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Rational design of a ligand-based antagonist of jasmonate perception

Nature Chemical Biology volume 10, pages 671–676 (2014)Cite this article

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Abstract

(+)-7-iso-Jasmonoyl-L-isoleucine (JA-Ile) regulates developmental and stress responses in plants. Its perception involves the formation of a ternary complex with the F-box COI1 and a member of the JAZ family of co-repressors and leads to JAZ degradation. Coronatine (COR) is a bacterial phytotoxin that functionally mimics JA-Ile and interacts with the COI1-JAZ co-receptor with higher affinity than JA-Ile. On the basis of the co-receptor structure, we designed ligand derivatives that spatially impede the interaction of the co-receptor proteins and, therefore, should act as competitive antagonists. One derivative, coronatine-O-methyloxime (COR-MO), has strong activity in preventing the COI1-JAZ interaction, JAZ degradation and the effects of JA-Ile or COR on several JA-mediated responses in Arabidopsis thaliana. Moreover, it potentiates plant resistance, preventing the effect of bacterially produced COR during Pseudomonas syringae infections in different plant species. In addition to the utility of COR-MO for plant biology research, our results underscore its biotechnological potential for safer and sustainable agriculture.

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Figure 1: Effect of COR-MO on COR-dependent anthocyanin accumulation, root growth inhibition and COI1/JAZ9 interaction.
Figure 2: Effect of COR-MO on COR-mediated JAZ9 degradation and JA- and COR-dependent JAZ2 gene expression.
Figure 3: COR-MO does not affect auxin perception and signaling.
Figure 4: Effect of COR-MO on the infection by the necrotrophic pathogen B. cinerea and the bacterial hemibiotroph strains Pst DC3000 and DC3118 (COR−).

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Acknowledgements

We thank K.-i. Hayashi (Okayama University) for important suggestions for the design of the antagonists. J. Browse (Washington State University) kindly provided the 35S:JAZ1-GUS seeds. M. Estelle (University of California–San Diego) kindly provided DR5:GUS and Dexp:TIR1-myc/tir1-1 seeds and the IAA7-GST clone. We obtained the fungal pathogen B. cinerea from E. Monte (Instituto Hispano-Luso de Investigaciones Agrarias (CIALE)). We also thank J. Paz-Ares (CNB-CSIC) and members of the lab for critical reading of the manuscript and suggestions. This work was financed by grants to R.S. (BIO2010-21739, CSD2007-00057 and EUI2008-03666) from the Spanish Ministerio de Ciencia e Innovación. I.M. was supported by a predoctoral fellowship from the Ministerio de Educación, Spain (grant AP2010-1410). A.C. and S.G.-I. were supported by postdoctoral fellowships from the Spanish Ministerio de Ciencia e Innovación ('Ramón y Cajal' 2010-05680 and 'Juan de la Cierva' JCI-2010-07532, respectively). M.B. was supported by a JAE-Doc fellowship (2010-01411) from CSIC.

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Authors and Affiliations

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

    Isabel Monte, Andrea Chini, Selena Gimenez-Ibanez, Marta Boter & Roberto Solano

  2. Division of Physiological Chemistry II, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden

    Mats Hamberg

  3. Genomics Unit, National Centre for Biotechnology, Consejo Superior de Investigaciones Científicas, Campus University Autónoma, Madrid, Spain

    Gloria García-Casado

  4. Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle, Germany

    Andrea Porzel

  5. Systems Biology Department, CNB, Consejo Superior de Investigaciones Científicas, Campus University Autónoma, Madrid, Spain

    Florencio Pazos

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  1. Isabel Monte
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Contributions

I.M., A.C. and R.S. designed the research. I.M., A.C., S.G.-I., G.G.-C. and M.B. performed experiments and wrote the corresponding methods. M.H. synthesized the derivatives and wrote the corresponding methods. A.P. obtained the NMR data. F.P. performed in silico analyses. I.M. and R.S. wrote the manuscript. All of the authors read and edited the manuscript.

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Correspondence to Roberto Solano.

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Supplementary information

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Supplementary Results, Supplementary Figures 1–8 and Supplementary Tables 1–4. (PDF 5504 kb)

Supplementary Table 1

Genes upregulated and downregulated by COR-MO in the profiling of plants treated with COR versus COR-COR-MO (XLSX 41 kb)

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Monte, I., Hamberg, M., Chini, A. et al. Rational design of a ligand-based antagonist of jasmonate perception. Nat Chem Biol 10, 671–676 (2014). https://doi.org/10.1038/nchembio.1575

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