Herbivore-induced volatile blends with both “fast” and “slow” components provide robust indirect defense in nature

Youngsung Joo, Meredith C. Schuman, Jay K. Goldberg, Sang-Gyu Kim, Felipe Yon, Christoph Brütting and Ian T. Baldwin

 

The scent of a damaged plant can attract predators and parasitoids of attacking herbivores, resulting in higher herbivore mortality and greater plant fitness. These scents are blends of odor molecules which can be highly specific e.g. to the identity, number, and parasitization status of attacking herbivores. Not surprisingly, blend composition is decisive for effective predator and parasitoid attraction. Yet the blends are complex: different odor molecules come from different biochemical pathways, and can be released at different times even after a single feeding event. Two extremes are represented by fatty acid-derived green leaf volatiles (GLVs), and sesquiterpenes. GLVs are released immediately upon damage from most plant leaves. In contrast, sesquiterpenes are usually released for hours to days even after herbivore feeding stops, often with a diurnal rhythm; and emission may not begin until the day (light period) following attack. Timing of release is partly controlled by environmental factors like light, which differs between laboratories and nature. Changes to blends over time are poorly understood, in part because they are often measured over long periods, like whole days, or under artificial conditions.

Here, we show that native herbivores of the ecological model plant Nicotiana attenuata have different activity patterns, and that feeding bouts at dawn or dusk (at the extreme ends of herbivore and predator activity windows) can result in distinct blends of GLVs. In contrast, sesquiterpenes are emitted mainly during light periods, and peak in early afternoon, regardless of when herbivores feed. Over two years of field studies, day-active predators responded more to GLV blends typical of dawn attack. Using transgenic plants lacking either GLVs, or both GLVs and sesquiterpenes, we find that GLVs are required to increase predation rates after a dawn attack, while sesquiterpenes increase predation rates in the day following a dusk attack, and also contribute to a continued elevation of predation rates in the second day post-attack. We conclude that transient GLV emission and diurnal, persistent sesquiterpene emission work together to increase predation of herbivores regardless of when they feed, defending plants under variable real-world conditions.

 

Read the article in full here.

Photograph provided by authors.

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