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A review of the environmental safety of the Cry1Ab protein

Published online by Cambridge University Press:  30 April 2012

Abstract

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Type
Review Article
Copyright
© Center for Environmental Risk Assessment, ILSI Research Foundation

References

Accinelli, C., Koskinen, W.C., Becker, J.M. and Sadowsky, M.J. (2008). Mineralization of the Bacillus thuringiensis Cry1Ac endotoxins in soil. Journal of Agricultural and Food Chemistry. 56 :10251028. CrossRefGoogle ScholarPubMed
Aronson, A.I, and Shai, Y. (2001). Why Bacillus thuringiensis insecticidal toxins are so effective : unique features of their mode of action. FEMS Microbiology Letters 195 :18. CrossRefGoogle ScholarPubMed
Baker, H.G. (1974). The evolution of weeds. Annual Review of Ecology and Systematics 5 :124. CrossRefGoogle Scholar
Baltazar, B.M., Sanchez-Gonzales, J.J., Cruz-Larios, L. and Schoper, J.B. (2005). Pollination between maize and teosinte : an important determinant of gene flow in Mexico. Theoretical Applied Genetics 110 :519526. CrossRefGoogle ScholarPubMed
Blumenthal, D. (2005). Interrelated causes of plant invasion. Science 310 :243244. CrossRefGoogle ScholarPubMed
Bravo, A., Gill, S.S. and Soberon, M. (2007). Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon. 49(4) :423435. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1857359. CrossRefGoogle ScholarPubMed
Chen, M., Zhao, J.-Z., Collins, H.L., Earle, E.D., Cao, J., andShelton, A.M., 2008. A critical assessment of the effects of Bt transgenic plants on parasitoids. PLoS ONE 3(5) : e2284. doi :10.1371/journal.pone.0002284. Google ScholarPubMed
Crecchio, C. and Stotsky, G. (1998). Insecticidal activity and biodegradation of the toxin from Bacillus thuringiensis subsp. Kurstaki bound to humic acids from soil. Soil Biology and Biochemistry 30(4) :463470. CrossRefGoogle Scholar
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. Microbiology and Molecular Biology Reviews 62(3) :807813. Google ScholarPubMed
Crickmore N., Zeigler D.R., Schnepf E., Van Rie J., Lereclus D., Baum J., Bravo A., and Dean D.H. (2005). Bacillus thuringiensis Toxin Nomenclature (Homepage). [cited January 2010]. http://www.lifesci.sussex.ac.uk/Home/Neil_Crickmore/Bt/.
Duan, J.J., Marvier, M., Huesing, J., Dively, G., Huang, Z.Y. (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera : Apidae). PLoS ONE 3(1) :e1415. CrossRefGoogle Scholar
Duan, J.J., Lundgren, J.G., Naranjo, S., Marvier, M. (2010) Extrapolating non-target risk of Bt crops from laboratory to field. Biology Letters 6 :7477. CrossRefGoogle ScholarPubMed
Hellmich, R.L., Siegfried, B.D., Sears, M.K., Stanley-Horn, D.E., Daniels, M.J., Mattila, H.R., Spencer, T., Bidne, K.G. and Lewis, L.C. (2001). Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proceedings of the National Academies of Science (U.S.A.) 98(21) :1192511930. CrossRefGoogle ScholarPubMed
Hofte, H. and Whiteley, H.R. (1989). Insecticidal crystal proteins of Bacillus thuringiensis. Microbiological Reviews 53(2) :242255. Google ScholarPubMed
Jenkins, J.L., Lee, M.K., Sangadala, S., Adang, M.J. and Dean, D.H. (1999). Binding of Bacillus thuringiensis Cry1Ac toxin to Manduca sexta aminopeptidase-N receptor is not directly related to toxicity. FEBS Letters 462 :373376. CrossRefGoogle ScholarPubMed
Jesse, L.C.H. and Obrycki, J.J. (2000). Field deposition of Bt transgenic corn pollen : lethal effects on the monarch butterfly. Oecologia 125 :241248. CrossRefGoogle Scholar
Keane, R.M. and Crawley, M.J. (2002). Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17(4) :164170. CrossRefGoogle Scholar
Koskella, J. and 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. Applied and Environmental Microbiology 63(9) :35613568. Google ScholarPubMed
Kumar, P.A., Sharma, R.P. and Malik, V.S. (1996). The insecticidal proteins of Bacillus thuringiensis. Advances in Applied Microbiology 42 :143. CrossRefGoogle ScholarPubMed
Li, Y., Romeis J., Wang P., Peng Y., and Shelton A.M. 2011. A comprehensive assessment of the potential effects of Bt cotton on Coleomegilla maculata demonstrates no detrimental effects by Cry1Ac and Cry2Ab. PLoS PLoS ONE 6(7) : e22185. doi :10.1371/journal.pone.0022185.
Losey, J.E., Rayor, L.S., Carter, M.E. (1999). Transgenic pollen harms monarch larvae. Nature 399(6733) :214. CrossRefGoogle ScholarPubMed
Mack, R.N. (1996) Predicting the identity and fate of plant invaders : emergent and emerging approaches. Biological Conservation 78 :107121. CrossRefGoogle Scholar
Mallory-Smith, C. and Zapiola, M. (2008). Gene flow from glyphosate-resistant crops. Pest Management Science 64 :428440. CrossRefGoogle ScholarPubMed
Marchetti, E., Accinelli, C., Talame, V. and Epifani, R. (2007). Persistence of Cry toxins and cry genes from genetically modified plants in two agricultural soils. Agronomy for Sustainable Development 27(3) :231236. CrossRefGoogle Scholar
Marvier, M., McCreedy, C., Regetz, J., Kareiva, P. (2007). A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316 :14751477. CrossRefGoogle ScholarPubMed
Mason, P., Braun, L., Warwick, S.I., Zhu, B., Stewart, Jr. C.N. (2003) Transgenic Bt-producing Brassica napus : Plutella xylostella selection pressure and fitness of weedy relatives. Environmental Biosafety Research 2(4) :263276. CrossRefGoogle ScholarPubMed
Naranjo S.E. (2009). Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Reviews : Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4(11) : http://fbae.org/2009/FBAE/website/images/pdf/imporatant-publication/impacts-of-bt-crops-on-non-target-invertebrates-and-insecticide-use-patterns.pdf.
Nickson T.E. and McKee M.J. (2002). Ecological assessment of crops derived through biotechnology. In Thomas J.A. and Fuchs R.L. (eds.) Biotechnology and safety assessment (third edition) (pp 233–252). Academic Press, San Diego, CA.
NRC (1989). Field testing genetically modified organisms : framework for decisions. National Academy of Sciences, National Research Council (NRC) committee on Scientific Evaluation of the Introduction of Genetically Modified Microorganisms and Plants into the Environment. National Academy Press, Washington, D.C.
Peterson, J.A., Lundgren, J.G., Harwood, J.D. (2011). Interaction of transgenic Bacillus thuringiensis insecticidal crops with spiders (Araneae). The Journal of Arachnology 39 :121http://www.bioone.org/doi/full/10.1636/M10-98.1. CrossRefGoogle Scholar
Pleasants, J.M., Hellmich, R.L., Dively, G.P., Sears, M.K., Stanley-Horn, D.E., Mattila, H.R., Foster, J.E., Clark, P. and Jones, G.D. (2001). Corn pollen deposition on milkweeds in and near cornfields. Proceedings of the National Academies of Sciences (USA) 98(21) :1191911924. http://www.pnas.org/content/98/21/11919.full. CrossRefGoogle ScholarPubMed
Rose R.I. (ed.) (2007) White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target invertebrates for regulatory risk assessment. USDA-APHIS and US Environmental Protection Agency, Washington, DC, USA. http://www.epa.gov/pesticides/biopesticides/pips/non-target-arthropods.pdf
Romeis, J., Meissle, M. and Bigler, F. (2006). Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 24(1) :6371. CrossRefGoogle ScholarPubMed
Romeis, J., Barsch, D., Bigler, F., Candolfi, M.P., Gielkens, M.M.C., Hartley, S.E., Hellmich, R.I., Huesing, J.E., Jepson, P.C., Layton, R., Quemada, H., Raybould, A., Rose, R.I., Schiemann, J., Sears, M.K., Shelton, A.M., Sweet, J., Vaituzis, Z., and Wolt, J.D. (2008). Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nature Biotechology 26 :203208. http://www.nature.com/nbt/journal/v26/n2/abs/nbt1381.html. CrossRefGoogle ScholarPubMed
Serratos J.A., Wilcox M.C., Castillo F. (Eds.) (1995). Proceedings of a Forum : Gene flow among maize landraces, improved maize varieties, and teosinte : implications for transgenic maize. The Mexican National Institute of Forestry Agriculture and Livestock Research (INIFAP), The International Maize and Wheat Improvement Center (CIMMYT), and The Mexican National Agricultural Biosafety Committee (CNBA).
Schnepf, E., Crickmore, N., van Rie, J., Lereclus, D., Baum, J., Fetelson, J., Ziegler, D.R. and Dean, D.H. (1998). Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62(3) : 775806. Google ScholarPubMed
Shelton,, A.M., and Sears, M.K. (2001). The monarch butterfly controversy : scientific interpretations of a phenomenon. The Plant Journal 27 :483488. CrossRefGoogle Scholar
Tabashnik, B.E. (1992). Evaluation of synergism among Bacillus thuringiensis toxins. Applied and Environmental Microbiology 58(10) :33433346. Google ScholarPubMed
Wolfenbarger L.L., Naranjo S.E., Lundgren J.G., Bitzer R.J. and Watrud L.S. (2008). Bt crops effects on functional guilds of non-target arthropods : a meta-analysis. PloS One 3(5) : e2118 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2346550/pdf/pone.0002118.pdf.
Zhang, X., Candas, M., Griko, N.B., Taussig, R., Bulla, L.A. Jr. (2006). A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proceedings of the National Academies of Science (U.S.A.) 103(26) :98979902. CrossRefGoogle ScholarPubMed
ANZFA (2000a). Final Risk Assessment Report Application A346 Food produced from insect protected corn line MON 810. Australia New Zealand Food Standards Agency, Canberra, Australia. http://www.foodstandards.gov.au/_srcfiles/Application%20A346%20Draft%20IR.pdf.
ANZFA (2000b). Final Risk Assessment Report Application A385 Food produced from insect protected Bt-176 corn line. Australia New Zealand Food Standards Agency, Canberra, Australia. http://www.foodstandards.gov.au/_srcfiles/A385IR.pdf.
ANZFA (2000c). Draft Final Risk Assessment Report Application A386 Food produced from insect protected, herbicide tolerant Bt-11 corn line. http://www.foodstandards.gov.au/_srcfiles/A386_IR.pdf.
CBD (2000a). Cartagena Protocol on Biosafety. Secretariat of the Convention on Biological Diversity (CBD), Montreal. http://www.cbd.int/biosafety/protocol.shtml.
CBD (2000b). Cartagena Protocol on Biosafety Annex III : Risk Assessment. Secretariat of the Convention on Biological Diversity (CBD), Montreal. http://www.cbd.int/biosafety/articles.shtml?a = cpb-43.
CFIA (1996a) Decision Document DD96-09 : Determination of Environmental Safety of Event 176 Bt Corn (Zea mays L.) Developed by Ciba Seeds and Mycogen Corporation. Canadian Food Inspection Agency, Ottawa, Canada. http://www.inspection.gc.ca/english/plaveg/bio/dd/dd9609e.shtml.
CFIA (1996b) Decision Document DD96-12 : Determination of Environmental Safety of Northrup King Seeds’ European Corn Borer (ECB) Resistant Corn (Zea mays L.). Canadian Food Inspection Agency, Ottawa, Canada. http://www.inspection.gc.ca/english/plaveg/bio/dd/dd9612e.shtml.
CFIA (1997) Decision Document 97–18 : Determination of the Safety of Pioneer Hi-Bred International Inc.’s European Corn Borer (ECB) Resistant Corn (Zea mays L.) Line MON809. Canadian Food Inspection Agency, Ottawa, Canada. http://www.inspection.gc.ca/english/plaveg/bio/dd/dd9718e.shtml.
CFIA (1997b) Decision Document 97–19 : Determination of the Safety of Monsanto Canada Inc.’s YieldgardInsect Resistant Corn (Zea mays L.) Line MON810. Canadian Food Inspection Agency, Ottawa, Canada. http://www.inspection.gc.ca/english/plaveg/bio/dd/dd9719e.shtml.
CFIA (1998) Decision Document 98–26 : Determination of the Safety of Monsanto Canada Inc.’s YieldgardInsect Resistant Corn (Zea mays L.) Line MON802. Canadian Food Inspection Agency, Ottawa, Canada. http://www.inspection.gc.ca/english/plaveg/bio/dd/dd9826e.shtml.
Codex (2003a). Principles for the risk analysis of foods derived through modern biotechnology. Codex Alimentarius Commission (Codex), Rome http://www.codexalimentarius.net/download/standards/10007/CXG_044e.pdf.
Codex (2003b). Guideline for the conduct of food safety assessment of foods derived from recombinant DNA plants. Codex Alimentarius Commission (Codex), Rome http://www.codexalimentarius.net/download/standards/10021/CXG_045e.pdf.
CTNBio (2005). Commercial release of genetically modified cotton, Bollgard Cotton (531). Brazilian National Biosafety Technical Commission (CTNBio), Sao Paulo http://www.ctnbio.gov.br/index.php/content/view/3663.html.
CTNBio (2009). Commercial release of genetically modified cotton, Bollgard Cotton (MON 15985) : Technical Opinion no. 1832/2009. Brazilian National Biosafety Technical Commission (CTNBio), Sao Paulo.
EC (1997) Commission Decision 97/98/EC of 23 January 1997 concerning the placing on the market of genetically modified maize (Zea mays L.) with the combined modification for insecticidal properties conferred by the Bt-endotoxin gene and increased tolerance to the herbicide glufosinate ammonium pursuant to Council Directive 90/220/EEC. http://www.biosafety.be/PDF/97_98.pdf.
EC (1998) Commission Decision of 22 April 1998 concerning the placing on the market of genetically modified maize (Zea mays L. line MON 810) pursuant to Council Directive 90/220/EEC. http://www.biosafety.be/PDF/98_294.pdf.
EFSA (2006). Guidance document of the scientific panel on genetically modified organisms for the risk assessment of genetically modified plants and derived food and feed. European Food Safety Authority (EFSA), Brussels, Belgium. http://www.efsa.europa.eu/en/scdocs/doc/gmo_guidance_derived_feed_food.pdf.
EU DG SANCO (2010). EU Pesticides Database [Search for Bacillus thuringiensis]. European Union Directorate General, Health and Consumers (EU DG SANCO) Brussels, Belgium http://ec.europa.eu/sanco_pesticides/public/index.cfm?event = activesubstance.selection.
FAO/WHO (1996). Biotechnology and food safety. Report of a Joint FAO/WHO Consultation. Food and Agriculture Organization (FAO)/World Health Organization (WHO), Food and Nutrition Paper 61, Rome, Italy. http://www.fao.org/ag/agn/food/pdf/biotechnology.pdf.
Japan BCH (2004) Outline of the Biological Diversity Risk Assessment Report : MON-00863-5 X MON-00810-6 X MON-00603-6 http://www.bch.biodic.go.jp/download/en_lmo/MON863_MON810_NK603enRi.pdf.
Japan BCH (2004b) Outline of the Biological Diversity Risk Assessment Report : MON-00603-6 X MON- 00810-6 http://www.bch.biodic.go.jp/download/en_lmo/NK603_MON810enRi.pdf.
Japan BCH (2004c) Outline of the Biological Diversity Risk Assessment Report : MON-00810-6 X MON-00863-5 http://www.bch.biodic.go.jp/download/en_lmo/MON810_863enRi.pdf.
Japan BCH (2004d) Outline of the Biological Diversity Risk Assessment Report : MON-00810-6 http://www.bch.biodic.go.jp/download/en_lmo/MON810enRi.pdf.
Japan BCH (2005) Outline of the Biological Diversity Risk Assessment Report : MON-00021-9 X MON-00810-6 http://www.bch.biodic.go.jp/download/en_lmo/GA21_MON810enRi.pdf.
Japan BCH (2005b) Outline of the Biological Diversity Risk Assessment Report : ACS-ZM003-2 X MON-00810-6 http://www.bch.biodic.go.jp/download/en_lmo/T25_MON810enRi.pdf.
Japan BCH (2006) Outline of the Biological Diversity Risk Assessment Report : MON-88017-3 X MON 00810-6 http://www.bch.biodic.go.jp/download/en_lmo/MON88017_MON810enRi.pdf.
Japan BCH (2007) Outline of the Biological Diversity Risk Assessment Report : SYN-BTØ11-1 http://www.bch.biodic.go.jp/download/en_lmo/Bt11enRi.pdf.
Japan BCH (2007b) Outline of the Biological Diversity Risk Assessment Report : SYN-EV176-9 http://www.bch.biodic.go.jp/download/en_lmo/Event176enRi.pdf.
Japan BCH (2007c) Outline of the Biological Diversity Risk Assessment Report : REN-00038-3 X MON-00810-6 http://www.bch.biodic.go.jp/download/en_lmo/LY038_MON810enRi.pdf.
OECD (1992). Recombinant DNA safety considerations. Organization for Economic Cooperation and Development (OECD), Paris, France.
OECD (2003). Consensus document on the biology of Zea mays subsp. Mays. . Organization for Economic Cooperation and Development (OECD), Paris, France.
OECD (2006). Points to consider for consensus documents on the biology of cultivated plants. Organization for Economic Cooperation and Development (OECD), Paris, France.
OECD (2007) Consensus Document on Safety Information on Transgenic Plants Expressing Bacillus thuringiensis –Derived Insect Control Protein. Series on Harmonisation of Regulatory Oversight in Biotechnology, No. 42. Organisation for Economic Co-operation and Development, Paris.
PMRA (2008). Re-evaluation decision document : Bacillus thuringiensis. Health Canada, Pest Management Regulatory Agency (PMRA), Ottawa. [accessed Feb18, 2010] http://www.hc-sc.gc.ca/cps-spc/pubs/pest/_decisions/rvd2008-18/index-eng.php.
USDA APHIS (1994). Petition for Determination of Nonregulated Status of Ciba Seeds’ Corn Genetically Engineered to Express the Cry1A(b) Protein from Bacillus thuringiensis subspecies kurstaki. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs/94_31901p.pdf.
USDA APHIS (1995). USDA/APHIS Petition 94-319-01 for Determination of Nonregulated Status for Event 176 Corn : Environmental Assessment and Finding of No Significant Impact. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs2/94_31901p_com.pdf.
USDA APHIS (1995b). Petition for Determination of Nonregulated Status : Insect Protected Corn (Zea mays L.) with the cryIA(b) Gene from Bacillus thuringiensis subsp. Kurstaki. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs/95_09301p.pdf.
USDA APHIS (1995c). USDA/APHIS Petition 95-093-01 for Determination of Nonregulated Status for Insect Protected Corn Line MON 80100 : Environmental Assessment and Finding of No Significant Impact. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs2/95_09301p_com.pdf.
USDA APHIS (1995d). Petition for determination of Nonregulated Status for : Insect Protected Corn (Zea mays L.) Expressing the Cry IA(b) Gene from Bacillus thuringiensis var. kurstaki. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs/95_19501p.pdf.
USDA APHIS (1996). USDA/APHIS Petition 95-195-01 for Determination of Nonregulated Status for Bt11 Corn : Environmental Assessment and Finding of No Significant Impact. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs2/95_19501p_com.pdf.
USDA APHIS (1996b). Petition for Determination of Nonregulated Status : Additional YieldGard Corn (Zea mays L.) Lines with the cry1A(b) Gene from Bacillus thuringiensis subsp. kurstaki. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs/96_01701p.pdf.
USDA APHIS (1996c). Addition of Two Genetically Engineered Insect Resistant Corn Lines to Determination of Nonregulated Status. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs2/96_01701p_com.pdf.
USDA APHIS (1996d). Petition for Determination of Nonregulated Status : Insect-Protected Roundup Ready Corn Line MON 802. APHIS Petition no. 96-317-01. United States Department of Agriculture, Animal and Plant Health Inspection Service, Washington D.C. http://www.aphis.usda.gov/brs/aphisdocs/96_31701p.pdf.
USEPA (2001). Bt Plant-Incorporated Protectants October 15, 2001 Biopesticides Registration Action Document. U.S. Environmental Protection Agency (USEPA), Washington D.C. http://www.epa.gov/pesticides/biopesticides/pips/bt_brad.htm.
USEPA (2007). White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target arthropods for regulatory risk assessments. U.S. Environmental Protection Agency (USEPA), Washington D.C. http://www.epa.gov/pesticides/biopesticides/pips/non-target-arthropods.pdf.
USEPA (2010). The Office of Prevention, Pesticides and Toxic Substances (OPPTS), Harmonized Test Guidelines. U.S. Environmental Protection Agency (USEPA), Washington D.C. http://epa.gov/oppts/pubs/frs/home/guidelin.htm.
WHO (1995). Application of the Principles of Substantial Equivalence to the Safety Evaluation of Foods or Food Components from Plants Derived by Modern Biotechnology. A Report of a WHO Workshop. World Health Organisation (WHO), Geneva.