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Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

ABSTRACT: Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (Plutella xylostella) to evaluate changes in fitness, and additionally examined the effects on a predatory lacewing (Chrysoperla carnea). Silencing glucosinolate sulfatase genes resulted in the systemic accumulation of toxic isothiocyanates in P. xylostella larvae, impairing larval development and adult reproduction. The predatory lacewing C. carnea, however, efficiently degraded ingested isothiocyanates via a general conjugation pathway, with no negative effects on survival, reproduction, or even prey preference. These results illustrate how plant defenses and their detoxification strongly influence herbivore fitness but might only subtly affect a third trophic level.

SUBMITTER: Sun R

PROVIDER: S-EPMC6934381 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

Sun Ruo R Jiang Xingcong X Reichelt Michael M Gershenzon Jonathan J Pandit Sagar Subhash SS Giddings Vassão Daniel D

eLife 20191216

Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (<i>Plutella xylostella</i>) to evaluate changes in fitness, and additionally examined the eff ...[more]

PMID: 31841109

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Project description:The tomato leafminer, Tuta absoluta is a destructive invasive pest of cultivated tomato and other Solanaceae plants, with yield losses of 80-100%. Mirid predators are key natural enemies of T. absoluta, but they also feed on host plants in the absence of their prey. Management of T. absoluta is a challenge due to its high biotic potential, resistance to many insecticides and the absence of sufficiently adapted auxiliary fauna in its new dispersion zones. Olfaction plays an important role in the tritrophic interaction between tomato, its herbivore pest T. absoluta and its mirid predators, which can be influenced by non-host plant odors. However, how non-host odours shape this interaction is poorly understood. Previously, we had demonstrated belowground crop protection properties of certain Asteraceae plants against the root-knot nematode Meloidogyne incognita, pest of tomato and other Solanaceae plants. Additionally, Asteraceae plants impact negatively on feeding behavior of above-ground pests of Solanaceae plants, including the greenhouse whitefly (Trialeurodes vaporariorum) and green peach aphid (Myzus persicae). Here, we tested the hypothesis that foliar volatiles from some of these non-host Asteraceae plants can influence the tomato-T. absoluta-mirid predator tritrophic interaction. In olfactometer assays, T. absoluta females were attracted to volatiles of the Solanaceae host plants tomato and giant nightshade but avoided volatiles of the Asteraceae plants, blackjack and marigold, and the positive control, wild tomato, when tested alone or in combination with the host plants. Coupled gas chromatography-mass spectrometry analysis showed that host and non-host plants varied in their emission of volatiles, mainly monoterpenes and sesquiterpenes. Random forest analysis combined with behavioral assays identified monoterpenes as the host plant attractive blend to T. absoluta and its mirid predator, with sesquiterpenes identified as the non-host plant repellent blend against T. absoluta. Contrastingly, the mirid predator was indifferent to the non-host plant repellent sesquiterpenes. Our findings indicate that terpenes influence the tomato-T. absoluta-mirid predator tritrophic interaction. Further, our results emphasize the importance of studying crop protection from a holistic approach to identify companion crops that serve multi-functional roles.

Project description:In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti-predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re-attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish-fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate-deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti-predator defense needs to be further evaluated in the field.

Dataset Information

Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

Publications

Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance.

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