Broad‐spectrum stress tolerance conferred by suppressing jasmonate signaling attenuation in Arabidopsis JASMONIC ACID OXIDASE mutants

• Published in: The Plant journal : for cell and molecular biology 2022-02, Vol.109 (4), p.856-872
• Main Authors: Marquis, Valentin, Smirnova, Ekaterina, Graindorge, Stéfanie, Delcros, Pauline, Villette, Claire, Zumsteg, Julie, Heintz, Dimitri, Heitz, Thierry
• Format: Article
• Language: English
• Subjects: Abscisic acid; Abscisic Acid - metabolism; Agmatine; Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Attenuation; basal defense; Biochemistry, Molecular Biology; Botanics; Botrytis - metabolism; Cyclopentanes - metabolism; Dioxygenases - genetics; Dioxygenases - metabolism; Drought; Gene Expression Regulation, Plant; Genetic suppression; Genomics; Homeostasis; Isoleucine; Isoleucine - analogs & derivatives; JAO/JOX; jasmonate; Jasmonic acid; Life Sciences; Metabolic networks; Metabolic Networks and Pathways; metabolism; Metabolomics; Mutants; Oxidoreductases - genetics; Oxidoreductases - metabolism; Oxylipins - metabolism; Phenotype; Phenotypes; Plant Leaves - metabolism; Signal transduction; Signal Transduction - physiology; Signaling; stress tolerance; Stress, Physiological; Survival; Transcriptome; Vegetal Biology
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15598

SUMMARY Jasmonate signaling for adaptative or developmental responses generally relies on an increased synthesis of the bioactive hormone jasmonoyl‐isoleucine (JA‐Ile), triggered by environmental or internal cues. JA‐Ile is embedded in a complex metabolic network whose upstream and downstream components strongly contribute to hormone homeostasis and activity. We previously showed that JAO2, an isoform of four Arabidopsis JASMONIC ACID OXIDASES, diverts the precursor jasmonic acid (JA) to its hydroxylated form HO‐JA to attenuate JA‐Ile formation and signaling. Consequently, JAO2‐deficient lines have elevated defenses and display improved tolerance to biotic stress. Here we further explored the organization and regulatory functions of the JAO pathway. Suppression of JAO2 enhances the basal expression of nearly 400 JA‐regulated genes in unstimulated leaves, many of which being related to biotic and abiotic stress responses. Consistently, non‐targeted metabolomic analysis revealed the constitutive accumulation of several classes of defensive compounds in jao2‐1 mutant, including indole glucosinolates and breakdown products. The most differential compounds were agmatine phenolamides, but their genetic suppression did not alleviate the strong resistance of jao2‐1 to Botrytis infection. Furthermore, jao2 alleles and a triple jao mutant exhibit elevated survival capacity upon severe drought stress. This latter phenotype occurs without recruiting stronger abscisic acid responses, but relies on enhanced JA‐Ile signaling directing a distinct survival pathway with MYB47 transcription factor as a candidate mediator. Our findings reveal the selected spectrum of JA responses controlled by the JAO2 regulatory node and highlight the potential of modulating basal JA turnover to pre‐activate mild transcriptional programs for multiple stress resilience. Significance Statement Jasmonic acid oxidase 2 (JAO2) defines a metabolic diversion mechanism to attenuate basal jasmonoyl‐isoleucine formation and signaling. We investigated here by transcriptome and metabolome analysis the spectrum of defense/adaptation responses that are under JAO2 control. These include several biotic stress defensive pathways, and we further established that JAO2 deficiency triggers a drought survival pathway, identifying the modulation of basal JA metabolism as an attractive means to tailor broad‐spectrum tolerance responses.