(3R, 7S)-11-hydroxy-jasmonic acid is a major oxidative shunt product of jasmonate catabolism in Arabidopsis thaliana

Abstract

Jasmonoyl-L-isoleucine (JA-Ile) is a pivotal oxylipin plant hormone that regulates numerous physiological processes and stress responses. Because JA-Ile is synthesized from jasmonic acid (JA), the cellular level of JA is tightly controlled. Although the oxidative catabolism of JA to 12-hydroxy-JA (12-OH-JA) is well-characterized, the biosynthesis, accumulation dynamics, and biological functions of 11-hydroxy-JA (11-OH-JA) remain poorly understood. Here, we conducted a comprehensive investigation of 11-OH-JA in Arabidopsis thaliana, encompassing its chemical synthesis, accumulation patterns, biological activity, and biosynthetic pathways. Using chemically synthesized 11-OH-JA of naturally occurring (3R,7S)-stereochemistry, we identified 11-OH-JA as the predominant hydroxylated JA derivative that accumulates following wounding. Enzymatic assays and in silico docking studies revealed that JOX1/2/3/4 exclusively catalyze the conversion of JA to 11-OH-JA, whereas 12-OH-JA is produced by distinct pathways. Notably, the quadruple mutant joxQ completely abolished 11-OH-JA accumulation without affecting 12-OH-JA levels. Furthermore, 11-OH-JA exhibited no binding affinity for the COI1-JAZ co-receptor, indicating that it acts as a biologically inactive shunt product of JA catabolism. Our findings establish JOX-mediated 11-hydroxylation of JA as a primary inactivation pathway, separate from 12-hydroxylation. Parallel, non-redundant inactivation routes deliver layered signal termination of costly defense signals. This study provides new insights into JA catabolism, highlighting 11-OH-JA as a crucial factor in the attenuation of jasmonate signaling, and thereby redefining the framework of JA turnover in A. thaliana.