrossRefGoogle Scholar
  162. Turrini A, Sbrana C, Nuti MP, Pietrangeli B, Giovannetti M (2004) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266:69–75CrossRefGoogle Scholar
  163. US National Research Council (2010) The impact of genetically engineered crops on farm sustainability in the United States. National Academies Press, Washington, DCGoogle Scholar
  164. van de Wiel CCM, Lotz LAP (2006) Coexistence of genetically modified with unmodified crops. NJAS 54(1):17–35Google Scholar
  165. van Frankenhuyzen K (1993) The challenge of Bacillus thuringiensis. In: Entwistle PF, Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringiensis, an environmental biopesticide: theory and practice. Wiley, Chichester, pp 1–36Google Scholar
  166. van Frankenhuyzen K (2009) Insecticidal activity of Bacillus thuringiensis insecticidal proteins. J Invertebr Pathol 101:1–16PubMedCrossRefGoogle Scholar
  167. Vazquez-Padron RI, de la Riva G, Agüero G, Silva Y, Pham SM, Soberón M, Bravo A, Aïtouche A (2004) Cryptic endotoxic nature of Bacillus thuringiensis Cry1Ab insecticidal crystal protein. FEBS Lett 570:30–36PubMedCrossRefGoogle Scholar
  168. Visser B, Bosch D, Honée G (1993) Domain-function studies of Bacillus thuringiensis crystal proteins: a genetic approach. In: Entwistle PF, Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringiensis, an environmental biopesticide: theory and practice. Wiley, New York, pp 71–88Google Scholar
  169. Volpe G, Ammid NH, Moscone D, Occhigrossi L, Palleschi G (2006) Development of an immunomagnetic electrochemical sensor for detection of BT-CRY1AB/CRY1AC proteins in genetically modified corn samples. Anal Lett 39:1599–1609CrossRefGoogle Scholar
  170. Winkler VW, Hansen GD, Yoder JM (1971) Immunochemical analysis of parasporal crystal digests of Bacillus thuringiensis as an index of insecticidal activity. J Invertebr Pathol 18:378–382CrossRefGoogle Scholar
  171. Xie X, Shu Q (2001) Studies on rapid quantitative analysis of Bt toxin by using Envirologix kits in transgenic rice. Sci Agric Sinic 34:465–468Google Scholar
  172. Zeilinger AR, Andow DA, Zwahlen C, 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 42:1284–1292CrossRefGoogle Scholar
  173. Zhao J-Z, Cao J, Collins HL, Bates SL, Roush RT, Earle ED, Shelton AM (2005) Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc Natl Acad Sci USA 102:8426–8430PubMedCrossRefGoogle Scholar
  174. Zwahlen C, Hilbeck A, Gugerli P, Nentwig W (2003) Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Mol Ecol 12:765–775PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Ecotoxicology and Environmental Analysis, Plant Protection InstituteHungarian Academy of SciencesBudapestHungary

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