Ndecky Simon, Malherbe Ludivine, Villette Claire, Chalvon Véronique, Meusnier Isabelle, Beltran-Valencia Dennisse, Baumberger Nicolas, Riemann Michael, Kroj Thomas, Champion Antony, Heitz Thierry
Institut de Biologie Moléculaire des Plantes (IBMP) du CNRS, Université de Strasbourg, 67000 Strasbourg, France.
PHIM Plant Health Institute, Université de Montpellier, INRAE, CIRAD, Institut Agro, IRD, 34000 Montpellier, France.
Plant Physiol. 2025 Apr 30;198(1). doi: 10.1093/plphys/kiaf161.
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 4 JAO-related homologs, 3 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.
茉莉酸途径中的分解代谢转化对植物激素信号输出有重大影响。在双子叶植物中,茉莉酸氧化酶(JAO)分解代谢途径导致茉莉酸(JA)羟基化,从而限制其缀合形成生物活性茉莉酰异亮氨酸(JA-Ile)。在此,我们对水稻(Oryza sativa)中的JAO途径进行了功能表征,并证明了其在促进营养组织生长和减弱JA反应中的关键作用。水稻基因组编码4个与JAO相关的同源物,其中3个在体外产生羟基-JA,并拯救了拟南芥jao2-2突变体的高防御表型。通过构建和分析一系列单突变到四突变的水稻jao突变体,我们发现累积JAO缺失对JA代谢、基础防御水平、生长抑制、适应性和整体代谢重编程具有累加效应。JAO缺陷系的生长在幼年期受到显著抑制,而在后期营养发育阶段影响较小,在此期间,植物对稻瘟病菌(Magnaporthe oryzae)的致病和无毒菌株具有增强的抗性。此外,jao突变体的育性略有降低,种子充实受损。我们的研究结果表明,JAO途径是基础JA/JA-Ile稳态的一个组成部分,也是水稻生长-防御权衡的一个重要决定因素。该途径的调节功能在单子叶植物中是保守的,为选择性调节主要谷类作物的基础JA反应以优化农艺性状开辟了可能性。