Encyclopedia of Sustainability Science and Technology

2012 Edition
| Editors: Robert A. Meyers

Genetic Engineering of Crops for Insect Resistance

Reference work entry
DOI: https://doi.org/10.1007/978-1-4419-0851-3_239

Definition of the Subject

Genetic engineering of crops for insect resistance is the introduction of specific DNA sequences into crop plants to enhance their resistance to insect pests. The DNA sequences used usually encode proteins with insecticidal activity, so that in plants which contain introduced DNA, an insecticidal protein is present. However, other strategies to improve plant defenses against insects have been explored. Genetically engineered crops that are protected against major insect pests by production of insecticidal proteins from a soil bacterium, Bacillus thuringiensis , have become widely used in global agriculture since their introduction in 1996.


Twenty years have elapsed since the first publications describing transgenic plants, which showed enhanced resistance to insect herbivores, as a result of the expression of a foreign gene encoding Bacillus thuringiensis (Bt) toxin [1, 2, 3]. In the intervening years, crops expressing these toxins have become...

This is a preview of subscription content, log in to check access.


Primary Literature

  1. 1.
    Barton KA, Whitely HR, Yang N-S (1987) Bacillus thuringiensis δ-endotoxin expressed in transgenic Nicotiana tabacum provides resistance to Lepidopteran insects. Plant Physiol 85:1103–1109CrossRefGoogle Scholar
  2. 2.
    Fischhoff DA, Bowdish KS, Perlak FJ, Marrone PG, McCormick SH, Niedermeyer JG, Dean DA, Kusano-Kretzmer K, Mayer EJ, Rochester DE, Rogers SG, Fraley RT (1987) Insect tolerant transgenic tomato plants. Bio/Technology 5:807–813CrossRefGoogle Scholar
  3. 3.
    Vaeck M, Reynaerts A, Hofte H, Jansens S, De Beuckeleer M, Dean C, Zabeau M, Van Montagu M, Leemans J (1987) Transgenic plants protected from insect attack. Nature (London) 328:33–37CrossRefGoogle Scholar
  4. 4.
    Toenniessen GH, O’Toole JC, DeVries J (2003) Advances in plant biotechnology and its adoption in developing countries. Curr Opin Plant Biol 6:191–198CrossRefGoogle Scholar
  5. 5.
    Shelton AM, Zhao J-Z, Roush RT (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu Rev Entomol 47:845–881CrossRefGoogle Scholar
  6. 6.
    Aronson AI, Shai Y (2001) Why Bacillus thuringiensis insecticidal toxins are so effective: unique features of their mode of action. FEMS Microbiol Lett 195:1–8CrossRefGoogle Scholar
  7. 7.
    de Maagd RA, Bravo A, Crickmore N (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199CrossRefGoogle Scholar
  8. 8.
    Damgaard PH, Hansen BM, Pedersen JC, Eilenberg J (1997) Natural occurrence of Bacillus thuringiensis on cabbage foliage and in insects associated with cabbage crops. J Appl Microbiol 82:253–258Google Scholar
  9. 9.
    Bizzarri MF, Bishop AH (2007) Recovery of Bacillus thuringiensis in vegetative form from the phylloplane of clover (Trifolium hybridum) during a growing season. J Inverteb Pathol 94:38–47CrossRefGoogle Scholar
  10. 10.
    Bernhard K, Jarrett P, Meadows M, Butt J, Ellis DJ, Roberts GM, Pauli S, Rodgers P, Burges HD (1997) Natural isolates of Bacillus thuringiensis: worldwide distribution, characterization, and activity against insect pests. J Inverteb Pathol 70:59–68CrossRefGoogle Scholar
  11. 11.
    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 62:807–813Google Scholar
  12. 12.
    Berry C, O’Neil S, Ben-Dov E, Jones AF, Murphy L, Quail MA, Holden MTG, Harris D, Zaritsky A, Parkhill J (2002) Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israeliensis. Appl Environ Microbiol 68:5082–5095CrossRefGoogle Scholar
  13. 13.
    Parker MW, Feil SC (2005) Pore-forming protein toxins: from structure to function. Prog Biophys Mol Biol 88:91–142CrossRefGoogle Scholar
  14. 14.
    Li J, Carrol J, Ellar DJ (1991) Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. Nature 353:815–821CrossRefGoogle Scholar
  15. 15.
    Grochulski P, Masson L, Borisova S, Pusztai-Carey M, Schwartz JL, Brousseau R, Cygler M (1995) Bacillus thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation. J Mol Biol 254:447–464CrossRefGoogle Scholar
  16. 16.
    Morse RJ, Yamamoto T, Stroud RM (2001) Structure of Cry2Aa suggests an unexpected receptor binding epitope. Structure 9:409–417CrossRefGoogle Scholar
  17. 17.
    Galitsky N, Cody V, Wojtczak A, Ghosh D, Luft JR, Pangborn W, English L (2001) Structure of the insecticidal bacterial δ-endotoxin CryBb1 of Bacillus thuringiensis. Acta Crystallogr D 57:1101–1109CrossRefGoogle Scholar
  18. 18.
    Boonserm P, Mo M, Angsuthanasombat C, Lescar J (2006) Structure of the functional form of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8-Angstrom resolution. J Bacteriol 188:3391–3401CrossRefGoogle Scholar
  19. 19.
    Boonserm P, Davis P, Ellar DJ, Li J (2005) Crystal structure of the mosquito-larvicidal toxin Cry4Ba and its biological implications. J Mol Biol 348:363–382CrossRefGoogle Scholar
  20. 20.
    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 37:409–433CrossRefGoogle Scholar
  21. 21.
    Bravo A, Sánchez J, Kouskoura T, Crickmore N (2002) N-terminal activation is an essential early step in the mechanism of action of the B. thuringiensis Cry1Ac insecticidal toxin. J Biol Chem 277:23985–23987CrossRefGoogle Scholar
  22. 22.
    Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435CrossRefGoogle Scholar
  23. 23.
    Knight P, Crickmore N, Ellar DJ (1994) The receptor for Bacillus thuringiensis CryIA(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol Microbiol 11:429–436CrossRefGoogle Scholar
  24. 24.
    Vadlamudi RK, Weber E, Ji I, Ji TH, Bulla LA Jr (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J Biol Chem 270:5490–5494CrossRefGoogle Scholar
  25. 25.
    Valaitis AP, Jenkins JL, Lee MK, Dean DH, Garner KJ (2001) Isolation and partial characterization of Gypsy moth BTR-270, an anionic brush border membrane glycoconjugate that binds Bacillus thuringiensis Cry1A toxins with high affinity. Arch Insect Biochem Physiol 46:186–200CrossRefGoogle Scholar
  26. 26.
    Jurat-Fuentes JL, Adang MJ (2004) Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur J Biochem 271:3127–3135CrossRefGoogle Scholar
  27. 27.
    Fernández LE, Aimanova KG, Gill SS, Bravo A, Soberón M (2006) A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae. Biochem J 394:77–84CrossRefGoogle Scholar
  28. 28.
    Krishnamoorthy M, Jurat-Fuentes JL, McNall RJ, Andacht T, Adang MJ (2007) Identification of novel CrylAc binding proteins in midgut membranes from Heliothis virescens using proteomic analyses. Insect Biochem Mol Biol 37:189–201CrossRefGoogle Scholar
  29. 29.
    Gahan LJ, Gould F, Heckel DG (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293:857–860CrossRefGoogle Scholar
  30. 30.
    Yang YJ, Chen HY, Wu SW, Yang YH, Xu XJ, Wu YD (2006) Identification and molecular detection of a deletion mutation responsible for a truncated cadherin of Helicoverpa armigera. Insect Biochem Mol Biol 36:735–740CrossRefGoogle Scholar
  31. 31.
    Xie R, Zhuang M, Ross LS, Gómez I, Oltean DI, Bravo A, Soberón M, Gill SS (2005) Single amino acid mutations in the cadherin receptor from Heliothis virescens affect its toxin binding ability to Cry1A toxins. J Biol Chem 280:8416–8425CrossRefGoogle Scholar
  32. 32.
    Tsuda Y, Nakatani F, Hashimoto K, Ikawa S, Matsuura C, Fukada T, Sugimoto K, Himeno M (2003) Cytotoxic activity of Bacillus thuringiensis Cry proteins on mammalian cells transfected with cadherin-like Cry receptor gene of Bombyx mori (silkworm). Biochem J 369:697–703CrossRefGoogle Scholar
  33. 33.
    Soberón M, Pardo-López L, López I, Gómez I, Tabashnik BE, Bravo A (2007) Engineering modified Bt toxins to counter insect resistance. Science 318:1640–1642CrossRefGoogle Scholar
  34. 34.
    Herrero S, Gechev T, Bakker PL, Moar WJ, de Maagd RA (2005) Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four aminopeptidase N genes. BMC Genomics 6:96CrossRefGoogle Scholar
  35. 35.
    Rajagopal R, Sivakumar S, Agrawal N, Malhotra P, Bhatnagar RK (2002) Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J Biol Chem 277:46849–46851CrossRefGoogle Scholar
  36. 36.
    Sivakumar S, Rajagopal R, Venkatesh GR, Srivastava A, Bhatnagar RK (2007) Knockdown of aminopeptidase-N from Helicoverpa armigera larvae and in transfected Sf21 cells by RNA interference reveals its functional interaction with Bacillus thuringiensis insecticidal protein Cry1Ac. J Biol Chem 282:7312–7319CrossRefGoogle Scholar
  37. 37.
    Gill M, Ellar D (2002) Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1. Insect Mol Biol 11:619–625CrossRefGoogle Scholar
  38. 38.
    Burton SL, Ellar DJ, Li J, Derbyshire DJ (1999) N-acetylgalactosamine on the putative insect receptor aminopeptidase N is recognised by a site on the domain III lectin-like fold of a Bacillus thuringiensis insecticidal toxin. J Mol Biol 287:1011–1022CrossRefGoogle Scholar
  39. 39.
    Knight PJK, Carroll J, Ellar DJ (2004) Analysis of glycan structures on the 120 kDa aminopeptidase N of Manduca sexta and their interactions with Bacillus thuringiensis CrylAc toxin. Insect Biochem Mol Biol 34:101–112CrossRefGoogle Scholar
  40. 40.
    de Maagd RA, Bakker PL, Masson L, Adang MJ, Sangadala S, Stiekema W, Bosch D (1999) Domain III of the Bacillus thuringiensis delta-endotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and to its purified aminopeptidase N. Mol Microbiol 31:463–471CrossRefGoogle Scholar
  41. 41.
    Jenkins JL, Lee MK, Valaitis AP, Curtiss A, Dean DH (2000) Bivalent sequential binding model of a Bacillus thuringiensis toxin to gypsy moth aminopeptidase N receptor. J Biol Chem 275:14423–14431CrossRefGoogle Scholar
  42. 42.
    Jimenez-Juarez N, Munoz-Garay C, Gomez I, Saab-Rincon G, Damian-Almazo JY, Gill SS, Soberon M, Bravo A (2007) Bacillus thuringiensis Cry1Ab mutants affecting oligomer formation are non-toxic to Manduca sexta larvae. J Biol Chem 282:21222–21229CrossRefGoogle Scholar
  43. 43.
    Rausell C, García-Robles I, Sánchez J, Muñoz-Garay C, Martínez-Ramírez AC, Real MD, Bravo A (2004) Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata [Say]. Biochem Biophys Acta 1660:99–105CrossRefGoogle Scholar
  44. 44.
    Gómez I, Sánchez J, Miranda R, Bravo A, Soberón M (2002) Cadherin-like receptor binding facilitates proteolytic cleavage of helix a-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Lett 513:242–246CrossRefGoogle Scholar
  45. 45.
    Chen J, Hua G, Jurat-Fuentes JL, Abdullah MA, Adang MJ (2007) Synergism of Bacillus thuringiensis toxins by a fragment of a toxin-binding cadherin. Proc Natl Acad Sci USA 104:13901–13906CrossRefGoogle Scholar
  46. 46.
    Parenti P, Morandi P, McGivan JD, Consonnic P, Leonardi G, Giordana B (1997) Properties of the aminopeptidase N from the silkworm midgut (Bombyx mori). Insect Biochem Mol Biol 27:397–403CrossRefGoogle Scholar
  47. 47.
    Zhuang M, Oltean DI, Gómez I, Pullikuth AK, Soberón M, Bravo A, Gill SS (2002) Heliothis virescens and Manduca sexta lipid rafts are involved in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J Biol Chem 277:13863–13872CrossRefGoogle Scholar
  48. 48.
    Bravo A, Gómez I, Conde J, Muñoz-Garay C, Sánchez J, Zhuang M, Gill SS, Soberón M (2004) Oligomerization triggers differential binding of a pore-forming toxin to a different receptor leading to efficient interaction with membrane microdomains. Biochem Biophys Acta 1667:38–46CrossRefGoogle Scholar
  49. 49.
    Pigott CR, Ellar DJ (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71:255–281CrossRefGoogle Scholar
  50. 50.
    Sacchi VF, Wolfsberger MG (1996) Amino acid absorption. In: Lehane MJ, Billingsley PF (eds) Biology of the insect midgut. Chapman and Hall, London, pp 265–292CrossRefGoogle Scholar
  51. 51.
    Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci USA 103:9897–9902CrossRefGoogle Scholar
  52. 52.
    Moellenbeck DJ, Peters ML, Bing JW, Rouse JR, Higgins LS, Sims L, Nevshemal T, Marshall L, Ellis RT, Bystrak PG, Lang BA, Stewart JL, Kouba K, Sondag V, Gustafson V, Nour K, Xu DP, Swenson J, Zhang J, Czapla T, Schwab G, Jayne S, Stockhoff BA, Narva K, Schnepf HE, Stelman SJ, Poutre C, Koziel M, Duck N (2001) Insecticidal proteins from Bacillus thuringiensis protect corn from corn rootworms. Nat Biotechnol 19:668–672CrossRefGoogle Scholar
  53. 53.
    Ellis RT, Stockhoff BA, Stamp L, Schnepf HE, Schwab GE, Knuth M, Russell J, Cardineau GA, Narva KE (2002) Novel Bacillus thuringiensis binary insecticidal crystal proteins active on western corn rootworm, Diabrotica virgifera virgifera LeConte. Appl Environ Microbiol 68:1137–1145CrossRefGoogle Scholar
  54. 54.
    Darboux I, Nielsen-LeRoux C, Charles JF, Pauron D (2001) The receptor of Bacillus sphaericus binary toxin in Culex pipiens (Diptera: Culicidae) midgut: molecular cloning and expression. Insect Biochem Mol Biol 31:981–990CrossRefGoogle Scholar
  55. 55.
    Charles JF, NielsenLeRoux C, Delecluse A (1996) Bacillus sphaericus toxins: molecular biology and mode of action. Annu Rev Entomol 41:451–472CrossRefGoogle Scholar
  56. 56.
    Warren GW (1997) Vegetative insecticidal proteins: novel proteins for control of corn pests. In: Carozzi NB, Koziel MG (eds) Advances in insect control: the role of transgenic plants. Taylor & Francis, London, UK, pp 109–121Google Scholar
  57. 57.
    Barth H, Aktories K, Popoff MR, Stiles BG (2004) Binary bacterial toxins: Biochemistry, biology, and applications of common Clostridium and Bacillus proteins. Microbiol Mol Biol Rev 68:373–402CrossRefGoogle Scholar
  58. 58.
    Leuber M, Orlik F, Schiffler B, Sickmann A, Benz R (2006) Vegetative insecticidal protein (Vip1Ac) of Bacillus thuringiensis HD201: Evidence for oligomer and channel formation. Biochemistry 45:283–288CrossRefGoogle Scholar
  59. 59.
    Estruch JJ, Warren GW, Mullins MA, Nye GJ, Craig JA, Koziel MG (1996) Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc Natl Acad Sci USA 93:5389–5394CrossRefGoogle Scholar
  60. 60.
    Yu CG, Mullins MA, Warren GW, Koziel MG, Estruch JJ (1997) The Bacillus thuringiensis vegetative insecticidal protein Vip3A lyses midgut epithelium cells of susceptible insects. Appl Environ Microbiol 63:532–536Google Scholar
  61. 61.
    Lee MK, Miles P, Chen JS (2006) Brush border membrane binding properties of Bacillus thuringiensis Vip3A toxin to Heliothis virescens and Helicoverpa zea midguts. Biochem Biophys Res Commun 339:1043–1047CrossRefGoogle Scholar
  62. 62.
    Lee MK, Walters FS, Hart H, Palekar N, Chen JS (2003) Mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab delta-endotoxin. Appl Environ Microbiol 69:4648–4657CrossRefGoogle Scholar
  63. 63.
    Fang J, Xu X, Wang P, Zhao J-Z, Shelton AM, Cheng J, Feng M-G, Shen Z (2007) Characterization of chimeric Bacillus thuringiensis Vip3 toxins. Appl Environ Microbiol 73:956–961CrossRefGoogle Scholar
  64. 64.
    Li J, Pandelakis AK, Ellar DJ (1996) Structure of the mosquitocidal δ-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. J Mol Biol 257:129–152CrossRefGoogle Scholar
  65. 65.
    Du J, Knowles BH, Li J, Ellar DJ (1999) Biochemical characterization of Bacillus thuringiensis cytolytic toxins in association with a phospholipid bilayer. Biochem J 338:185–193CrossRefGoogle Scholar
  66. 66.
    Promdonkoy B, Ellar DJ (2003) Investigation of the pore-forming mechanism of a cytolytic δ-endotoxin from Bacillus thuringiensis. Biochem J 374:255–259CrossRefGoogle Scholar
  67. 67.
    Koni PA, Ellar DJ (1994) Biochemical characterization of Bacillus thuringiensis cytolytic δ-endotoxins. Microbiology 140:1869–1880CrossRefGoogle Scholar
  68. 68.
    Wirth MC, Georghiou GP, Federeci BA (1997) CytA enables CryIV endotoxins of Bacillus thuringiensis to overcome high levels of CryIV resistance in the mosquito, Culex quinquefasciatus. Proc Natl Acad Sci USA 94:10536–10540CrossRefGoogle Scholar
  69. 69.
    Pérez C, Fernández LE, Sun J, Folch JL, Gill SS, Soberón M, Bravo A (2005) Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc Natl Acad Sci USA 102:18303–18308CrossRefGoogle Scholar
  70. 70.
    Mazier M, Pannetier C, Tourneur J, Jouanin L, Giband M (1997) The expression of Bacillus thuringiensis toxin genes in plant cells. Biotechnol Annu Rev 3:313–347CrossRefGoogle Scholar
  71. 71.
    Zheng SJ, Henken B, de Maagd RA, Purwito A, Krens FA, Kik C (2005) Two different Bacillus thuringiensis toxin genes confer resistance to beet armyworm (Spodoptera exigua Hubner) in transgenic Bt-shallots (Allium cepa L.). Transgenic Res 14:261–272CrossRefGoogle Scholar
  72. 72.
    Fujimoto H, Itoh K, Yamamoto M, Kyozuka J, Shimamoto K (1993) Insect resistant rice generated by introduction of a modified δ–endotoxin gene of Bacillus thuringiensis. Bio/Technology 11:194–200CrossRefGoogle Scholar
  73. 73.
    Wunn J, Kloti A, Burkhardt PK, Biswas GCG, Launis K, Iglesias VA, Potrykus I (1996) Transgenic Indica rice breeding line IR58 expressing a synthetic cryIA(b) gene from Bacillus thuringiensis provides effective insect pest control. Bio/Technology 14:171–176CrossRefGoogle Scholar
  74. 74.
    Nayak P, Basu D, Das S, Basu A, Ghosh D, Ramakrishnan NA, Ghosh M, Sen SK (1997) Transgenic elite indica rice plants expressing CryIAc delta-endotoxin of Bacillus thuringiensis are resistant against yellow stem borer (Scirpophaga incertulas). Proc Natl Acad Sci USA 94:2111–2116CrossRefGoogle Scholar
  75. 75.
    Vaughn T, Cavato T, Brar G, Coombe T, DeGooyer T, Ford S, Groth M, Howe A, Johnson S, Kolacz K, Pilcher C, Purcell J, Romano C, English L, Pershing J (2005) A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci 45:931–938CrossRefGoogle Scholar
  76. 76.
    Breitler JC, Cordero MJ, Royer M, Meynard D, San Segundo B, Guiderdoni E (2001) The-689/+197 region of the maize protease inhibitor gene directs high level, wound-inducible expression of the cry1B gene which protects transgenic rice plants from stemborer attack. Mol Breed 7:259–274CrossRefGoogle Scholar
  77. 77.
    Breitler JC, Vassal JM, Catala MD, Meynard D, Marfa V, Mele E, Royer M, Murillo I, San Segundo B, Guiderdoni E, Messeguer J (2004) Bt rice harbouring Cry genes controlled by a constitutive or wound-inducible promoter: protection and transgene expression under Mediterranean field conditions. Plant Biotechnol J 2:417–430CrossRefGoogle Scholar
  78. 78.
    Miklos JA, Alibhai MF, Bledig SA, Connor-Ward DC, Gao A-G, Holmes BA, Kolacz KH, Kabuye VT, MacRae TC, Paradise MS, Toedebusch AS, Harrison LA (2007) Characterization of soybean exhibiting high expression of a synthetic Bacillus thuringiensis cry1A transgene that confers a high degree of resistance to lepidopteran pests. Crop Sci 47:148–157CrossRefGoogle Scholar
  79. 79.
    Perlak FJ, Fuchs RL, Dean DA, McPherson SL, Fischhoff DA (1991) Modification of the coding sequence enhances plant expression of insect controlling protein genes. Proc Natl Acad Sci USA 88:3324–3328CrossRefGoogle Scholar
  80. 80.
    De Rocher EJ, Vargo-Gogola TC, Diehn SH, Green PJ (1998) Direct evidence for rapid degradation of Bacillus thuringiensis toxin mRNA as a cause of poor expression in plants. Plant Physiol 117:1445–1461CrossRefGoogle Scholar
  81. 81.
    Murray EE, Rocheleau T, Eberle M, Stock C, Sekar V, Adang M (1991) Analysis of unstable RNA transcripts of insecticidal crystal protein genes of Bacillus thuringiensis in transgenic plants and electroporated protoplasts. Plant Mol Biol 16:1035–1050CrossRefGoogle Scholar
  82. 82.
    Diehn PJ, Chiu SH, De Rocher WL, Green EJ (1998) Premature polyadenylation at multiple sites within a Bacillus thuringiensis toxin gene-coding region. Plant Physiol 117:1433–1443CrossRefGoogle Scholar
  83. 83.
    Misztal LH, Mostowska A, Skibinska M, Bajsa J, Musial WG, Jarmolowski A (2004) Expression of modified Cry1Ac gene of Bacillus thuringiensis in transgenic tobacco plants. Mol Biotechnol 26:17–26CrossRefGoogle Scholar
  84. 84.
    McBride KE, Svab Z, Schael DJ, Hogan PS, Stalker KM, Maliga P (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Bio/Technology 13:362–365CrossRefGoogle Scholar
  85. 85.
    Bock R (2001) Transgenic plastids in basic research and plant biotechnology. J Mol Biol 312:425–438CrossRefGoogle Scholar
  86. 86.
    Maliga P (2003) Progress towards commercialization of plastid transformation technology. Trends Biotechnol 21:20–28CrossRefGoogle Scholar
  87. 87.
    Daniell H, Khan MS, Allison L (2002) Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci 7:84–91CrossRefGoogle Scholar
  88. 88.
    Chakrabarti SK, Lutz KA, Lertwiriyawong B, Svab Z, Maliga P (2006) Expression of the cry9Aa2 B.t. gene in tobacco chloroplasts confers resistance to potato tuber moth. Transgenic Res 15:481–488CrossRefGoogle Scholar
  89. 89.
    De Cosa B, Moar W, Lee SB, Miller M, Daniell H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19:71–74CrossRefGoogle Scholar
  90. 90.
    Kota M, Daniell H, Varma S, Garczynski SF, Gould F, Moar WJ (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci USA 96:1840–1845CrossRefGoogle Scholar
  91. 91.
    Reddy VS, Leelavathi S, Selvapandiyan A, Raman R, Giovanni F, Shukla V, Bhatnagar RK (2002) Analysis of chloroplast transformed tobacco plants with cry1Ia5 under rice psbA transcriptional elements reveal high level expression of Bt toxin without imposing yield penalty and stable inheritance of transplastome. Mol Breed 9:259–269CrossRefGoogle Scholar
  92. 92.
    Dufourmantel N, Tissot G, Goutorbe F, Garcon F, Muhr C, Jansens S, Pelissier B, Peltier G, Dubald M (2005) Generation and analysis of soybean plastid transformants expressing Bacillus thuringiensis Cry1Ab protoxin. Plant Mol Biol 58:659–668CrossRefGoogle Scholar
  93. 93.
    Chrispeels MJ, Sadava DE (1994) Plants, genes and agriculture. Jones and Bartlett, LondonGoogle Scholar
  94. 94.
    Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol 43:701–726CrossRefGoogle Scholar
  95. 95.
    Gould F, Anderson A, Jones A, Sumerford D, Heckel DG, Lopez J, Micinski S, Leonard R, Laster M (1997) Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proc Natl Acad Sci USA 94:3519–3523CrossRefGoogle Scholar
  96. 96.
    Andreadis SS, Álvarez-Alfagene A, Sánchez-Ramos I, Stodola TJ, Andow DA, Milonas PG, Savopoulou-Soultani M, Castánera P (2007) Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in Greek and Spanish population of Sesamia nonagrioides (Lepidoptera: Noctuidae). J Econ Entomol 100:195–201CrossRefGoogle Scholar
  97. 97.
    Tabashnik BE, Patin AL, Dennehy TJ, Liu Y-B, Carrière Y, Sims M, Antilla L (2000) Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proc Natl Acad Sci USA 97:12980–12984CrossRefGoogle Scholar
  98. 98.
    Tabashnik BE, Dennehy TJ, Carrière Y (2005) Delayed resistance to transgenic cotton in pink bollworm. Proc Natl Acad Sci USA 102:15389–15393CrossRefGoogle Scholar
  99. 99.
    Cristofoletti PT, de Sousa FAM, Rahbe Y, Terra WR (2006) Characterization of a membrane-bound aminopeptidase purified from Acyrthosiphon pisum midgut cells. FEBS J 273:5574–5588CrossRefGoogle Scholar
  100. 100.
    Stewart SD, Adamczyk JJ, Knighten KS, Davis FM (2001) Impact of Bt cottons expressing one or two insecticidal proteins of Bacillus thuringiensis Berliner on growth and survival of noctuid (Lepidoptera) larvae. J Econ Entomol 94:752–760CrossRefGoogle Scholar
  101. 101.
    Chitkowski RL, Turnipseed SG, Sullivan MJ, Bridges WC (2003) Field and laboratory evaluations of transgenic cottons expressing one or two Bacillus thuringiensis var. kurstaki Berliner proteins for management of noctuid (Lepidoptera) pests. J Econ Entomol 96:755–762CrossRefGoogle Scholar
  102. 102.
    Zhao JZ, Cao J, Li YX, Collins HL, Roush RT, Earle ED, Shelton AM (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat Biotechnol 21:1493–1497CrossRefGoogle Scholar
  103. 103.
    Christou P, Capell T, Kohli A, Gatehouse JA, Gatehouse AMR (2006) Recent developments and future prospects in insect pest control in transgenic crops. Trends Plant Sci 11:302–308CrossRefGoogle Scholar
  104. 104.
    Gahan LJ, Ma YT, Coble MLM, Gould F, Moar WJ, Heckel DG (2005) Genetic basis of resistance to Cry1Ac and Cry2Aa in Heliothis virescens (Lepidoptera: Noctuidae). J Econ Entomol 98:1357–1368CrossRefGoogle Scholar
  105. 105.
    Bashir K, Husnain T, Fatima T, Riaz N, Makhdoom R, Riazuddin S (2005) Novel indica basmati line (B-370) expressing two unrelated genes of Bacillus thuringiensis is highly resistant to two lepidopteran insects in the field. Crop Prot 24:870–879CrossRefGoogle Scholar
  106. 106.
    Dively GP (2005) Impact of transgenic VIP3A x Cry1Ab lepidopteran-resistant field corn on the nontarget arthropod community. Environ Entomol 34:1267–1291CrossRefGoogle Scholar
  107. 107.
    Han LZ, Wu KM, Peng YF, Wang F, Guo YY (2006) Evaluation of transgenic rice expressing Cry1Ac and CpTI against Chilo suppressalis and intrapopulation variation in susceptibility to Cry1Ac. Environ Entomol 35:1453–1459CrossRefGoogle Scholar
  108. 108.
    Grainnet (2007) Monsanto and Dow Agrosciences launch “SmartStax,” industry’s first-ever eight-gene stacked combination in corn. http://www.grainnet.com/articles/Monsanto_and_Dow_Agrosciences_Launch_SmartStax_Industry_s_First_Ever_Eight_Gene_Stacked_Combination_in_Corn_-48374.html
  109. 109.
    Sanchis V, Agaisse H, Chaufaux J, Lereclus D (1996) Construction of new insecticidal Bacillus thuringiensis recombinant strains by using the sporulation non-dependent expression system of cryIIIA and a site specific recombination vector. J Biotechnol 48:81–96CrossRefGoogle Scholar
  110. 110.
    Bosch D, Schipper B, van der Kleij H, de Maagd R, Stiekema W (1994) Recombinant Bacillus thuringiensis crystal proteins with new properties: possibilities for resistance management. Bio/Technology 12:915–919CrossRefGoogle Scholar
  111. 111.
    de Maagd RA, Kwa MSG, van der Klei H, Yamamoto T, Schipper B, Vlak JM, Stiekema WJ, Bosch D (1996) Domain III substitution in Bacillus thuringiensis delta-endotoxin Cry1A(b) results in superior toxicity for Spodoptera exigua and altered membrane protein recognition. Appl Environ Microbiol 62:1537–1543Google Scholar
  112. 112.
    de Maagd RA, Weemen-Hendriks M, Stiekema W, Bosch D (2000) Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in different, but not all, Cry1-Cry1C hybrids. Appl Environ Microbiol 66:1559–1563CrossRefGoogle Scholar
  113. 113.
    Rang C, Vachon V, Coux F, Carret C, Moar WJ, Brousseau R, Schwartz JL, Laprade R, Frutos R (2001) Exchange of domain I from Bacillus thuringiensis Cry1 toxins influences protoxin stability and crystal formation. Curr Microbiol 43:1–6CrossRefGoogle Scholar
  114. 114.
    Naimov S, Dukiandjiev S, de Maagd RA (2003) A hybrid Bacillus thuringiensis delta-endotoxin gives resistance against a coleopteran and a lepidopteran pest in transgenic potato. Plant Biotechnol J 1:51–57CrossRefGoogle Scholar
  115. 115.
    Dean DH, Rajamohan F, Lee MK, Wu SJ, Chen XJ, Alcantara E, Hussain SR (1996) Probing the mechanism of action of Bacillus thuringiensis insecticidal proteins by site-directed mutagenesis: a minireview. Gene 179:111–117CrossRefGoogle Scholar
  116. 116.
    Rajamohan F, Alzate O, Cotrill JA, Curtiss A, Dean DH (1996) Protein engineering of Bacillus thuringiensis delta-endotoxin: mutations at domain II of CryIAb enhance receptor affinity and toxicity toward gypsy moth larvae. Proc Natl Acad Sci USA 93:14338–14343CrossRefGoogle Scholar
  117. 117.
    Wu SJ, Koller CN, Miller DL, Bauer LS, Dean DH (2000) Enhanced toxicity of Bacillus thuringiensis Cry3A delta-endotoxin in coleopterans by mutagenesis in a receptor binding loop. FEBS Lett 473:227–232CrossRefGoogle Scholar
  118. 118.
    Abdullah MAF, Alzate O, Mohammad M, McNall RJ, Adang MJ, Dean DH (2003) Introduction of Culex toxicity into Bacillus thuringiensis Cry4Ba by protein engineering. Appl Environ Microbiol 69:5343–5353CrossRefGoogle Scholar
  119. 119.
    Tuntitippawan T, Boonserm P, Katzenmeier G, Angsuthanasombat C (2005) Targeted mutagenesis of loop residues in the receptor-binding domain of the Bacillus thuringiensis Cry4Ba toxin affects larvicidal activity. FEMS Microbiol Lett 242:325–332CrossRefGoogle Scholar
  120. 120.
    Abdullah MAF, Dean DH (2004) Enhancement of Cry19Aa mosquitocidal activity against Aedes aegypti by mutations in the putative loop regions of domain II. Appl Environ Microbiol 70:3769–3771CrossRefGoogle Scholar
  121. 121.
    Liu XS, Dean DH (2006) Redesigning Bacillus thuringiensis Cry1Aa toxin into a mosquito toxin. Protein Eng Des Sel 19:107–111CrossRefGoogle Scholar
  122. 122.
    Ishikawa H, Hoshino Y, Motoki Y, Kawahara T, Kitajima M, Kitami M, Watanabe A, Bravo A, Soberon M, Honda A, Yaoi K, Sato R (2007) A system for the directed evolution of the insecticidal protein from Bacillus thuringiensis. Mol Biotechnol 36:90–101CrossRefGoogle Scholar
  123. 123.
    Chandra A, Ghosh P, Mandaokar AD, Bera AK, Sharma RP, Das S, Kumar PA (1999) Amino acid substitution in alpha-helix 7 of Cry1Ac delta-endotoxin of Bacillus thuringiensis leads to enhanced toxicity to Helicoverpa armigera Hubner. FEBS Lett 458:175–179CrossRefGoogle Scholar
  124. 124.
    Rupar MJ, Donovan WP, Groat RG, Slaney AC, Mattison JW, Johnson TB, Charles JF, Dumanior VC, DeBarjac H (1991) Two novel strains of Bacillus thuringiensis toxic to coleopterans. Appl Environ Microbiol 57:3337–3344Google Scholar
  125. 125.
    Bohorova N, Frutos R, Royer M, Estanol P, Pacheco M, Rascon Q, McLean S, Hoisington D (2001) Novel synthetic Bacillus thuringiensis cry1B gene and the cry1B-cry1Ab translational fusion confer resistance to southwestern corn borer, sugarcane borer and fall armyworm in transgenic tropical maize. Theor Appl Genet 103:817–826CrossRefGoogle Scholar
  126. 126.
    Ho NH, Baisakh N, Oliva N, Datta K, Frutos R, Datta SK (2006) Translational fusion hybrid Bt genes confer resistance against yellow stem borer in transgenic elite vietnamese rice (Oryza sativa L.) cultivars. Crop Sci 46:781–789CrossRefGoogle Scholar
  127. 127.
    Mehlo L, Gahakwa D, Nghia PT, Loc NT, Capell T, Gatehouse JA, Gatehouse AMR, Christou P (2005) An alternative strategy for sustainable pest resistance in genetically enhanced crops. Proc Natl Acad Sci USA 102:7812–7816CrossRefGoogle Scholar
  128. 128.
    Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169CrossRefGoogle Scholar
  129. 129.
    Barbosa JARG, Silva LP, Teles RCL, Esteves GF, Azevedo RB, Ventura MM, Freitas SM (2007) Crystal Structure of the Bowman-Birk inhibitor from Vigna unguiculata seeds in complex with beta-trypsin at 1.55 Å resolution and its structural properties in association with proteinases. Biophys J 92:1638–1650CrossRefGoogle Scholar
  130. 130.
    Garcia-Olmedo F, Salmedo G, Sanchez-Monge R, Gomez L, Royo J, Carbonero P (1987) Plant proteinaceous inhibitors of proteinases and α-amylases. Oxf Surv Plant Mol Cell Biol 4:275–334Google Scholar
  131. 131.
    Ryan CA (1990) Protease inhibitors in plants – genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28:425–449CrossRefGoogle Scholar
  132. 132.
    Orozco-Cardenas M, McGurl B, Ryan CA (1993) Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc Natl Acad Sci USA 90:8273–8276CrossRefGoogle Scholar
  133. 133.
    Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328CrossRefGoogle Scholar
  134. 134.
    Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–163CrossRefGoogle Scholar
  135. 135.
    Johnson R, Narvaez J, An G, Ryan C (1989) Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 86:9871–9875CrossRefGoogle Scholar
  136. 136.
    McManus MT, White DWR, McGregor PG (1994) Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests. Transgenic Res 3:50–58CrossRefGoogle Scholar
  137. 137.
    Duan X, Li X, Xue Q, Abo-El-Saad M, Xu D, Wu R (1996) Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat Biotechnol 14:494–496CrossRefGoogle Scholar
  138. 138.
    Xu DP, Xue QZ, McElroy D, Mawal Y, Hilder VA, Wu R (1996) Constitutive expression of a cowpea trypsin-inhibitor gene, CpTI, in transgenic rice plants confers resistance to 2 major rice insect pests. Mol Breed 2:167–173CrossRefGoogle Scholar
  139. 139.
    McGurl B, Orozco-Cardenas M, Pearce G, Ryan CA (1994) Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc Natl Acad Sci USA 91:9799–9802CrossRefGoogle Scholar
  140. 140.
    Ren F, Lu Y-T (2006) Overexpression of tobacco hydroxyproline-rich glycopeptide systemin precursor A gene in transgenic tobacco enhances resistance against Helicoverpa armigera larvae. Plant Sci 171:286–292CrossRefGoogle Scholar
  141. 141.
    Bolter CJ, Jongsma MA (1995) Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. J Insect Physiol 41:1071–1078CrossRefGoogle Scholar
  142. 142.
    Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekma WJ (1995) Adaptations of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc Natl Acad Sci USA 92:8041–8045CrossRefGoogle Scholar
  143. 143.
    Harsulkar AM, Giri AP, Patankar AG, Gupta VS, Sainani MN, Ranjekar PK, Deshpande VV (1999) Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol 121:497–506CrossRefGoogle Scholar
  144. 144.
    Bown DP, Wilkinson HS, Gatehouse JA (1997) Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem Mol Biol 27:625–638CrossRefGoogle Scholar
  145. 145.
    De Leo F, Bonade-Bottino MA, Ceci LR, Gallerani R, Jouanin L (1998) Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiol 118:997–1004CrossRefGoogle Scholar
  146. 146.
    Leplé JC, Bonade-Bottino M, Augustin S, Pilate G, Letan VD, Delplanque A, Cornu D, Jouanin L (1995) Toxicity to Chrysomela tremulae (Coleoptera, Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Mol Breed 1:319–328CrossRefGoogle Scholar
  147. 147.
    Lecardonnel A, Chauvin L, Jouanin L, Beaujean A, Prevost G, Sangwan-Norreel B (1999) Effects of rice cystatin I expression in transgenic potato on Colorado potato beetle larvae. Plant Sci 140:71–79CrossRefGoogle Scholar
  148. 148.
    Outchkourov NS, de Kogel WJ, Schuurman-de Bruin A, Abrahamson M, Jongsma MA (2004) Specific cysteine protease inhibitors act as deterrents of western flower thrips, Frankliniella occidentalis (Pergande), in transgenic potato. Plant Biotechnol J 2:439–448CrossRefGoogle Scholar
  149. 149.
    Outchkourov NS, de Kogel WJ, Wiegers GL, Abrahamson M, Jongsma MA (2004) Engineered multidomain cysteine protease inhibitors yield resistance against western flower thrips (Franklinielia occidentalis) in greenhouse trials. Plant Biotechnol J 2:449–458CrossRefGoogle Scholar
  150. 150.
    Outchkourov NS, Rogelj B, Strukelj B, Jongsma MA (2003) Expression of sea anemone equistatin in potato: effects of plant proteases on heterologous protein production. Plant Physiol 133:379–390CrossRefGoogle Scholar
  151. 151.
    Abdeen A, Virgos A, Olivella E, Villanueva J, Aviles X, Gabarra R, Prat S (2005) Multiple insect resistence in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Mol Biol 57:189–202CrossRefGoogle Scholar
  152. 152.
    Franco OL, Rigden DJ, Melo FR, Grossi-de-Sa MF (2002) Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases - structure, function and potential for crop protection. Eur J Biochem 269:397–412CrossRefGoogle Scholar
  153. 153.
    Suzuki K, Ishimoto M, Kikuchi F, Kitamura K (1993) Growth-inhibitory effect of an alpha-amylase inhibitor from the wild common bean resistant to the mexican bean weevil (Zabrotes subfasciatus). Jpn J Breed 43:257–265Google Scholar
  154. 154.
    Ishimoto M, Kitamura K (1991) Effect of absence of seed alpha-amylase inhibitor on the growth inhibitory activity to azuki bean weevil (Callosobruchus chinensis) in common bean (Phaseolus vulgaris L.). Jpn J Breed 41:231–240Google Scholar
  155. 155.
    Moreno J, Chrispeels MJ (1989) A lectin gene encodes the α − amylase inhibitor of common bean. Proc Natl Acad Sci USA 86:7885–7889CrossRefGoogle Scholar
  156. 156.
    Nahoum V, Farisei F, Le-Berre-Anton V, Egloff MP, Rouge P, Poerio E, Payan F (1999) A plant-seed inhibitor of two classes of alpha-amylases: X-ray analysis of Tenebrio molitor larvae alpha-amylase in complex with the bean Phaseolus vulgaris inhibitor. Acta Crystallogr Sect D 55:360–362CrossRefGoogle Scholar
  157. 157.
    Silva CP, Terra WR, de Sa MFG, Samuels RI, Isejima EM, Bifano TD, Almeida JS (2001) Induction of digestive alpha-amylases in larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae) in response to ingestion of common bean alpha-amylase inhibitor 1. J Insect Physiol 47:1283–1290CrossRefGoogle Scholar
  158. 158.
    Shade RE, Schroeder HE, Pueyo JJ, Tabe LM, Murdock LL, Higgins TJV, Chrispeels MJ (1994) Transgenic pea seeds expressing the alpha-amylase inhibitor of the common bean are resistant to bruchid beetles. Bio/Technology 12:793–796CrossRefGoogle Scholar
  159. 159.
    Schroeder HE, Gollasch S, Moore A, Tabe LM, Craig S, Hardie DC, Chrispeels MJ, Spencer D, Higgins TJV (1995) Bean alpha-amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L). Plant Physiol 107:1233–1239Google Scholar
  160. 160.
    Ishimoto M, Sato T, Chrispeels MJ, Kitamura K (1996) Bruchid resistance of transgenic azuki bean expressing seed alpha-amylase inhibitor of common bean. Entomol Exp Appl 79:309–315CrossRefGoogle Scholar
  161. 161.
    Morton RL, Schroeder HE, Bateman KS, Chrispeels MJ, Armstrong E, Higgins TJV (2000) Bean alpha-amylase inhibitor 1 in transgenic peas (Pisum sativum) provides complete protection from pea weevil (Bruchus pisorum) under field conditions. Proc Natl Acad Sci USA 97:3820–3825CrossRefGoogle Scholar
  162. 162.
    Sarmah BK, Moore A, Tate W, Molvig L, Morton RL, Rees DP, Chiaiese P, Chrispeels MJ, Tabe LM, Higgins TJV (2004) Transgenic chickpea seeds expressing high levels of a bean alpha-amylase inhibitor. Mol Breed 14:73–82CrossRefGoogle Scholar
  163. 163.
    Prescott VE, Campbell PM, Moore A, Mattes J, Rothenberg ME, Foster PS, Higgins TJV, Hogan SP (2005) Transgenic expression of bean alpha-amylase inhibitor in peas results in altered structure and immunogenicity. J Agric Food Chem 53:9023–9030CrossRefGoogle Scholar
  164. 164.
    Collins CL, Eason PJ, Dunshea FR, Higgins TJV, King RH (2006) Starch but not protein digestibility is altered in pigs fed transgenic peas containing alpha-amylase inhibitor. J Sci Food Agric 86:1894–1899CrossRefGoogle Scholar
  165. 165.
    Li XH, Higgins TJV, Bryden WL (2006) Biological response of broiler chickens fed peas (Pisum sativum L.) expressing the bean (Phaseolus vulgaris L.) alpha-amylase inhibitor transgene. J Sci Food Agric 86:1900–1907CrossRefGoogle Scholar
  166. 166.
    Peumans WJ, van Damme EJM (1995) Lectins as plant defence proteins. Plant Physiol 109:347–352CrossRefGoogle Scholar
  167. 167.
    van Damme EJM, Peumans WJ, Barre A, Rougé P (1998) Plant lectins: a composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Crit Rev Plant Sci 17:575–692CrossRefGoogle Scholar
  168. 168.
    Czalpa TH, Lang BA (1990) Effect of plant lectins on the larval development of European corn borer (Lepidoptera: Pyralidae) and southern corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 83:2480–2485Google Scholar
  169. 169.
    Murdock LL, Huesing JE, Nielsen SS, Pratt RC, Shade RE (1990) Biological effects of plant lectins on the cowpea weevil. Phytochemistry 29:85–89CrossRefGoogle Scholar
  170. 170.
    Fitches E, Gatehouse AMR, Gatehouse JA (1997) Effects of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on the development of tomato moth (Lacanobia oleracea) larvae in laboratory and glasshouse trials. J Insect Physiol 43:727–739CrossRefGoogle Scholar
  171. 171.
    Boulter D, Edwards GA, Gatehouse AMR, Gatehouse JA, Hilder VA (1990) Additive protective effects of incorporating two different higher plant derived insect resistance genes in transgenic tobacco plants. Crop Prot 9:351–354CrossRefGoogle Scholar
  172. 172.
    Gatehouse AMR, Davison GM, Newell CA, Merryweather A, Hamilton WDO, Burgess EPJ, Gilbert RJC, Gatehouse JA (1997) Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Mol Breed 3:49–63CrossRefGoogle Scholar
  173. 173.
    Powell KS, Gatehouse AMR, Hilder VA, Gatehouse JA (1993) Antimetabolic effects of plant lectins and plant and fungal enzymes on the nymphal stages of two important rice pests, Nilaparvata lugens and Nephotettix cinciteps. Entomol Exp Appl 66:119–126CrossRefGoogle Scholar
  174. 174.
    Powell KS, Gatehouse AMR, Hilder VA, van Damme EJM, Peumans WJ, Boonjawat J, Horsham K, Gatehouse JA (1995) Different antimetabolic effects of related lectins towards nymphal stages of Nilaparvata lugens. Entomol Exp Appl 75:61–65CrossRefGoogle Scholar
  175. 175.
    Rao KV, Rathore KS, Hodges TK, Fu X, Stoger E, Sudhakar D, Williams S, Christou P, Bharathi M, Bown DP, Powell KS, Spence J, Gatehouse AMR, Gatehouse JA (1998) Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant J 15:469–477CrossRefGoogle Scholar
  176. 176.
    Nagadhara D, Ramesh S, Pasalu IC, Kondala Rao Y, Krishnaiah NV, Sarma NP, Bown DP, Gatehouse JA, Reddy VD, Rao KV (2003) Transgenic indica rice resistant to sap-sucking insects. Plant Biotechnol 1:231–240CrossRefGoogle Scholar
  177. 177.
    Foissac X, Loc NT, Christou P, Gatehouse AMR, Gatehouse JA (2000) Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA). J Insect Physiol 46:573–583CrossRefGoogle Scholar
  178. 178.
    Nagadhara D, Ramesh S, Pasalu IC, Rao YK, Sarma NP, Reddy VD, Rao KV (2004) Transgenic rice plants expressing the snowdrop lectin gene (gna) exhibit high-level resistance to the whitebacked planthopper (Sogatella furcifera). Theor Appl Genet 109:1399–1405CrossRefGoogle Scholar
  179. 179.
    Loc NT, Tinjuangjun P, Gatehouse AMR, Christou P, Gatehouse JA (2002) Linear transgene constructs lacking vector backbone sequences generate transgenic rice plants which accumulate higher levels of proteins conferring insect resistance. Mol Breed 9:231–244CrossRefGoogle Scholar
  180. 180.
    Poulsen M, Kroghsbo S, Schroder M, Wilcks A, Jacobsen H, Miller A, Frenzel T, Danier J, Rychlik M, Shu QY, Emami K, Sudhakar D, Gatehouse A, Engel KH, Knudsen I (2007) A 90-day safety study in Wistar rats fed genetically modified rice expressing snowdrop lectin Galanthus nivalis (GNA). Food Chem Toxicol 45:350–363CrossRefGoogle Scholar
  181. 181.
    Gatehouse AMR, Down RE, Powell KS, Sauvion N, Rahbe Y, Newell CA, Merryweather A, Hamilton WDO, Gatehouse JA (1996) Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae. Entomol Exp Appl 79:295–307CrossRefGoogle Scholar
  182. 182.
    Wang ZY, Zhang KW, Sun XF, Tang KX, Zhang JR (2005) Enhancement of resistance to aphids by introducing the snowdrop lectin gene gna into maize plants. J Biosci 30:627–638CrossRefGoogle Scholar
  183. 183.
    Bandyopadhyay S, Roy A, Das S (2001) Binding of garlic (Allium sativum) leaf lectin to the gut receptors of homopteran pests is correlated to its insecticidal activity. Plant Sci 161:1025–1033CrossRefGoogle Scholar
  184. 184.
    Dutta I, Saha P, Majumder P, Sarkar A, Chakraborti D, Banerjee S, Das S (2005) The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnol J 3:601–611CrossRefGoogle Scholar
  185. 185.
    Dutta I, Majumder P, Saha P, Ray K, Das S (2005) Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea). Plant Sci 169:996–1007CrossRefGoogle Scholar
  186. 186.
    Saha P, Majumder P, Dutta I, Ray T, Roy SC, Das S (2006) Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap-sucking insect pests. Planta 223:1329–1343CrossRefGoogle Scholar
  187. 187.
    Saha P, Chakraborti D, Sarkar A, Dutta I, Basu D, Das S (2007) Characterization of vascular-specific RSs1 and rolC promoters for their utilization in engineering plants to develop resistance against hemipteran insect pests. Planta 226:429–442CrossRefGoogle Scholar
  188. 188.
    Saha P, Dasgupta I, Das S (2006) A novel approach for developing resistance in rice against phloem limited viruses by antagonizing the phloem feeding hemipteran vectors. Plant Mol Biol 62:735–752CrossRefGoogle Scholar
  189. 189.
    Ryan CA (2000) The system in signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121CrossRefGoogle Scholar
  190. 190.
    Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore, Spodoptera exigua. J Insect Physiol 38:277–285CrossRefGoogle Scholar
  191. 191.
    Melo GA, Shimizu MM, Mazzafera P (2006) Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry 67:277–285CrossRefGoogle Scholar
  192. 192.
    Wang JH, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96CrossRefGoogle Scholar
  193. 193.
    Dowd PF, Lagrimini LM (1997) Examination of different tobacco (Nicotiana spp.) types under- and overproducing tobacco anionic peroxidase for their leaf resistance to Helicoverpa zea. J Chem Ecol 23:2357–2370CrossRefGoogle Scholar
  194. 194.
    Dowd PF, Lagrimini LM (2006) Examination of the biological effects of high anionic peroxidase production in tobacco plants grown under field conditions. I. Insect pest damage. Transgenic Res 15:197–204CrossRefGoogle Scholar
  195. 195.
    Dowd PF, Zuo WN, Gillikin JW, Johnson ET, Boston RS (2003) Enhanced resistance to Helicoverpa zea in tobacco expressing an activated form of maize ribosome-inactivating protein. J Agric Food Chem 51:3568–3574CrossRefGoogle Scholar
  196. 196.
    Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol Lett 28:593–599CrossRefGoogle Scholar
  197. 197.
    Dowd PF, Johnson ET, Pinkerton TS (2007) Oral toxicity of beta-N-acetyl hexosaminidase to insects. J Agric Food Chem 55:3421–3428CrossRefGoogle Scholar
  198. 198.
    Fitches E, Wilkinson H, Bell H, Bown DP, Gatehouse JA, Edwards JP (2004) Cloning, expression and functional characterisation of chitinase from larvae of tomato moth (Lacanobia oleracea): a demonstration of the insecticidal activity of insect chitinase. Insect Biochem Mol Biol 34:1037–1050CrossRefGoogle Scholar
  199. 199.
    Ding XF, Gopalakrishnan B, Johnson LB, White FF, Wang XR, Morgan TD, Kramer KJ, Muthukrishnan S (1998) Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res 7:77–84CrossRefGoogle Scholar
  200. 200.
    Saguez J, Hainez R, Cherqui A, Van Wuytswinkel O, Jeanpierre H, Lebon G, Noiraud N, Beaujean A, Jouanin L, Laberche JC, Vincent C, Giordanengo P (2005) Unexpected effects of chitinases on the peach-potato aphid (Myzus persicae Sulzer) when delivered via transgenic potato plants (Solanum tuberosum Linne) and in vitro. Transgenic Res 14:57–67CrossRefGoogle Scholar
  201. 201.
    Corrado G, Arciello S, Fanti P, Fiandra L, Garonna A, Digilio MC, Lorito M, Giordana B, Pennacchio F, Rao R (2007) The Chitinase A from the baculovirus AcMNPV enhances resistance to both fungi and herbivorous pests in tobacco. Transgenic Res. 17:557–571. (published online: DOI: 10.1007/s11248-007-9129-4)Google Scholar
  202. 202.
    Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:300–307CrossRefGoogle Scholar
  203. 203.
    Tattersall DB, Bak S, Jones PR, Olsen CE, Nielsen JK, Hansen ML, Hoj PB, Moller BL (2001) Resistance to an herbivore through engineered cyanogenic glucoside synthesis. Science 293:1826–1828CrossRefGoogle Scholar
  204. 204.
    Bak S, Olsen CE, Halkier BA, Møller BL (2000) Transgenic tobacco and Arabidopsis plants expressing the two multifunctional sorghum cytochrome P450 enzymes, CYP79A1 and CYP71E1, are cyanogenic and accumulate metabolites derived from intermediates in dhurrin biosynthesis. Plant Physiol 123:1437–1448CrossRefGoogle Scholar
  205. 205.
    Kristensen C, Morant M, Olsen CE, Ekstrom CT, Galbraith DW, Moller BL, Bak S (2005) Metabolic engineering of dhurrin in transgenic Arabidopsis plants with marginal inadvertent effects on the metabolome and transcriptome. Proc Natl Acad Sci USA 102:1779–1784CrossRefGoogle Scholar
  206. 206.
    Ogunlabi OO, Agboola FK (2007) A soluble beta-cyanoalanine synthase from the gut of the variegated grasshopper Zonocerus variegatus (L.). Insect Biochem Mol Biol 37:72–79CrossRefGoogle Scholar
  207. 207.
    Mikkelsen MD, Halkier BA (2003) Metabolic engineering of valine- and isoleucine-derived glucosinolates in Arabidopsis expressing CYP79D2 from cassava. Plant Physiol 131:773–779CrossRefGoogle Scholar
  208. 208.
    Franks TK, Powell KS, Choimes S, Marsh E, Iocco P, Sinclair BJ, Ford CM, van Heeswijck R (2006) Consequences of transferring three sorghum genes for secondary metabolite (cyanogenic glucoside) biosynthesis to grapevine hairy roots. Transgenic Res 15:181–195CrossRefGoogle Scholar
  209. 209.
    Kim YS, Uefuji H, Ogita S, Sano H (2006) Transgenic tobacco plants producing caffeine: a potential new strategy for insect pest control. Transgenic Res 15:667–672CrossRefGoogle Scholar
  210. 210.
    Wei S, Semel Y, Bravdo BA, Czosnek H, Shoseyov O (2007) Expression and subcellular compartmentation of Aspergillus niger beta-glucosidase in transgenic tobacco result in an increased insecticidal activity on whiteflies (Bemisia tabaci). Plant Sci 172:1175–1181CrossRefGoogle Scholar
  211. 211.
    Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602CrossRefGoogle Scholar
  212. 212.
    Wang E, Wang R, DeParasis J, Loughrin JH, Gan S, Wagner GJ (2001) Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat Biotechnol 19:371–374CrossRefGoogle Scholar
  213. 213.
    Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884CrossRefGoogle Scholar
  214. 214.
    Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072CrossRefGoogle Scholar
  215. 215.
    Schnee C, Kollner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103:1129–1134CrossRefGoogle Scholar
  216. 216.
    Beale MH, Birkett MA, Bruce TJA, Chamberlain K, Field LM, Huttly AK, Martin JL, Parker R, Phillips AL, Pickett JA, Prosser IM, Shewry PR, Smart LE, Wadhams LJ, Woodcock CM, Zhang YH (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc Natl Acad Sci USA 103:10509–10513CrossRefGoogle Scholar
  217. 217.
    Johnson ET, Dowd PF (2004) Differentially enhanced insect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J Agric Food Chem 52:5135–5138CrossRefGoogle Scholar
  218. 218.
    Johnson ET, Berhow MA, Dowd PF (2007) Expression of a maize Myb transcription factor driven by a putative silk-specific promoter significantly enhances resistance to Helicoverpa zea in transgenic maize. J Agric Food Chem 55:2998–3003CrossRefGoogle Scholar
  219. 219.
    Maiti IB, Dey N, Pattanaik S, Dahlman DL, Rana RL, Webb BA (2003) Antibiosis-type insect resistance in transgenic plants expressing a teratocyte secretory protein (TSP14) gene from a hymenopteran endoparasite (Microplitis croceipes). Plant Biotechnol J 1:209–219CrossRefGoogle Scholar
  220. 220.
    Tortiglione C, Fogliano V, Ferracane R, Fanti P, Pennacchio F, Monti LM, Rao R (2003) An insect peptide engineered into the tomato prosystemin gene is released in transgenic tobacco plants and exerts biological activity. Plant Mol Biol 53:891–902CrossRefGoogle Scholar
  221. 221.
    Bowen DJ, Ensign JC (1998) Purification and characterization of a high-molecular-weight insecticidal protein complex produced by the entomopathogenic bacterium Photorhabdus luminescens. Appl Environ Microbiol 64:3029–3035Google Scholar
  222. 222.
    Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E, Bhartia R, ffrench-Constant RH (1998) Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280:2129–2132CrossRefGoogle Scholar
  223. 223.
    ffrench-Constant RH, Dowling A, Waterfield NR (2007) Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon 49:436–451CrossRefGoogle Scholar
  224. 224.
    Guo LN, Fatig RO, Orr GL, Schafer BW, Strickland JA, Sukhapinda K, Woodsworth AT, Petell JK (1999) Photorhabdus luminescens W-14 insecticidal activity consists of at least two similar but distinct proteins - purification and characterization of toxin A and toxin B. J Biol Chem 274:9836–9842CrossRefGoogle Scholar
  225. 225.
    Liu D, Burton S, Glancy T, Li ZS, Hampton R, Meade T, Merlo DJ (2003) Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat Biotechnol 21:1222–1228CrossRefGoogle Scholar
  226. 226.
    Purcell JP, Greenplate JT, Jennings MG, Ryerse JS, Pershing JC, Sims SR, Prinsen MJ, Corbin DR, Tran M, Sammons RD, Stonard RJ (1993) Cholesterol oxidase - a potent insecticidal protein active against boll weevil larvae. Biochem Biophys Res Commun 196:1406–1413CrossRefGoogle Scholar
  227. 227.
    Shen Z, Corbin DR, Greenplate JT, Grebenok RJ, Galbraith DW, Purcell JP (1997) Studies on the mode of action of cholesterol oxidase on insect midgut membranes. Arch Insect Biochem Physiol 34:429–442CrossRefGoogle Scholar
  228. 228.
    Corbin DR, Grebenok RJ, Ohnmeiss TE, Greenplate JT, Purcell JP (2001) Expression and chloroplast targeting of cholesterol oxidase in transgenic tobacco plants. Plant Physiol 126:1116–1128CrossRefGoogle Scholar
  229. 229.
    Morgan TD, Oppert B, Czapla TH, Kramer KJ (1993) Avidin and streptavidin as insecticidal and growth-inhibiting dietary proteins. Entomol Exp Appl 69:97–108CrossRefGoogle Scholar
  230. 230.
    Markwick NP, Christeller JT, Docherty LC, Lilley CM (2001) Insecticidal activity of avidin and streptavidin against four species of pest Lepidoptera. Entomol Exp Appl 98:59–66CrossRefGoogle Scholar
  231. 231.
    Hood EE, Witcher DR, Maddock S, Meyer T, Baszczynski C, Bailey M, Flynn P, Register J, Marshall L, Bond D, Kulisek E, Kusnadi A, Evangelista R, Nikolov Z, Wooge C, Mehigh RJ, Hernan R, Kappel WK, Ritland D, Li CP, Howard JA (1997) Commercial production of avidin from transgenic maize: characterization of transformant, production, processing, extraction and purification. Mol Breed 3:291–306CrossRefGoogle Scholar
  232. 232.
    Kramer KJ, Morgan TD, Throne JE, Dowell FE, Bailey M, Howard JA (2000) Transgenic avidin maize is resistant to storage insect pests. Nat Biotechnol 18:670–674CrossRefGoogle Scholar
  233. 233.
    Burgess EPJ, Malone LA, Christeller JT, Lester MT, Murray C, Philip BA, Phung MM, Tregidga EL (2002) Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests, Helicoverpa armigera and Spodoptera litura. Transgenic Res 11:185–198CrossRefGoogle Scholar
  234. 234.
    Murray C, Sutherland PW, Phung MM, Lester MT, Marshall RK, Christeller JT (2002) Expression of biotin-binding proteins, avidin and streptavidin, in plant tissues using plant vacuolar targeting sequences. Transgenic Res 11:199–214CrossRefGoogle Scholar
  235. 235.
    Markwick NP, Docherty LC, Phung MM, Lester MT, Murray C, Yao JL, Mitra DS, Cohen D, Beuning LL, Kutty-Amma S, Christeller JT (2003) Transgenic tobacco and apple plants expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber moth and lightbrown apple moth, respectively. Transgenic Res 12:671–681CrossRefGoogle Scholar
  236. 236.
    Yoza K, Imamura T, Kramer KJ, Morgan TD, Nakamura S, Akiyama K, Kawasaki S, Takaiwa F, Ohtsubo K (2005) Avidin expressed in transgenic rice confers resistance to the stored-product insect pests Tribolium confusum and Sitotroga cerealella. Biosci Biotechnol Biochem 69:966–971CrossRefGoogle Scholar
  237. 237.
    Ginzberg I, Perl A, Genser M, Wininger S, Nemas C, Kapulnik Y (2004) Expression of streptavidin in tomato resulted in abnormal plant development that could be restored by biotin application. J Plant Physiol 161:611–620CrossRefGoogle Scholar
  238. 238.
    Flinn PW, Kramer KJ, Throne JE, Morgan TD (2006) Protection of stored maize from insect pests using a two-component biological control method consisting of a hymenopteran parasitoid, Theocolax elegans, and transgenic avidin maize powder. J Stored Prod Res 42:218–225CrossRefGoogle Scholar
  239. 239.
    Cooper SG, Douches DS, Grafius EJ (2006) Insecticidal activity of avidin combined with genetically engineered and traditional host plant resistance against Colorado potato beetle (Coleoptera: Chrysomelidae) larvae. J Econ Entomol 99:527–536CrossRefGoogle Scholar
  240. 240.
    Turner CT, Davy MW, MacDiarmid RM, Plummer KM, Birch NP, Newcomb RD (2006) RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Mol Biol 15:383–391CrossRefGoogle Scholar
  241. 241.
    Mao Y-B, Cai W-J, Wang J-W, Hong G-J, Tao X-Y, Wang L-J, Huang Y-P, Chen X-Y (2007) Silencing a cotton bollworm P450 monoxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313CrossRefGoogle Scholar
  242. 242.
    Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326CrossRefGoogle Scholar
  243. 243.
    Benbrook C (2009) Impacts of genetically engineered crops on pesticide use in the United States: The first thirteen years. The Organic Centre; Critical Issue Report. http://www.organic-center.org/reportfiles/13Years20091126_FullReport.pdf
  244. 244.
    Gatehouse AMR, Ferry N, Raemaekers RJM (2002) The case of the monarch butterfly: a verdict is returned. Trends Genet 18:249–251CrossRefGoogle Scholar
  245. 245.
    Tabashnik BE, Van Rensburg JBJ, Carriere Y (2009) Field-evolved insect resistance to Bt crops: Definition, theory, and data. J Econ Entomol 102:2011–2025CrossRefGoogle Scholar
  246. 246.
    Nunez-Farfan J, Fornoni J, Luis Valverde P (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566CrossRefGoogle Scholar

Books and reviews

  1. Carozzi N, Koziel M, eds. (1997) Advances in Insect Control; The Role of Transgenic Plants. Taylor and Francis, LondonGoogle Scholar
  2. Romeis J, Shelton AM, Kennedy G eds. (2008) Integration of Insect-Resistant Genetically Modified Crops within IPM Programs (Progress in Biological Control). SpringerGoogle Scholar
  3. Lemaux PG (2008) Genetically engineered plants and foods: a scientist’s analysis of the issues (part I). Annu Rev Plant Biol 59:771–812CrossRefGoogle Scholar
  4. Lemaux PG (2009) Genetically engineered plants and foods: a scientist’s analysis of the issues (part II). Annu Rev Plant Biol 60:511–559CrossRefGoogle Scholar
  5. Park JR, McFarlane I, Phipps RH, Ceddia G (2011) The role of transgenic crops in sustainable development. Plant Biotech J 9:2–21CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.School of Biological and Biomedical SciencesDurham UniversityDurhamUK