Bt Crops: Past and Future

The development and commercialization of transgenic plants expressing insecticidal toxin genes from the bacterium Bacillus thuringiensis (Bt) has revolutionized agriculture in the past two decades. Development of this revolutionary insect pest control technology was facilitated by the identification and characterization of insecticidal Bt proteins and advancements in plant transformation and genetic engineering. While commercialization of this technology is currently limited to a number of countries, these transgenic “Bt crops” are replacing in most cases conventional crop varieties due to their insect resistance, lower spraying requirements, and higher yields. However, concerns related to the increasing adoption of this technology include gene flow to wild relatives, evolution of resistance in target pests, and unintended effects on the environment. In this chapter, we discuss key events in the history of Bt crop development and summarize current regulations aimed at reducing the risks associated with increased adoption of this technology. By analyzing the history of Bt transgenic crops and the current marketplace trends and issues, we aim to examine the outlook of current and impending Bt crops as well as potential issues that may emerge during their future use.

[1]  Juan Luis Jurat-Fuentes,et al.  Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin , 2007, Proceedings of the National Academy of Sciences.

[2]  Peter Kareiva,et al.  A Meta-Analysis of Effects of Bt Cotton and Maize on Nontarget Invertebrates , 2007, Science.

[3]  J. Bennett,et al.  A two-year field study with transgenic Bacillus thuringiensis maize: effects on soil microorganisms. , 2008, The Science of the total environment.

[4]  D. Stalker,et al.  Amplification of a Chimeric Bacillus Gene in Chloroplasts Leads to an Extraordinary Level of an Insecticidal Protein in Tobacco , 1995, Bio/Technology.

[5]  E. Waltz.  GM crops: Battlefield , 2009, Nature.

[6]  Richard L. Hellmich,et al.  Impact of Bt corn pollen on monarch butterfly populations: A risk assessment , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[7]  P. Quail,et al.  Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation , 1992, Plant Molecular Biology.

[8]  K. Frankenhuyzen.  Insecticidal activity of Bacillus thuringiensis crystal proteins , 2009 .

[9]  R. T. Roush,et al.  Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? , 1998 .

[10]  A. Abad,et al.  A cytoplasmic male sterility-associated mitochondrial protein causes pollen disruption in transgenic tobacco. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Williams,et al.  Contribution of the individual components of the δ-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensis subsp. israelensis , 1995 .

[12]  A. Ives,et al.  The evolution of resistance to two-toxin pyramid transgenic crops. , 2011, Ecological applications : a publication of the Ecological Society of America.

[13]  G. Gujar,et al.  Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. , 2011, Pest management science.

[14]  D. Onstad,et al.  Western Corn Rootworm (Coleoptera: Chrysomelidae) Dispersal and Adaptation to Single-Toxin Transgenic Corn Deployed with Block or Blended Refuge , 2011, Environmental entomology.

[15]  M. Montagu,et al.  Transgenic plants protected from insect attack , 1987, Nature.

[16]  O. Perera,et al.  Production of mRNA from the cry1Ac transgene differs among Bollgard® lines which correlates to the level of subsequent protein , 2009, Transgenic Research.

[17]  B. Wingerd,et al.  Bt: mode of action and use. , 2003, Archives of insect biochemistry and physiology.

[18]  T. M. Brown.  Molecular genetics and evolution of pesticide resistance. , 1996 .

[19]  H. Agaisse,et al.  Genetic analysis of cryIIIA gene expression in Bacillus thuringiensis. , 1996, Microbiology.

[20]  F. Gould,et al.  Histopathological Effects and Growth Reduction in a Susceptible and a Resistant Strain of Heliothis virescens (Lepidoptera: Noctuidae) Caused by Sublethal Doses of Pure Cry1A Crystal Proteins from Bacillus thuringiensis , 1999 .

[21]  L. Watrud,et al.  Integration of the delta-endotoxin gene of Bacillus thuringiensis into the chromosome of root-colonizing strains of pseudomonads using Tn5. , 1986, Gene.

[22]  Xinsheng Zhang,et al.  Dramatic reduction of crop-to-crop gene flow within a short distance from transgenic rice fields. , 2007, The New phytologist.

[23]  N. Griffiths,et al.  Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape , 2010, Proceedings of the National Academy of Sciences.

[24]  A. Gatehouse,et al.  Insect-resistant biotech crops and their impacts on beneficial arthropods , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  J. Wilen,et al.  Natural refuge crops, buildup of resistance, and zero-refuge strategy for Bt cotton in China , 2010, Science China Life Sciences.

[26]  D. Andow,et al.  Transgenic Insecticidal Crops and Natural Enemies: A Detailed Review of Laboratory Studies , 2009, Environmental entomology.

[27]  S. Jansens,et al.  Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in a midgut membrane receptor. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[28]  C. N. Stewart,et al.  Transgenic perennial biofuel feedstocks and strategies for bioconfinement , 2010 .

[29]  M. Koziel,et al.  Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Jansens,et al.  Transgenic corn expressing a Cry9C insecticidal protein from Bacillus thuringiensis protected from European corn borer damage , 1997 .

[31]  J. Hyde,et al.  Economic considerations for the adoption of transgenic crops: the case of bt corn. , 2001, Journal of nematology.

[32]  C. N. Stewart,et al.  'GM-gene-deletor': fused loxP-FRT recognition sequences dramatically improve the efficiency of FLP or CRE recombinase on transgene excision from pollen and seed of tobacco plants. , 2007, Plant biotechnology journal.

[33]  V. Sanchis.  From microbial sprays to insect-resistant transgenic plants: history of the biospesticide Bacillus thuringiensis. A review , 2011, Agronomy for Sustainable Development.

[34]  Kongming Wu,et al.  Suppression of Cotton Bollworm in Multiple Crops in China in Areas with Bt Toxin–Containing Cotton , 2008, Science.

[35]  V. Hilder.  GM Plants and Protection Against Insects – Alternative Strategies Based on Gene Technology , 2003 .

[36]  F. Bigler,et al.  Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). , 2004, Journal of insect physiology.

[37]  Jing Zhao,et al.  Early Warning of Cotton Bollworm Resistance Associated with Intensive Planting of Bt Cotton in China , 2011, PloS one.

[38]  A. Shelton,et al.  Economic, ecological, food safety, and social consequences of the deployment of bt transgenic plants. , 2002, Annual review of entomology.

[39]  S. G. Rogers,et al.  Insect Tolerant Transgenic Tomato Plants , 1987, Bio/Technology.

[40]  Chenxi Liu,et al.  Increased toxicity of Bacillus thuringiensis Cry3Aa against Crioceris quatuordecimpunctata, Phaedon brassicae and Colaphellus bowringi by a Tenebrio molitor cadherin fragment. , 2011, Pest management science.

[41]  A. Shelton,et al.  Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution , 2003, Nature Biotechnology.

[42]  Jeremy J. W. Chen,et al.  Expression of a Bacillus thuringiensis toxin (cry1Ab) gene in cabbage (Brassica oleracea L. var. capitata L.) chloroplasts confers high insecticidal efficacy against Plutella xylostella , 2008, Theoretical and Applied Genetics.

[43]  L. Crossland,et al.  Field Performance of Elite Transgenic Maize Plants Expressing an Insecticidal Protein Derived from Bacillus thuringiensis , 1993, Bio/Technology.

[44]  J. Wyman,et al.  Genetically improved potatoes: protection from damage by Colorado potato beetles , 1993, Plant Molecular Biology.

[45]  R. D. de Maagd,et al.  Lack of Detrimental Effects of Bacillus thuringiensis Cry Toxins on the Insect Predator Chrysoperla carnea: a Toxicological, Histopathological, and Biochemical Analysis , 2006, Applied and Environmental Microbiology.

[46]  L. Bulla,et al.  Characterization of the entomocidal parasporal crystal of Bacillus thuringiensis , 1977, Journal of bacteriology.

[47]  R. Beeman,et al.  Proteinase-mediated Insect Resistance to Bacillus thuringiensis Toxins* , 1997, The Journal of Biological Chemistry.

[48]  David Zilberman,et al.  Yield Effects of Genetically Modified Crops in Developing Countries , 2003, Science.

[49]  Geert Plaetinck,et al.  Control of coleopteran insect pests through RNA interference , 2007, Nature Biotechnology.

[50]  J. Losey,et al.  Transgenic pollen harms monarch larvae , 1999, Nature.

[51]  W. Kaniewski,et al.  NewLeaf Plus® Russet Burbank potatoes: replicase-mediated resistance to potato leafroll virus , 2004, Molecular Breeding.

[52]  J. Adamczyk,et al.  Field Efficacy and Seasonal Expression Profiles for Terminal Leaves of Single and Double Bacillus thuringiensis Toxin Cotton Genotypes , 2001, Journal of economic entomology.

[53]  R. Fuchs,et al.  Modification of the coding sequence enhances plant expression of insect control protein genes. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[54]  A. Nath,et al.  Expression of insecticidal activity in Rhizobium containing the δ-endotoxin gene cloned from Bacillus thuringiensis subsp. tenebrionis , 1990, Plant and Soil.

[55]  Wenke Liu.  Do genetically modified plants impact arbuscular mycorrhizal fungi? , 2010, Ecotoxicology.

[56]  Characterization of Cry34Ab1 and Cry35Ab1 insecticidal crystal proteins expressed in transgenic corn plants and Pseudomonas fluorescens. , 2004 .

[57]  F. Wäckers,et al.  Indian Bt Cotton Varieties Do Not Affect the Performance of Cotton Aphids , 2009, PloS one.

[58]  J. R. Bradley,et al.  Comparative Production of Helicoverpa zea (Lepidoptera: Noctuidae) from Transgenic Cotton Expressing Either One or Two Bacillus thuringiensis Proteins with and without Insecticide Oversprays , 2004, Journal of economic entomology.

[59]  M. Gray.  Relevance of traditional integrated pest management (IPM) strategies for commercial corn producers in a transgenic agroecosystem: a bygone era? , 2011, Journal of agricultural and food chemistry.

[60]  B. Tabashnik,et al.  Field-Evolved Insect Resistance to Bt Crops: Definition, Theory, and Data , 2009, Journal of economic entomology.

[61]  T. Rocheleau,et al.  Analysis of unstable RNA transcripts of insecticidal crystal protein genes of Bacillus thuringiensis in transgenic plants and electroporated protoplasts , 1991, Plant Molecular Biology.

[62]  Gary P. Fitt,et al.  Implementation and Impact of Transgenic Bt Cottons in Australia , 2004 .

[63]  Felicia Wu,et al.  Mycotoxin Reduction in Bt Corn: Potential Economic, Health, and Regulatory Impacts , 2006, Transgenic Research.

[64]  P. Lemaux,et al.  Transformation of Maize Cells and Regeneration of Fertile Transgenic Plants. , 1990, The Plant cell.

[65]  H. R. Whiteley,et al.  Diversity of locations for Bacillus thuringiensis crystal protein genes , 1983, Journal of bacteriology.

[66]  J. B.J. van Rensburg,et al.  First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize , 2007 .

[67]  X. Guan,et al.  Cloning and localization of vip3A gene of Bacillus thuringiensis , 2004, Biotechnology Letters.

[68]  M. Van Montagu,et al.  Ti plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity , 1983, The EMBO journal.

[69]  F. Gould,et al.  Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[70]  A. Viktorov.  Transfer of Bt corn byproducts from terrestrial to stream ecosystems , 2011, Russian Journal of Plant Physiology.

[71]  H. R. Whiteley,et al.  Bacillus thuringiensis §-Endotoxin Expressed in Transgenic Nicotiana tabacum Provides Resistance to Lepidopteran Insects , 1987 .

[72]  W C Bridges,et al.  Field and laboratory evaluations of transgenic cottons expressing one or two Bacillus thuringiensis var. kurstaki Berliner proteins for management of noctuid (Lepidoptera) pests. , 2003, Journal of economic entomology.

[73]  J. Ferré,et al.  Biochemistry and Genetics of Insect Resistance to Bacillus thuringiensis , 2002 .

[74]  D. Llewellyn,et al.  Field performance and seasonal changes in the efficacy against Helicoverpa armigera (Hübner) of transgenic cotton expressing the insecticidal protein vip3A , 2007 .

[75]  Q. Fang,et al.  Bt rice expressing Cry1Ab does not stimulate an outbreak of its non-target herbivore, Nilaparvata lugens , 2011, Transgenic Research.

[76]  J. T. Turner,et al.  Integrative Cloning, Expression, and Stability of the cryIA(c) Gene from Bacillus thuringiensis subsp. kurstaki in a Recombinant Strain of Clavibacter xyli subsp. cynodontis , 1994, Applied and environmental microbiology.

[77]  H. R. Whiteley,et al.  Cloning and expression of the Bacillus thuringiensis crystal protein gene in Escherichia coli. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Denis Bourguet,et al.  Regulating insect resistance management: the case of non-Bt corn refuges in the US. , 2005, Journal of environmental management.

[79]  A. Gatehouse,et al.  The case of the monarch butterfly: a verdict is returned. , 2002, Trends in genetics : TIG.

[80]  Wei Wang,et al.  Enhanced yield performance of Bt rice under target-insect attacks: implications for field insect management , 2011, Transgenic Research.

[81]  M. Meissle,et al.  Consumption of Bt Maize Pollen Expressing Cry1Ab or Cry3Bb1 Does Not Harm Adult Green Lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae) , 2008, PloS one.

[82]  H. de Barjac,et al.  A classification of strains of Bacillus thuringiensis Berliner with a key to their differentiation. , 1968, Journal of invertebrate pathology.

[83]  R. Fuchs,et al.  Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. , 2000, Regulatory toxicology and pharmacology : RTP.

[84]  Henry Daniell,et al.  Molecular strategies for gene containment in transgenic crops , 2002, Nature Biotechnology.

[85]  M. Poverene,et al.  Genetically modified sunflower release: Opportunities and risks , 2007 .

[86]  Yanhui Lu,et al.  Mirid Bug Outbreaks in Multiple Crops Correlated with Wide-Scale Adoption of Bt Cotton in China , 2010, Science.

[87]  L. Bulla,et al.  The biotechnology of Bacillus thuringiensis. , 1987, Critical reviews in biotechnology.

[88]  M. Koziel,et al.  Expression of a chimeric CaMV 35S Bacillus thuringiensis insecticidal protein gene in transgenic tobacco , 1992, Plant Molecular Biology.

[89]  F. S. Walters,et al.  Lepidopteran-Active Variable-Region Sequence Imparts Coleopteran Activity in eCry3.1Ab, an Engineered Bacillus thuringiensis Hybrid Insecticidal Protein , 2010, Applied and Environmental Microbiology.

[90]  A. Shelton,et al.  The monarch butterfly controversy: scientific interpretations of a phenomenon. , 2001, The Plant journal : for cell and molecular biology.

[91]  F. Gould.  Evolutionary Biology and Genetically Engineered CropsConsideration of evolutionary theory can aid in crop design , 1988 .

[92]  Jorge Fernandez-Cornejo,et al.  THE SEED INDUSTRY IN U.S. AGRICULTURE: AN EXPLORATION OF DATA AND INFORMATION ON CROP SEED MARKETS, REGULATION, INDUSTRY STRUCTURE, AND RESEARCH AND DEVELOPMENT , 2004 .

[93]  P. Vary,et al.  Gene dosage effect on the expression of the delta-endotoxin genes of Bacillus thuringiensis subsp. kurstaki in Bacillus subtilis and Bacillus megaterium. , 1989, Gene.

[94]  W. Werf,et al.  Effect of Pyramiding Bt and CpTI Genes on Resistance of Cotton to Helicoverpa armigera (Lepidoptera: Noctuidae) Under Laboratory and Field Conditions , 2011, Journal of economic entomology.

[95]  P. Dowd.  Indirect Reduction of Ear Molds and Associated Mycotoxins in Bacillus thuringiensis Corn Under Controlled and Open Field Conditions: Utility and Limitations , 2000, Journal of economic entomology.

[96]  M. Stam,et al.  cry IA(b) transcript formation in tobacco is inefficient , 1995, Plant Molecular Biology.

[97]  I. Burton,et al.  Environmental risk assessment , 1980 .

[98]  A. Shelton,et al.  Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Steven E. Naranjo,et al.  Impacts of Bt crops on non-target invertebrates and insecticide use patterns , 2009 .

[100]  D. Crowder,et al.  Modeling the Effects of Plant-to-Plant Gene Flow, Larval Behavior, and Refuge Size on Pest Resistance to Bt Cotton , 2011 .

[101]  G. Brookes,et al.  Global impact of biotech crops: income and production effects, 1996-2007. , 2009 .

[102]  Scott Rozelle,et al.  Five years of Bt cotton in China - the benefits continue. , 2002, The Plant journal : for cell and molecular biology.

[103]  Wei Tang,et al.  Development and characterisation of transgenic rice expressing two Bacillus thuringiensis genes. , 2011, Pest management science.

[104]  G. Thompson,et al.  Discovery and Characterization of Field Resistance to Bt Maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico , 2010, Journal of economic entomology.

[105]  S. Kaur.  Molecular approaches for identification and construction of novel insecticidal genes for crop protection , 2006 .

[106]  J. Fernandez-Cornejo,et al.  Adoption of Bioengineered Crops , 2005 .

[107]  R. Twyman,et al.  Bacillus thuringiensis: a century of research, development and commercial applications. , 2011, Plant biotechnology journal.

[108]  Robert Kay,et al.  Duplication of CaMV 35S Promoter Sequences Creates a Strong Enhancer for Plant Genes , 1987, Science.

[109]  R. Horsch.  Commercialization of genetically engineered crops. , 1993, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[110]  B. Tabashnik,et al.  Engineering Modified Bt Toxins to Counter Insect Resistance , 2007, Science.

[111]  M. Koziel,et al.  Field Evaluation of Transgenic Tobacco Containing a Bacillus thuringiensis Insecticidal Protein Gene , 1992 .

[112]  L. Kim.  Advanced Engineered Pesticides , 1993 .

[113]  Jukon Kim,et al.  Chloroplast-targeted expression of synthetic cry1Ac in transgenic rice as an alternative strategy for increased pest protection , 2009, Planta.

[114]  K. W. Campbell,et al.  Lower fumonisin mycotoxin levels in the grain of Bt corn grown in the United States in 2000-2002. , 2004, Journal of agricultural and food chemistry.

[115]  S. Seetharam.  Should the Bt brinjal controversy concern healthcare professionals and bioethicists? , 2010, Indian journal of medical ethics.

[116]  W. H. Mcgaughey,et al.  Mechanism of insect resistance to the microbial insecticide Bacillus thuringiensis. , 1990, Science.

[117]  F. Gould.  Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. , 1998, Annual review of entomology.

[118]  D. Quist,et al.  Transgenic DNA introgressed into traditional maize landraces in Oaxaca, Mexico , 2001, Nature.

[119]  J. J. Valdez-Alarcón,et al.  Molecular characterization of Bacillus thuringiensis strains from Argentina , 2004, Antonie van Leeuwenhoek.

[120]  C. Ellers-kirk,et al.  Large-Scale Management of Insect Resistance to Transgenic Cotton in Arizona: Can Transgenic Insecticidal Crops be Sustained? , 2001, Journal of economic entomology.

[121]  F. S. Walters,et al.  An Engineered Chymotrypsin/Cathepsin G Site in Domain I Renders Bacillus thuringiensis Cry3A Active against Western Corn Rootworm Larvae , 2007, Applied and Environmental Microbiology.

[122]  H. Agaisse,et al.  How does Bacillus thuringiensis produce so much insecticidal crystal protein? , 1995, Journal of bacteriology.

[123]  Rosalind J Wright,et al.  Areawide Suppression of European Corn Borer with Bt Maize Reaps Savings to Non-Bt Maize Growers , 2010, Science.

[124]  B. Tabashnik.  Managing resistance with multiple pesticide tactics: theory, evidence, and recommendations. , 1989, Journal of economic entomology.

[125]  P. Rossignol,et al.  Biological Parameters of Convergent Lady Beetle (Coleoptera: Coccinellidae) Feeding on Aphids (Homoptera: Aphididae) on Transgenic Potato , 1996 .

[126]  M. Otto,et al.  A synthesis of laboratory and field studies on the effects of transgenic Bacillus thuringiensis (Bt) maize on non‐target Lepidoptera , 2010 .

[127]  K. S. Jayaraman,et al.  Illegal Bt cotton in India haunts regulators , 2001, Nature Biotechnology.

[128]  C. L. Hannay,et al.  The protein crystals of Bacillus thuringiensis Berliner. , 1955, Canadian journal of microbiology.

[129]  P. Christou.  No Credible Scientific Evidence is Presented to Support Claims that Transgenic DNA was Introgressed into Traditional Maize Landraces in Oaxaca, Mexico , 2002, Transgenic Research.

[130]  M. Koziel,et al.  Transgenic plants: An emerging approach to pest control , 1997, Nature Biotechnology.

[131]  J. Adamczyk,et al.  Impact of Bt Cottons Expressing One or Two Insecticidal Proteins of Bacillus thuringiensis Berliner on Growth and Survival of Noctuid (Lepidoptera) Larvae , 2001, Journal of economic entomology.