Jasmonic Acid Oxidases (JAO) define a new branch in jasmonate metabolism towards 11OH-jasmonic acid and its glucosylated derivative

Jasmonates (JAs) occur in plants as a group of related compounds undergoing complex metabolic conversions that shape signatures unique to a given organ or physiological status. Previous studies have shown that several JAs result from direct or indirect catabolism of the master hormonal regulator jasmonoyl-isoleucine (JA-Ile) that controls most jasmonate responses triggered by developmental or environmental cues. Hydroxylation of the precursor jasmonic acid (JA) by Jasmonic Acid Oxidases (JAO) holds a peculiar regulatory function, by attenuating basal JA-Ile formation and action, and promoting growth. Here we reinvestigated biochemically and genetically the nature and origins of hydroxy-JAs and their derivatives in Arabidopsis. Using refined analytical methods and pathway-impaired mutants, we show that JAO enzymes produce exclusively 11OH-JA and are preferentially recruited in response to fungal infection where 11-O-Glc-JA accumulates as its main glucosylated derivative. In contrast, mechanical wounding triggers the dominant formation of 12-OH-JA (and its derivatives 12-O-Glc-JA and 12-HSO4-JA) as a cleavage product of the JA-Ile catabolite 12OH-JA-Ile by the amido hydrolases IAR3 and ILL6. Our results identify the elusive 11OH-JA biosynthetic pathway and provide a revisited picture of JA metabolism where two separate enzyme systems lead to stress-modulated formation of hydroxy-JAs position isomers to attenuate signaling.