Rice JASMONIC ACID OXIDASES control resting jasmonate metabolism to promote growth and repress basal immune responses

Abstract

Catabolic conversions within the jasmonate pathway have substantial consequences on phytohormone signaling output. In dicots, the jasmonic acid oxidase (JAO) catabolic route leads to jasmonic acid (JA) hydroxylation, which limits its conjugation into bioactive jasmonoyl-isoleucine (JA-Ile). Here, we functionally characterized the JAO pathway in rice (Oryza sativa) and demonstrated its key function in promoting growth and attenuating JA responses in vegetative tissues. The rice genome encodes four JAO-related homologs, three of which generate hydroxy-JA in vitro and rescue the high-defense phenotype of the Arabidopsis jao2-2 mutant. By generating and analyzing a series of single to quadruple rice jao mutants, we showed additive effects of cumulative JAO depletion on JA metabolism, basal defense levels, growth inhibition, fitness and global metabolic reprogramming. The growth of JAO-deficient lines was substantially repressed at the juvenile stage, while the impact was milder in later vegetative development, during which plants opposed enhanced resistance to virulent and avirulent strains of Magnaporthe oryzae, the causal agent of fungal blast disease. Moreover, jao mutants exhibited slightly reduced fertility and impaired seed filling. Our findings identify the JAO pathway as an integral component of basal JA/JA-Ile homeostasis and an important determinant of the growth-defense tradeoff in rice. The regulatory function of this pathway is conserved in monocots, opening possibilities for selectively modulating basal JA responses in major cereal crops to optimize agronomic traits.