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bioRxiv · 10.1101/686709

Stress- and pathway-specific impacts of impaired jasmonoyl-isoleucine (JA-Ile) catabolism on defense signaling and biotic stress resistance in Arabidopsis

Marquis, V.·Smirnova, E.·Poirier, L.·Zumsteg, J.·Schweizer, F.·Reymond, P.·Heitz, T.
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Abstract

Jasmonate (JA) synthesis and signaling are essential for plant defense upregulation upon herbivore or microbial attacks. Stress-induced accumulation of jasmonoyl-isoleucine (JA-Ile), the bioactive hormonal form triggering major transcriptional changes, is often dynamic and transient, due to the existence of potent removal mechanisms. Two distinct but interconnected JA-Ile turnover pathways have been described in Arabidopsis, either via cytochrome P450 (CYP94)-mediated oxidation, or through deconjugation by the amidohydrolases (AH) IAR3 and ILL6. Their impact was not well known because of gene redundancy and compensation mechanisms when each pathway was partially impaired. Here we address the consequences of fully blocking either or both pathways on JA homeostasis and defense signaling in three mutant backgrounds: a double iar3 ill6 (2ah) mutant, a triple cyp94b1 b3 c1 mutant (3cyp), and a newly generated quintuple (5ko) mutant deficient in all known JA-Ile-degrading activities. These lines behaved very differently in response to either mechanical wounding, insect attack or fungal infection, highlighting the stress-specific contributions and impacts of JA-Ile catabolic pathways. Deconjugation and oxidative pathways contributed additively to JA-Ile removal upon wounding, but their genetic impairement had opposite impacts on Spodoptera littoralis larvae feeding: 2ah line was more resistant whereas 3cyp was more susceptible to insect attack. In contrast, 2ah, 5ko but not 3cyp overaccumulated JA-Ile upon inoculation by Botrytis cinerea, yet 3cyp was most resistant to the fungus. Despite of building-up unprecedented JA-Ile levels, 5ko displayed near WT levels of resistance in both bioassays. Molecular and metabolic analysis indicated that restrained JA-Ile catabolism resulted in enhanced defense and resistance levels only if genes encoding JAZ or JAM negative regulators were not simultaneously overstimulated. Our data demonstrate that despite of acting on a shared hormonal substrate, AH or/and CYP94 deficiency differentially impacts JA homeostasis, responses and tolerance to related biotic stresses.

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Marquis, V., Smirnova, E., Poirier, L., Zumsteg, J., Schweizer, F., Reymond, P., Heitz, T.. 2019-06-28. Stress- and pathway-specific impacts of impaired jasmonoyl-isoleucine (JA-Ile) catabolism on defense signaling and biotic stress resistance in Arabidopsis. https://doi.org/10.1101/686709

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