Abstract
The European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae), is an introduced crop pest in North America that causes major damage to corn and reduces yield of food, feed, and biofuel materials. The Cry1F toxin from Bacillus thuringiensis (Bt) expressed in transgenic hybrid corn is highly toxic to O. nubilalis larvae and effective in minimizing feeding damage. A laboratory colony of O. nubilalis was selected for high levels of Cry1F resistance (>12,000-fold compared to susceptible larvae) and is capable of survival on transgenic hybrid corn. Genetic linkage maps with segregating AFLP markers show that the Cry1F resistance trait is controlled by a single quantitative trait locus (QTL) on linkage group 12. The map position of single nucleotide polymorphism (SNP) markers indicated that midgut Bt toxin-receptor genes, alkaline phosphatase, aminopeptidase N, and cadherin, are not linked with the Cry1F QTL. Evidence suggests that genes within this genome interval may give rise to a novel Bt toxin resistance trait for Lepidoptera that appears independent of known receptor-based mechanisms of resistance.
Similar content being viewed by others
References
Archer TL, Schuster G, Patrick C, Cronholm G, Bynum ED, Morrison WP (2000) Whorl and stalk damage by European and southwestern corn borers to four events of Bacillus thuringiensis transgenic maize. Crop Protect 19:181–190
Baxter S, Zhao JZ, Gahan LJ, Shelton AM, Tabashnik BE, Heckel DG (2005) Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol Biol 14:327–334
Baxter S, Zhao JZ, Shelton AM, Vogel H, Heckel DG (2008) Genetic mapping of Bt-toxin binding proteins in a Cry1A-toxin resistant strain of diamondback moth Plutella xylostella. Insect Biochem Mol Biol 38:125–135
Beldade P, Saenko SV, Pul N, Long AD (2009) A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidopteran reference genome. PLoS Genetics 5:e1000366
Bolin PC, Hutchison WD, Andow DA (1999) Selection and characterization of Bt resistance in the European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae). J Econ Entomol 92:1021–1031
Casida JE, Quistad GB (2004) Why insecticides are more toxic to insects than people: the unique toxicology of insects. J Pestic Sci 29:81–86
Chang WXZ, Gahan LJ, Tabashnik BE, Heckel DG (1999) A new aminopeptidase from diamondback moth provides evidence for a gene duplication event in Lepidoptera. Insect Mol Biol 8:171–177
Chaufaux J, Seguin M, Swanson JJ, Bourguet D, Siegfried BD (2001) Chronic exposure of the European corn borer (Lepidoptera: Crambidae) to Cry1Ab Bacillus thuringiensis toxin. J Econ Entomol 94:1564–1570
Coates BS, Sumerford DV, Hellmich RL, Lewis LC (2005) Sequence variation in the cadherin gene of Ostrinia nubilalis: a tool for field monitoring. Insect Biochem Mol Biol 35:129–139
Coates BS, Sumerford DV, Lewis LC (2007) A β-1, 3-galactosyltransferase and brainiac/bre5 homolog expressed in the midgut did not contribute to a Cry1Ab toxin resistance trait in Ostrinia nubilalis. Insect Biochem Mol Biol 37:346–355
Coates BS, Sumerford DV, Lewis LC (2008a) Segregation of Ostrinia nubilalis aminopeptidase 1 (APN1), cadherin, and bre5-like alleles from a Cry1Ab resistant colony are not associated with F2 larval weights when fed on toxin-containing diet. J Insect Sci 8:21
Coates BS, Sumerford DV, Hellmich RL, Lewis LC (2008b) ) Mining an Ostrinia nubilalis midgut expressed sequence tag (EST) library for candidate genes and single nucleotide polymorphisms (SNPs). Insect Mol Biol 17:607–621
Coates BS, Sumerford DV, Hellmich RL, Lewis LC (2009) Repetitive genomic elements in a European corn borer, Ostrinia nubilalis, bacterial artificial chromosome library were indicated by bacterial artificial chromosome end sequencing and development of sequence tag site markers: implications for lepidopteran genomic research. Genome 52:57–67
Crava CM, Bel Y, Lee SF, Manachini B, Heckel DG, Escriche B (2010) Study of the aminopeptidase N gene family in the lepidopterans Ostrinia nubilalis (Hübner) and Bombyx mori (L.): Sequences, mapping and expression. Insect Biochem Mol Biol 40:506–515
Crespo AB, Spencer T, 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 10:1071–1081
Dopman EB, Bogdanowicz SM, Harrison RG (2004) Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn borer (Ostrinia nubilalis). Genetics 167:301–309
Ferré J, Van Rie J (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47:501–533
ffrench-Constant RH, Steichen J, Rocheleau TA, Aronstein K, Roush RT (1993) A single amino acid substitution in a γ-aminobutyric acid subtype a receptor locus associated with cyclodiene insecticide resistance in Drosophila populations. Proc Natl Acad Sci USA 90:1957–1961
Flannagan RD, Yo CG, Mathis JP, Meyer TE, Shi X, Siqueira HAA, Siegfried BD (2005) Identification, cloning and expression of a Cry1Ab cadherin receptor from European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae). Insect Mol Biol 35:33–40
Francis BR, Bulla LA Jr (1997) Further characterization of BT-R1, the cadherin-like receptor for Cry1Ab toxin in tobacco hornworm (Manduca sexta) midguts. Insect Biochem Mol Biol 27:541–550
Gahan LJ, Gould F, Heckel DG (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293:857–860
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 98:1357–1368
Georghiou GP, Lagunes-Tejeda A (1991) The occurrence of resistance to pesticides in arthropods. Food and Agriculture Organization of the United Nations, Rome
Glasser JA, Matten SR (2003) Sustainability of insect resistance management strategies for transgenic Bt corn. Biotechnol Adv 22:45–69
Göring HH, Terwilliger JD (2000) Linkage analysis in the presence of Errors II: marker-locus genotyping errors modeled with hypercomplex recombination fractions. Am J Hum Genet 66:1107–1118
Griffitts JS, Aroian RV (2005) Many roads to resistance: how invertebrates adapt to Bt toxins. Bioessays 27:614–624
Griffitts JS, Whitacre JL, Stevens DE, Aroian RV (2001) Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 293:860–864
Guthrie WD, Dollinger EJ, Stetson JF (1965) Chromosome studies of the European corn borer, smartweed borer, and lotis borer. Annals Entomol Soc Am 58:100–105
Harshman LG, Hoffmann AA (2000) Laboratory selection experiments using Drosophila: what do they really tell us? Trends Ecol Evol 15:32–36
Heckel DG, Gahan LJ, Daly JC, Trowell S (1998) A genomic approach to understanding Heliothis and Helicoverpa resistance to chemical and biological insecticides. Phil Trans R Soc Lond B 353:1713–1722
Heckel DG, Gahan LJ, Liu YB, Tabashnik BE (1999) Genetic mapping of resistance to Bacillus thuringiensis toxins in diamondback moth using biphastic linkage analysis. Proc Natl Acad Sci USA 96:8373–8377
Heckel DG, Gahan LJ, Baxter SW, Zhao JZ, Shelton AM, Gould F, Tabashnik BE (2007) The diversity of Bt resistance genes in species of Lepidoptera. J Invert Pathol 95:192–197
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 6:96
Hua G, Masson L, Jurat-Fuentes JL, Schwab G, Adang MJ (2001) Binding analyses of Bacillus thuringiensis Cry-endotoxins using brush border membrane vesicles of Ostrinia nubilalis. Appl Environ Microbiol 67:872–879
Huang F, Higgins RA, Buschman LT (1997) Baseline susceptibility and changes in susceptibility to Bacillus thuringiensis subsp. kurstaki under selection pressure in European corn borer (Lepidoptera: Pyralidae). J Econ Entomol 90:1137–1143
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
Jurat-Fuentes JL, Adang MJ (2004) Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Helitothis virescens larvae. Eur J Biochem 271:3127–3135
Jurat-Fuentes JL, Gould FL, Adang MJ (2002) Altered Glycosylation of 63- and 68-kilodalton microvillar proteins in Heliothis virescens correlates with reduced Cry1 toxin binding, decreased pore formation, and increased resistance to Bacillus thuringiensis Cry1 toxins. Appl Environ Microbiol 68:5711–5717
Knight PJK, Crickmore N, Ellar DJ (1994) The receptor for Bacillus thuringiensis Cry1A(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase-N. Mol Microbiol 11:429–436
Knowles BH, Knight PJK, Ellar DJ (1991) N-acetylgalactosamine is part of the receptor in insect gut epithelia that recognizes an insecticidal protein from Bacillus thuringiensis. Proc R Soc Lond Biol 245:31–35
Koziel MG, Beland GL, Bowman C, Carozzi NB, Crenshaw R, Crossland L, Dawson J, Desai N, Hill M, Kadwell S, Launis K, Lewis K, Maddox D, McPherson K, Meghigi MR, Merlin E, Rhodes R, Warren GW, Wright M, Evola S (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Biotechnology 11:194–200
Lambert N, Peferoen M (1992) Insecticidal promise of Bacillus thuringiensis: Facts and mysteries about a successful biopesticide. Bioscience 42:112–122
Lincoln S, Daly M, Lander E (1992) Constructing Genetic Maps with MAPMAKER/EXP 3.0. 3rd edn. Whitehead Institute Technical Report
Matten SR, Head GP, Quemada HD (2008) How governmental regulation can help or hinder the integration of Bt crops into IPM programs. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer, New York, pp 27–39
McGaughey WH (1985) Insect resistance to the biological insecticide Bacillus thuringiensis. Science 229:193–194
Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117
Miao XX, Xu SJ, Li MH, Li MW, Huang JH, Dia FY, Marino SW, Mills DR, Zeng PZ, Mita K, Jia SH, Zhang Y, Liu WB, Xiang H, Guo QH, Xu WY, Kong XY, Lin HX, Shi YZ, Lu G, Zhang X, Huang W et al (2005) Simple sequence repeat-based consensus linkage map of Bombyx mori. Proc Natl Acad Sci USA 102:16303–16308
Morin S, Biggs RW, Sisterson MS, Shriver L, Ellers-Kirk C, Higginson D, Holley D, Gahan LJ, Heckel DG, Carrière Y, Dennehy TJ, Brown JK, Tabashnik BE (2003) Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc Natl Acad Sci USA 100:5004–5009
O’Callaghan M, Glare TR, Burgess EPJ, Malone LA (2005) Effects of plants genetically modified for insect resistance on nontarget organisms. Annu Rev Entomol 50:271–292
Pereira EJG, Lang BA, Storer NP, Siegfried BD (2008a) Selection for Cry1F resistance in the European corn borer and cross resistance to other Cry toxins. Entomol Exper Appl 126:115–121
Pereira EJG, Storer NP, Siegfried BD (2008b) Inheritance of Cry1F resistance in laboratory-selected European corn borer and its survival on transgenic corn expressing the Cry1F toxin. Bull Entomol Res 98:621–629
Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature (Lond.) Biotechnol 24:63–71
Siqueira HAA, Gonzáles-Cabrera J, Ferré J, Flannagan R, Siegfried BD (2006) Analysis of Cry1Ab binding in resistant and susceptible strains of the European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Cramdidae). Appl Environ Microbiol 72:5318–5324
Siqueria HAA, Moelenbeck DJ, Spencer TA, Siegfried BD (2004) Cross-resistance of Cry1Ab-selected Ostrinia nubilalis (Lepidoptera: Crambidae) to Bacillus thuringiensis endotoxins. J Econ Entomol 97:1049–1057
Tabashnik BE (2008) Delaying insect resistance to transgenic crops. Proc Natl Acad Sci USA 105:19029–19030
Tabashnik BE, Cushing NL, Finson N, Johnson MW (1990) Field Development of Resistance to Bacillus thuringiensis in Diamondback Moth (Lepidoptera: Plutellidae). J Econ Entomol 83:1671–1676
Tang K, Fu DJ, Julien D, Braun A, Cantor CR, Koster H (1999) Chip–based genotyping by mass spectrometry. Proc Natl Acad Sci USA 96:10016–10020
Traut W (1977) A study of recombination, formation of chiasmata and synaptonemal complexes in female and male meiosis of Ephestia kuehniella (Lepidoptera). Genetica 47:135–142
Traut W, Marec F (1997) Sex chromosome differentiation in some species of Lepidoptera. Chromosome Res 5:283–291
Urban T, Ricci S, Grange JD, Lacave R, Boudghene F, Breittmayer F, Languille O, Roland J, Bernaudin JF (1993) Detetion of c-Ki-ras mutation by PCR/RFLP analysis and diagnosis of pancreatic adenocarcinomas. J Natl Cancer Institute 85:2008–2012
Vadlamudi RK, Ji TH, Bulla LA (1993) A specific binding protein from Manduca sexta for the insecticidal toxin of Bacillus thuringiensis ssp. berliner. J Biol Chem 268:12334–12340
van Rensburg JBJ (2007) First field report of field resistance by the stem borer, Busseola fusca (Fuller) to transgenic maize. S Afr J Plant Soil 24:147–151
Van Rie J, Jansens S, Hofte H, Degheele D, Van Mellaert H (1989) Specificity of Bacillus thuringiensis δ-endotoxins:importance of specific receptors on the brush border membrane of the midgut of target insects. Eur J Biochem 186:239–247
Vos P, Hogers R, Bleeker M, Reijans M, Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414
Williamson MS, Martinez-Torrez D, Hick CA, Devonshire AL (1996) Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol Gen Genet 252:51–60
Xie R, Zhuang M, Ross LS, Gomez I, Oltean DI, Bravo A, Soberon M, Gill SS (2005) Single amino acid mutations in the cadherin receptor from Heliothis virescens affect it toxin binding ability to Cry1A toxins. J Biol Chem 280:8416–8425
Xu L, Wang Z, Zhang J, He K, Ferry N, Gatehouse AMR (2010) Cross-resistance of Cry1Ab-selected Asian corn borer to other Cry toxins. J Appl Entomol 134:429–438
Yamamoto K, Narukawa J, Kadono-Okuda K, Nohata J, Sasanuma M, Suetsugu Y, Banno Y, Fujii H, Goldsmith MR, Mita K (2006) Construction of a single nucleotide polymorphism linkage map for the silkworm, Bombyx mori, based on bacterial artificial chromosome end sequences. Genetics 173:151–161
Zhang S, Cheng H, Gao Y, Wang G, Liang G, Wu K (2009) Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochem Mol Biol 39:421–429
Acknowledgments
This research was a joint contribution from the USDA, Agricultural Research Service (CRIS Project 3625-22000-017-00), the Iowa Agriculture and Home Economics Experiment Station, Ames, IA (Project 3543), and the University of Nebraska. Funding also was provided by a USDA, Biotechnology and Risk Assessment Grant (BRAG) “Quantifying risk factors for evolution of European corn borer resistance to Cry11F expressing corn hybrids: Contribution to a framework for managing insect resistance to transgenic crop” (2006-03697). This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by USDA, Iowa State University or the University of Nebraska for its use.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Coates, B.S., Sumerford, D.V., Lopez, M.D. et al. 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 (2011). https://doi.org/10.1007/s10709-011-9590-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-011-9590-0