Metabolic Control within the Jasmonate Biochemical Pathway

Regulation of defense and developmental responses by jasmonates (JAs) has been intensively investigated at genetic and transcriptional levels. Plasticity in the jasmonic acid (JA) metabolic pathway as a means to control signal output has received less attention. Although the amplitude of JA responses generally follows the accumulation dynamics of the active hormone jasmonoyl-isoleucine (JA-Ile), emerging evidence has identified cases where this relationship is distorted and that we discuss in this review. JA-Ile is turned over in Arabidopsis by two inducible, intertwined catabolic pathways; one is oxidative and mediated by cytochrome P450 enzymes of the subfamily 94 (CYP94), and the other proceeds via deconjugation by amidohydrolases. Their genetic inactivation has profound effects on JAs homeostasis, including strong JA-Ile overaccumulation, but this correlates with enhanced defense and tolerance to microbial or insect attacks only in the absence of overinduction of negative signaling regulators. By contrast, the impairment of JA oxidation in the jasmonic acid oxidase 2 (jao2) mutant turns on constitutive defense responses without elevating JA-Ile levels in naive leaves and enhances resistance to subsequent biotic stress. This latter and other recent cases of JA signaling are associated with JA-Ile catabolites accumulation rather than more abundant hormone, reflecting increased metabolic flux through the pathway. Therefore, manipulating upstream and downstream JA-Ile homeostatic steps reveals distinct metabolic nodes controlling defense signaling output.