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Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid.
Proc Natl Acad Sci U S A. 2017 06 13; 114(24):6388-6393.PN

Abstract

The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JA-responsive gene expression by the bioactive form JA-isoleucine have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. Because they are induced by JA we named them JASMONATE-INDUCED OXYGENASES (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in overaccumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses.

Authors+Show Affiliations

Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands.Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands.Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands.Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands.Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The Netherlands.Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands.Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands.Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The Netherlands.Plant-Microbe Interactions, Department of Biology, Utrecht University, 3508 TB Utrecht, The Netherlands; g.vandenackerveken@uu.nl.

Pub Type(s)

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

Language

eng

PubMed ID

28559313

Citation

Caarls, Lotte, et al. "Arabidopsis JASMONATE-INDUCED OXYGENASES Down-regulate Plant Immunity By Hydroxylation and Inactivation of the Hormone Jasmonic Acid." Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 24, 2017, pp. 6388-6393.
Caarls L, Elberse J, Awwanah M, et al. Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc Natl Acad Sci U S A. 2017;114(24):6388-6393.
Caarls, L., Elberse, J., Awwanah, M., Ludwig, N. R., de Vries, M., Zeilmaker, T., Van Wees, S. C. M., Schuurink, R. C., & Van den Ackerveken, G. (2017). Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proceedings of the National Academy of Sciences of the United States of America, 114(24), 6388-6393. https://doi.org/10.1073/pnas.1701101114
Caarls L, et al. Arabidopsis JASMONATE-INDUCED OXYGENASES Down-regulate Plant Immunity By Hydroxylation and Inactivation of the Hormone Jasmonic Acid. Proc Natl Acad Sci U S A. 2017 06 13;114(24):6388-6393. PubMed PMID: 28559313.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. AU - Caarls,Lotte, AU - Elberse,Joyce, AU - Awwanah,Mo, AU - Ludwig,Nora R, AU - de Vries,Michel, AU - Zeilmaker,Tieme, AU - Van Wees,Saskia C M, AU - Schuurink,Robert C, AU - Van den Ackerveken,Guido, Y1 - 2017/05/30/ PY - 2017/6/1/pubmed PY - 2018/5/15/medline PY - 2017/6/1/entrez KW - 12-OH-JA KW - 2OG oxygenases KW - jasmonic acid KW - plant defense SP - 6388 EP - 6393 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc Natl Acad Sci U S A VL - 114 IS - 24 N2 - The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JA-responsive gene expression by the bioactive form JA-isoleucine have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. Because they are induced by JA we named them JASMONATE-INDUCED OXYGENASES (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in overaccumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/28559313/Arabidopsis_JASMONATE_INDUCED_OXYGENASES_down_regulate_plant_immunity_by_hydroxylation_and_inactivation_of_the_hormone_jasmonic_acid_ L2 - http://www.pnas.org/cgi/pmidlookup?view=long&pmid=28559313 DB - PRIME DP - Unbound Medicine ER -