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Modifying the Alkylglucosinolate Profile in Arabidopsis thaliana Alters the Tritrophic Interaction with the Herbivore Brevicoryne brassicae and Parasitoid Diaeretiella rapae

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Abstract

Arabidopsis thaliana was used as an experimental model plant to investigate a tritrophic interaction between the plant, a specialist aphid herbivore, Brevicoryne brassicae, and its natural enemy, the parasitoid Diaeretiella rapae. The A. thaliana ecotype Col-5 was transformed with a functional 2-oxoglutarate dependent dioxygenase (BniGSL-ALK) that converts 3-methylsulfinylpropylglucosinolate and 4-methylsulfinylbutylglucosinolate to 2-propenylglucosinolate and 3-butenylglucosinolate, respectively. This transformation results in a change in the glucosinolate hydrolysis profile where 3-butenylisothiocyanate, 2-propenylisothiocyanate and 5-vinyloxazolidine-2-thione are produced in contrast to the wild-type plant where 4-methylsulfinylbutylisothiocyanate is the main product. Performance of B. brassicae was affected negatively by transforming Col-5 with BniGSL-ALK in terms of mean relative growth rates. In a series of behavioral bioassays, naïve D. rapae females were able to discriminate between B. brassicae infested and uninfested Col-5 plants transformed with BniGSL-ALK, with parasitoids showing a preference for B. brassicae infested plants. By contrast, naïve D. rapae females were unable to discriminate between aphid infested and uninfested Col-5 plants. Subsequent air entrainments of B. brassicae infested Col-5 plants transformed with BniGSL-ALK further confirmed the presence of 3-butenylisothiocyanate in the headspace. By contrast, no glucosinolate hydrolysis products were recorded from similarly infested Col-5 plants.

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Acknowledgments

This work was supported by the BBSRC (Biotechnology and Biological Sciences Research Council) (grant 32/P17268). Rothamsted receives grant-aided support from the BBSRC. We thank Wendy Byrne and Valerie Elliot for their excellent technical assistance.

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  1. Ralph Kissen

    Present address: Department of Biology, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway

  2. Tom W. Pope

    Present address: ADAS, Battlegate Road, Boxworth, Cambridge, CB3 8NN, UK

Authors and Affiliations

  1. Division of Biology, Imperial College London, Sir Alexander Fleming Building, South Kensington, London, UK, SW7 2AZ

    Ralph Kissen, Tom W. Pope, John T. Rossiter & Glen Powell

  2. School of Biosciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK

    Murray Grant

  3. Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    John A. Pickett

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Correspondence to John T. Rossiter.

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Ralph Kissen and Tom W. Pope contributed equally

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Kissen, R., Pope, T.W., Grant, M. et al. Modifying the Alkylglucosinolate Profile in Arabidopsis thaliana Alters the Tritrophic Interaction with the Herbivore Brevicoryne brassicae and Parasitoid Diaeretiella rapae . J Chem Ecol 35, 958–969 (2009). https://doi.org/10.1007/s10886-009-9677-6

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