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

Abstract

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.

Constitutive expression of JASMONATE RESISTANT 1 induces molecular changes that prime the plants to better withstand drought

“…They could thus play a role in balancing JA‐Ile homeostasis as well as responses induced by JA‐Ile signalling. This fit well with recent findings from Marquis et al (2022) on the jao2 mutant, in which changes in JA catabolism affect JA‐Ile formation and signalling. Especially intriguing is the general high amount of the JA‐derivative 12‐ O ‐JA‐Glc and its further JAR1‐dependent increase under drought.…”

“…The results further indicate that priming, that is, changes happening long before the onset of the drought stress, as well as direct stress responses both shape the drought resistance of 35S::JAR1 (Supporting Information: Figure S7). These findings are in line with results from Marquis and coworkers (Marquis et al, 2022) showing that modulating JA turnover improved the resistance of Arabidopsis to drought and that the drought tolerance of the jao2 mutant requires JA-Ile formation by JAR1. Thus, constitutively altering jasmonate homeostasis can be a way to adapt plants to better withstand drought but possible detrimental variations in growth and life-cycle length under more favourable conditions have to be considered.…”

“…This relationship between jasmonate and drought stress was also reported for several crops (Creelman & Mullet, 1995; Du et al, 2013; Gao et al, 2004; Tayyab et al, 2020; Wang et al, 2021). Moreover, Marquis et al (2022) showed recently that an Arabidopsis mutant in the JASMONATE OXIDASE 2 ( JAO2 ) gene locus, which is affected in jasmonate homeostasis, was more resistance to drought. Its drought resistant phenotype was dependent on JA‐Ile signalling.…”

Use of sugarcane mosaic virus for virus-induced gene silencing in maize

“…Similarly, knockout of the two Arabidopsis JA-Ile hydrolase genes, IAR3 and ILL6, decreased S. littoralis caterpillar growth (Marquis et al, 2020) and knockout of jasmonate hydroxylases increased resistance to multiple biotic and abiotic stresses (Caarls et al, 2017;Smirnova et al, 2017;Marquis et al, 2021).…”

“…Conversely, RNA interference targeting JIH1 in N. attenuata made these plants more resistant to both Manduca sexta (tobacco hornworm) and Spodoptera littoralis (Egyptian cotton leafworms) (Woldemariam et al, 2012), and silencing expression of N. attenuata JA hydroxylases increased resistance to Spodoptera litura (Tang et al, 2020). Similarly, knockout of the two Arabidopsis JA-Ile hydrolase genes, IAR3 and ILL6 , decreased S. littoralis caterpillar growth (Marquis et al, 2020) and knockout of jasmonate hydroxylases increased resistance to multiple biotic and abiotic stresses (Caarls et al, 2017; Smirnova et al, 2017; Marquis et al, 2021).…”