How Plants Sense Wounds: Damaged-Self Recognition Is Based on Plant-Derived Elicitors and Induces Octadecanoid Signaling

BACKGROUND: Animal-derived elicitors can be used by plants to detect herbivory but they function only in specific insect–plant interactions. How can plants generally perceive damage caused by herbivores? Damaged-self recognition occurs when plants perceive molecular signals of damage: degraded plant molecules or molecules localized outside their original compartment. METHODOLOGY/PRINCIPAL FINDINGS: Flame wounding or applying leaf extract or solutions of sucrose or ATP to slightly wounded lima bean (Phaseolus lunatus) leaves induced the secretion of extrafloral nectar, an indirect defense mechanism. Chemically related molecules that would not be released in high concentrations from damaged plant cells (glucose, fructose, salt, and sorbitol) did not elicit a detectable response, excluding osmotic shock as an alternative explanation. Treatments inducing extrafloral nectar secretion also enhanced endogenous concentrations of the defense hormone jasmonic acid (JA). Endogenous JA was also induced by mechanically damaging leaves of lima bean, Arabidopsis, maize, strawberry, sesame and tomato. In lima bean, tomato and sesame, the application of leaf extract further increased endogenous JA content, indicating that damaged-self recognition is taxonomically widely distributed. Transcriptomic patterns obtained with untargeted 454 pyrosequencing of lima bean in response to flame wounding or the application of leaf extract or JA were highly similar to each other, but differed from the response to mere mechanical damage. We conclude that the amount or concentration of damaged-self signals can quantitatively determine the intensity of the wound response and that the full damaged-self response requires the disruption of many cells. CONCLUSIONS/SIGNIFICANCE: Numerous compounds function as JA-inducing elicitors in different plant species. Most of them are, contain, or release, plant-derived molecular motifs. Damaged-self recognition represents a taxonomically widespread mechanism that contributes to the perception of herbivore feeding by plants. This strategy is independent of insect-derived elicitors and, therefore, allows plants to maintain evolutionary control over their interaction with herbivores.