Sequential oxidation of Jasmonoyl-Phenylalanine and Jasmonoyl-Isoleucine by multiple cytochrome P450 of the CYP94 family through newly identified aldehyde intermediates

Widemann, Émilie; Grausem, Bernard; Renault, H; Pineau, Emmanuelle; Heinrich, Clément F.; Lugan, Raphaël; Ullmann, Pascaline; Miesch, Laurence; Aubert, Yann; Miesch, Michel; Heitz, Thierry; Pinot, Franck

doi:10.1016/j.phytochem.2015.06.027

Cited by 28 publications

(25 citation statements)

References 54 publications

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“…Our study thus extends the role of versatile 2OGD enzymes to JAs, another class of important plant hormones. Within JA metabolism, the data indicate a clear specialization of JAO action on free JA, whereas oxidative turnover of JA-Ile and other JA-amino acid conjugates is specifically achieved by CYP94 enzymes (Kitaoka et al, 2014;Widemann et al, 2015).…”

Section: Discussion Ja Oxidation By Jao Enzymes Identifies a Missing mentioning

confidence: 95%

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

et al. 2017

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Jasmonates (JAs) orchestrate immune responses upon wound/herbivore injury or infection by necrotrophic pathogens. Elucidation of catabolic routes has revealed new complexity in jasmonate metabolism. Two integrated pathways attenuate signaling by turning over the active hormone jasmonoyl-isoleucine (JA-Ile) through ω-oxidation or deconjugation, and define an indirect route forming the derivative 12OH-JA. Here, we provide evidence for a second 12OH-JA formation pathway by direct jasmonic acid (JA) oxidation. Three jasmonic acid oxidases (JAOs) of the 2-oxoglutarate dioxygenase family catalyze specific oxidation of JA to 12OH-JA, and their genes are induced by wounding or infection by the fungus Botrytis cinerea. JAO2 exhibits the highest basal expression, and its deficiency in jao2 mutants strongly enhanced antifungal resistance. The resistance phenotype resulted from constitutive expression of antimicrobial markers rather than from their higher induction in infected jao2 plants and could be reversed by ectopic expression of any of the three JAOs in jao2. Elevated defense in jao2 was dependent on the activity of JASMONATE RESPONSE 1 (JAR1) and CORONATINE-INSENSITIVE 1 (COI1) but was not correlated with enhanced JA-Ile accumulation. Instead, jao2 mutant lines displayed altered accumulation of several JA species in healthy and challenged plants, suggesting elevated metabolic flux through JA-Ile. Collectively, these data identify the missing enzymes hydroxylating JA and uncover an important metabolic diversion mechanism for repressing basal JA defense responses.

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Section: Discussion Ja Oxidation By Jao Enzymes Identifies a Missing mentioning

confidence: 95%

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

et al. 2017

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“…Consistently, knocking-out or overexpressing ILR1 had no measurable impact on the endogenous JA profile or visible JA-deficient phenotypes. However, we cannot rule out the possibility that ILR1’s function as a JA conjugate hydrolase could become important in certain conditions, cell types, or plants species, where these rarer JA conjugates accumulate to higher concentrations ( Widemann et al , 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Hormone crosstalk in wound stress response: wound-inducible amidohydrolases can simultaneously regulate jasmonate and auxin homeostasis inArabidopsis thaliana

Zhang

Poudel

Jewell

et al. 2015

EXBOTJ

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“…Indeed, whereas 12OH-JA-Ile is still able to weakly promote the formation of COI1-JAZ complexes or to induce detectable transcriptional responses, 12COOH-JA-Ile is completely inactive [ 15 , 19 ]. CYP94 catalysis may be even more diversified as CYP94B1, B3 and C1 enzymes can also oxidize other JA conjugates including JA-valine or JA-phenylalanine [ 20 , 21 ], and CYP94C1 activity generates 12CHO-JA-Ile aldehyde in planta [ 21 ].…”

Section: Introductionmentioning

confidence: 99%

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

Widemann

Smirnova

Aubert

et al. 2016

Plants

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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.

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Sequential oxidation of Jasmonoyl-Phenylalanine and Jasmonoyl-Isoleucine by multiple cytochrome P450 of the CYP94 family through newly identified aldehyde intermediates

Cited by 28 publications

References 54 publications

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

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

Hormone crosstalk in wound stress response: wound-inducible amidohydrolases can simultaneously regulate jasmonate and auxin homeostasis inArabidopsis thaliana

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

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