Skip to main content
Log in

A QTL that enhances and broadens Bt insect resistance in soybean

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Effective strategies are needed to manage insect resistance to Bacillus thuringiensis (Bt) proteins expressed in transgenic crops. To evaluate a multiple resistance gene pyramiding strategy, eight soybean (Glycine max) lines possessing factorial combinations of two quantitative trait loci (QTLs) from plant introduction (PI) 229358 and a synthetic Bt cry1Ac gene were developed using marker-assisted selection with simple sequence repeat markers. Field studies were conducted in 2000 and 2001 to evaluate resistance to corn earworm (Helicoverpa zea) and soybean looper (Pseudoplusia includens), and detached leaf bioassays were used to test antibiosis resistance to Bt-resistant and Bt-susceptible strains of tobacco budworm (TBW; Heliothis virescens). Based on defoliation in the field and larval weight gain on detached leaves, lines carrying a combination of cry1Ac and the PI 229358 allele at a QTL on linkage group M were significantly more resistant to the lepidopteran pests, including the Bt-resistant TBW strain, than were the other lines. This is the first report of a complementary additive effect between a Bt transgene and a plant insect resistance QTL with an uncharacterized mode of action that was introgressed using marker-assisted selection.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adamczyk JJ, Adams LC, Hardee DD (2001) Field efficacy and seasonal expression profiles for terminal leaves of single and double Bacillus thuringiensis toxin cotton genotypes. J Econ Entomol 94:1589–1593

    CAS  PubMed  Google Scholar 

  • Ashfaq M, Young SY, McNew RW (2001) Larval mortality and development of Pseudoplusia includens (Lepidoptera: Noctuidae) reared on a transgenic Bacillus thuringiensis -cotton cultivar expressing Cry1Ac insecticidal protein. J Econ Entomol 94:1053–1058

    CAS  PubMed  Google Scholar 

  • Bell JV (1978) Development and mortality in bollworms fed resistant and susceptible soybean cultivars treated with Nomuraea riley and Bacillus thuringiensis. J Ga Entomol Soc 13:50–55

    Google Scholar 

  • Boethel DJ (1999) Assessment of soybean germplasm for multiple insect resistance. In: Clement SL, Quisenbury SS (eds) Global plant genetic resources for insect resistant crops. CRC, Boca Raton, pp 101–129

  • Caprio MA (1994) Bacillus thuringiensis gene development and resistance management in single- and multi-tactic environments. Biocontrol Sci Technol 4:487–497

    Google Scholar 

  • Coombs JL, Douches DS, Li W, Grafius EJ, Pett WA (2002) Combining engineered (Bt-cry3A) and natural resistance mechanisms in potato for control of Colorado potato beetle. J Am Soc Hortic Sci 127:62–68

    CAS  Google Scholar 

  • Cregan PB, Jarvik T, Bush AL, Shoemaker RC, Lark KG, Kahler AL, Kaya N, VanToai TT, Lohnes DG, Chung J, Specht JE (1999) An integrated genetic linkage map of the soybean genome. Crop Sci 39:1464–1490

    CAS  Google Scholar 

  • Douches DS, Kisha TJ, Coombs JJ, Li W, Pett WL, Grafius EJ (2001) Effectiveness of natural and engineered host plant resistance in potato to the Colorado potato beetle. Hortic Sci 36:967–970

    Google Scholar 

  • Fehr WE, Caviness CE, Burmood DT, Pennington JS (1971) Stages of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931

    Google Scholar 

  • Frutos R, Rang C, Royer M (1999) Managing insect resistance to plants producing Bacillus thuringiensis toxins. Crit Rev Biotechnol 19:227–276

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Giustolin TA, Vendramim JD, Alves SB, Viera SA, Pereira RM (2001) Susceptibility of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) reared on two species of Lycopersicon to Bacillus thuringiensis var. kurstaki. J Appl Entomol 125:551–556

    Article  Google Scholar 

  • Gore J, Leonard BR, Adamczyk JJ (2001) Bollworm (Lepidoptera: Noctuidae) survival on ‘Bollgard’ and ‘Bollgard II’ cotton flower bud and flower components. J Econ Entomol 94:1445–1451

    CAS  PubMed  Google Scholar 

  • Gould F (1988a) Evolutionary biology and genetically engineered crops. BioSience 38:26–33

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gould F, Anderson A, Reynolds A, Bumgarner L, Moar W (1995) Selection and genetic analysis of a Heliothis virescens (Lepidoptera: Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. J Econ Entomol 88:1545–1559

    CAS  Google Scholar 

  • Hammond RB, Bierman P, Levine E, Cooper RL (2001) Field resistance of two soybean germplasm lines, HC95-15MB and HC95-24MB, against bean leaf beetle (Coleoptera: Chrysomelidae), western corn rootworm (Coleoptera: Chrysomelidae), and Japanese beetles (Coleoptera: Scarabidae) J Econ Entomol 94:1594–1601

    Google Scholar 

  • Kilen TC, Lambert L (1986) Evidence for different genes controlling insect resistance in three soybean genotypes. Crop Sci 26:869–871

    Google Scholar 

  • Kilen TC, Hatchett JH, Hartwig EE (1977) Evaluation of early generation soybeans for resistance to soybean looper. Crop Sci 17:397–398

    Google Scholar 

  • Kogan M, Ortman EE (1978) Antixenosis: a new term proposed to replace Painter’s ‘nonpreference’ modality of resistance. Bull Entomol Soc Am 24:175–176

    Google Scholar 

  • Lambert L, Kilen TC (1984) Multiple insect resistance in several soybean genotypes. Crop Sci 24:887–890

    Google Scholar 

  • Lambert L, Tyler J (1999) Appraisal of insect-resistant soybeans. In: Webster JA, Wiseman BR (eds) Economic, environmental, and social benefits of insect resistance in field crops. Thomas Say, Lanham, pp 131–148

  • Li Z, Wilson RF, Rayford WE, Boerma HR (2002) Molecular mapping genes conditioning reduced palmitic acid content in N87-2122-4 soybean. Crop Sci 42:373–378

    CAS  Google Scholar 

  • MacIntosh SC, Stone TB, Sims SR, Hunst PL, Greenplate JT, Marrone PG, Perlak FJ, Fischhoff DA, Fuchs RL (1990) Specificity and efficacy of purified Bacillus thuringiensis against agronomically important pests. J Invert Pathol 56:258–266

    CAS  Google Scholar 

  • Maqbool SB, Riazuddin S, Loc NT, Gatehouse AMR, Gatehouse JA, Christou P (2001) Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Mol Breed 7:85–93

    Article  CAS  Google Scholar 

  • Mascarenhas RN, Boethel DJ (1997) Responses of field-collected strains of soybean looper (Lepidoptera: Noctuidae) to selected insecticides using and artificial diet overlay bioassay. J Econ Entomol 90:1117–1124

    CAS  Google Scholar 

  • McGaughey WH, Whalon ME (1992) Managing insect resistance to Bacillus thuringiensis toxins. Science 258:1451–1455

    CAS  Google Scholar 

  • McGaughey WH, Gould F, Gelernter W (1998) Bt resistance management. Nat Biotechnol 16:144–146

    CAS  PubMed  Google Scholar 

  • McIntosh MS (1983) Analysis of combined experiments. Agron J 75:153–155

    Google Scholar 

  • Meade T, Hare JD (1994) Effects of genetic and environmental host plant variation on the susceptibility of two noctuids to Bacillis thuringiensis. Entomol Exp Appl 70:165–178

    Google Scholar 

  • Meade T, Hare JD (1995) Integration of host plant resistance and Bacillus thuringiensis insecticides in the management of lepidopterous pests of celery. J Econ Entomol 88:1787–1794

    Google Scholar 

  • Narvel JM, Walker DR, Rector BG, All JN, Parrott WA, Boerma HR (2001) A retrospective DNA marker assessment of the development of insect resistant soybean. Crop Sci 41:1931–1939

    CAS  Google Scholar 

  • Painter RH (1951) Insect resistance in crop plants. Macmillan, New York

  • Rector BG, All JN, Parrott WA, Boerma HR (1998) Identification of molecular markers linked to quantitative trait loci for soybean resistance to corn earworm. Theor Appl Genet 96:786–790

    Article  CAS  Google Scholar 

  • Rector BG, All JN, Parrott WA, Boerma HR (1999) Quantitative trait loci for antixenosis resistance to corn earworm in soybean. Crop Sci 39:531–538

    Google Scholar 

  • Rector BG, All JN, Parrott WA, Boerma HR (2000) Quantitative trait loci for antibiosis resistance to corn earworm in soybean. Crop Sci 40:233–238

    Google Scholar 

  • Roush RT (1996) Can we slow adaptation by pests to insect transgenic crops? In: Persley GJ (ed) Biotechnology and integrated pest management. CAB International, Wallingford, pp 242–263

  • Roush R (1997) Managing insect resistance to transgenic crops. In: Carozzi N, Koziel M (eds) Advances in insect control: the role of transgenic plants. Taylor and Francis, London, pp 513–541

  • Sachs ES, Bendict JH, Taylor JF, Stelly DM, Davis SK, Altman DW (1996) Pyramiding CryIA(b) insecticidal protein and terpenoids in cotton to resist tobacco budworm (Lepidoptera: Noctuidae). Environ Entomol 25:1257–1266

    CAS  Google Scholar 

  • Santos MO, Adang MJ, All JN, Boerma HR, Parrott WA (1996) Testing transgenes for insect resistance using Arabidopsis. Mol Breed 3:183–194

    Article  Google Scholar 

  • Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill, New York, pp 233–237

    Google Scholar 

  • Stewart CN Jr, Adang MJ, All JN, Boerma HR, Cardineau G, Tucker D, Parrott WA (1996) Genetic transformation, recovery and characterization of fertile soybean transgenic for a synthetic Bacillus thuringiensis cryIAc transgene. Plant Physiol 112:121–129

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • US Environmental Protection Agency (2000) Bt plant-pesticides biopesticides registration action document-insect resistance management. Environmental Protection Agency, Washington, DC http://www.epa.gov/oscpmont/sap/2000/october/brad4_irm.pdf

  • Walker DR, All JN, McPherson RM, Boerma HR, Parrott WA (2000) Field evaluation of soybean engineered with a synthetic cry1Ac transgene for resistance to corn earworm, soybean looper, and velvetbean caterpillar (Lepidoptera: Noctuidae), and lesser cornstalk borer (Lepidoptera: Pyralidae). J Econ Entomol 93:613–622

    CAS  PubMed  Google Scholar 

  • Walker DR, Boerma HR, All JN, Parrott WA (2002) Combining cry1Ac with QTL alleles from PI 229358 to improve soybean resistance to lepidopteran pests. Mol Breed 9:38–51

    Article  Google Scholar 

  • Wiseman BR, Davis FM, Campbell JE (1980) Mechanical infestation device used in fall armyworm plant resistance programs. Fla Entomol 63:425–438

    Google Scholar 

  • Zhao J-Z, Cao J, Li Y, Collins HL, Roush RT, Earle ED, Shelton AM (2003) Transgenic plants expressing two Bacillus thurinigiensis toxins delay insect resistance evolution. Nat Biotechnol 21:1493–1497

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Fred Gould of North Carolina State University, Raleigh, N.C., USA, for furnishing the tobacco budworm eggs, and Kurk Lance, Dale Wood, Gina Rowan, Earl Baxter, and Erin Leggett for assistance with the field, greenhouse, and laboratory studies. This work was funded through the USDA National Research Initiative Competitive Grants Program (Grant no. 9801149).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wayne A. Parrott.

Additional information

Communicated by J. Snape

Rights and permissions

Reprints and permissions

About this article

Cite this article

Walker, D.R., Narvel, J.M., Boerma, H.R. et al. A QTL that enhances and broadens Bt insect resistance in soybean. Theor Appl Genet 109, 1051–1057 (2004). https://doi.org/10.1007/s00122-004-1714-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1714-9

Keywords

Navigation