The 11-hydroxy-jasmonic acid pathway expands jasmonate catabolic repertoire for stress-specific hormone attenuation in Arabidopsis

Abstract The plant hormone jasmonoyl-isoleucine (JA-Ile) reallocates resources from growth towards induced defenses upon microbial or herbivore attacks or other environmental threats. JA-Ile and its precursor jasmonic acid (JA) undergo complex enzymatic turnover that shape hormonal dynamics for optimal signaling. JA-Ile is inactivated through gradual oxidation by CYP94 monooxygenases, followed by 12-OH-JA-Ile deconjugation towards 12-OH-JA. 12-OH-JA was believed to originate also from direct JA hydroxylation by JAO/JOX dioxygenases. Here we investigate the nature and origins of hydroxy-JAs and their derivatives upon stress responses in Arabidopsis. Using a set of analytical methods to explore enzyme assays and multiple pathway-impaired mutants, we show that JAO enzymes produce exclusively 11-OH-JA rather than 12-OH-JA and define a separate branch in JA catabolism. Upon leaf wounding, the CYP94/AH and, to a lesser extent, the JAO pathways direct the respective accumulation of 12- and 11-OH-JAs and their 11/12-glucosylated and 12-sulfated derivatives with isoform-specific occurrences. In contrast, Botrytis infection triggers the exclusive accumulation of 11-OH-JA and 11-Glc- O -JA with complex patterns of HSO 4 -JA. Finally, treatment of jar1 seedlings with 11-OH-JA does not trigger transcriptional changes, reinforcing the notion that the JAO/11-OH-JA pathway represents a metabolic sink modulating JA-Ile formation. Our findings elucidate the 11-OH-JA biosynthetic pathway and highlight stress-specific hydroxylation signatures.