Abstract

Biosynthesis of the phytohormone jasmonoyl-isoleucine (JA-Ile) requires reduction of the JA precursor 12-oxo-phytodienoic acid (OPDA) by OPDA reductase 3 (OPR3). Previous analyses of the opr3-1 Arabidopsis mutant suggested an OPDA signaling role independent of JA-Ile and its receptor COI1; however, this hypothesis has been challenged because opr3-1 is a conditional allele not completely impaired in JA-Ile biosynthesis. To clarify the role of OPR3 and OPDA in JA-independent defenses, we isolated and characterized a loss-of-function opr3-3 allele. Strikingly, opr3-3 plants remained resistant to necrotrophic pathogens and insect feeding, and activated COI1-dependent JA-mediated gene expression. Analysis of OPDA derivatives identified 4,5-didehydro-JA in wounded wild-type and opr3-3 plants. OPR2 was found to reduce 4,5-didehydro-JA to JA, explaining the accumulation of JA-Ile and activation of JA-Ile-responses in opr3-3 mutants. Our results demonstrate that in the absence of OPR3, OPDA enters the β-oxidation pathway to produce 4,5-ddh-JA as a direct precursor of JA and JA-Ile, thus identifying an OPR3-independent pathway for JA biosynthesis.

  • Compound

    N-[2-[3-oxo-2-(2Z)-2-penten-1-yl-cyclopentyl]acetyl]-L-isoleucine

  • Compound

    N-[2-[(1R,2S)-3-oxo-2-(2Z)-2-penten-1-yl-cyclopentyl]acetyl]-L-isoleucine

  • Compound

    3-Oxo-2-(2Z)-2-penten-1-yl-cyclopentane-1-acetic acid

  • Compound

    (1S,5S)-4-Oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-octanoic acid

  • Compound

    4-Oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-hexanoic acid

  • Compound

    4-Oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-acetic acid

  • Compound

    N-[2-[4-oxo-5-(2Z)-2-penten-1-yl-2-cyclopenten-1-yl]acetyl]-L-isoleucine

  • Compound

    4-Oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-butanoic acid

  • Compound

    (1S,5R)-4-Oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-acetic acid

  • Compound

    (1R,5S)-4-Oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-acetic acid

  • Compound

    N-[2-[(1S,5R)-4-oxo-5-(2Z)-2-penten-1-yl-2-cyclopenten-1-yl]acetyl]-L-isoleucine

  • Compound

    N-[2-[(1R,5S)-4-oxo-5-(2Z)-2-penten-1-yl-2-cyclopenten-1-yl]acetyl]-L-isoleucine

  • Compound

    Methyl 4-oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-acetate

  • Compound

    Methyl (1S,5R)-4-oxo-5-(2Z)-2-penten-1-yl-2-cyclopentene-1-acetate

  • Compound

    (1S,5R,6S)-2-Aza-(1-carboxy-2-methylbut-1-yl)-6-(2Z)-2-penten-1-yl-bicyclo[3.3.0]octane-3,7-dione

  • Compound

    (1S,5R,6R)-2-Aza-(1-carboxy-2-methylbut-1-yl)-6-(2Z)-2-penten-1-yl-bicyclo[3.3.0]octane-3,7-dione

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Acknowledgements

We thank V. Rubio, J.J. Sánchez-Serrano, J. Salinas and members of R.S.'s lab for critical reading of the manuscript and C. Mark for English editing. U. Olsson, Karolinska Institutet, is thanked for her assistance with NMR analysis and F. Schaller (Ruhr-University Bochum, Germany) for OPR1/2 constructs. Work in R.S.'s lab was funded by the Spanish Ministry for Science and Innovation grant BIO2016-77216-R (AEI/FEDER, EU) and Fundación UAM Grant 2015007. P.R. and S.L. are funded by the Swiss National Science Foundation Grant Nr. 31003A_169278. Work in A.S.'s lab was supported by the German Research Foundation (DFG; SCHA 591/6-1, STI 295/2-1).

Author information

Affiliations

  1. Department of Plant Molecular Genetics, National Centre for Biotechnology, Consejo Superior de Investigaciones Científicas (CNB-CSIC), Madrid, Spain.

    • Andrea Chini
    • , Isabel Monte
    •  & Roberto Solano
  2. Environmental Biology Department, University of Navarra, Navarre, Spain.

    • Angel M Zamarreño
    •  & José M García-Mina
  3. Division of Physiological Chemistry II, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden.

    • Mats Hamberg
  4. Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland.

    • Steve Lassueur
    •  & Philippe Reymond
  5. Institute of Plant Physiology and Biotechnology, University of Hohenheim, Stuttgart, Germany.

    • Sally Weiss
    • , Annick Stintzi
    •  & Andreas Schaller
  6. Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, Germany.

    • Andrea Porzel

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Contributions

A.C., M.H., A. Schaller, A. Stintzi, P.R., J.M.G.-M. and R.S. designed the experiments, A.C. performed experiments in Figures 1, 2, 4c, and 6e,f and Supplementary Figures 2, 3, 7 and 8 and prepared the material for measurements in Figures 3, 5, and 6a–c and SF4. I.M. performed experiments in Figure 4a,b. A.M.Z. made metabolite measurements in Figures 3, 5 and 6 and Supplementary Figures 4–7. M.H. synthesized all chemicals described in methods. S.L. performed insect assays. S.W. performed experiments in Figure 6d. A. Schaller and A. Stintzi obtained the double opr mutants. A.P. recorded NMR data. All authors interpreted the results. A.C. and R.S. wrote the manuscript. All authors edited and commented on the manuscript. R.S. supervised the work.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Roberto Solano.

Supplementary information

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    Supplementary Text and Figures

    Supplementary Tables 1–3 and Supplementary Figures 1–8

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    Life Sciences Reporting Summary

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    Supplementary Note 1

    Synthetic Procedures

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DOI

https://doi.org/10.1038/nchembio.2540

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