Skip to main content
SpringerLink
Log in

Transgenic Approaches to Western Corn Rootworm Control

  • Chapter
  • First Online:
Yellow Biotechnology II

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 136))

Abstract

The western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) is a significant corn pest throughout the United States corn belt. Rootworm larvae feed on corn roots causing yield losses and control expenditures that are estimated to exceed US$1 billion annually. Traditional management practices to control rootworms such as chemical insecticides or crop rotation have suffered reduced effectiveness due to the development of physiological and behavioral resistance. Transgenic maize expressing insecticidal proteins are very successful in protecting against rootworm damage and preserving corn yield potential. However, the high rate of grower adoption and early reliance on hybrids expressing a single mode of action and low-dose traits threatens the durability of commercialized transgenic rootworm technology for rootworm control. A summary of current transgenic approaches for rootworm control and the corresponding insect resistance management practices is included. An overview of potential new modes of action based on insecticidal proteins, and especially RNAi targeting mRNA coding for essential insect proteins is provided.

Graphical Abstract

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BBMV:

Brush border membrane vesicles

Bt:

Bacillus thuringiensis

CERA:

Center for Environmental Risk Assessment

EPA:

Environmental Protection Agency

IRM:

Insect resistance management

WCR:

Western corn rootworm

References

  1. Sappington TW, Siegfried BD, Guillemaud T (2006) Coordinated Diabrotica genetics research: accelerating progress on an urgent insect pest problem. Am Entomol 52:90–97

    Google Scholar 

  2. Gray ME, Sappington TW, Miller NJ, Moeser J, Bohn MO (2009) Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu Rev Entomol 54:303–321

    CAS  Google Scholar 

  3. Miller NJ, Guillemaud T, Giordano R, Siegfried BD, Gray ME, Meinke LJ, Sappington TW (2009) Genes, gene flow and adaptation of Diabrotica virgifera virgifera. Agric Forest Entomol 11:47–60

    Google Scholar 

  4. Branson TF, Krysan JL (1981) Feeding and oviposition behavior and life cycle strategies for Diabrotica: an evolutionary view with implications for pest management. Environ Entomol 10:826–831

    Google Scholar 

  5. Metcalf RL (1986) Foreword, pp. vii-xv. In: Krysan JL, Miller TA (eds) Methods for the study of pest Diabrotica. Springer, New York

    Google Scholar 

  6. Meinke LJ, Siegfried BD, Wright RJ, Chandler LD (1998) Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. J Econ Entomol 91:594–600

    CAS  Google Scholar 

  7. Parimi S, Meinke LJ, French BW, Chandler LD, Siegfried BD (2006) Stability and persistence of aldrin and methyl-parathion resistance in western corn rootworm populations (Coleoptera: Chrysomelidae). Crop Prot 25:269–274

    CAS  Google Scholar 

  8. Siegfried BD, Meinke LJ, Parimi S, Scharf ME, Nowatzki TJ et al (2004) Monitoring western corn rootworm (Coleoptera: Chrysomelidae) susceptibility to carbaryl and cucurbitacin baits in the area-wide management pilot program. J Econ Entomol 97:1726–1733

    CAS  Google Scholar 

  9. Meinke LJ, Sappington TW, Onstad DW, Guillemaud T, Miller NJ et al (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric Forest Entomol 11:29–46

    Google Scholar 

  10. Levine E, Spencer JL, Isard SA, Onstad DW, Gray ME (2002) Adaptation of the western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) to crop rotation: evolution of a new strain in response to a cultural management practice. Am Entomol 48:94–107

    Google Scholar 

  11. Metcalf RL (1983) Implication and prognosis of resistance to insecticides. In: Georghiou GP, Sato T (eds) Pest resistance to pesticides. Plenum Press, New York, pp 703–733

    Google Scholar 

  12. Ciosi M, Toepfer S, Li H, Haye T, Kuhlmann U et al (2009) Are the invading Western corn rootworm (Coleoptera: Chrysomelidae) populations in Europe resistant against insecticides as in the USA? J Entomol Sci. doi:10.1111/j.1439-0418.2008.01363.x

    Google Scholar 

  13. Gillette CP (1912) Diabrotica virgifera LeC. as a corn root-worm. J Econ Entomol 5:364–366

    Google Scholar 

  14. Clark TL, Hibbard BE (2004) Comparison of nonmaize hosts to support western corn rootworm (Coleoptera: Chrysomelidae) larval biology. Environ Entomol 33:681–689

    Google Scholar 

  15. Oyediran IO, Higdon ML, Clark TL, Hibbard BE (2007) Interactions of alternate hosts, postemergence grass control, and rootworm-resistant transgenic corn on western corn rootworm (Coleoptera: Chrysomelidae) damage and adult emergence. J Econ Entomol 100:557–565

    Google Scholar 

  16. Krysan JL (1986) Introduction: biology, distribution and identification of pest Diabrotica. In: Krysan JL, Miller TA (eds) Methods of the study of pest Diabrotica. Springer, New York, pp 25–47

    Google Scholar 

  17. Sutter GR (1999) Western corn rootworm. In: Steffey Kl, Rice ME, All J, Andow DA, Gray ME, Van Duyn JW (eds) Handbook of corn insects. Entomol Soc Am, Lanham, MD, pp 64–65

    Google Scholar 

  18. Kiss J, Edwards CR, Berger HK, Cate P, Cean M et al (2005) Monitoring of western corn rootworm (Diabrotica virgifera virgifera LeConte) in Europe 1992–2003. In: Vidal S, Kuhlmann U, Edwards CR (eds) Western corn rootworm: ecology and management. CABI Publishing, CAB International, Wallingford, pp 29–39

    Google Scholar 

  19. Miller NJ, Estoup A, Toepfer S, Bourguet D, Lapchin L et al (2005) Multiple transatlantic introduction of the western corn rootworm. Science 310:992

    CAS  Google Scholar 

  20. Ciosi M, Miller N, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    CAS  Google Scholar 

  21. Levine E, Oloumi-Sadeghi H (1996) Western corn rootworm (Coleoptera: Chrysomelidae) larval injury to corn grown for seed production following soybeans grown for seed production. J Econ Entomol 89:1010–1016

    Google Scholar 

  22. Sammons AE, Edwards CR, Bledsoe LW, Boeve PJ, Stuart JJ (1997) Behavioral and feeding assays reveal a western corn rootworm variant that is attracted to soybean. Environ Entomol 26:1336–1342

    Google Scholar 

  23. Isard SA, Levine E, Onstad DW, Spencer JL (1998) Status of the rootworm problem in first-year corn in Illinois. Poster presentation at the ESA annual meeting, Las Vegas

    Google Scholar 

  24. Rondon SI, Gray ME (2003) Captures of western corn rootworm (Coleoptera: Chrysomelidae) adults with Pherocon AM and vial traps in four crops in east central Illinois. J Econ Entomol 96:737–747

    Google Scholar 

  25. Rondon SI, Gray ME (2004) Ovarian development and ovipositional preference of the western corn rootworm (Coleoptera: Chrysomelidae) variant in east central Illinois. J Econ Entomol 97:390–396

    Google Scholar 

  26. Muma MH, Hill RE, Hixon E (1949) Soil treatments for corn rootworm control. J Econ Entomol 42:822–824

    CAS  Google Scholar 

  27. Ball HJ, Hill RE (1953) You can control corn rootworm. Nebraska Experiment Station Quarterly Winter 1952–53, Nebraska Agricultural Experiment Station, Lincoln

    Google Scholar 

  28. Ball HJ, Roselle, RE (1954) You can control corn rootworms. University of Nebraska Extension Circular 1567

    Google Scholar 

  29. Ball HJ (1983) Aldrin and dieldrin residues in Nebraska (USA) soils as related to decreasing LD50 values for the adult western corn rootworm (Diabrotica virgifera),1962–1981. J Environ Sci Health B18:735–744

    CAS  Google Scholar 

  30. Roselle RE, Anderson LW, Simpson GW, Webb MC (1959) Cooperative extension work in entomology. Annual Report for 1959, Lincoln

    Google Scholar 

  31. Roselle RE, Anderson LW, Simpson RC, Bergman PW (1960) Cooperative extension work in entomology. Annual Report for 1960, Lincoln

    Google Scholar 

  32. Roselle RE, Anderson LW, Bergman PW (1961) Cooperative extension work in entomology. Annual Report for 1961, Lincoln

    Google Scholar 

  33. Ball HJ, Weekman GT (1962) Insecticide resistance in the adult western corn rootworm in Nebraska. J Econ Entomol 55:439–441

    Google Scholar 

  34. Ball HJ, Weekman GT (1963) Differential resistance of corn rootworms to insecticides in Nebraska and adjoining states. J Econ Entomol 56:553–555

    CAS  Google Scholar 

  35. Pruess KP, Witkowski JF, Raun ES (1974) Population suppression of western corn rootworm by adult control with ULV malathion. J Econ Entomol 67:541–545

    Google Scholar 

  36. Siegfried BD, Mullin CA (1989) Influence of alternative host plant feeding on aldrin susceptibility and detoxification enzymes in western and northern corn rootworms. Pestic Biochem Physiol 35:155–164

    CAS  Google Scholar 

  37. Zhou X, Scharf ME, Parimi S, Meinke LJ, Wright RJ, Chandler LD, Siegfried BD (2002) Diagnostic assays based on esterase-mediated resistance mechanisms in western corn rootworms (Coleoptera: Chrysomelidae). J Econ Entomol 95:1261–1266

    CAS  Google Scholar 

  38. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806

    CAS  Google Scholar 

  39. 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 37:409–433

    Google Scholar 

  40. van Frankenhuyzen K (2009) Insecticidal activity of Bacillus thuringiensis crystal proteins. J Invertebr Path 101:1–16

    Google Scholar 

  41. Crickmore N, Zeigler DR, Schnepf E, Van Rie J, Lereclus D, Baum J, Bravo A, Dean, DH (2012) Bacillus thuringiensis toxin nomenclature. http://www.lifesci.sussex.ac.uk/Home/Neil_Crickmore/Bt/ Accessed 30 Nov 2012

  42. Bravo A, Gill SS, Soberon M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435

    CAS  Google Scholar 

  43. Vachon V, Laprade R, Schwartz J-L (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol http://dx.doi.org/10.1016/j.jip.2012.05.001

  44. Mendelsohn M, Kough J, Vaituzis Z, Matthews K (2003) Are Bt crops safe? Nat. Biotechnol. 21:1003Ð1009

    Google Scholar 

  45. U.S. Environmental Protection Agency (2012) Current & previously registered section 3 PIP registrations http://www.epa.gov/pesticides/biopesticides/pips/pip_list.htm

  46. Devos Y, Meihls LN, Kiss J, Hibbard BE (2012) Resistance evolution to the first generation of genetically modified Diabrotica-active Bt-maize events by western corn rootworm: management and monitoring considerations. Transgenic Res. doi:10.1007/s11248-012-9657-4

    Google Scholar 

  47. Marra MC, Piggott NE, Goodwin BK (2012) The impact of corn rootworm protected biotechnology traits in the United States. AgBioForum 15:217–230

    Google Scholar 

  48. Roush RT (1998) Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil Trans R Soc Lond B 353:1777–1786

    CAS  Google Scholar 

  49. Li J, Carroll J, Ellar DJ (1991) Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. Nature 353:815–821

    CAS  Google Scholar 

  50. Galitsky N, Cody V, Wojtczak A, Ghosh D, Luft JR, Pangborn W, English L (2001) Structure of the insecticidal bacterial delta-endotoxin Cry3Bb1 of Bacillus thuringiensis. Acta Crystallogr D Biol Crystallogr 57:1101–1109

    CAS  Google Scholar 

  51. Fabrick J, Oppert C, Lorenzen MD, Morris K, Oppert B, Jurat-Fuentes JL (2009) A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J Biol Chem 284:18401–18410

    CAS  Google Scholar 

  52. Ochoa-Campuzano C, Real MD, Martínez-Ramírez AC, Bravo A, Rausell C (2007) An ADAM metalloprotease is a Cry3Aa Bacillus thuringiensis toxin receptor. Biochem Biophys Res Commun 362:437–442

    CAS  Google Scholar 

  53. Park Y, Abdullah MAF, Taylor MD, Rahman K, Adang MJ (2009) Enhancement of Bacillus thuringiensis Cry3Aa and Cry3Bb toxicities to Coleopteran larvae by a toxin-binding fragment of an insect cadherin. Appl Environ Microbiol 75:3086–3092

    CAS  Google Scholar 

  54. Walters FS, Stacy CM, Lee MK, Palekar N, Chen JS (2008) An engineered chymotrypsin/cathepsin G site in domain I renders Bacillus thuringiensis Cry3A active against Western corn rootworm larvae. Appl Environ Microbiol 74:367–374

    CAS  Google Scholar 

  55. Walters FS, deFontes CM, Hart H, Warren GW, Chen JS (2010) Lepidopteran-active variable-region sequence imparts Coleopteran activity in eCry3.1Ab, an engineered Bacillus thuringiensis hybrid insecticidal protein. Appl Environ Microbiol 76:3082–3088

    CAS  Google Scholar 

  56. Vaughn T, Cavato T, Brar G, Coombe T, DeGooyer T et al (2005) A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci 45:931–938

    CAS  Google Scholar 

  57. Herrnstadt C, Gilroy TE, Sobieski DA, Bennett BD, Gaertner FH (1986) Nucleotide sequence and deduced amino acid sequence of a coleopteran-active delta-endotoxin gene from Bacillus thuringiensis subsp. San Diego. Gene 57:37–46

    Google Scholar 

  58. Sekar V, Thompson DV, Maroney MJ, Bookland RG, Adang MJ (1987) Molecular cloning and characterization of the insecticidal crystal protein gene of Bacillus thuringiensis var. tenebrionis. Proc Natl Acad Sci USA 84:7036–7040

    CAS  Google Scholar 

  59. MacIntosh SC, Stone TB, Sims SR, Hunst PL, Greenplate JT et al (1990) Specificity and efficacy of purified Bacillus thuringiensis proteins against agronomically important insects. J Invertebr Pathol 56:258–266

    CAS  Google Scholar 

  60. Slaney AC, Robbins HL, English L (1992) Mode of action of Bacillus thuringiensis toxin CryIIIA: an analysis of toxicity in Leptinotarsa decemlineata (Say) and Diabrotica undecempunctata Howardi Barber. Insect Biochem Mol Biol 22:9–18

    CAS  Google Scholar 

  61. Carroll J, Li J, Ellar DJ (1989) Proteolytic processing of a Coleopteran specific-endotoxin produced by Bacillus thuringiensis var. tenebrionis. Biochem J 261:99–105

    CAS  Google Scholar 

  62. Carroll J, Convents D, Van Damme J, Boets A, Van Rie J, Ellar DJ (1997) Intramolecular proteolytic cleavage of Bacillus thuringiensis Cry3A-endotoxin may facilitate its Coleopteran toxicity. J Invertebr Pathol 70:41–49

    CAS  Google Scholar 

  63. de Maagd RA, Bravo A, Crickmore N (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199

    Google Scholar 

  64. de Maagd RA, Kwa MSG, van der Klei H, Yamamoto T, Schipper B et al (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 62:1537–1543

    Google Scholar 

  65. 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 66:1559–1563

    Google Scholar 

  66. Donovan WP, Rupar MJ, Slaney AC, Malvar T, Gawron-Burke MC, Johnson TB (1992) Characterization of two genes encoding Bacillus thuringiensis insecticidal crystal proteins toxic to Coleoptera species. Appl Environ Microbiol 58:3921–3927

    CAS  Google Scholar 

  67. Von Tersch MA, Slatin SL, Kulesza CA, English LH (1994) Membrane-permeabilizing activities of Bacillus thuringiensis Coleopteran-active toxin CryIIIB2 and CryIIIB2 domain I peptide. Appl Environ Microbiol 60:3711–3717

    Google Scholar 

  68. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6(7):e22629. doi:10.1371/journal.pone.0022629

    CAS  Google Scholar 

  69. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2012) Western corn rootworm and Bt maize: challenges of pest resistance in the field. GM Crops Food 3:235–244

    Google Scholar 

  70. Ellis TR, Stockhoff BA, Stamp L, Schnepf HE, Schwab GE et al (2002) Novel Bacillus thuringiensis binary insecticidal crystal proteins active on western corn rootworm, Diabrotica virgifera virgifera LeConte. Appl Environ Microbiol 68:1137–1145

    CAS  Google Scholar 

  71. Schnepf HE, Lee S, Dojillo J, Burmeister P, Fencil K, Morera L, Nygaard L, Narva KE, Wolt J (2005) Characterization of Cry34/Cry35 binary insecticidal proteins from diverse Bacillus thuringiensis strain collections. Appl Environ Microbiol 71:1765–1774

    CAS  Google Scholar 

  72. Berne S, Lah L, Sepcic K (2009) Aegerolysins: structure, function, and putative biological role. Protein Sci 18:694–706

    CAS  Google Scholar 

  73. Jones GW, Nielsen-Leroux C, Yang Y, Yuan Z, Dumas VF, Monnerat RG, Berry C (2007) A new Cry toxin with a unique two-component dependency from Bacillus sphaericus. FASEB J 21:4112–4120

    CAS  Google Scholar 

  74. Moellenbeck DJ, Peters ML, Bing JW, Rouse JR, Higgins LS et al (2001) Insecticidal proteins from Bacillus thuringiensis protect corn from corn rootworms. Nat Biotechnol 19:668–672

    CAS  Google Scholar 

  75. Masson L, Schwab G, Mazza A, Brousseau R, Potvin L, Schwartz JL (2004) A novel Bacillus thuringiensis (PS149B1) containing a Cry34/35Ab1 binary toxin specific for the western corn rootworm Diabrotica virgifera virgifera LeConte forms ion channels in lipid membranes. Biochemistry 43:12349–12357

    CAS  Google Scholar 

  76. Li H, Olson M, Lin G, Hey T, Tan S-Y, Narva KE (2012) Bacillus thuringiensis Cry34Ab1/Cry35Ab1 interactions with Western corn rootworm midgut membrane binding sites. PLoS One accepted

    Google Scholar 

  77. MacIntosh SC (2010) Managing the risk of insect resistance to transgenic insect control traits: Practical approaches in local environments. Pest Manag Sci 66:100–106

    CAS  Google Scholar 

  78. Mellon M (1998) UCS introduction. In: Mellon M, Rissler J (eds) Now or never: serious new plans to save a natural pest control. Union of Concerned Scientists, Cambridge, pp 1–12

    Google Scholar 

  79. Gould F (1998) Sustainability of transgenic insecticidal cultivars: Integrating pest genetics and ecology. Annu Rev Entomol 43:701–726

    CAS  Google Scholar 

  80. Tabashnik BE (1994) Evolution of resistance to Bacillus thuringiensis. Annu Rev Entomol 39:47–79

    Google Scholar 

  81. Janmaat AF, Myers J (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, trichoplusia ni. Proc R Soc Lond B 270:2263–2270

    Google Scholar 

  82. U.S. Environmental Protection Agency (2001a) Biopesticides registration action document—Bacillus thuringiensis plant-incorporated protectants. http://www.epa.gov/pesticides/biopesticides/pips/bt_brad.htm

  83. U.S. Environmental Protection Agency (2001b) A set of scientific issues being considered by the environmental protection agency regarding: Bt plant-pesticides risk and benefit assessments: Insect resistance management. FIFRA scientific advisory panel report no. 2000–07a

    Google Scholar 

  84. Huang FN, Andow DA, Buschman LL (2011) Success of the high-dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomologia Entomol Exp Appl 140:1–16

    Google Scholar 

  85. Bates SL, Zhao J-Z, Roush RT, Shelton AM (2005) Insect resistance management in GM crops: past, present and future. Nat Biotechnol 23:57–62

    CAS  Google Scholar 

  86. Storer NP, Babcock JM, Edwards JM (2006) Field measures of western corn rootworm (Coleoptera: Chrysomelidae) mortality caused by Cry34/35Ab1 proteins expressed in maize event 59122 and implications for trait durability. J Econ Entomol 99:1381–1387

    CAS  Google Scholar 

  87. Meihls LN, Higdon ML, Siegfried BD, Miller NJ, Sappington TW (2008) Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc Natl Acad Sci USA 105:19177–19182

    CAS  Google Scholar 

  88. Binning RR, Lefko SA, Millsap AY, Thompson SD, Nowatzki TM (2010) Estimating western corn rootworm (Coleoptera: Chrysomelidae) larval susceptibility to event DAS-59122-7 maize. J Appl Entomol 134:551–561

    Google Scholar 

  89. Hibbard BE, Clark TL, Ellersieck MR, Meihls LN, El Khishen AA et al (2010) Mortality of western corn rootworm larvae on mir604 transgenic maize roots: field survivorship has no significant impact on survivorship of f1 progeny on mir604. J Econ Entomol 103:2187–2196

    Google Scholar 

  90. Hibbard BE, Frank DL, Kurtz R, Boudreau E, Ellersieck MR, Odhiambo JF (2011) Mortality impact of Bt transgenic maize roots expressing ecry3.1ab, mCry3A, and ecry3.1ab plus mCry3A on western corn rootworm larvae in the field. J Econ Entomol 104:1584–1591

    CAS  Google Scholar 

  91. Tabashnik BE, Liu Y-B, Dennehy TJ, Sims MA, Sisterson MS, Biggs RW, Carrière Y (2002) Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 95:1018–1026

    CAS  Google Scholar 

  92. Pereira EJG, Lang BA, Storer NP, Siegfried BD (2008) Selection for Cry1F resistance in the European corn borer and cross-resistance to other cry toxins. Entomol Exp Appl 126:115–121

    CAS  Google Scholar 

  93. Storer NP, Babcock JM, Schlenz JM, Meade T, Thompson GD, Bing JW, Huckaba RM (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103:1031–1038

    Google Scholar 

  94. Coates BS, Sumerford DV, Lopez MD, Wang HC, Fraser LM et al (2011) A single major QTL controls expression of larval Cry1F resistance trait in Ostrinia nubilalis (Lepidoptera: Crambidae) and is independent of midgut receptor genes. Genetica 139:961–972

    Google Scholar 

  95. Gahan LJ, Gould F, Heckel DG (2001) Identification of a gene associated with bit resistance in Heliothis virescens. Science 293:857–860

    CAS  Google Scholar 

  96. Ferré J, Van Rie J (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47:501–533

    Google Scholar 

  97. Crespo ALB, Spencer TA, Alves AP, Hellmich RL, Blankenship EE, Magalhaes LC, Siegfried BD (2009) On-plant survival and inheritance of resistance to Cry1Ab toxin from Bacillus thuringiensis in a field-derived strain of European corn borer, Ostrinia nubilalis. Pest Manag Sci 65:1071–1081

    CAS  Google Scholar 

  98. Lefko SA, Nowatzki TM, Thompson SD, Binning RR, Pascual MA et al (2008) Characterizing laboratory colonies of western corn rootworm (Coleoptera: Chrysomelidae) selected for survival on maize containing event DAS-59122-7. J Appl Entomol 13:189–204

    Google Scholar 

  99. Oswald KJ, French BW, Nielson C, Bagley M (2011) Selection for Cry3Bb1 resistance in a genetically diverse population of nondiapausing western corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 104:1038–1044

    CAS  Google Scholar 

  100. Gassmann AJ, Carrière Y, Tabashnik BE (2009) Fitness costs of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 54:147–163

    CAS  Google Scholar 

  101. Kruger M, Van Rensburg JBJ, Van den Berg J (2009) Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot 28:684–689

    Google Scholar 

  102. U.S. Environmental Protection Agency (2011) Updated EPA review of ABSTC’s 2010 corn insect resistance management compliance assurance program. http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2011-0922-0010

  103. Meihls LN, Higdon ML, Ellersieck M, Hibbard BE (2011) Selection for resistance to mCry3A-expressing transgenic corn in western corn rootworm. J Econ Entomol 104:1045–1054

    CAS  Google Scholar 

  104. Porter P, Cullen E, Sappington T, Schaafsma A, Pueppke S, Andow D, Bradshaw J, Buschman L, Cardoza YJ, DiFonzo C, French BW, Gassmann A, Gray ME, Hammond RB, Hibbard B, Krupke CH, Lundgren JG, Ostlie KR, Shields E, Spencer JL, Tooker JF, Youngman R (2012) Comment submitted by Patrick Porter, North Central Coordinating Committee nccc46. http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2011-0922-0013

  105. Tabashnik BE (1989) Managing resistance with multiple pesticide tactics—theory, evidence, and recommendations. J Econ Entomol 82:1263–1269

    CAS  Google Scholar 

  106. Gould F (1986) Simulation models for predicting durability of insect-resistant germ plasm: a deterministic diploid, two-locus model. Environ Entomol 15:1–10

    Google Scholar 

  107. Gould F, Cohen MB, Bentur JS, Kennedy GG, Van Duyn J (2006) Impact of small fitness costs on pest adaptation to crop varieties with multiple toxins: a heuristic model. J Econ Entomol 99:2091–2099

    CAS  Google Scholar 

  108. Onstad DW, Meinke LJ (2010) Modeling evolution of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to transgenic corn with two insecticidal traits. J Econ Entomol 103:849–860

    Google Scholar 

  109. Ives AR, Glaum PR, Ziebarth NL, Andow DA (2011) The evolution of resistance to two-toxin pyramid transgenic crops. Ecol Appl 21:503–515

    Google Scholar 

  110. Gryspeirt A, Grégoire J-C (2012) Effectiveness of the high dose/refuge strategy for managing pest resistance to Bacillus thuringiensis (Bt) plants expressing one or two toxins. Toxins 4:810–835

    CAS  Google Scholar 

  111. Zhao J-Z, Cao J, Li Y, Collins HL, Roush RT et al (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat Biotechnol 21:1493–1497

    CAS  Google Scholar 

  112. Storer NP, Thompson GD, Head GP (2012) Application of pyramided traits against Lepidoptera in insect resistance management for Bt crops. GM Crops Food 3

    Google Scholar 

  113. Marra MC, Piggott NE, Goodwin BK (2009) The anticipated value of SmartStax™ for US corn growers. AgBioForum 13:1–12

    Google Scholar 

  114. Carroll MW, Head G, Caprio MA (2012) When and where a seed mix refuge makes sense for managing insect resistance to Bt plants. Crop Prot 38:74–79

    Google Scholar 

  115. Mallet J, Porter P (1992) Preventing adaptation to insect-resistant crops: are seed mixtures or refugia the best strategy? Proc R Soc Lond B 250:165–169

    Google Scholar 

  116. Davis PM, Onstad DW (2000) Seed mixtures as a resistance management strategy for European corn borers (Lepidoptera: Crambidae) infesting transgenic corn expressing Cry1Ab protein. J Econ Entomol 93:937–948

    CAS  Google Scholar 

  117. Zhao JZ, Cao J, Collins HL, Bates SL, Roush RT, Earle ED, Shelton AM (2005) Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc Natl Acad Sci USA 102:8426–8430

    CAS  Google Scholar 

  118. Tabashnik BE, Gould F (2012) Delaying corn rootworm resistance to Bt corn. J Econ Entomol 105:767–776

    Google Scholar 

  119. Narva KE, Schwab GE, Bradfisch GA (1993) Novel Bacillus thuringiensis gene encoding coleopteran-active toxin. U.S. patent 5,186,934

    Google Scholar 

  120. Thompson M, Knuth M, Cardineau G (1999) Bacillus thuringiensis toxins with improved activity. U.S. patent 5,874,288

    Google Scholar 

  121. Li XQ, Wei JZ, Tan A, Aroian RV (2007) Resistance to root-knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant Biotechnol J 5:455–464

    CAS  Google Scholar 

  122. Yu Z, Bai P, Bai P, Ye W, Zhang F et al (2008) A novel negative regulatory factor for nematicidal Cry protein gene expression in Bacillus thuringiensis. J Microbiol Biotechnol 18:1033–1039

    CAS  Google Scholar 

  123. Carozzi N, Koziel MG, Hargiss T, Duck NB, Kahn TW (2006) AXMI-028 and AXMI-029, family of novel delta-endotoxin genes and methods for their use. International patent application no. WO2006/119457A1

    Google Scholar 

  124. Abad AR, Duck NB, Feng X, Flanagan RD, Kahn TW, Sims LE (2002) Genes encoding novel proteins with pesticidal activity against coleopterans, international patent application no. WO 02/34774 A2

    Google Scholar 

  125. Soberon M, Lopez-Diaz JA, Bravo A (2012) Cyt toxins produced by Bacillus thuringiensis: a protein fold conserved in several pathogenic microorganisms. Peptides. doi:10.1016/j.peptides.2012.05.023

    Google Scholar 

  126. Payne JM, Narva KE, Uyeda KA, Stalder CJ, Michaels TM (1995) Bacillus thuringiensis isolate PS201T6 toxin. U.S. patent 5,436,002

    Google Scholar 

  127. Rupar MJ, Donovan WP, Tan Y, Slaney AC (2000) Bacillus thuringiensis CryET29 compositions toxic to coleopteran insects and Ctenocephalides spp. U.S. patent 6,093,695

    Google Scholar 

  128. Li J, Koni PA, Ellar DJ (1996) Structure of the mosquitocidal δ-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. J Mol Biol 257:129–152

    CAS  Google Scholar 

  129. Cohen S, Dym O, Albeck S, Ben-Dov E, Cahan R, Firer M et al (2008) High-resolution crystal structure of activated Cyt2Ba monomer from Bacillus thuringiensis subsp. israelensis. J Mol Biol 380:820–827

    CAS  Google Scholar 

  130. Cohen S, Albeck S, Ben-Dov E, Cahan R, Firer M, Zaritsky A et al (2011) Cyt1Aa toxin: crystal structure reveals implications for its membrane perforating function. J Mol Biol 413:804–814

    CAS  Google Scholar 

  131. Thomas WE, Ellar DJ (1983) Mechanism of action of Bacillus thuringiensis var israelensis insecticidal delta-endotoxin. FEBS Lett 154:362–368

    CAS  Google Scholar 

  132. Butko P (2003) Cytolytic toxin Cyt1A and its mechanism of membrane damage: data and hypotheses. Appl Environ Microbiol 69:2415–2422

    CAS  Google Scholar 

  133. Crickmore N, Bone EJ, Williams JA, Ellar DJ (1995) Contribution of the individual components of the delta-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensis subsp. israelensis. FEMS Microbiol Lett 131:249–254

    CAS  Google Scholar 

  134. Georghiou GP, Wirth MC (1997) Influence of exposure to single versus multiple toxins of Bacillus thuringiensis subsp. israelensis on development of resistance in the mosquito Culex quinquefasciatus (Diptera: Culicidae). Appl Environ Microbiol 63:1011–1095

    Google Scholar 

  135. Wirth MC, Park H-W, Walton WE, Federici BA (2005) Cyt of Bacillus thuringiensis delays evolution of resistance to Cry11A in the mosquito Culex quinquefasciatus. Appl Environ Microbiol 71:185–189

    CAS  Google Scholar 

  136. Federici BA, Bauer LS (1998) Cyt1Aa protein of Bacillus thuringiensis is toxic to the cottonwood leaf beetle, Chrysomela scripta, and suppresses high levels of resistance to Cry3Aa. Appl Environ Microbiol 64:4368–4371

    CAS  Google Scholar 

  137. Donovan WP, Engleman JT, Donovan JC, Baum JA, Bunkers GJ et al (2006) Discovery and characterization of Sip1A: a novel secreted protein from Bacillus thuringiensis with activity against coleopteran larvae. Appl Microbiol Biotechnol 72:713–771

    CAS  Google Scholar 

  138. Warren GW, Koziel MG, Mullins MA, Nye GJ, Desai N et al (1994) Novel pesticidal proteins and strains, international patent application no. WO 94/21795

    Google Scholar 

  139. Warren G (1997) Vegetative insecticidal proteins: novel proteins for control of corn pests. In: Carozzi N, Koziel M (eds) Advances in insect control: the role of transgenic plants. Taylor & Francis, London, pp 109–121

    Google Scholar 

  140. Han S, Craig JA, Putnam C, Carozzi NB, Tainer JA (1999) Evolution and mechanism from structures of an ADP-ribosylating toxin and NAD complex. Nat Struct Biol 6:932–936

    CAS  Google Scholar 

  141. Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E et al (1998) Insecticidal toxins from the bacterium photorhabdus luminescens. Science 280:2129–2132

    CAS  Google Scholar 

  142. ffrench-Constant R, Waterfield N, Daborn P, Joyce S, Bennett H et al (2003) Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev 26:433–456

    CAS  Google Scholar 

  143. Sergeant M, Jarrett P, Ousley M, Morgan JAW (2003) Interactions of insecticidal toxin gene products from Xenorhabdus nematophilus PMFI296. Appl Environ Microbiol 69:3344–3349

    CAS  Google Scholar 

  144. Hurst MR, Glare TR, Jackson TA, Ronson CW (2000) Plasmid-located pathogenicity determinants of Serratia entomophila, the causal agent of amber disease of grass grub, show similarity to the insecticidal toxins of Photorhabdus luminescens. J Bacteriol 182:5127–5138

    CAS  Google Scholar 

  145. Hinchliffe SJ, Isherwood KE, Stabler RA, Prentice MB, Rakin A et al (2003) Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. Genome Res 13:2018–2029

    CAS  Google Scholar 

  146. ffrench-Constant RH, Dowling A, Waterfield NR (2007) Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon 49:436–451

    CAS  Google Scholar 

  147. Guo L, Fatig RO III, Orr GL, Schafer BW, Strickland JA et al (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 274:9836–9842

    CAS  Google Scholar 

  148. Liu D, Burton S, Glancy T, Li ZS, Hampton R et al (2003) Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat Biotechnol 21:1222–1228

    CAS  Google Scholar 

  149. Lang AE, Schmidt G, Schlosser A, Hey TD, Larrinua IM et al (2010) Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering. Science 327:1139–1142

    CAS  Google Scholar 

  150. Aktories K, Lang AE, Schwan C, Mannherz HG (2011) Actin as target for modification by bacterial protein toxins. FEBS J 278:4526–4543

    CAS  Google Scholar 

  151. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    CAS  Google Scholar 

  152. Center for Environmental Risk Assessment (2011) Problem formulation for the environmental Risk assessment of RNAi plants, Conference Proceedings. ILSI Research Foundation, Washington D.C

    Google Scholar 

  153. Yang G, You M, Vasseur L, Zhao Y Liu C (2011) Development of RNAi in insects and RNAi-based pest control, pesticides in the modern world—pests control and pesticides exposure and toxicity assessment. In: Stoytcheva M (ed), ISBN: 978-953-307-457-3, InTech. http://www.intechopen.com/books/pesticides-in-the-modern-world-pests-control-and-pesticides-exposure-and-toxicity-assessment/development-of-rnai-in-insects-and-rnai-based-pest-control

  154. Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: A review. J Insect Physiol 56:227–235

    CAS  Google Scholar 

  155. Burand JP, Hunter WB (2012) RNAi: future in insect management. J Invert Pathol doi: 10.1016/j.bbr.2011.03.031

  156. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H et al (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57:231–245

    CAS  Google Scholar 

  157. Alves AP, Lorenzen MD, Beeman RW, Foster JE Siegfried BD (2010) RNA interference as a method for target-site screening in the western corn rootworm, Diabrotica virgifera virgifera. J Insect Sci 10:162 available online: insectscience.org/10.162

    Google Scholar 

  158. Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ et al (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Nat Acad Sci 102:11337–11342

    CAS  Google Scholar 

  159. Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, Lorenzen MD, Kanost M, Beeman RW et al (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 14:453–463

    CAS  Google Scholar 

  160. Valencia A, Alves AP, Siegfried BD (2012) Molecular cloning and functional characterization of an endogenous endoglucanase belonging to GHF45 from the western corn rootworm, Diabrotica virgifera virgifera. Gene 513:260–267

    Google Scholar 

  161. Price DRG, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400

    CAS  Google Scholar 

  162. Auer C, Frederick R (2009) Crop improvement using small RNAs; applications and predictive ecological risk assessments. Trends Biotechnol 27:644–651

    CAS  Google Scholar 

  163. Gordon KHJ, Waterhouse PM (2007) RNAi for insect-proof plants. Nature Biotechnol 25:1231–1232

    CAS  Google Scholar 

  164. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P et al (2007) Control of coleopteran insect pests through RNA interference. Nature Biotechnol 11:1322–1326

    Google Scholar 

  165. Rangasamy M, Siegfried BD (2011) Validation of RNA interference in western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) adults. Pest Manag Sci 68:587–591

    Google Scholar 

  166. Bolognesi R, Ramaseshadri P, Anderson J, Bachman P, Clinton W et al (2012) Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoS ONE 7(10):e47534. doi:10.1371/journal.pone.0047534

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dow AgroSciences, 9330 Zionsville Road, Indianapolis, IN, 46268, USA

    Kenneth E. Narva & Nicholas P. Storer

  2. Department of Entomology, University of Nebraska, Lincoln, NE, 68583, USA

    Blair D. Siegfried

Authors
  1. Kenneth E. Narva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Blair D. Siegfried
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicholas P. Storer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenneth E. Narva .

Editor information

Editors and Affiliations

  1. Bioresources Project Group, Fraunhofer Institute for Molecular Biology, Giessen, Germany

    Andreas Vilcinskas

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Narva, K.E., Siegfried, B.D., Storer, N.P. (2013). Transgenic Approaches to Western Corn Rootworm Control. In: Vilcinskas, A. (eds) Yellow Biotechnology II. Advances in Biochemical Engineering/Biotechnology, vol 136. Springer, Berlin, Heidelberg. https://doi.org/10.1007/10_2013_195

Download citation

Publish with us

Policies and ethics

Search

Navigation