Abstract

BackgroundPlant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production. A successful approach to protect crops from these pests is the in planta expression of nematotoxic or entomotoxic proteins such as crystal proteins from Bacillus thuringiensis (Bt) or plant lectins. However, the efficacy of this approach is threatened by emergence of resistance in nematode and insect populations to these proteins. To solve this problem, novel nematotoxic and entomotoxic proteins are needed. During the last two decades, several cytoplasmic lectins from mushrooms with nematicidal and insecticidal activity have been characterized. In this study, we tested the potential of Marasmius oreades agglutinin (MOA) to furnish Arabidopsis plants with resistance towards three economically important crop pests: the two plant-parasitic nematodes Heterodera schachtii and Meloidogyne incognita and the herbivorous diamondback moth Plutella xylostella.ResultsThe expression of MOA does not affect plant growth under axenic conditions which is an essential parameter in the engineering of genetically modified crops. The transgenic Arabidopsis lines showed nearly complete resistance to H. schachtii, in that the number of female and male nematodes per cm root was reduced by 86–91 % and 43–93 % compared to WT, respectively. M. incognita proved to be less susceptible to the MOA protein in that 18–25 % and 26–35 % less galls and nematode egg masses, respectively, were observed in the transgenic lines. Larvae of the herbivorous P. xylostella foraging on MOA-expression lines showed a lower relative mass gain (22–38 %) and survival rate (15–24 %) than those feeding on WT plants.ConclusionsThe results of our in planta experiments reveal a robust nematicidal and insecticidal activity of the fungal lectin MOA against important agricultural pests which may be exploited for crop protection.

Highlights

  • Plant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production

  • We have recently demonstrated that the expression of C. cinerea lectin2 (CCL2) in Arabidopsis protects the plants against the plantparasitic nematode Heterodera schachtii

  • The expression of Marasmius oreades agglutinin (MOA) in Arabidopsis did not alter the size and the morphology, judged by rosette and root architecture, of the transgenic lines compared to wild-type plants (Fig. 1a)

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Summary

Introduction

Plant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production. A successful approach to protect crops from these pests is the in planta expression of nematotoxic or entomotoxic proteins such as crystal proteins from Bacillus thuringiensis (Bt) or plant lectins. Besides plants, fruiting bodies (sporocarps) of mushrooms are a rich source of lectins with entomotoxic and nematotoxic activity These cytoplasmically localized proteins, referred to as fruiting body lectins, are considered as an essential part of the fungal innate defense system against predators and parasites [14, 15]. CCL2 expression promotes plant growth, suggesting that CCL2 has, besides its direct binding to glycoepitopes in the antagonist, the ability to improve plant disease resistance and biomass production via binding to endogenous glycoepitopes [21] These results motivated us to evaluate the toxicity of another mushroom lectin, Marasmius oreades agglutinin (MOA), towards two different plant-parasitic nematodes and an insect herbivore. The nematotoxicity of MOA is dependent on both the N-terminal carbohydrate-binding activity and the C-terminal cysteine protease activity, and the target in C. elegans has been identified as the Galα1,3Galβ1,4GlcNAc-epitope on glycosphingolipids, similar to bacterial crystal toxin Cry5B [27, 28]

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