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Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection.
Mol Plant. 2017 09 12; 10(9):1159-1173.MP

Abstract

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.

Authors+Show Affiliations

Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France.Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France.Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France.Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France.Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France.Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France.Laboratoire de Chimie Organique Synthétique, Institut de Chimie, Université de Strasbourg, CNRS, Strasbourg, France.Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg, Strasbourg, France. Electronic address: thierry.heitz@ibmp-cnrs.unistra.fr.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28760569

Citation

Smirnova, Ekaterina, et al. "Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses Against Botrytis Cinerea Infection." Molecular Plant, vol. 10, no. 9, 2017, pp. 1159-1173.
Smirnova E, Marquis V, Poirier L, et al. Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection. Mol Plant. 2017;10(9):1159-1173.
Smirnova, E., Marquis, V., Poirier, L., Aubert, Y., Zumsteg, J., Ménard, R., Miesch, L., & Heitz, T. (2017). Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection. Molecular Plant, 10(9), 1159-1173. https://doi.org/10.1016/j.molp.2017.07.010
Smirnova E, et al. Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses Against Botrytis Cinerea Infection. Mol Plant. 2017 09 12;10(9):1159-1173. PubMed PMID: 28760569.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection. AU - Smirnova,Ekaterina, AU - Marquis,Valentin, AU - Poirier,Laure, AU - Aubert,Yann, AU - Zumsteg,Julie, AU - Ménard,Rozenn, AU - Miesch,Laurence, AU - Heitz,Thierry, Y1 - 2017/07/29/ PY - 2017/05/15/received PY - 2017/07/12/revised PY - 2017/07/19/accepted PY - 2017/8/2/pubmed PY - 2018/5/16/medline PY - 2017/8/2/entrez KW - 2-oxoglutarate oxygenase KW - Botrytis KW - defense regulation KW - hormone metabolism KW - jasmonic acid SP - 1159 EP - 1173 JF - Molecular plant JO - Mol Plant VL - 10 IS - 9 N2 - 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. SN - 1752-9867 UR - https://www.unboundmedicine.com/medline/citation/28760569/Jasmonic_Acid_Oxidase_2_Hydroxylates_Jasmonic_Acid_and_Represses_Basal_Defense_and_Resistance_Responses_against_Botrytis_cinerea_Infection_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1674-2052(17)30206-X DB - PRIME DP - Unbound Medicine ER -