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Induction of systemic acquired resistance in Zea mays also enhances the plant's attractiveness to parasitoids

2008, Rostas, Michael, Turlings, Ted

Plants under attack by caterpillars emit volatile compounds that attract the herbivore's natural enemies. In maize, the caterpillar-induced production of volatiles involves the phytohormone jasmonic acid (JA). In contrast, pathogen attack usually up-regulates the salicylic acid (SA)-pathway and results in systemic acquired resistance (SAR) against plant diseases. Activation of the SA-pathway has often been found to repress JA-dependent direct defenses, but little is known about the effects of SAR induction on indirect defenses such as volatile emission and parasitoid attraction. We examined if induction of SAR in maize, by chemical elicitation with the SA-mimic benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH), attenuates the emission of volatiles induced by Spodoptera littoralis or exogenously applied JA. In addition, we determined how these treatments affected the attractiveness of the plants to the parasitoid Microplitis rufiventris in a six-arm-olfactometer. BTH treatment alone resulted in significant systemic resistance of maize seedlings against the pathogen Setosphaeria turcica, but had no detectable effect on volatile emissions. Induction of SAR significantly reduced the emission rates of two compounds (indole and (E)-beta-caryophyllene) in JA-treated plants, whereas no such negative cross-talk was found in caterpillar-damaged plants. Surprisingly, however, BTH treatment prior to caterpillar-feeding made the plants far more attractive to the parasitoid than plants that were only damaged by the herbivore. Control experiments showed that this response was due to plant-mediated effects rather than attractiveness of BTH itself. We conclude that in the studied system, plant protection by SAR activation is compatible with and can even enhance indirect defense against herbivores. (C) 2008 Elsevier Inc. All rights reserved.

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Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field

2006, Lou, Yonggen, Hua, Xiaoyan, Turlings, Ted, Cheng, Jiaan, Chen, Xuexin, Ye, Gongyin

We compared the volatiles of JA-treated plants of six rice varieties and then determined, in the laboratory and field, if they differed in attractiveness to Anagrus nilaparavate Pand et Wang, an egg parasitoid of rice planthoppers. Analyses of volatiles revealed significant differences among varieties, both in total quantity and quality of the blends emitted. On the basis of these differences, the six varieties could be roughly divided into three groups. In a Y-tube olfactometer, female wasps preferred odors from two groups. These preferences corresponded to observed parasitism rates in a field experiment. A comparison of the volatiles with results from behavioral assays and field experiments indicates that the quality (composition) of the blends is more important for attraction than the total amount emitted. The results imply that the foraging success of natural enemies of pests can be enhanced by breeding for crop varieties that release specific volatiles.

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The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps

2006, D'Alessandro, Marco, Held, Matthias, Triponez, Yann, Turlings, Ted

After herbivore attack, plants release a plethora of different volatile organic compounds (VOCs), which results in odor blends that are attractive to predators and parasitoids of these herbivores. VOCs in the odor blends emitted by maize plants (Zea mays) infested by lepidopteran larvae are well characterized. They are derived from at least three different biochemical pathways, but the relative importance of each pathway for the production of VOCs that attract parasitic wasps is unknown. Here, we studied the importance of shikimic acid derived VOCs for the attraction of females of the parasitoids Cotesia marginiventris and Microplitis rufiventris. By incubating caterpillar-infested maize plants in glyphosate, an inhibitor of the 5-enolpyruvylshikimate-3-phospate (EPSP) synthase, we obtained induced odor blends with only minute amounts of shikimic acid derived VOCs. In olfactometer bioassays, the inhibited plants were as attractive to naive C. marginiventris females as control plants that released normal amounts of shikimic acid derived VOCs, whereas naive M. rufiventris females preferred inhibited plants to control plants. By adding back synthetic indole, the quantitatively most important shikimic acid derived VOC in induced maize odors, to inhibited plants, we showed that indole had no effect on the attraction of C. marginiventris and that M. rufiventris preferred blends without synthetic indole. Exposing C. marginiventris females either to odor blends of inhibited or control plants during oviposition experiences shifted their preference in subsequent olfactometer tests in favor of the experienced odor. Further learning experiments with synthetic indole showed that C. marginiventris can learn to respond to this compound, but that this does not affect its choices between natural induced blends with or without indole. We hypothesize that for naive wasps the attractiveness of an herbivore-induced odor blend is reduced due to masking by nonattractive compounds, and that during oviposition experiences in the presence of complex odor blends, parasitoids strongly associate some compounds, whereas others are largely ignored.

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An elicitor of plant volatiles from beet armyworm oral secretion

1997, Alborn, Hans, Turlings, Ted, Jones, Tappey, Stenhagen, G, Loughrin, John H, Tumlinson, James H

The compound N-(17-hydroxylinolenoyl)-L-glutamine (named here volicitin) was isolated from oral secretions of beet armyworm caterpillars. When applied to damaged leaves of corn seedlings, volicitin induces the seedlings to emit volatile compounds that attract parasitic wasps, natural enemies of the caterpillars. Mechanical damage of the leaves, without application of this compound, did not trigger release of the same blend of volatiles. Volicitin is a key component in a chain of chemical signals and biochemical processes that regulate tritrophic interactions among plants, insect herbivores, and natural enemies of the herbivores.

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Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naive parasitoids

2006, Rostas, Michael, Ton, Jurriaan, Mauch-Mani, Brigitte, Turlings, Ted

Plants attacked by insects release volatile compounds that attract the herbivores' natural enemies. This so-called indirect defense is plastic and may be affected by an array of biotic and abiotic factors. We investigated the effect of fungal infection as a biotic stress agent on the emission of herbivore-induced volatiles and the possible consequences for the attraction of two parasitoid species. Maize seedlings that were simultaneously attacked by the fungus Setosphaeria turcica and larvae of Spodoptera littoralis emitted a blend of volatiles that was qualitatively similar to the blend emitted by maize that was damaged by only the herbivore, but there was a clear quantitative difference. When simultaneously challenged by fungus and herbivore, the maize plants emitted in total 47% less of the volatiles. Emissions of green leaf volatiles were unaffected. In a six-arm olfactometer, the parasitoids Cotesia marginiventris and Microplitis rufiventris responded equally well to odors of herbivore-damaged and fungus- and herbivore-damaged maize plants. Healthy and fungus-infected plants were not attractive. An additional experiment showed that the performance of S. littoralis caterpillars was not affected by the presence of the pathogen, nor was there an effect on larvae of M. rufiventris developing inside the caterpillars. Our results confirm previous indications that naive wasps may respond primarily to the green leaf volatiles.