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Transgene products in honeydew: estimating risks for non-target insects

Petronella Alida Maria Hogervorst

Published 2006 in Unknown venue

ABSTRACT

Plants genetically modified to express Galanthus nivalis agglutinin (GNA) have been found to confer partial resistance to homopteran pests. Laboratory experiments were conducted to investigate direct effects of GNA on larvae of three species of aphid predators that differ in their feeding and digestive physiology, i.e. Chrysoperla carnea, Adalia bipunctata and Coccinella septempunctata. Longevity of all three predator species was directly affected by GNA, when they were fed a sucrose solution containing 1% GNA. However, a difference in sensitivity towards GNA was observed when comparing the first and last larval stage of the three species. In vitro studies revealed that gut enzymes from none of the three species were able to break down GNA. In vivo feed-chase studies demonstrated accumulation of GNA in the larvae. After the larvae had been transferred to a diet devoid of GNA, the protein stayed present in the body of C. carnea, but decreased over time in both ladybirds. Binding studies showed that GNA binds to glycoproteins that can be found in the guts of larvae of all three predator species. Immunoassay by Western blotting of haemolymph samples only occasionally showed the presence of GNA. Fluorescence microscopy confirmed GNA accumulation in the midgut of C. carnea larvae. Implications of these findings for non-target risk assessment of GNA-transgenic crops are discussed. 1 Based on: Hogervorst P.A.M., Ferry N., Gatehouse A.M.R., Wäckers F.L. and Romeis J., 2006. Direct effects of snowdrop lectin (GNA) on larvae of three aphid predators and fate of GNA after ingestion. Journal of Insect Physiology 52: 614-624 GNA effects on predator larvae 19 Introduction Insect-resistant transgenic crops expressing cry genes from the soil bacterium Bacillus thuringiensis (Bt) have been grown commercially since 1996 (Shelton et al. 2002). However, many other insecticidal proteins, including endogenous plant defence proteins have been studied for expression in transgenic plants. One of the most widely studied is snowdrop lectin (Galanthus nivalis agglutinin; GNA). The particular interest in this protein is based on the fact that it acts on sap-sucking insects; pest species that are not targeted by the known Bt-toxins. GNA delivered in artificial diet has been shown to result in reduced performance of homopteran pests belonging to the Aphididae (Rahbé et al. 1995, Sauvion et al. 1996), Cicadellidae and Delphacidae (Powell et al. 1993, 1995, 1998, Powell 2001). Partial resistance to homopteran pests has been achieved in several crop plants as a result of having been genetically modified to express GNA. These include tobacco (Hilder et al. 1995, Yuan et al. 2001), potato (Down et al. 1996, Gatehouse et al. 1996), rice (Rao et al. 1998, Foissac et al. 2000, Sun et al. 2002, Wu et al. 2002), and wheat (Stoger et al. 1999). In addition to effects on sap-sucking pests, insecticidal effects of GNA were also found to extend to lepidopteran pests (Fitches et al. 1997, Gatehouse et al. 1997, Fitches and Gatehouse 1998, Sétamou et al. 2002b, 2003) and a coleopteran herbivore (Nutt et al. 1999). These studies have revealed the broad activity of GNA, but the exact mechanism of action is complex and not yet fully elucidated. Binding to glycoproteins in the midgut of the insect is considered a prerequisite for toxicity of lectins (Czapla 1997), but binding is not an absolute predictor of subsequent toxicity (Harper et al. 1995). GNA binds specifically to D-mannose (Van Damme et al. 1995). Furthermore, it is resistant to gut proteolysis in lepidopteran larvae (Gatehouse et al. 1995). For the homopteran Nilaparvata lugens (Stål.) and lepidopteran Lacanobia oleracea L., GNA has been reported to be transported across the midgut epithelial barrier into the circulatory system (Powell et al. 1998, Fitches et al. 2001). Du et al. (2000) demonstrated that one of the major receptors for GNA in N. lugens was a subunit of ferritin, suggesting that this particular lectin may interfere with the insects’ iron homeostasis. As studies on GNA-transgenic plants have only revealed partial resistance against different pests, the additional impact of biological control organisms is required to further regulate pest populations (Van Emden 1999). Thus possible effects of GNA on entomophagous insects have been widely studied. Studies on larvae of hymenopteran aphid parasitoids, where GNA was delivered to the target pests via transgenic plants or artificial diet, reported sublethal effects on Aphelinus abdominalis (Dalman) (Couty et al. 2001a, c), and Aphidius ervi Haliday (Couty et al. 2001b). However, the studies did not allow to distinguish whether these effects

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