Can a salad taste you back?

Normally when a headline asks a stupid question the answer is 'no', but new research suggests a better answer is 'maybe'.

When you’re attacked by a herbivore, who are you going to call? If you’re a plant attacked by a predator, then the enemy of your enemy is your friend. If you’re attacked by a caterpillar, then calling in a parasitic wasp, by releasing the right odour, will help, but you need to call in the right help for the right attacker. A new paper by Danner et al. in New Phytologist has found this is what Brassica rapa does. It knows how it’s been attacked.

They found this out by setting up a series of experiments with mustard plants bagged in plastic, so they could analyse the volatile compounds given off. In with the plants were the herbivores who couldn’t escape, so they were just stuck with the food. Among the twelve different herbivores tested were caterpillars, aphids and even a slug, and the herbivore selection included specialist and generalist, sucking and chewing, as well as exotic and native species.

A lot of plants in plastic bags
Herbivore Induced Plant Volatiles Experiment. Photo: Holger Danner

The researchers identified subtle differences in the odours emitted by the mustard plants using a gas chromatograph with a highly accurate mass spectrometer. They found that the reactions to exotic and native herbivore species were not defined by a single volatile substance, but by the ratio of different volatiles. “This is consistent with what we know about the perception and behaviour of parasitic wasps and other predators. They use a bouquet of odours released by the plant to obtain information about their prey,” said study leader Nicole van Dam.

The problem with exotic herbivores is that they may induce similar odours as native herbivores, thereby confusing native enemies that may not be able to handle the new hosts. This was not the case in the study of van Dam and her colleagues: exotic herbivores, even if they had a similar way of feeding as their native counterparts, induced significantly different odour profiles.

Van Dam sees the results as “spectacular proof” of how specifically plants respond to their environment. “The plants may not have a nervous system, eyes, ears, or mouths, but they are capable of determining who is attacking them. Based on this, they can transmit reliable information to specialized parasitic wasps that can learn the odours to find their preferred host. What I find truly amazing is that they’re even capable of distinguishing between a native and an exotic herbivore.”

Deer saliva dripped onto a bud
Simulated browsing: After a young maple tree has been cut, roe deer saliva is applied with a pipette to the cut surface. Photo: Bettina Ohse/UL/iDiv.

But how do plants know who is attacking them? This is answered in another paper from the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig.

They looked at young beeches (Fagus sylvatica) and maples (Acer pseudoplatanus). These are popular food for Roe deer (Capreolus capreolus). The plants can defend themselves by producing tannins to make their buds unpalatable for deer, but this is complex chemistry. If you’re not being attacked, then it’s far better to invest your resources into growing than defence.

Maybe you only build defences when you sense a break. But even then, if it’s storm damage or similar, then it’s still a waste of time making tannins. Instead you should be boosting your healthy buds. How can you tell what the problem is, without eyes.

Bettina Ohse thought the answer was in the deer saliva, so she devised an experiment to test this, which you can read in Ohse et al. in Functional Ecology. The trick was to snap trees, and on some dribble roe deer saliva and watch the results. If the plants reacted, then it was effectively the ‘taste’ of the saliva that spurred the trees into building defences.

I’ve put taste in quotes, because it’s an analogy rather than a strict comparison. A recent review in Annals of Botany (FREE) looked at the electrical and chemical signals that trigger plant defences.

The plant defence response.
The plant defence response. Mechanical damage and exposure to oral secretions from herbivores lead to osmotic stress, cause ion fluxes and elicit signalling cascades leading to rapid accumulation of jasmonates (JAs). Jasmonoyl isoleucine diffuses into the nucleus, where it associates with a protein complex including its receptor encoded by the coi (coronatine insensitive) gene. Binding to this complex initiates degradation of transcriptional suppressor proteins, thereby stimulating defence gene expression. Jasmonate also stimulates increased accumulation of secondary metabolites (phytotoxins). Together, these changes make plant tissues less palatable. Upstream processes are shown in black, the defence substances produced by the plant in green. Image: Kant et al. 2015

What I like about the Danner et al. paper is considering the released volatiles as information-rich communication. They use the phrase seen elsewhere ‘info-chemical network’, used by plants, herbivores and their predators. This brings me back to a paper I read last year In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants by Monica Gagliano.

She states: “The total process of receiving, organizing and interpreting such an enormous variety of inputs culminates into what is generally referred to as perception.” Gershenzon has argued that transmission of volatiles could be as much part of internal signalling as a public signal.

If there’s a clear mechanism for transmitting information when a plant gets chemical signals from the saliva of an attacker, then maybe it’s not such a stretch to argue that a plant can taste its attacker, while the herbivore is tasting it.

Source press releases:
https://www.eurekalert.org/pub_releases/2017-01/gcfi-psd013117.php
https://www.idiv.de/news/press_releases/press_release_single_view/article//trees-recogn.html

References

Danner, H., Desurmont, G. A., Cristescu, S. M., & van Dam, N. M. (2017). Herbivore-induced plant volatiles accurately predict history of coexistence, diet breadth, and feeding mode of herbivores. New Phytologist. https://doi.org/10.1111/nph.14428

Ohse, B., Hammerbacher, A., Seele, C., Meldau, S., Reichelt, M., Ortmann, S., & Wirth, C. (2016). Salivary cues: simulated roe deer browsing induces systemic changes in phytohormones and defence chemistry in wild-grown maple and beech saplings. Functional Ecology. https://doi.org/10.1111/1365-2435.12717

Kant, M. R., Jonckheere, W., Knegt, B., Lemos, F., Liu, J., Schimmel, B. C. J., … Alba, J. M. (2015). Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Annals of Botany, 115(7), 1015–1051. https://doi.org/10.1093/aob/mcv054

Gagliano, M. (2014). In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants. AoB PLANTS, 7(0), plu075–plu075. https://doi.org/10.1093/aobpla/plu075

Gershenzon, J. (2007). Plant volatiles carry both public and private messages. Proceedings of the National Academy of Sciences, 104(13), 5257–5258. https://doi.org/10.1073/pnas.0700906104