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Dynamics of Jasmonate Metabolism upon Flowering and across Leaf Stress Responses in Arabidopsis thaliana

Institut de Biologie Moléculaire des Plantes, CNRS-UPR2357, associée à l'Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France
Laboratoire de Chimie Organique Synthétique, Unité Mixte de Recherche 7177, Université de Strasbourg, 67008 Strasbourg Cedex, France
These authors contributed equally to the paper.
Author to whom correspondence should be addressed.
Academic Editor: Debora Gasperini
Received: 7 December 2015 / Revised: 22 December 2015 / Accepted: 28 December 2015 / Published: 6 January 2016
(This article belongs to the Special Issue The Jasmonate Pathway)
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The jasmonic acid (JA) signaling pathway plays important roles in adaptation of plants to environmental cues and in specific steps of their development, particularly in reproduction. Recent advances in metabolic studies have highlighted intricate mechanisms that govern enzymatic conversions within the jasmonate family. Here we analyzed jasmonate profile changes upon Arabidopsis thaliana flower development and investigated the contribution of catabolic pathways that were known to turnover the active hormonal compound jasmonoyl-isoleucine (JA-Ile) upon leaf stress. We report a rapid decline of JA-Ile upon flower opening, concomitant with the massive accumulation of its most oxidized catabolite, 12COOH-JA-Ile. Detailed genetic analysis identified CYP94C1 as the major player in this process. CYP94C1 is one out of three characterized cytochrome P450 enzymes that define an oxidative JA-Ile turnover pathway, besides a second, hydrolytic pathway represented by the amido-hydrolases IAR3 and ILL6. Expression studies combined with reporter gene analysis revealed the dominant expression of CYP94C1 in mature anthers, consistent with the established role of JA signaling in male fertility. Significant CYP94B1 expression was also evidenced in stamen filaments, but surprisingly, CYP94B1 deficiency was not associated with significant changes in JA profiles. Finally, we compared global flower JA profiles with those previously reported in leaves reacting to mechanical wounding or submitted to infection by the necrotrophic fungus Botrytis cinerea. These comparisons revealed distinct dynamics of JA accumulation and conversions in these three biological systems. Leaf injury boosts a strong and transient JA and JA-Ile accumulation that evolves rapidly into a profile dominated by ω-oxidized and/or Ile-conjugated derivatives. In contrast, B. cinerea-infected leaves contain mostly unconjugated jasmonates, about half of this content being ω-oxidized. Finally, developing flowers present an intermediate situation where young flower buds show detectable jasmonate oxidation (probably originating from stamen metabolism) which becomes exacerbated upon flower opening. Our data illustrate that in spite conserved enzymatic routes, the jasmonate metabolic grid shows considerable flexibility and dynamically equilibrates into specific blends in different physiological situations. View Full-Text
Keywords: Arabidopsis; JA-Ile; cytochrome P450; CYP94; amidohydrolase; hormone homeostasis; jasmonate catabolism Arabidopsis; JA-Ile; cytochrome P450; CYP94; amidohydrolase; hormone homeostasis; jasmonate catabolism

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This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. (CC BY 4.0).

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Widemann, E.; Smirnova, E.; Aubert, Y.; Miesch, L.; Heitz, T. Dynamics of Jasmonate Metabolism upon Flowering and across Leaf Stress Responses in Arabidopsis thaliana. Plants 2016, 5, 4.

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