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The JAZ family of repressors is the missing link in jasmonate signalling

Nature volume 448, pages 666–671 (2007)Cite this article

Abstract

Jasmonates are essential phytohormones for plant development and survival. However, the molecular details of their signalling pathway remain largely unknown. The identification more than a decade ago of COI1 as an F-box protein suggested the existence of a repressor of jasmonate responses that is targeted by the SCFCOI1 complex for proteasome degradation in response to jasmonate. Here we report the identification of JASMONATE-INSENSITIVE 3 (JAI3) and a family of related proteins named JAZ (jasmonate ZIM-domain), in Arabidopsis thaliana. Our results demonstrate that JAI3 and other JAZs are direct targets of the SCFCOI1 E3 ubiquitin ligase and jasmonate treatment induces their proteasome degradation. Moreover, JAI3 negatively regulates the key transcriptional activator of jasmonate responses, MYC2. The JAZ family therefore represents the molecular link between the two previously known steps in the jasmonate pathway. Furthermore, we demonstrate the existence of a regulatory feed-back loop involving MYC2 and JAZ proteins, which provides a mechanistic explanation for the pulsed response to jasmonate and the subsequent desensitization of the cell.

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Figure 1: JAI3-dependent gene expression and identification of JAI3.
Figure 2: JAI3–COI1 interaction and COI1-dependent proteasome degradation of JAI3.
Figure 3: Regulation of MYC2 by JAI3.
Figure 4: Functional redundancy among JAZ proteins.
Figure 5: Feed-back regulation of JAZ expression by MYC2.

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Acknowledgements

We thank C. Castresana, J. A. García, J. Paz-Ares and S. Prat for critical reading of the manuscript and V. Rubio , J. C. del Pozo and J. M. Iglesias-Pedraz for advice on pull-down and proteasome degradation experiments. We also thank M. Laos and S. Gutiérrez for technical assistance. We are grateful to B. Thines and J. Browse for sharing results before publication. We also thank J. Turner for providing coi1-1 seeds, P. Staswick for jar1 and NASC for T-DNA insertions lines and full-length cDNAs. This work was supported by funding from the Ministerio de Educación y Ciencia of Spain (to R.S., J.L.M. and M.R.P.), and the Comunidad de Madrid and European Comission (to R.S.). A.C. was supported by an EMBO long-term Fellowship, and S.F. by a Portuguese FCT fellowship.

Author Contributions A.C. was responsible for experiments of Fig. 1b–h and Fig. 2c–i, S.F. performed all pull-down experiments, G.F., in vitro degradation experiments and EMSA, B.A., two-hybrid assays, J.M.C., G.G.-C. and I.L.-V., microarray analysis and A.C., O.L., F.M.L., J.L.M. and M.R.P. mapped jai3-1. R.S. designed experiments, supervised the work and wrote the manuscript. All authors discussed the results and commented on the manuscript.

MIAMExpress Accession numbers for all microarray experiments are: E-ATMX-15, E-ATMX-16, E-ATMX-17 and E-ATMX-18. Accession numbers for JAZ family members are: JAZ1, At1g19180; JAZ2, At1g74950; JAI3(JAZ3), At3g17860; JAZ4, At1g48500; JAZ5, At1g17380; JAZ6, At1g72450; JAZ7, At2g34600; JAZ8, At1g30135; JAZ9, At1g70700; JAZ10, At5g13220; JAZ11, At3g43440; and JAZ12, At5g20900.

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Author notes

  1. O. Lorenzo

    Present address: Present address: Dpto. de Fisiología Vegetal. Centro Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca, Plaza de los Doctores de la Reina s/n, 37007 Salamanca, Spain.,

  2. A. Chini, S. Fonseca and G. Fernández: These authors contributed equally to this work.

Authors and Affiliations

  1. Departamento de Genética Molecular de Plantas and,,

    A. Chini, S. Fonseca, G. Fernández, B. Adie, J. M. Chico, O. Lorenzo & R. Solano

  2. Unidad de Genómica, Centro Nacional de Biotecnología-CSIC, Campus Universidad Autónoma, 28049 Madrid, Spain,

    G. García-Casado, I. López-Vidriero & R. Solano

  3. División de Genética and Instituto de Bioingeniería, Universidad Miguel Hernández, Campus de Elche, 03202 Elche, Spain,

    F. M. Lozano, M. R. Ponce & J. L. Micol

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Chini, A., Fonseca, S., Fernández, G. et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671 (2007). https://doi.org/10.1038/nature06006

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