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      Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

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          Abstract

          Herbivore-induced plant defences influence the behaviour of insects associated with the plant. For biting–chewing herbivores the octadecanoid signal-transduction pathway has been suggested to play a key role in induced plant defence. To test this hypothesis in our plant—herbivore—parasitoid tritrophic system, we used phenidone, an inhibitor of the enzyme lipoxygenase (LOX), that catalyses the initial step in the octadecanoid pathway. Phenidone treatment of Brussels sprouts plants reduced the accumulation of internal signalling compounds in the octadecanoid pathway downstream of the step catalysed by LOX, i.e. 12-oxo-phytodienoic acid (OPDA) and jasmonic acid. The attraction of Cotesia glomerata parasitoids to host-infested plants was significantly reduced by phenidone treatment. The three herbivores investigated, i.e. the specialists Plutella xylostella, Pieris brassicae and Pieris rapae, showed different oviposition preferences for intact and infested plants, and for two species their preference for either intact or infested plants was shown to be LOX dependent. Our results show that phenidone inhibits the LOX-dependent defence response of the plant and that this inhibition can influence the behaviour of members of the associated insect community.

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          Most cited references42

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          Plant responses to insect herbivory: the emerging molecular analysis.

          Plants respond to herbivore attack with a bewildering array of responses, broadly categorized as direct and indirect defenses, and tolerance. Plant-herbivore interactions are played out on spatial scales that include the cellular responses, well-studied in plant-pathogen interactions, as well as responses that function at whole-plant and community levels. The plant's wound response plays a central role but is frequently altered by insect-specific elicitors, giving plants the potential to optimize their defenses. In this review, we emphasize studies that advance the molecular understanding of elicited direct and indirect defenses and include verifications with insect bioassays. Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses. Such organizational elements could help elucidate the molecular control over the diversity of responses elicited by herbivore attack.
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            The lipoxygenase pathway.

            Lipid peroxidation is common to all biological systems, both appearing in developmentally and environmentally regulated processes of plants. The hydroperoxy polyunsaturated fatty acids, synthesized by the action of various highly specialized forms of lipoxygenases, are substrates of at least seven different enzyme families. Signaling compounds such as jasmonates, antimicrobial and antifungal compounds such as leaf aldehydes or divinyl ethers, and a plant-specific blend of volatiles including leaf alcohols are among the numerous products. Cloning of many lipoxygenases and other key enzymes within the lipoxygenase pathway, as well as analyses by reverse genetic and metabolic profiling, revealed new reactions and the first hints of enzyme mechanisms, multiple functions, and regulation. These aspects are reviewed with respect to activation of this pathway as an initial step in the interaction of plants with pathogens, insects, or abiotic stress and at distinct stages of development.
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              Herbivory: caterpillar saliva beats plant defences.

              Blood-feeding arthropods secrete special salivary proteins that suppress the defensive reaction they induce in their hosts. This is in contrast to herbivores, which are thought to be helpless victims of plant defences elicited by their oral secretions. On the basis of the finding that caterpillar regurgitant can reduce the amount of toxic nicotine released by the tobacco plant Nicotiana tabacum, we investigate here whether specific salivary components from the caterpillar Helicoverpa zea might be responsible for this suppression. We find that the enzyme glucose oxidase counteracts the production of nicotine induced by the caterpillar feeding on the plant.
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                Author and article information

                Contributors
                +31-317-482791 , +31-317-484821 , Joop.vanLoon@wur.nl
                Journal
                Oecologia
                Oecologia
                Springer-Verlag (Berlin/Heidelberg )
                0029-8549
                1432-1939
                6 October 2009
                6 October 2009
                February 2010
                : 162
                : 2
                : 393-404
                Affiliations
                [1 ]Laboratory of Entomology, Wageningen University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands
                [2 ]Laboratory of Organic Chemistry, Wageningen University, P.O. Box 8026, 6700 EG Wageningen, The Netherlands
                [3 ]Julius-von-Sachs-Institut für Biowissenschaften, Pharmazeutische Biologie, Julius-von-Sachs-Platz 2, 97082 Würzburg, Germany
                [4 ]Institute of Biology, Leiden University, P.O. Box 9505, 2300 RA Leiden, The Netherlands
                Author notes

                Communicated by Richard Karban.

                Article
                1459
                10.1007/s00442-009-1459-x
                2808510
                19806367
                1f21559a-2454-4c0b-baba-e0ad74b85260
                © The Author(s) 2009
                History
                : 15 April 2009
                : 31 August 2009
                Categories
                Plant-Animal Interactions - Original Paper
                Custom metadata
                © Springer-Verlag 2010

                Ecology
                octadecanoid pathway,phenidone,parasitoid behaviour,herbivore-induced plant volatiles,oviposition

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