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EC-sponsored Research on Safety of Genetically Modified Organisms - A Review of Results
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image Environmental impact of transgenic plants on beneficial insects

Background and objectives

Crop protection plays a vital and integral role in modern-day agricultural production. At present, crop protection against insect and nematode pests in agricultural systems relies almost exclusively on the use of agrochemicals. Genetic engineering offers the plant breeder the opportunity not only to use a large "gene pool" of pest resistance genes, but also to significantly shorten the time period involved in the breeding of resistant crops.

This project concerns research on the environmental impact of transgenic crop plants on beneficial insects e.g. pollinating insects or the natural enemies of pest insects. Biological control using parasitoid insects represents an important aspect of integrated pest management strategies, and pollinating insects play a major role for seed production and fruit set of many crops. Thus, it is crucial to evaluate the effects of the introduction of engineered plants on the parasitoid/host complex and on the pollinating insect/plant interactions. In this project we investigate the effects of transgenic crop plants or of gene products on the different steps involved in host or plant recognition by beneficial insects.


Proteinase inhibitors are not expressed in nectars, resulting in normal foraging behaviour of honeybees on transformed oilseed rape flowers.   Proteinase inhibitors are not expressed in nectars, resulting in normal foraging behaviour of honeybees on transformed oilseed rape flowers.
     
Olfactory learning of honeybees tested under laboratory conditions is not affected by proteinase inhibitors at doses expressed in transformed plants.   Olfactory learning of honeybees tested under laboratory conditions is not affected by proteinase inhibitors at doses expressed in transformed plants.
     
Long-term exposure to proteinase inhibitors at doses expressed in transformed plants does not affect the foraging activity of honeybee hives.   Long-term exposure to proteinase inhibitors at doses expressed in transformed plants does not affect the foraging activity of honeybee hives.
     
GNA accumulation in aphids is not accutely toxic to ladybirds, a natural enemy of aphids.   GNA accumulation in aphids is not accutely toxic to ladybirds, a natural enemy of aphids.
     
GNA accumulating in tomato moth larvae does not prevent successful parasitism by a natural enemy, the parasitic wasp Eulophus pennicornis.   GNA accumulating in tomato moth larvae does not prevent successful parasitism by a natural enemy, the parasitic wasp Eulophus pennicornis.


Approach and methodology

We began by investigating the multiplication of selected transgenic and control plants, including a quantitative determination of transgene products, specifically in plant tissues in contact with beneficial insects. We also developed the production of purified recombinant proteins for bioassays, the chemical characterisation of nutritionally related and secondary metabolites of transformed and control plants, and measured the short-term and long-term effects of gene product ingestion on the behaviour, digestive physiology and development of beneficial insects.

This involved the investigation of the accumulation of gene products in pest insects, determination of the dynamics of gene product accumulation associated with beneficial insects, specifically in the honeybee hive, and the population dynamics of parasitoids and predators.

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Main findings and outcome

Genetically modified seeds and plants were produced and partially characterised. The evaluation protocols and methodologies for plants secretion analyses and insect studies were established.

We evaluated the long-term effects of foreign proteins on honeybees using chronic toxicity tests, study of the learning abilities and study of the accumulation of foreign proteins in the hive. Our experiments included chemical analyses of plant nectars, analyses of volatiles in transformed and controlled oilseed rape and potato plants, and honeybee recognition of such volatiles. In addition, we performed biochemical analyses of bumblebees’ digestive proteinases. Behavioural experiments on honeybees were performed and the results used for modelling.

Our studies of the effect of transgenic plants on parasitoids included the study of the major proteolytic enzymes in larvae of parasitoid wasps, the accumulation of transgene products in preys or hosts of predators and parasitoids, and the effects of pesticidal toxins on predators.
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Conclusions

To date, no acute toxicity of insecticidal proteins towards beneficial insects has been observed either when expressed in plants or when incorporated into artificial diets at levels found in the leaves of transformed plants. However, when incorporated into diets at concentration orders of magnitude higher than expressed in GM plants, and under extreme laboratory conditions, some significant effects were observed on insect behaviour and physiology.

Work is still required to validate these bio-assays under more natural conditions.
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  Bioassay of control and GNA-expressing potato plants against larvae of Lacanobia oleracea (tomato moth). Control plant (LHS) showing severe levels of damage; transgenic plant showing significantly reduced levels of damage. image Bioassay of control and GNA-expressing potato plants against larvae of Lacanobia oleracea (tomato moth). Control plant (LHS) showing severe levels of damage; transgenic plant showing significantly reduced levels of damage.
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  Larvae of Lacanobia oleracea image Larvae of Lacanobia oleracea (tomato moth) being parasitised by larvae of the ectoparasitoid wasp Eulophus pennicornis.
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  Identification of the proteolytic activities of fourth-instar larval image  
 
Identification of the proteolytic activities of fourth-instar larval (lanes 1,3, and 5; approx. 25 µg protein lane-1) and adult (lanes 2,4, and 6; approx. 13 µg protein lane-1) midgut extracts in polyacrylamide gels containing azocasein. Gel slices 1 to 3 from left to right: slice 1 was incubated in 50 mM MES buffer (pH 6.0) containing 1 mM DTT, whereas slices 2 and 3 were incubated in buffer containing 20 µM E-64 and 20 µM E-64 + 10 mM EDTA. The pre-stained molecular weight markers were phosphorylase B (Mr 104,000), bovine serum albumin (Mr 82,000), ovalbumin (Mr 48,300), carbonic anhydrase (Mr 33,400), soybean trypsin inhibitor (Mr 28,000) and lysozyme (Mr 19,400).

 

Major publications

Agelopoulos N., Hooper A., Maniar S., Pickett J., Wadhams L., “A novel approach for the isolation of volatile chemicals released by individual leaves of a plant in situ”.
J. Chem. Ecol., 25, 1999, pp. 1411-1425.

Bell H.A., Fitches E.C., Down R.E., Marris G.C., Edwards J.P., Gatehouse J.A., Gatehouse A.M.R., “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)”.
J. Insect Physiol., 45, 1999, pp. 983-991.

Down R.E., Ford L., Mosson H.J., Fitches E.C., Gatehouse J.A., Gatehouse A.M.R., “Protease activity in the larval stage of the parasitoid wasp, Eulophus pennicornis (Nees) (Hymenoptera: Eulophidae): effects of protease inhibitors”.
Parasitology, 119, 1999, pp. 157-166.

Pham-Delègue M.H., Girard C., Le Métayer M., Sandoz G., Picard-Nizou A.L., Hennequet C., Pons O., Jouanin L., “Long-term effects of soybean proteinase inhibitors on digestive enzymes, survival and learning abilities of honeybees”.
Entomol. Exp. Applic., 92, 2000, pp. 21-29.

Walker A.J., Ford L., Majerus M.E.N., Geoghegan I.E., Birch A.N.E., Gatehouse J.A., Gatehouse A.M.R., “Characterisation of the proteolytic activity in larval midgut of two-spot ladybird (Adalia bipunctata L.)”.
Insect. Biochem., Mol. Biol., 28, 1998, pp. 173-180.
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imageResearch project
 

Contract number
BIO4-CT96-0365

Period
October 1996 – September 1999

Coordinator
M-H. Pham-Delègue
INRA
Bures-sur-Yvette (FR)

 
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Partners


L.J. Wadhams
Institute of Arable Crop Research
Harpenden (UK)

A.M.R. Gatehouse
University of Newcastle (UK)

A. Toppan
Rustica Prograin Génétique
Mondonville (FR)

J-L. Deneubourg
Université Libre de Bruxelles (BE)

 
 
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