Plants must “call for help” both early and late to be heard

Plants can effectively get rid of herbivores by "calling for help" using odors which attract animals that eat herbivores; but herbivores feed on plants day and night, and may try to escape danger by choosing to feed when their enemies are not active. By producing a combination of rapidly and slowly released odors, both of which are attractive to herbivores' enemies, plants can always "call for help" at the right time, regardless of when herbivores feed.

HFSP Program Grant holder Ian Baldwin and colleagues
authored on Thu, 25 January 2018

When attacked, plants emit herbivore-induced volatiles as one avenue of defense. These lightweight molecules which diffuse out around the plant can defend it by attracting predators and parasitoids to feed on the attacking herbivores. This is called indirect defense, because plants call on others to act as defenders. This strategy can be fast and effective for plants, causing up to a 95% reduction in herbivore load within a single week (Kessler & Baldwin, 2001), and increasing plant reproduction (Schuman et al, 2012). However, the success of this strategy requires that plants can reliably attract predators and parasitoids to their herbivorous prey.

Figure: A schematic model depicting the hypothesized synchronization of plant indirect defense signals and predator activities. 
Ecological interactions are all about timing. Herbivore activity is temporally variable in the native habitat of wild tobacco, but these plants mostly rely on a day-active predator. To resolve this dilemma, wild tobacco plants produced both rapidly and slowly released odors when herbivores feed.

Herbivore-induced plant volatiles comprise complex blends of molecules. These blends can be highly specific to the identity of the attacking herbivores, for example, and reveal other important information such as herbivore numbers and parasitization status – a possible indicator of how suitable the herbivores are as prey for any approaching enemies. Blend composition is thus decisive for effective predator and parasitoid attraction. Individual blend components differ in when and how quickly they are synthesized and released, resulting in changes to blend composition over time, which are not well understood. In particular, some herbivore-induced plant volatiles are released transiently when herbivores feed, while the emission of others persists long after feeding stops. The fatty acid-derived green leaf volatiles (GLVs) are immediately released from damaged leaf tissue by most plants, although the specific blend differs by plant species and type of damage (e.g. herbivory versus mechanical wounding). While GLVs can reliably indicate herbivore feeding, their transience could allow herbivores to escape predation by not feeding when predators are active. Sesquiterpenes are another common component of herbivore-induced volatile blends, although plants differ in which structures they produce, of the thousands of known possibilities. Sesquiterpenes are usually emitted for hours to days, even after herbivore feeding stops, often with a typical daily rhythm; and emission may not begin until the next day (light period) following attack. Although these time-dependent changes are common to most herbivore-induced plant volatile blends studied so far, it was not known whether or how they affect plants’ ability to “call for help” at the right time.

We asked whether time-dependent changes in herbivore-induced volatiles affect the ability of wild tobacco (Nicotiana attenuata) plants to attract native predators and get rid of their herbivores. First, we monitored the feeding activity of two specialist herbivores of N. attenuata, and found that these only partly overlapped with the activity of their native predators on field-grown plants. Both herbivore and predator activity also fluctuated with time of day. We then monitored the GLVs and sesquiterpenes emitted by field-grown N. attenuata plants after a standardized “mock herbivore attack” at either the beginning of the day, when predators are becoming active, or at the end of the day, when predator activity ceases. We found striking differences in the composition of GLVs after this morning versus evening “mock attack”, while sesquiterpenes were emitted mainly during light periods, and peaked in early afternoon around the time of peak daily predator activity. Under controlled conditions, we showed that timing of herbivore attack has a greater effect on herbivore-induced volatiles than either light cues, or the plant’s internal clock, although these factors also play a role. Over two years of field studies, we found that day-active predators removed more herbivores from both field-grown and naturally occurring wild plants, when plants were supplemented with a GLV blend typical of dawn attack, versus a blend typical of dusk attack. This could be attributed to different ratios of specific GLV molecules produced at each time of day, rather than differences in the total amount of GLVs. We then conducted experiments with plants that were genetically modified so that they could either no longer make GLVs, or could no longer make GLVs or herbivore-induced sesquiterpenes – except in very small trace amounts. Using these plants, we found that after a dawn attack, GLVs were required to increase predation rates, while sesquiterpenes did not help even though they are also released. In contrast, sesquiterpenes increased predation rates in the day following a dusk attack, and also contributed to the prolonged elevation of predation rates in the second day after attack. The field work reported in this study was conducted in the USA over two years, while all of the laboratory work was conducted in Germany. The uncomplicated and non-bureaucratic funding procedures of the HFSP greatly facilitated the logistics of this work.

We conclude that the combination of transient GLV emission with rhythmic, persistent sesquiterpene emission provides a robust defense response that works to reliably increase predation of herbivores, defending wild tobacco plants under real-world conditions. GLVs and sesquiterpenes provide two ways of conveying timely information to predators: sesquiterpenes are persistent and temporally synchronized with predator activity, while GLVs are transient but convey relevant temporal information as a result of qualitative blend differences.

Reference

Herbivore-induced volatile blends with both ‘fast’ and ‘slow’ components provide robust indirect defence in nature. Joo Y, Schuman MC, Goldberg JK, Kim S-G, Yon F, Brütting C & Baldwin IT (2018) Funct. Ecol. 32: 136–149.

Other references

Defensive function of herbivore-induced plant volatile emissions in nature. Kessler A & Baldwin IT (2001) Science 291: 2141–2144.

Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature. Schuman MC, Barthel K & Baldwin IT (2012) eLife 1: e00007

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