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Effects of Galanthus nivalis agglutinin (GNA) expressed in tomato leaves on larvae of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and the effect of GNA on the development of the endoparasitoid Meteorus gyrator (Hymenoptera: Braconidae)

  • M.E. Wakefield (a1), H.A. Bell (a1), E.C. Fitches (a1), J.P. Edwards (a1) and A.M.R. Gatehouse (a2)...


The effect of ingestion of transgenic tomato leaves expressing the plant lectin Galanthus nivalis agglutinin (GNA) on development of larvae of Lacanobia oleracea (Linnaeus) was studied under laboratory conditions. When L. oleracea larvae were fed on tomato line 14.1H, expressing approximately 2.0% GNA, significant increases in the mean larval weight and in the amount of food consumed were found. This resulted in an overall reduction in the mean development time to the pupal stage of approximately 7 days. A significant increase in the percentage survival to the adult moth was also recorded when newly hatched larvae were reared on transgenic tomato leaves (72%) compared to larvae reared on untransformed leaves (40%). The effects of ingestion of GNA by L. oleracea larvae, via artificial diet or the leaves of transgenic tomato or potato plants, on the subsequent development of its solitary endoparasitoid Meteorus gyrator (Thunberg) was also studied. No significant effects on the life cycle parameters of M. gyrator developing in L. oleracea fed on GNA-containing diets were observed. Experiments with transgenic potato plants indicated that the stadium of the host larvae at parasitism had a greater influence on M. gyrator development than the presence of GNA. Potential GNA-binding glycoproteins were detected in the gut and body tissues of larval M. gyrator. Despite detection in host tissues, GNA could not be detected in adult M. gyrator and therefore it is likely that at the time of pupation M. gyrator are able to void the GNA in the meconial pellet.


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Bell, H.A., Fitches, E.C., Down, R.E., Marris, G.C., Edwards, J.P., Gatehouse, J.A. & Gatehouse, A.M.R. (1999) The effect of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on Eulophus pennicornis (Hymenoptera: Eulophidae), a parasitoid of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae). Journal of Insect Physiology 45, 983991.
Bell, H.A., Marris, G.C., Bell, J. & Edwards, J.P. (2000) The biology of Meteorus gyrator (Hymenoptera: Braconidae), a solitary endoparasitoid of the tomato moth, Lacanobia oleracea (Lepidoptera: Noctuidae). Bulletin of Entomological Research 90, 299308.
Bell, H.A., Fitches, E.C., Marris, G.C., Bell, J., Edwards, J.P., Gatehouse, J.A. & Gatehouse, A.M.R. (2001a) Transgenic GNA-expressing potato plants augment the beneficial biocontrol of Lacanobia oleracea (Lepidoptera; Noctuidae) by the parasitoid Eulophus pennicornis (Hymenoptera; Eulophidae). Transgenic Research 10, 3542.
Bell, H.A., Fitches, E.C., Down, R.E., Ford, L., Marris, G.C., Edwards, J.P., Gatehouse, J.A. & Gatehouse, A.M.R. (2001b) Effect of dietary cowpea trypsin inhibitor (CpTI) on the growth and development of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and on the success of the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Pest Management Science 57, 5765.
Bell, H.A., Down, R.E., Fitches, E.C., Edwards, J.P. & Gatehouse, A.M.R. (2003a) Impact of genetically modified potato expressing plant-derived resistance genes on the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae). Biocontrol Science and Technology 13, 729741.
Bell, H.A., Marris, G.C., Smethurst, F. & Edwards, J.P. (2003b) The effect of host stage and temperature on selected developmental parameters of the solitary endoparasitoid Meteorus gyrator (Thun.) (Hym., Braconidae). Journal of Applied Entomology 127, 332339.
Bell, H.A., Kirkbride-Smith, A.E., Marris, G.C., Edwards, J.P. & Gatehouse, A.M.R. (2004) Oral toxicity and impact on fecundity of three insecticidal proteins on the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Agricultural and Forest Entomology 6, 215222.
Birch, A.N.E., Geoghegan, I.E., Majerus, M., McNicol, J.W., Hackett, C., Gatehouse, A.M.R. & Gatehouse, J.A. (1999) Ecological impact on predatory 2-spot ladybirds of transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding 5, 7583.
Cellini, F., Chesson, A., Colquhoun, I., Constable, A., Davies, H.V., Engel, K.H., Gatehouse, A.M.R., Kärenlampi, S., Kok, E.J., Leguay, J.-J., Lehesranta, S., Noteborn, H.P.J.M., Pedersen, J. & Smith, M. (2004) Unintended effects and their detection in genetically modified crops. Food and Chemical Toxicology 42, 10891125.
Corbitt, T.S., Bryning, G., Olieff, S. & Edwards, J.P. (1996) Reproductive, developmental and nutritional biology of the tomato moth, Lacanobia oleracea (Lepidoptera: Noctuidae) reared on artificial diet. Bulletin of Entomological Research 86, 647657.
Couty, A., De la Viña, G., Clark, S.J., Kaiser, L., Pham-Delegue, M.H., Poppy, G.M. (2001a) Direct and indirect sublethal effects of Galanthus nivalis agglutinin (GNA) on the development of a potato-aphid parasitoid, Aphelinus abdominalis (Hymenoptera: Aphelinidae). Journal of Insect Physiology 47, 553561.
Couty, A., Down, R.E., Gatehouse, A.M.R., Kaiser, L., Pham-Delegue, M.H. & Poppy, G.M. (2001b) Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae). Journal of Insect Physiology 47, 13571366.
De Leo, F., Bonadé-Bottino, M.A., Ceci, L.R., Gallerani, R. & Jouanin, L. (1998) Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiology 118, 9971004.
Down, R.E., Gatehouse, A.M.R., Hamilton, W.D.O. & Gatehouse, J.A. (1996) Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants in laboratory and glasshouse trials. Journal of Insect Physiology 42, 10351045.
Down, R.E., Ford, L., Woodhouse, S.E., Raemaekers, R.J.M., Leitch, B., Gatehouse, J.A. & Gatehouse, A.M.R. (2000) Snowdrop lectin (GNA) has no acute toxic effects on a beneficial predator, the 2-spot ladybird (Adalia bipunctata L.). Journal of Insect Physiology 46, 379391.
Dutton, A., Romeis, J. & Bigler, F. (2003) Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: BT-maize expressing Cry1Ab as a case study. Biocontrol 48, 611636.
Fitches, E., Gatehouse, A.M.R. & Gatehouse, J.A. (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. Journal of Insect Physiology 43, 727739.
Fitches, E., Woodhouse, S., Edwards, J.P. & Gatehouse, J.A. (2001) In vitro and in vivo binding of snowdrop (Galanthus nivalis agglutinin; GNA) and jackbean (Canavalia ensiformis; Con A) lectins within Lacanobia oleracea larvae; mechanisms of insecticidal action. Journal of Insect Physiology 47, 777787.
Fossiac, X., Loc, N.T., Christou, P., Gatehouse, A.M.R. & Gatehouse, J.A. (2000) Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA). Journal of Insect Physiology 46, 573583.
Gatehouse, A.M.R., Down, R.E., Powell, K.S., Newell, C.A., Hamilton, W.D.O. & Gatehouse, J.A. (1996) Transgenic potato plants with enhanced resistance to the peach–potato aphid Myzus persicae. Entomologia Experimentalis et Applicata 79, 295307.
Gatehouse, A.M.R., Davison, G.M., Newell, C.A., Merryweather, A., Hamilton, W.D.O., Burgess, E.P.J., Gilbert, R.J.C. & Gatehouse, J.A. (1997) Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Molecular Breeding 3, 4963.
Lloyd, L. (1920) The habits of the glasshouse tomato moth Hadena (Polia) oleracea and its control. Annals of Applied Biology 7, 66102.
Longstaff, M., Powell, K.S., Gatehouse, J.A., Raemaekers, R., Newell, C.A. & Hamilton, W.D.O. (1998) Production and purification of active snowdrop lectin in Escherichia coli. European Journal of Biochemistry 252, 5965.
Poitout, S. & Bues, R. (1974) Elevage des chenilles de vingt-huit espéces de lépidopteres Noctuidae et de deux espéces d'Arctiidae sur milieu artificiel simple. Particularities de l'elevage selon les espéces. Annales de Zoologie Ecologie Animale 6, 431441.
Poppy, G.M. & Sutherland, J.P. (2004) Can biological control benefit from genetically-modified crops? Tritrophic interactions on insect-resistant transgenic plants. Physiological Entomology 29, 257268.
Powell, K.S., Gatehouse, A.M.R., Hilder, V.A. & Gatehouse, J.A. (1993) Antimetabolic effects of plant lectins and plant and fungal enzymes on the nymphal stages of two important rice pests, Nilaparvata lugens and Nephotettix cincticeps. Entomologia Experimentalis et Applicata 66, 119126.
Raemaekers, R.J., de Muro, L., Gatehouse, J.A., Fordham-Skelton, A.P. (1999) Functional phytohaemagglutinin (PHA) and Galanthus nivalis agglutinin (GNA) expressed in Pichia pastoris. European Journal of Biochemistry 265, 395403.
Rao, K.V., Rathore, K.S., Hodges, T.K., Fu, X., Stoger, E., Sudhakar, D., Williams, S., Christou, P., Bharathi, M., Bown, D.P., Powell, K.S., Spence, J., Gatehouse, A.M.R. & Gatehouse, J.A. (1998) Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant Journal 15, 469477.
Romeis, J., Brabendreier, D., Wäckers, F.L. (2003) Consumption of snowdrop lectin (Galanthus nivalis agglutinin) causes direct effects on adult parasitic wasps. Oecologia 134, 528536.
Sétamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E., Legaspi, B.C. Jr. (2002a) Evaluation of lectin-expessing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): effects on life history parameters. Journal of Economic Entomology 95, 469477.
Sétamou, M., Bernal, J.S., Legaspi, J.C. & Mirkov, T.E. (2002b) Effects of snowdrop lectin (Galanthus nivalis agglutinin) expressed in transgenic sugarcane on fitness of Cotesia flavipes (Hymenoptera: Braconidae), a parasitoid of the nontarget pest Diatraea saccharalis (Lepidoptera: Crambidae). Annals of the Entomological Society of America 95, 7583.
Tomov, B.V. & Bernal, J.S. (2003) Effects of GNA transgenic sugarcane on life history parameters of Parallorhogas pyralophagus (Marsh) (Hymenoptera: Braconidae), a parasitoid of Mexican rice borer. Journal of Economic Entomology 96, 570576.
Tomov, B.V., Bernal, J.S. & Vinson, S.B. (2003) Impacts of transgenic sugarcane expressing GNA lectin on parasitism of Mexican rice borer by Parallorhogas pyralophagus (Marsh) (Hymenoptera: Braconidae). Environmental Entomology 32, 866872.



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