A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis

Abstract

Summary: Jasmonic acid (JA) and its biologically active derivatives (bioactive JAs) perform a critical role in regulating plant responses to wound stress. The perception of bioactive JAs by the F‐box protein COI1 triggers the SCF COI1/ubiquitin‐dependent degradation of JASMONATE ZIM‐DOMAIN (JAZ) proteins that repress the expression of JA‐response genes. JA is required for many wound‐inducible systemic defense responses, but little is known about the role of the hormone in long‐distance signal relay between damaged and undamaged leaves. Here, we show that the wounding of Arabidopsis thaliana leaves results in the rapid (<5 min) accumulation of jasmonoyl‐l‐isoleucine (JA‐Ile), the bioactive form of JA, in leaves distal to the wound site. The rapid systemic increase in JA‐Ile preceded the onset of early transcriptional responses, and was associated with JAZ degradation. Wound‐induced systemic production of JA‐Ile required the JA biosynthetic enzyme 12‐oxo‐phytodienoic acid (OPDA) reductase 3 (OPR3) in undamaged responding leaves, but not in wounded leaves, and was largely dependent on the JA‐conjugating enzyme JAR1. Interestingly, the wound‐induced synthesis of JA/JA‐Ile in systemic leaves was correlated with a rapid decline in OPDA levels. These results are consistent with a model in which a rapidly transmitted wound signal triggers the systemic synthesis of JA, which, upon conversion to JA‐Ile, activates the expression of early response genes by the SCF COI1/JAZ pathway.