BIOTECHNOLOGY IN CROP PROTECTION: TOWARDS SUSTAINABLE INSECT CONTROL

  • Martin G. Edwards
  • Angharad M. R. Gatehouse
Part of the NATO Security through Science Series book series

Abstract

With a projected increase in world population to 10 billion over the next four decades, an immediate priority for agriculture is to achievemaximum production of food and other products in a manner that is environmentally sustainable and cost effective. Whilst insecticides are very effective in combating the immediate problem of insect attack on crops, nonspecific insecticides are harmful to beneficial organisms including predators and parasitoids of the target pest species.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    O. Olsson, The rise of Neolithic agriculture, Working Paper in Economics No 57 (2001).Google Scholar
  2. 2.
    J. Hill, E. Nelson, D. Tilman, S. Polasky, and D. Tiffany, Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels, Proc. Natl. Acad. Sci. U S A 103(30), 11206–11210 (2006).PubMedCrossRefGoogle Scholar
  3. 3.
    S. A. Hassan, F. Bigler, H. Bogenschutz, E. Boller, J. Brun, J. N. M. Calis, J. Coremanspelseneer, C. Duso, A. Grove, U. Heimbach, N. Helyer, H. Hokkanen, G. B. Lewis, F. Mansour, L. Moreth, L. Polgar, L. Samsoepetersen, B. Sauphanor, A. Staubli, G. Sterk, A. Vainio, M. Vandeveire, G. Viggiani, and H. Vogt, Results of the 6th Joint Pesticide Testing Program of the Iobc/Wprs Working Group Pesticides and Beneficial Organisms, Entomophaga 39(1), 107–119 (1994).CrossRefGoogle Scholar
  4. 4.
    A. G. Renwick, Pesticide residue analysis and its relationship to hazard characterisation (ADI/ARfD) and intake estimations (NEDI/NESTI), Pest Manag. Sci. 58, 1073–1082 (2002).PubMedCrossRefGoogle Scholar
  5. 5.
    C. James, ISAAA Brief 34 (2005).Google Scholar
  6. 6.
    J. Gatehouse and A. Gatehouse, in Biological and Biotechnological Control of Insect Pests, edited by J. Reichcigl and N. Reichcigl (CRC Press, Boca Raton, FL, 1999), pp. 211–241.Google Scholar
  7. 7.
    R. A. de Maagd, A. Bravo, and N. Crickmore, How Bacillus thuringiensis has evolved specific toxins to colonize the insect world, Trends Genet. 17(4), 193–199 (2001).PubMedCrossRefGoogle Scholar
  8. 8.
    A. M. R. Gatehouse, N. Ferry, and R. J. M. Raemaekers, The case of the monarch butterfly: A verdict is returned, Trends Genet. 18(5), 249–251 (2002).PubMedCrossRefGoogle Scholar
  9. 9.
    S. S. Gill, E. A. Cowles and V. Francis, Identification, isolation, and cloning of a Bacillus-Thuringiensis CryIac toxin-binding protein from the midgut of the Lepidopteran insect Heliothis-Virescens, J. Biol. Chem. 270(45), 27277–27282 (1995).PubMedCrossRefGoogle Scholar
  10. 10.
    P. J. K. Knight, N. Crickmore, and D. J. Ellar, The receptor for Bacillus-Thuringiensis Cryla(C) delta-endotoxin in the brush-border membrane of the Lepidopteran Manduca-Sexta is aminopeptidase-N, Mol. Microbiol. 11(3), 429–436 (1994).PubMedCrossRefGoogle Scholar
  11. 11.
    K. Luo, S. Sangadala, L. Masson, A. Mazza, R. Brousseau, and M. J. Adang, The Heliothis virescens 170 kDa aminopeptidase functions as “receptor A” by mediating specific Bacillus thuringiensis Cry1A delta-endotoxin binding and pore formation, J. Biochem. Mol. Biol. 27 (8/9), 735–743 (1997).CrossRefGoogle Scholar
  12. 12.
    S. Sangadala, F. S. Walters, L. H. English, and M. J. Adang, A mixture of Manduca-Sexta aminopeptidase and phosphatase enhances Bacillus-Thuringiensis insecticidal CryIa(C) toxin binding and (Rb+-K+)-Rb-86 efflux in vitro, J. Biol. Chem. 269(13), 10088–10092 (1994).PubMedGoogle Scholar
  13. 13.
    L. J. Gahan, F. Gould, and D. G. Heckel, Identification of a gene associated with bit resistance in Heliothis virescens, Science 293(5531), 857–860 (2001).PubMedCrossRefGoogle Scholar
  14. 14.
    Y. Nagamatsu, S. Toda, T. Koike, Y. Miyoshi, S. Shigematsu, and M. Kogure, Cloning, sequencing, and expression of the Bombyx mori receptor for Bacillus thuringiensis insecticidal CryIA(a) toxin, Biosci. Biotechnol. Biochem. 62(4), 727–734 (1998).PubMedCrossRefGoogle Scholar
  15. 15.
    R. K. Vadlamudi, E. Weber, I. H. Ji, T. H. Ji, and L. A. Bulla, Cloning and expression of a receptor for an insecticidal toxin of Bacillus-Thuringiensis, J. Biol. Chem. 270(10), 5490–5494 (1995).PubMedCrossRefGoogle Scholar
  16. 16.
    P. Denolf, Isolation, cloning and characterisation of Bacillus thuringiensis delta-endotoxin receptors in Lepidoptera, Ph.D. thesis (University of Gent, 1996).Google Scholar
  17. 17.
    J. S. Griffitts, J. L. Whitacre, D. E. Stevens, and R. V. Aroian, Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme, Science 293(5531), 860–864 (2001).PubMedCrossRefGoogle Scholar
  18. 18.
    M. Vaeck, A. Reynaerts, H. Hofte, S. Jansens, M. Debeuckeleer, C. Dean, M. Zabeau, M. Vanmontagu, and J. Leemans, Transgenic plants protected from insect attack, Nature 328(6125), 33–37 (1987).CrossRefGoogle Scholar
  19. 19.
    R. A. de Maagd, D. Bosch, and W. Stiekema, Bacillus thuringiensis toxin-mediated insect resistance in plants, Trends Plant Sci. 4(1), 9–13 (1999).PubMedCrossRefGoogle Scholar
  20. 20.
    M. Peferoen, in Advances in Insect Control: The Role of Transgenic Plants, edited by N. Carozzi and M. Koziel (Taylor and Francis, London, pp. 21–38 (1997).Google Scholar
  21. 21.
    A. M. Shelton, J. Z. Zhao, and R. T. Roush, Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants, Annu. Rev. Entomol. 47, 845–881 (2002).PubMedCrossRefGoogle Scholar
  22. 22.
    N. Ferry, M. Edwards, J. Gatehouse, T. Capell, P. Christou, and A. Gatehouse, Transgenic plants for insect pest control: A forward looking scientific perspective, Transgenic Res. 15(1), 13–19 (2006).PubMedCrossRefGoogle Scholar
  23. 23.
    B. E. Tabashnik, F. R. Groeters, N. Finson, Y. B. Liu, M. W. Johnson, D. G. Heckel, K. Luo, and M. J. Adang, in Molecular Genetics and Evolution of Pesticide Resistance, edited by T. Brown (Oxford University Press, USA, 1996), pp. 130–140.Google Scholar
  24. 24.
    P. Christou, T. Capell, A. Kohli, J. A. Gatehouse, and A. M. R. Gatehouse, Recent developments and future prospects in insect pest control in transgenic crops, Trends Plant Sci. 11(6), 302–308 (2006).PubMedCrossRefGoogle Scholar
  25. 25.
    J. A. Gatehouse, Plant resistance towards insect herbivores: A dynamic interaction, New Phytol. 156(2), 145–169 (2002).CrossRefGoogle Scholar
  26. 26.
    J. Harborne, Introduction to Ecological Chemistry (Academic Press, London, 1988).Google Scholar
  27. 27.
    J. Gatehouse, A. Gatehouse, and D. Bown, in Recombinant Protease Inhibitors in Plants, edited by D. Michaud (Landes Bioscience, Austin, TX, 2000), pp. 9–26.Google Scholar
  28. 28.
    L. Jouanin, M. Bonade-Bottino, C. Girard, G. Morrot, and M. Giband, Transgenic plants for insect resistance, Plant Sci. 131(1), 1–11 (1998).CrossRefGoogle Scholar
  29. 29.
    V. A. Hilder, A. M. R. Gatehouse, S. E. Sheerman, R. F. Barker, and D. Boulter, A novel mechanism of insect resistance engineered into tobacco, Nature 330(6144), 160–163 (1987).CrossRefGoogle Scholar
  30. 30.
    A. M. R. Gatehouse, V. A. Hilder, K. S. Powell, M. Wang, G. M. Davison, L. N. Gatehouse, R. E. Down, H. S. Edmonds, D. Boulter, C. A. Newell, A. Merryweather, W. D. O. Hamilton, and J. A. Gatehouse, Insect-resistant transgenic plants–Choosing the gene to do the job, Biochem. Soc. Trans. 22(4), 944–949 (1994).PubMedGoogle Scholar
  31. 31.
    J. Graham, R. J. McNicol, and K. Greig, Towards genetic based insect resistance in strawberry using the Cowpea trypsin inhibitor gene, Ann. Appl. Biol. 127 (1), 163–173 (1995).CrossRefGoogle Scholar
  32. 32.
    D. P. Xu, Q. Z. Xue, D. McElroy, Y. Mawal, V. A. Hilder, and R. Wu, Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests, Mol. Breed. 2(2), 167–173 (1996).CrossRefGoogle Scholar
  33. 33.
    R. M. Broadway, Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors, J. Insect Physiol. 43(9), 855–874 (1997).PubMedCrossRefGoogle Scholar
  34. 34.
    F. De Leo, M. Bonade-Bottino, L. R. Ceci, R. Gallerani, and L. Jouanin, Effects of a mustard trypsin inhibitor expressed in different plants on three lepidopteran pests, J. Biochem. Mol. Biol. 31(6/7), 593–602 (2001).CrossRefGoogle Scholar
  35. 35.
    J. C. Leple, M. Bonadebottino, S. Augustin, G. Pilate, V. D. Letan, A. Delplanque, D. Cornu, and L. Jouanin, Toxicity to Chrysomela-Tremulae (Coleoptera, Chrysomelidae) of transgenic poplars expressing a cysteine proteinase-inhibitor, Mol. Breed. 1(4), 319–328 (1995).CrossRefGoogle Scholar
  36. 36.
    C. Pannetier, M. Giband, P. Couzi, V. LeTan, M. Mazier, J. Tourneur, and B. Hau, Introduction of new traits into cotton through genetic engineering: Insect resistance as example, J. Biochem. Mol. Biol. 96(1), 163–166 (1997).Google Scholar
  37. 37.
    P. E. Urwin, H. J. Atkinson, D. A. Waller, and M. J. McPherson, Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance to Globodera-Pallida, Plant J. 8(1), 121–131 (1995).PubMedCrossRefGoogle Scholar
  38. 38.
    N. S. Outchkourov, B. Rogelj, B. Strukelj, and M. A. Jongsma, Expression of sea anemone equistatin in potato. Effects of plant proteases on heterologous protein production, Plant Physiol. 133(1), 379–390 (2003).PubMedCrossRefGoogle Scholar
  39. 39.
    A. Abdeen, A. Virgos, E. Olivella, J. Villanueva, X. Aviles, R. Gabarra, and S. Prat, Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors, Plant Mol. Biol. 57(2), 189–202 (2005).PubMedCrossRefGoogle Scholar
  40. 40.
    D. P. Bown, H. S. Wilkinson, and J. A. Gatehouse, Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigara, are members of complex multigene families, J. Biochem. Mol. Biol. 27 (7), 625–638 (1997).CrossRefGoogle Scholar
  41. 41.
    M. A. Jongsma and C. Bolter, The adaptation of insects to plant protease inhibitors, J. Insect Physiol. 43(10), 885–895 (1997).PubMedCrossRefGoogle Scholar
  42. 42.
    S. C. Dias, O. L. Franco, C. P. Magalhaes, O. B. de Oliveira-Neto, R. A. Laumann, E. L. Z. Figueira, F. R. Melo, and M. F. Grossi-de-Sa, Molecular cloning and expression of an alpha-amylase inhibitor from rye with potential for controlling insect pests, Protein J. 24(2), 113–123 (2005).PubMedCrossRefGoogle Scholar
  43. 43.
    A. L. Marsaro, S. M. N. Lazzari, E. L. Z. Figueira, and E. Y. Hirooka, Arnylase inhibitors in corn hybrids as a resistance factor to Sitophilus zeamais (Coleoptera: Curculionidae), Neotrop. Entomol. 34 (3), 443–450 (2005).CrossRefGoogle Scholar
  44. 44.
    H. E. Schroeder, S. Gollasch, A. Moore, L. M. Tabe, S. Craig, D. C. Hardie, M. J. Chrispeels, D. Spencer, and T. J. V. Higgins, Bean alpha-amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L) (Vol 107, Pg 1233, 1995), Plant Physiol. 109(3), 1129–1129 (1995).Google Scholar
  45. 45.
    R. E. Shade, H. E. Schroeder, J. J. Pueyo, L. M. Tabe, L. L. Murdock, T. J. V. Higgins, and M. J. Chrispeels, Transgenic pea-seeds expressing the alpha-amylase inhibitor of the common bean are resistant to bruchid beetles, Bio-Technology 12(8), 793–796 (1994).Google Scholar
  46. 46.
    M. J. Chrispeels and N. V. Raikhel, Lectins, lectin genes, and their role in plant defense, Plant Cell 3(1), 1–9 (1991).PubMedCrossRefGoogle Scholar
  47. 47.
    W. J. Peumans and E. J. M. Vandamme, Lectins as plant defense proteins, Plant Physiol. 109(2), 347–352 (1995).PubMedCrossRefGoogle Scholar
  48. 48.
    A. Gatehouse, K. Powell, W. Peumans, E. V. Damme, and J. Gatehouse, in Lectins Biomedical Perspectives, edited by A. Pusztai and S. Bardocz (Taylor and Francis, London, 1995), pp. 35–57.Google Scholar
  49. 49.
    X. Foissac, N. T. Loc, P. Christou, A. M. R. Gatehouse, and J. A. Gatehouse, Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA), J. Insect Physiol. 46(4), 573–583 (2000).PubMedCrossRefGoogle Scholar
  50. 50.
    A. M. R. Gatehouse, G. M. Davison, C. A. Newell, A. Merryweather, W. D. O. Hamilton, E. P. J. Burgess, R. J. C. Gilbert, and J. A. Gatehouse, Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: Growth room trials, Mol. Breed. 3(1), 49–63 (1997).CrossRefGoogle Scholar
  51. 51.
    K. S. Powell, A. M. R. Gatehouse, V. A. Hilder, and J. A. Gatehouse, Antifeedant effects of plant-lectins and an enzyme on the adult stage of the rice brown planthopper, Nilaparvata-Lugens, Entomol. Exp. Appl. 75(1), 51–59 (1995).CrossRefGoogle Scholar
  52. 52.
    N. Sauvion, Y. Rahbe, W. J. Peumans, E. J. M. VanDamme, J. A. Gatehouse, and A. M. R. Gatehouse, Effects of GNA and other mannose binding lectins on development and fecundity of the peach-potato aphid Myzus persicae, Entomol. Exp. Appl. 79(3), 285–293 (1996).CrossRefGoogle Scholar
  53. 53.
    K. V. Rao, K. S. Rathore, T. K. Hodges, X. Fu, E. Stoger, D. Sudhakar, S. Williams, P. Christou, M. Bharathi, D. P. Bown, K. S. Powell, J. Spence, A. M. R. Gatehouse, and J. A. Gatehouse, Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper, Plant J. 15(4), 469–477 (1998).PubMedCrossRefGoogle Scholar
  54. 54.
    P. Tinjuangjun, N. T. Loc, A. M. R. Gatehouse, J. A. Gatehouse, and P. Christou, Enhanced insect resistance in Thai rice varieties generated by particle bombardment, Mol. Breed. 6(4), 391–399 (2000).CrossRefGoogle Scholar
  55. 55.
    S. B. Maqbool, S. Riazuddin, N. T. Loc, A. M. R. Gatehouse, J. A. Gatehouse, and P. Christou, Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests, Mol. Breed. 7(1), 85–93 (2001).CrossRefGoogle Scholar
  56. 56.
    R. E. Down, A. M. R. Gatehouse, W. D. O. Hamilton, and J. A. Gatehouse, Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials, J. Insect Physiol. 42(11/12), 1035–1045 (1996).CrossRefGoogle Scholar
  57. 57.
    E. Stoger, S. Williams, P. Christou, R. E. Down, and J. A. Gatehouse, Expression of the insecticidal lectin from snowdrop (Galanthus nivalis agglutinin; GNA) in transgenic wheat plants: Effects on predation by the grain aphid Sitobion avenae, Mol. Breed. 5(1), 65–73 (1999).CrossRefGoogle Scholar
  58. 58.
    K. S. Powell, J. Spence, M. Bharathi, J. A. Gatehouse, and A. M. R. Gatehouse, Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal), J. Insect Physiol. 44(7/8), 529–539 (1998).PubMedCrossRefGoogle Scholar
  59. 59.
    J. P. Du, X. Foissac, A. Carss, A. M. R. Gatehouse, and J. A. Gatehouse, Ferritin acts as the most abundant binding protein for snowdrop lectin in the midgut of rice brown planthoppers (Nilaparvata lugens), J. Biochem. Mol. Biol. 30(4), 297–305 (2000).CrossRefGoogle Scholar
  60. 60.
    L. R. Ceci, M. Volpicella, Y. Rahbe, R. Gallerani, J. Beekwilder, and M. A. Jongsma, Selection by phage display of a variant mustard trypsin inhibitor toxic against aphids, Plant J. 33(3), 557–566 (2003).PubMedCrossRefGoogle Scholar
  61. 61.
    N. T. Loc, P. Tinjuangjun, A. M. R. Gatehouse, P. Christou, and J. A. Gatehouse, Linear transgene constructs lacking vector backbone sequences generate transgenic rice plants which accumulate higher levels of proteins conferring insect resistance, Mol. Breed. 9(4), 231–244 (2002).CrossRefGoogle Scholar
  62. 62.
    Y. Rahbe, C. Deraison, M. Bonade-Bottino, C. Girard, C. Nardon, and L. Jouanin, Effects of the cysteine protease inhibitor oryzacystatin (OC-I) on different aphids and reduced performance of Myzus persicae on OC-I expressing transgenic oilseed rape, Plant Sci. 164(4), 441–450 (2003).CrossRefGoogle Scholar
  63. 63.
    E. P. J. Burgess, L. A. Malone, J. T. Christeller, M. T. Lester, C. Murray, B. A. Philip, M. M. Phung, and E. L. Tregidga, Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests, Helicoverpa armigera and Spodoptera litura, Transgenic Res. 11(2), 185–198 (2002).PubMedCrossRefGoogle Scholar
  64. 64.
    E. Fitches, N. Audsley, J. A. Gatehouse, and J. P. Edwards, Fusion proteins containing neuropeptides as novel insect control agents: Snowdrop lectin delivers fused allatostatin to insect haemolymph following oral ingestion, J. Biochem. Mol. Biol. 32(12), 1653–1661 (2002).CrossRefGoogle Scholar
  65. 65.
    J. T. Christeller, E. P. J. Burgess, V. Mett, H. S. Gatehouse, N. P. Markwick, C. Murray, L. A. Malone, M. A. Wright, B. A. Philip, D. Watt, L. N. Gatehouse, G. L. Lovei, A. L. Shannon, M. M. Phung, L. M. Watson, and W. A. Laing, The expression of a mammalian proteinase inhibitor, bovine spleen trypsin inhibitor in tobacco and its effects on Helicoverpa armigera larvae, Transgenic Res. 11(2), 161–173 (2002).PubMedCrossRefGoogle Scholar
  66. 66.
    R. A. de Maagd, A. Bravo, C. Berry, N. Crickmore, and H. E. Schnepf, Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria, Annu. Rev. Genet. 37, 409–433 (2003).PubMedCrossRefGoogle Scholar
  67. 67.
    C. G. Yu, M. A. Mullins, G. W. Warren, M. G. Koziel, and J. J. Estruch, The Bacillus thuringiensis vegetative insecticidal protein Vip3A lyses midgut epithelium cells of susceptible insects, Appl. Environ. Microbiol. 63(2), 532–536 (1997).PubMedGoogle Scholar
  68. 68.
    A. Chattopadhyay, N. B. Bhatnagar, and R. Bhatnagar, Bacterial insecticidal toxins, Crit. Rev. Microbiol. 30(1), 33–54 (2004).PubMedCrossRefGoogle Scholar
  69. 69.
    D. Liu, S. Burton, T. Glancy, Z. S. Li, R. Hampton, T. Meade, and D. J. Merlo, Insect resistance conferred by 283 kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana, Nat. Biotechnol. 21(10), 1222–1228 (2003).PubMedCrossRefGoogle Scholar
  70. 70.
    L. Mehlo, D. Gahakwa, P. T. Nghia, N. T. Loc, T. Capell, J. A. Gatehouse, A. M. R. Gatehouse, and P. Christou, An alternative strategy for sustainable pest resistance in genetically enhanced crops, Proc. Natl. Acad. Sci. U S A 102(22), 7812–7816 (2005).PubMedCrossRefGoogle Scholar
  71. 71.
    E. Fitches, M. G. Edwards, C. Mee, E. Grishin, A. M. R. Gatehouse, J. P. Edwards, and J. A. Gatehouse, Fusion proteins containing insect-specific toxins as pest control agents: Snowdrop lectin delivers fused insecticidal spider venom toxin to insect haemolymph following oral ingestion, J. Insect Physiol. 50(1), 61–71 (2004).PubMedCrossRefGoogle Scholar
  72. 72.
    I. T. Baldwin, R. Halitschke, A. Kessler, and U. Schittko, Merging molecular and ecological approaches in plant–insect interactions, Ecol. Appl. 4(4), 351–358 (2001).Google Scholar
  73. 73.
    B. A. Bailey, M. D. Strem, H. H. Bae, G. A. de Mayolo, and M. J. Guiltinan, Gene expression in leaves of Theobroma cacao in response to mechanical wounding, ethylene, and/or methyl jasmonate, Plant Sci. 168(5), 1247–1258 (2005).CrossRefGoogle Scholar
  74. 74.
    D. Hermsmeier, U. Schittko, and I. T. Baldwin, Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata I: Large-scale changes in the accumulation of growth- and defense-related plant mRNAs, Plant Physiol. 125(2), 683–700 (2001).PubMedCrossRefGoogle Scholar
  75. 75.
    M. J. Stout, A. L. Fidantsef, S. S. Duffey, and R. M. Bostock, Signal interactions in pathogen and insect attack: Systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum, Plant Pathol. 54(3/4), 115–130 (1999).Google Scholar
  76. 76.
    F. Zhang, L. Zhu, and G. C. He, Differential gene expression in response to brown planthopper feeding in rice, J. Plant Physiol. 161(1), 53–62 (2004).PubMedCrossRefGoogle Scholar
  77. 77.
    W. Q. Chen, N. J. Provart, J. Glazebrook, F. Katagiri, H. S. Chang, T. Eulgem, F. Mauch, S. Luan, G. Z. Zou, S. A. Whitham, P. R. Budworth, Y. Tao, Z. Y. Xie, X. Chen, S. Lam, J. A. Kreps, J. F. Harper, A. Si-Ammour, B. Mauch-Mani, M. Heinlein, K. Kobayashi, T. Hohn, J. L. Dangl, X. Wang, and T. Zhu, Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses, Plant Cell 14(3), 559–574 (2002).PubMedCrossRefGoogle Scholar
  78. 78.
    D. D. Schmidt, C. Voelckel, M. Hartl, S. Schmidt, and I. T. Baldwin, Specificity in ecological interactions. Attack from the same lepidopteran herbivore results in species-specific transcriptional responses in two solanaceous host plants, Plant Physiol. 138(3), 1763–1773 (2005).PubMedCrossRefGoogle Scholar
  79. 79.
    E. Rojo, R. Solano, and J. J. Sanchez-Serrano, Interactions between signaling compounds involved in plant defense, J. Plant Growth Regul. 22(1), 82–98 (2003).CrossRefGoogle Scholar
  80. 80.
    R. A. Dixon, Engineering of plant natural product pathways, Ecol. Appl. 8(3), 329–336 (2005).Google Scholar
  81. 81.
    Cropgen (2002); available at http://www.cropgen.org/.Google Scholar
  82. 82.
    GM Science Review (2003); available at http://www.gmsciencedebate.org.uk.Google Scholar
  83. 83.
    E. Abergel and K. Barrett, Putting the cart before the horse: A review of biotechnology policy in Canada, J. Can. Stud/REC 37(3), 135–161 (2002).Google Scholar
  84. 84.
    E. A. Clark, Environmental risks of genetic engineering, J. Biochem. Mol. Biol. 148(1/2), 47–60 (2006).Google Scholar
  85. 85.
    M. J. Crawley, S. L. Brown, R. S. Hails, D. D. Kohn, and M. Rees, Biotechnology—Transgenic crops in natural habitats, Nature 409(6821), 682–683 (2001).PubMedCrossRefGoogle Scholar
  86. 86.
    P. J. Dale, B. Clarke, and E. M. G. Fontes, Potential for the environmental impact of transgenic crops (Nat. Biotechnol. vol 20, p. 567, 2002), Nat. Biotechnol. 20(8), 843(2002) (erratum).PubMedCrossRefGoogle Scholar
  87. 87.
    J. Davison, Risk mitigation of genetically modified bacteria and plants designed for bioremediation, J. Ind. Microbiol. Biotechnol. 32(11/12), 639–650 (2005).PubMedCrossRefGoogle Scholar
  88. 88.
    D. Lee and E. Natesan, Evaluating genetic containment strategies for transgenic plants, Trends Biotechnol. 24(3), 109–114 (2006).PubMedCrossRefGoogle Scholar
  89. 89.
    D. Michaud, Environmental impact of transgenic crops, I: Transgene migration, Phytoprotection 86(2), 93–105 (2005).Google Scholar
  90. 90.
    A. A. Snow, D. A. Andow, P. Gepts, E. M. Hallerman, A. Power, J. M. Tiedje, and L. L. Wolfenbarger, Genetically engineered organisms and the environment: Current status and recommendations, Ecol. Appl. 15(2), 377–404 (2005).Google Scholar
  91. 91.
    A. T. Groot and M. Dicke, Insect-resistant transgenic plants in a multi-trophic context, Plant J. 31(4), 387–406 (2002).PubMedCrossRefGoogle Scholar
  92. 92.
    P. A. M. Hogervorst, N. Ferry, A. M. R. Gatehouse, F. L. Wackers, and J. Romeis, Direct effects of snowdrop lectin (GNA) on larvae of three aphid predators and fate of GNA after ingestion, J. Insect Physiol. 52(6), 614–624 (2006).PubMedCrossRefGoogle Scholar
  93. 93.
    L. B. Obrist, A. Dutton, J. Romeis, and F. Bigler, Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea, Biocontrol 51(1), 31–48 (2006).CrossRefGoogle Scholar
  94. 94.
    T. H. Schuler, R. P. J. Potting, I. Denholm, and G. M. Poppy, Parasitoid behaviour and Bt plants, Nature 400(6747), 825–826 (1999).PubMedCrossRefGoogle Scholar
  95. 95.
    E. Vojtech, M. Meissle, and G. M. Poppy, Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesta marginiventris (Hymenoptera: Braconidae), Transgenic Res. 14(2), 133–144 (2005).PubMedCrossRefGoogle Scholar
  96. 96.
    E. B. Dogan, R. E. Berry, G. L. Reed, and P. A. Rossignol, Biological parameters of convergent lady beetle (Coleoptera: Coccinellidae) feeding on aphids (Homoptera: Aphididae) on transgenic potato, J. Econ. Entomol. 89(5), 1105–1108 (1996).Google Scholar
  97. 97.
    R. E. Down, L. Ford, S. J. Bedford, L. N. Gatehouse, C. Newell, J. A. Gatehouse, and A. M. R. Gatehouse, Influence of plant development and environment on transgene expression in potato and consequences for insect resistance, Transgenic Res. 10(3), 223–236 (2001).PubMedCrossRefGoogle Scholar
  98. 98.
    G. Head, C. R. Brown, M. E. Groth, and J. J. Duan, Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: Implications for secondary exposure risk assessment, Entomol. Exp. Appl. 99(1), 37–45 (2001).CrossRefGoogle Scholar
  99. 99.
    H. A. Bell, E. C. Fitches, G. C. Marris, J. Bell, J. P. Edwards, J. A. Gatehouse, and A. M. R. Gatehouse, Transgenic GNA expressing potato plants augment the beneficial biocontrol of Lacanobia oleracea (Lepidoptera: Noctuidae) by the parasitoid Eulophus pennicornis (Hymenoptera: eulophidae), Transgenic Res. 10(1), 35–42 (2001).PubMedCrossRefGoogle Scholar
  100. 100.
    M. E. Wakefield, H. A. Bell, E. C. Fitches, J. P. Edwards, and A. M. R. Gatehouse, Effects of Galanthus nivalis agglutinin (GNA) expressed in tomato leaves on larvae of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and the effect of GNA on the development of the endoparasitoid Meteorus gyrator (Hymenoptera: Braconidae), Bull. Entomol. Res. 96(1), 43–52 (2006).PubMedCrossRefGoogle Scholar
  101. 101.
    H. A. Bell, R. E. Down, E. C. Fitches, J. P. Edwards, and A. M. R. Gatehouse, Impact of genetically modified potato expressing plant-derived insect resistance genes on the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae), Biocontrol Sci. Technol. 13(8), 729–741 (2003).CrossRefGoogle Scholar
  102. 102.
    R. E. Down, L. Ford, S. D. Woodhouse, G. M. Davison, M. E. N. Majerus, J. A. Gatehouse, and A. M. R. Gatehouse, Tritrophic interactions between transgenic potato expressing snowdrop lectin (GNA), an aphid pest (peach-potato aphid; Myzus persicae (Sulz.) and a beneficial predator (2-spot ladybird; Adalia bipunctata L.), Transgenic Res. 12(2), 229–241 (2003).PubMedCrossRefGoogle Scholar
  103. 103.
    R. E. Down, L. Ford, S. D. Woodhouse, R. J. M. Raemaekers, B. Leitch, J. A. Gatehouse, and A. M. R. Gatehouse, Snowdrop lectin (GNA) has no acute toxic effects on a beneficial insect predator, the 2-spot ladybird (Adalia bipunctata L.), J. Insect Physiol. 46(4), 379–391 (2000).PubMedCrossRefGoogle Scholar
  104. 104.
    N. Ferry, R. J. M. Raemaekers, M. E. N. Majerus, L. Jouanin, G. Port, J. A. Gatehouse, and A. M. R. Gatehouse, Impact of oilseed rape expressing the insecticidal cysteine protease inhibitor oryzacystatin on the beneficial predator Harmonia axyridis (multicoloured Asian ladybeetle), Mol. Ecol. 12(2), 493–504 (2003).PubMedCrossRefGoogle Scholar
  105. 105.
    N. Ferry, L. Jouanin, L. R. Ceci, A. Mulligan, K. Emami, J. A. Gatehouse, and A. M. R. Gatehouse, Impact of oilseed rape expressing the insecticidal serine protease inhibitor, mustard trypsin inhibitor-2 on the beneficial predator Pterostichus madidus, Mol. Ecol. 14(1), 337–349 (2005).PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Martin G. Edwards
    • 1
  • Angharad M. R. Gatehouse
    • 1
  1. 1.Institute for Research on Environment and Sustainability, Division of BiologyNewcastle UniversityNewcastle upon TyneUK

Personalised recommendations