April 14, 2015

Listening in on Plant Defenses

Music and plants has long captured our imagination. Now we have evidence that plants really benefit from responding to vibrations.
By Eric Hamilton

 In a widely-reported study released last year, two researchers over at the University of Missouri, Columbia tested the effects on plant defenses of the vibrations caused by a caterpillar chewing on a leaf. Although much of the reporting fell prey to the temptation to claim the plants “heard” the chewing and responded, the real answer is both more complicated and more interesting. I had the opportunity to attend a talk Drs. Appel and Cocroft gave at Washington University a few months ago where I learned more than I could have extracted from their paper, published in Oecologia, alone.

Dr. Cocroft studies insect communication, especially the ability of insects to find mates and prey by sensing the vibrations of other insects on a plant. Like sound, the information is encoded in vibrational waves passing through a substance. Instead of a pressure wave like sound that varies in the same direction of travel—a longitudinal wave—insect vibrations on plants are transverse waves, moving up and down like a wave on the ocean (see figure).

We could never hear these kinds of waves ourselves, but their frequency can be directly translated to sounds we can hear. Cocroft played a number of humming soundscapes recorded with a laser on a wild prairie—the result of hundreds or thousands of insects communicating silently on stalks of grass. A plant, Cocroft noted, is a great conductor for these vibrations, flexible yet strong. His field studies how insects benefit from communicating this way, but he joined forces with Appel to ask: Do plants respond to the vibrations of insect herbivores in an adaptive way?

One major defense that plants have against pests is producing noxious compounds to deter feeding. Appel and Cocroft hypothesized that Arabidopsis plants would produce more defense compounds if they were exposed to the vibrations of herbivorous insects before actually being attacked. This effect is called priming, and could help defend against a second wave of insect damage.

To test this, the researchers first used lasers to record the vibrations of caterpillars allowed to eat the leaves of Arabidopsis plants. To play the vibrations back to undamaged plants, Cocroft attached leaves to tiny pistons driven, essentially, by speakers, ones that could replicate the vibrations of an insect chewing. Then caterpillars were allowed to feed on either the leaf that was vibrated or another, untouched leaf.

Both vibrated and distant leaves responded more vigorously to caterpillar attack than leaves on untouched plants. The plants that were primed by recorded caterpillar vibrations produced more glucosinolates, or mustard oils, than those of unvibrated plants. This is evidence of an adaptive response to insect vibrations, but leaves open the possibility that any vibration encouraged plant defenses.

To see if the effect really was specific to the herbivorous caterpillars, Appel and Cocroft played back vibrations of harmless insects, wind, or caterpillars on different plants and again measured defense compounds—this time anthocyanins, responsible for the deep reds and purples of many plants. Only caterpillar vibrations could prime plants to increase their defense response to herbivory; wind and the neutral insects had no effect.

One important caveat: although the researchers looked for an effect of vibrations alone, they found none. Only vibrations plus actual insect feeding induced higher defenses; the plants were primed for future attack, but vibrations alone made no difference. Of course, a real insect is more than just its vibrations. Herbivore attack is a physical, chemical, and auditory assault, and plants likely respond to each stimulus in different ways.

But how are plants able to sense the vibrations of caterpillars, and even differentiate them from similar sounds in nature? It’s entirely unknown. A very good candidate is a diverse group of proteins bound together by their responsiveness to physical forces—mechanoreceptors. These proteins can signal within a cell in response to vibration or touch and are potentially behind the priming effect that Appel and Cocroft observed.

In fact, to test this, the Haswell lab is working with Appel and Cocroft to see if our favorite mechanosensitive ion channels are part of the vibrational-response pathway. I got to see Liz’s face pop up in the corner at the end of their presentation over on the medical campus as they told us that work was underway. We’ll just have to wait to find out.