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18-Glucosidase: an Elicitor of Herbivore-Induced Plant Odor That

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18-Glucosidase: an Elicitor of Herbivore-Induced Plant Odor That Proc. Natl. Acad. Sci. USA Vol. 92, pp. 2036-2040, March 1995 Plant Biology 18-Glucosidase: An elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps (plant defense/chemical ecology/beneficial insects/tritrophic interactions/behavior) LETIZIA MATTIACCI*, MARCEL DICKE*t, MAARTEN A. POSTHUMUSt *Department of Entomology, Wageningen Agricultural University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands; and tDepartment of Organic Chemistry, Wageningen Agricultural University, Dreijenplein 8, 6703 RB Wageningen, The Netherlands Communicated by Andre T. Jagendorf, Cornell University, Ithaca, NY, November 14, 1994 (received for review July 19, 1994) ABSTRACT Cabbage plants respond to caterpillar (Pieris production of volatile terpenoids and indole that attract the brassicae) herbivory by releasing a mixture of volatiles that parasitoid Cotesia marginiventris. The exogenous elicitor in the makes them highly attractive to parasitic wasps (Cotesia regurgitant has not been identified. A very interesting clue on glomerata) that attack the herbivores. Cabbage leaves that are the identity of the elicitor of herbivore-induced plant odors artificially damaged and subsequently treated with gut re- comes from a study of the biosynthesis of two homoterpenes gurgitant of P. brassicae caterpillars release a volatile blend that are emitted by spider mite-infested lima bean and by similar to that of herbivore-damaged plants. We demonstrate regurgitant-treated corn plants. Boland et al. (15) showed that the presence of 8-glucosidase in P. brassicae regurgitant. application of 3-glucosidase into a mechanical wound in lima Leaves treated with commercial j8-glucosidase (from al- bean leaves resulted in the production of these carnivore monds) release a volatile blend similar to that ofleaves treated attractants. Application of j3-glucosidase onto undamaged with P. brassicae regurgitant. In a flight bioassay, leaves leaves had no effect, nor did mechanical damage without treated with almond j8-glucosidase are highly attractive to the application of 3-glucosidase. Lipases were not effective. This parasitic wasp C. glomerata. Furthermore, the wasps do not suggests that ,B-glucosidase may be an herbivore-related elic- discriminate between cabbage leaves treated with almond itor. However, this cannot be concluded until the following j3-glucosidase and leaves treated with larval regurgitant. have been demonstrated: (i) its existence in herbivore secre- 13-Glucosidase was also recorded in cabbage leaf extract, but tions, (ii) its effect on the total volatile blend emitted, and (iii) this is not as effective as caterpillar 38-glucosidase in eliciting the attraction of carnivores toward ,B-glucosidase-treated the volatile production. Caterpillars that feed on a 8-gluco- leaves. There are reasons to this because sidase-free diet secrete the enzyme, and their regurgitant is an good investigate effective elicitor of the plant response. These findings show glucosidases have been found in several insect orders including that 8-glucosidase is a P. brassicae-secreted elicitor of the Lepidoptera, where they are usually reported in the caterpillar defense response of cabbage plants to herbivore injury, in- gut (16, 17). ducing the emission ofvolatiles that are used by parasitoids of We investigated whether P-glucosidase is an elicitor that the herbivore to locate their victims. affects the production of carnivore attractants in a system of cabbage plants, caterpillars of the large cabbage white butter- fly Pieris brassicae and the parasitoid Cotesia glomerata. The It is well-known that plants may react to herbivory or to infested P. pathogen infestation by phytochemical responses (reviewed in parasitoid is highly attracted to cabbage plants by refs. 1-3). The first step in such responses is the recognition of brassicae caterpillars (18) and caterpillar oral secretions are the attack by the plant. How plants recognize infestation of a known to contain an elicitor that has the same effect on pathogen has been intensively studied and many pathogen- mechanically damaged cabbage leaves as caterpillar feeding derived exogenous elicitors of phytoalexins have been identi- (19, 20). Here we demonstrate that 3-glucosidase has the same fied (4). In contrast, knowledge on the recognition of herbiv- effect on cabbage plants as regurgitant of the caterpillar P. orous arthropods by plants is scarce, being mostly restricted to brassicae; it results in the emission of a similar bouquet of the involvement of herbivore secretions (e.g., see refs. 5-7). volatiles and in the attraction of the parasitoid C. glomerata. Yet, a wealth ofknowledge is available on endogenous elicitors Moreover, the parasitoids do not discriminate between regur- that originate from mechanical damage (8) and on subsequent gitant-treated leaves and ,3-glucosidase-treated leaves. Finally, steps in the signal transduction pathway (8, 9) in responses of we show that 13-glucosidase is present in caterpillar regurgitant. plants to herbivores. A phytochemical response that has been studied in the past MATERIALS AND METHODS decade is the production of volatiles that attract carnivorous arthropods such as predators and parasitic wasps (parasitoids) Rearing Procedures. Plants (Brussels sprouts; Brassica ol- that attack the herbivore (2). For instance, lima bean plants eracea L. var. gemmifera cv. Titurel), herbivores (P. brassicae respond to infestation by the spider mite Tetranychus urticae by L., Lepidoptera, Pieridae), and parasitoids (C. glomerata L., producing volatile terpenoids and methyl salicylate that attract Hymenoptera, Braconidae) were reared according to a pre- a predator (Phytoseiulus persimilis) of these herbivores (2, viously described procedure (21). 10-12). Recently, studies have been initiated on exogenous Bioassay. The behavioral response of individual C. herbivore elicitors of such plant responses. For instance, the glomerata females toward individual leaves of different treat- response of corn plants to herbivory by fall armyworm cater- ments was observed in an earlier described greenhouse flight pillars is similar to the response to administration of caterpillar chamber setup during a series of dual-choice tests (20, 21). To regurgitant into a mechanical wound or fed through the petiole increase their responsiveness, 4- to 5-day-old female parasi- of an intact corn leaf (13, 14). These treatments result in the toids were given an experience (20 s) on leaves with host The publication costs of this article were defrayed in part by page charge Abbreviations: ADold, artificial damage inflicted 1 day before the payment. This article must therefore be hereby marked "advertisement" in bioassay; ADfresh, artificial damage inflicted during the bioassay. accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 2036 Downloaded by guest on September 29, 2021 Plant Biology: Mattiacci et aL Proc. Natl. Acad Sci. USA 92 (1995) 2037 feeding damage 1 day before the experiment (20, 21). Every to the volume of liquid used to treat the test leaf. (i) REG art. parasitoid was allowed only one flight attempt. diet on ADold vs. ADold. The test leaf was treated with 25 ,.d Enzymes. P3-Glucosidase (from almonds; 4-6 units per mg of regurgitant obtained from larvae fed on artificial diet (22). of protein; Sigma) and a-amylase (from Aspergillus oryzae; 35 (ii) Leafjuice on ADold vs. ADold. Leafjuice was obtained by units per mg of solid; Sigma) solutions were applied to cabbage crushing 1 g of cabbage leaf with 750 ,ul of citrate buffer with leaves to assay their elicitor activity with the behavioral test. a mortar and pestle. The resulting slur was filtered through Enzymes were dissolved in 0.1 M NaOH citrate buffer at pH glass wool and centrifuged at 14,000 x g for 30 min, and the 6 (50 ,ug/ml). The pH value was the same as that ofP. brassicae supernatant was used. The test leaf was treated with 60 ,ul or regurgitant. 2 ml of leaf juice. (iii) Boiled REG on ADold vs. ADold. This Plant Treatments. Experiments were conducted with leaves combination was tested to determine whether the elicitor excised from 8-week-old cabbage plants. Leaves were fully enzyme was rendered ineffective by denaturation. A 50% expanded and of the same size within each bioassayed com- (vol/vol) solution ofregurgitant in buffer was boiled for 10 min bination. Enzyme solutions were applied to leaves that under- and 50 ,ul was applied on the wounded test leaf. went different types of mechanical damage inflicted on the Enzyme Assay. The presence of ,B-glucosidase activity was leaves the day before the experiment (day 1) or the day of the determined in the test materials. Freshly collected samples experiment (day 2). (i) Old artificial damage (ADold): - 1/3rd were assayed in triplicate. Caterpillar head extract was ob- of the surface of one leaf was rubbed with 180-grit carborun- tained by dissecting the head of 10 fifth-instar caterpillars, dum powder on a wet cotton wool pad. This damage was which were thoroughly rinsed with citrate buffer to avoid inflicted on day 1. (ii) Fresh artificial damage (ADfresh): on contamination with the gut contents, and crushed with a day 1, undamaged leaves were excised and incubated with their mortar and pestle in 375 Al ofbuffer. Artificial diet extract was petiole in enzyme solutions or in water. During the flight obtained by crushing 1 g of artificial diet in 1 ml of buffer. In bioassay, on day 2, one 0.8-cm-diameter hole was punched in both cases, the slur was filtered and centrifuged as explained the leaf blade with a cork borer every 15 min, starting 1 h for the leaf juice. The incubation mixture contained 5 mM before the bioassay (18). (iii) Undamaged leaves: leaves were 4-nitrophenyl f3-D-glucopyranoside (Boehringer Mannheim) excised on day 1 and incubated with their petiole in enzyme in 1 ml of 0.1 M NaOH citrate buffer (pH 6.0) and either 25 solution or in water. No mechanical damage was inflicted to pl of caterpillar regurgitant, 300 pl of head extract, 500 ,ul of the leaf blade before or during the bioassay.
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