Editor’s Choice 104:2

Issue 104:2 of Journal of Ecology is available online. The latest Editor’s Choice paper is Herbivore intoxication as a potential primary function of an inducible volatile plant signal by Veyrat et al. 

Senior Editor Amy Austin has written a commentary on what makes the paper so important below.

Far from indolent, maize plants work to emit volatiles that signal bad news for herbivorous insects

A Spodoptera littoralis larvae feeding on a maize leaf. Picture: Thomas Roder.

A Spodoptera littoralis larvae feeding on a maize leaf. Picture: Thomas Roder.

There has been a virtual explosion of studies and interest in herbivore induced plant volatiles (HIPVs) in the last three decades since the publication of the original ‘talking trees’ articles that focused on  interplant communication and upregulation of plant defenses when neighboring trees were attacked (Baldwin & Schultz 1983; Rhoades 1983).  Since that time, the evolution of the field of plant-plant signaling has been a hotbed of controversy and discovery (Fowler & Lawton 1985; Heil 2014) with the dawning realization for many plant ecologists that plants have a hidden arsenal of chemical responses to attack from their worst enemies – herbivores. HIPVs can function as a warning for neighboring plants, but have also been shown to be important as an attractant for natural enemies of herbivorous arthropods (Dicke & Sabelis 1988; Vet & Dicke 1992; Rasmann et al. 2005).

First author Nathalie Veyrat is inducing maize plants by wounding the leaves and applying Spodoptera littoralis oral secretions. This treatment triggers indole release similar to real herbivory. Picture: Christelle Robert.

First author Nathalie Veyrat is inducing maize plants by wounding the leaves and applying Spodoptera littoralis oral secretions. This treatment triggers indole release similar to real herbivory. Picture: Christelle Robert.

The Editor’s Choice for this issue of Journal of Ecology, authored by Nathalie Veyrat, Christelle Robert, Ted Turlings and Matthias Erband titled Herbivore intoxication as a potential primary function of an inducible volatile plant signal concretely demonstrates a less well-established role for  HIPVs: volatile compounds, in this case indole, directly affected the metabolism and behaviour of the herbivores themselves.  Indole has been recently identified as a key HIPV, shown to be a priming agent in maize (Erb et al. 2015), meaning that plants exposed to indole compounds produced under herbivore attack in neighbors are better defended prior to actual herbivory events.  The creative insight of these authors in this study is that they demonstrate another role for indole in plant-insect interactions: plants may benefit from the emission of indole by directly altering herbivore fitness and behaviour. Using wild-type maize plants and maize plants that were indole-deficient, the researchers conducted a series of choice and growth experiments with some interesting results: insects growing on wild-type plants that emitted indole had lower survival and reduced leaf consumption; caterpillars chose indole-deficient plants when provided with a choice; and even at a distance, caterpillars directly avoided leaves that were emitting indole. Perhaps more importantly, however, was that the attraction and choice of the indole-deficient mutants could be reversed for all variables by the addition of synthetic indole, and direct application of indole to the caterpillars resulted in rapid, negative effects on caterpillar survival and consumption of leaf material.

Larval preferences between wild type and indole-deficient mutants were determined using a custom made setup. Picture: Nathalie Veyrat.

Larval preferences between wild type and indole-deficient mutants were determined using a custom made setup. Picture: Nathalie Veyrat.

What to make of these effects of indole? Taken together, the experiments suggest what appears to be a direct effect of indole through toxicity or induction of metabolic changes in the caterpillars themselves.  This highlights a novel function for this HIPV, and speaks to the tripartite role for indole in plant-interactions – as a repellant for herbivores, as a priming signal for neighboring plants (Erb et al. 2015) and with additional direct toxic impacts on herbivore survival and performance.  This is not trivial, given that indole is a common plant volatile in a number of plant species.  The authors highlight that these results also speak to one of the largest unanswered questions in current researchof plant volatiles, which is the evolutionary origin of these compounds as signaling cues (Dicke & Baldwin 2010; Heil 2014). This study suggests that the evolution of plant indole emission could have originated not due to volatile signaling for plant-plant communication, but rather due to the fitness benefits for plants of herbivore toxicity.

Amy Austin
Senior Editor, Journal of Ecology

References 

Baldwin, I. T. & Schultz, J. C. (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science, 221, 277-279.

Dicke, M. & Baldwin, I. T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science, 15, 167-175.

Dicke, M. & Sabelis, M. (1988) How plants obtain predatory mites as bodyguards. Netherlands Journal of Zoology, 38, 148-165.

Erb, M., Veyrat, N., Robert, C. A., Xu, H., Frey, M., Ton, J. & Turlings, T. C. (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nature communications, 6, 6273

Fowler, S. V. & Lawton, J. H. (1985) Rapidly induced defenses and talking trees: the devil’s advocate position. The American Naturalist, 126, 181-195.

Heil, M. (2014) Herbivore‐induced plant volatiles: targets, perception and unanswered questions. New Phytologist, 204, 297-306.

Rasmann, S., Köllner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J. & Turlings, T. C. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732-737.

Rhoades, D. F. (1983) Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. Plant resistance to insects (ed P. A. Hedin), pp. 55-68. American Chemical Society, Washington D.C.

Vet, L. E. & Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology, 37, 141-172.

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