Molecular Breeding

, Volume 5, Issue 1, pp 75–83 | Cite as

Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance

  • A. Nicholas E. Birch
  • Irene E. Geoghegan
  • Michael E.N. Majerus
  • James W. McNicol
  • Christine A. Hackett
  • Angharad M.R. Gatehouse
  • John A. Gatehouse


Transgenic crops genetically engineered for enhanced insect resistance should be compatible with other components of IPM for the pest resistance to be durable and effective. An experimental potato line was genetically engineered to express an anti-aphid plant protein (snowdrop lectin, GNA), and assessed for possible interactions of the insect resistance gene with a beneficial pest predator. These extended laboratory studies are the first to demonstrate adverse tri-trophic interactions involving a lectin- expressing transgenic crop, a target pest aphid and a beneficial aphidophagous predator. When adult 2-spot ladybirds (Adalia bipunctata[L.]) were fed for 12 days on peach-potato aphids (Myzus persicae Sulzer) colonising transgenic potatoes expressing GNA in leaves, ladybird fecundity, egg viability and longevity significantly decreased over the following 2–3 weeks. No acute toxicity due to the transgenic plants was observed, although female ladybird longevity was reduced by up to 51%. Adverse effects on ladybird reproduction, caused by eating peach-potato aphids from transgenic potatoes, were reversed after switching ladybirds to feeding on pea aphids from non-transgenic bean plants. These results demonstrate that expression of a lectin gene for insect resistance in a transgenic potato line can cause adverse effects to a predatory ladybird via aphids in its food chain. The significance of these potential ecological risks under field conditions need to be further evaluated.

Adalia bipunctata Myzus persicae snowdrop lectin (GNA) transgenic potato tri-trophic interactions 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Chrispeels M, Raikhel NV: Lectins, lectin genes and their role in plant defence. Plant Cell 3: 1–9 (1991).Google Scholar
  2. 2.
    Dogan EB, Berry RE, Rossignol PA: Biological parameters of convergent lady beetle feeding on aphids on transgenic potato. J Econ Ent 89: 1105–1108 (1996).Google Scholar
  3. 3.
    Down RE, Gatehouse AMR, Hamilton WDO, Gatehouse JA: Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulocorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials. J Insect Physiol 42: 1035–1045 (1996).Google Scholar
  4. 4.
    Estruch JJ, Carozzi NB, Desai N, Duck NB, Warren GW, Koziel MG: Transgenic plants: An emerging approach to pest control. Nature Biotechnol 15: 137–141 (1997).Google Scholar
  5. 5.
    Gatehouse AMR, Davison GM, Newell CA, Merryweather A, Hamilton WDO, Burgess EPJ, Gilbert RJC, Gatehouse JA: Transgenic potato plants with enhanced resistance to the potato moth, Laconobia oleracea: growth room trials. Mol Breed 3: 49–63 (1997).Google Scholar
  6. 6.
    Gatehouse AMR, Down RE, Powell KS, Sauvion N, Rahbé Y, Newell CA, Merryweather A, Hamilton WDO, Gatehouse JA: Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae. Entomol Exp Appl 79: 295–307 (1996).Google Scholar
  7. 7.
    Gatehouse AMR, Powell KS, Van Damme EJM, Peumans WJ, Gatehouse JA: Insecticidal properties of lectins: their potential in plant protection. In: Pusztai AJ, & Bardocz S (eds) Lectins: Biomedical Perspectives, pp. 35–57. Taylor & Francis, Hants, UK (1995).Google Scholar
  8. 8.
    Hilbeck A, Baumgartner M, Fried PM, Bigler F: Effects of transgenic Bacillus thuringiensis-fed prey onmortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae). J Environ Entomol 27 (2): 480–487 (1998).Google Scholar
  9. 9.
    Hilder VA, Powell KS, Gatehouse AMR, Gatehouse JA, Shi Y, Hamilton WDO, Merryweather A, Newell CA, Timans JC, Peumans WJ, Van Damme E, Boulter D: Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgen Res 4: 18–25 (1995).Google Scholar
  10. 10.
    Hodek I: Habitat and food specificity in aphidophagous predators. Biocontrol Sci Technol 3: 91–100 (1993).Google Scholar
  11. 11.
    Mascarenhas VJ, Luttrell RG: Combined effect of sublethal exposure to cotton expressing the endotoxin protein of Bacillus thuringiensis and natural enemies on survival of bollworm (Lepidoptera: Noctuidae) larvae. Environ Entomol 26: 939–945 (1997).Google Scholar
  12. 12.
    Peumans WJ, Van Damme EJM: Lectins as plant defense proteins. Plant Physiol 109: 347–352 (1995).Google Scholar
  13. 13.
    Powell KS, Gatehouse AMR, Hilder VA, Gatehouse JA: 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: 119–126 (1993).Google Scholar
  14. 14.
    Rahbé Y, Febvay G: Protein toxicity to aphids: an in vitro test on Acyrthosiphon pisum. Entomol Exp Appl 67: 149–160 (1993).Google Scholar
  15. 15.
    Rahbé Y, Sauvion N, Febvay G, Peumans WJ, Gatehouse AMG: Toxicity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 76: 143–155 (1995).Google Scholar
  16. 16.
    Sauvion N: Effects and mechanisms of toxicity of two lectins of the glucose/ mannose group towards the pea aphid, Acyrthosiphon pisum (Harris) Ph.D. thesis, University of Lyon, 196 pp. (1995).Google Scholar
  17. 17.
    Sauvion N, Rahbé Y, Peumans WJ, Van Damme EJM, Gatehouse JA, Gatehouse AMR: Effects of GNA and other mannose binding lectins on development and fecundity of the peach-potato aphid Myzus persicae. Entomol Exp Appl 79: 285–293 (1996).Google Scholar
  18. 18.
    Shi Y, Wang MB, Powell KS, Van Damme E, Hilder VA, Gatehouse AMR, Boulter D, Gatehouse JA: Use of rice sucrose synthase-1 promoter to direct phloem-specific expression of ß-glucuronidase and snowdrop lectin genes in transgenic tobacco plants. J Expt Bot 45: 623–631 (1994).Google Scholar
  19. 19.
    Tang J, Gilboa S, Roush RT, Shelton AM: Inheritance, stability and lack of fitness costs of selected resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae) from Florida. J Econ Entomol 90: 732–741 (1997).Google Scholar
  20. 20.
    Van Damme EJM, De Clerq N, Claessens F, Hemschoote K, Peeters B, Peumans WJ: Molecular cloning and characterisation of multiple isoforms of the snowdrop (Galanthus nivalis) lectin. Planta 186: 35–43 (1991).Google Scholar
  21. 21.
    Waage J: What does biotechnology bring to integrated pest management? Biotech Dev Monitor 32: 19–21 (1997).Google Scholar
  22. 22.
    Woodford JAT, Gordon SC, Foster GN: Side-band application of systemic granular pesticides for the control of aphids and potato leafroll virus. Crop Prot 7: 96–105 (1988).Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • A. Nicholas E. Birch
    • 1
  • Irene E. Geoghegan
    • 1
  • Michael E.N. Majerus
    • 2
  • James W. McNicol
    • 3
  • Christine A. Hackett
    • 3
  • Angharad M.R. Gatehouse
    • 4
  • John A. Gatehouse
    • 4
  1. 1.Scottish Crop Research InstituteInvergowrie, DundeeUK
  2. 2.Department of GeneticsUniversity of CambridgeCambridgeUK
  3. 3.Biomathematics and Statistics ScotlandInvergowrie, DundeeUK
  4. 4.Department of Biological SciencesUniversity of DurhamDurhamUK

Personalised recommendations