A beta-glucosidase of an insect herbivore determines both toxicity and deterrence of a dandelion defense metabolite
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Evaluation Summary:
This paper is of interest to a broad audience interested in the coevolutionary arms race between plants and their herbivores. In a thoroughly investigated case study, the detoxification strategy of cockchafer larvae towards the major defensive compound of one of their preferred host plants, dandelion, is revealed and effects on the behavior of the larvae are described.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)
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Abstract
Gut enzymes can metabolize plant defense compounds and thereby affect the growth and fitness of insect herbivores. Whether these enzymes also influence feeding preference is largely unknown. We studied the metabolization of taraxinic acid β-D-glucopyranosyl ester (TA-G), a sesquiterpene lactone of the common dandelion ( Taraxacum officinale ) that deters its major root herbivore, the common cockchafer larva ( Melolontha melolontha ). We have demonstrated that TA-G is rapidly deglucosylated and conjugated to glutathione in the insect gut. A broad-spectrum M. melolontha β-glucosidase, Mm_bGlc17, is sufficient and necessary for TA-G deglucosylation. Using cross-species RNA interference, we have shown that Mm_bGlc17 reduces TA-G toxicity. Furthermore, Mm_bGlc17 is required for the preference of M. melolontha larvae for TA-G-deficient plants. Thus, herbivore metabolism modulates both the toxicity and deterrence of a plant defense compound. Our work illustrates the multifaceted roles of insect digestive enzymes as mediators of plant-herbivore interactions.
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Evaluation Summary:
This paper is of interest to a broad audience interested in the coevolutionary arms race between plants and their herbivores. In a thoroughly investigated case study, the detoxification strategy of cockchafer larvae towards the major defensive compound of one of their preferred host plants, dandelion, is revealed and effects on the behavior of the larvae are described.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)
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Reviewer #1 (Public Review):
In this manuscript, Huber et al. tested the function of three putative beta-glucosidases in the common cockchafer larva by silencing those genes using RNAi. Genetic modifications of TA-G synthesis in the common dandelion and TA-G deglycosylation in the herbivore allow to directly access the role of the herbivore digestive enzyme both in the plant defense sabotage and the host finding behavior of herbivore. The authors nicely combined a series of various experiments which are molecular biology, analytical chemistry, and bioassay. Based on the convincing approaches, the authors conclude that herbivore digestive enzyme (Mm_bGluc17) enhance herbivore performance and involve in the host finding behavior. I think the conclusions of this study are well supported by solid data and the overall manuscript is …
Reviewer #1 (Public Review):
In this manuscript, Huber et al. tested the function of three putative beta-glucosidases in the common cockchafer larva by silencing those genes using RNAi. Genetic modifications of TA-G synthesis in the common dandelion and TA-G deglycosylation in the herbivore allow to directly access the role of the herbivore digestive enzyme both in the plant defense sabotage and the host finding behavior of herbivore. The authors nicely combined a series of various experiments which are molecular biology, analytical chemistry, and bioassay. Based on the convincing approaches, the authors conclude that herbivore digestive enzyme (Mm_bGluc17) enhance herbivore performance and involve in the host finding behavior. I think the conclusions of this study are well supported by solid data and the overall manuscript is well-written. Particularly, the method sections are very informative that the readers can judge and replicate the experiments.
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Reviewer #2 (Public Review):
The paper by Huber et al. analyzes the detoxification strategy of an insect herbivore, the cockchafer, against a prominent defensive compound, taraxinic acid glucopyranosyl ester (TA-G), of dandelions, one of the beetle larvae's preferred food plants. As the authors can convincingly show a beta glucosidase, a digesting enzyme in the herbivore's gut, acts as a detoxification enzyme and simultaneously seems to induce the beetle larvae to avoid plants with this defensive compound. The data presented cover the full range from physiological and chemical analytical data exploring the fate of the plant defense compound in the larvae's digestive system to transcriptomic analyses identifying the beetle's relevant beta glucosidase with their tissue and diet specific expression level to cell culture expression of those …
Reviewer #2 (Public Review):
The paper by Huber et al. analyzes the detoxification strategy of an insect herbivore, the cockchafer, against a prominent defensive compound, taraxinic acid glucopyranosyl ester (TA-G), of dandelions, one of the beetle larvae's preferred food plants. As the authors can convincingly show a beta glucosidase, a digesting enzyme in the herbivore's gut, acts as a detoxification enzyme and simultaneously seems to induce the beetle larvae to avoid plants with this defensive compound. The data presented cover the full range from physiological and chemical analytical data exploring the fate of the plant defense compound in the larvae's digestive system to transcriptomic analyses identifying the beetle's relevant beta glucosidase with their tissue and diet specific expression level to cell culture expression of those beta glucosidases and functional verification whether they are able to deglycosylate TAG. The authors thereby home in on one specific enzyme that has the strongest TAG cleaving activity and further demonstrate its effect by silencing it via RNAi. This knock down results in significantly reduced growth of larvae exposed to the toxin, on the other hand, the presence of the enzyme was necessary to elicit the TAG avoidance behavior previously reported for cockchafer larvae.
The manuscript flawlessly follows up on the observed detoxification ability of the beetle larvae from one organismic level to the next and provides an in depth analysis of the phenomenon. All analyses have been carefully performed, correctly analysed and fully support the conclusions drawn. The manuscript is well written and provides a well laid out case study on how digestive enzymes of an insect herbivore can be coopted to provide a specific adaptation to a preferred host plant and not only circumvent its main defense but also modulate the herbivores behavior.
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Reviewer #3 (Public Review):
The manuscript describes the metabolic profile of the plant defensive glucoside, TA-G, in the root-feeding beetle larvae and the identification of an insect beta-glucosidase enzyme that hydrolyze TA-G. The gene expression and enzyme activity assays after RNAi further demonstrate that the enzyme is not only responsible for the detoxification, but also for the larval deterrent behavior. This study shows a novel and interesting involvement of an herbivore-derived hydrolyase in the deglucosylation, providing an important insight on how the below-ground herbivorous insect can cope with the root-producing toxin.
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