Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

Abstract

The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JAresponsive gene expression by the bioactive form JA-isoleucine have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. Because they are induced by JA we named them JASMONATE-INDUCED OXYGENASES (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae. In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in overaccumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses.jasmonic acid | 2OG oxygenases | 12-OH-JA | plant defense

Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection

“…Coregulation analysis with confirmed JA pathway components identified three 2OGDs genes out of four in the DOXC46 subclade (Kawai et al, 2014) as prime candidates to perform such a reaction. In the course of this work, Caarls et al (2017) reported the partial characterization of these enzymes, named JASMONATE-INDUCED OXYGENASES 1 to 4 (JOX). Here, we performed extensive functional analysis of the three most expressed genes, encoding JAO/JOX2, -3, and -4 enzymes, focusing on leaf wounding and necrotrophic fungal challenges, and two stimuli triggering strong JA metabolism and signaling.…”

Green leaf volatiles and jasmonic acid enhance susceptibility to anthracnose diseases caused by Colletotrichum graminicola in maize

“…OPC‐8:0 undergoes three rounds of β‐oxidation to form (+)‐7‐ iso ‐JA, which itself is biologically inactive (Staswick and Tiryaki, ). Once synthesized, JA may be converted into a variety of derivatives, including methyl jasmonate (MeJA) and the main biologically active conjugate (+)‐7‐ iso ‐JA‐Ile (JA‐Ile) (Vick and Zimmerman, ; Staswick and Tiryaki, ; Fonseca et al , ; Yan et al , ; Caarls et al , ; Wasternack and Strnad, ). JA signalling regulates many diverse physiological processes and is a key regulator of the defence response to wounding, herbivory, and pathogen infection via induction of defensive metabolites and proteolytic enzymes (Farmer and Ryan, ; Rodriguez‐Saona et al , ; Howe and Jander, ) or emission of volatile organic compounds (VOCs), such as GLVs (Kessler and Baldwin, ), which recruit insect parasitoids (Turlings et al , ; Allman and Baldwin, ).…”

WRKY40, WRKY70, and Downy Mildew Resistant 6 (DMR6)-Like Oxygenase 1 are universal marker genes for the salicylic acid pathway in bananas

“…Studies showed that DLO1 catabolizes SA by converting SA to 2,3-dihydroxybenzoic acid (2,3-DHBA) and is a component of a negative feedback regulation system of SA levels during senescence [58]. Similar hydroxylation mechanisms to control levels of other plant hormones jasmonate and auxin have also been observed [59,60]. Since the induction of DLO1 in the negative feedback regulation of cytoplasmic SA levels may be critical to maintain the homeostasis of SA concentration.…”