Abstract
Jasmonate and related signalling compounds have a crucial role in both host immunity and development in plants, but the molecular details of the signalling mechanism are poorly understood. Here we identify members of the jasmonate ZIM-domain (JAZ) protein family as key regulators of jasmonate signalling. JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Jasmonate treatment causes JAZ1 degradation and this degradation is dependent on activities of the SCFCOI1 ubiquitin ligase and the 26S proteasome. Furthermore, the jasmonoyl–isoleucine (JA–Ile) conjugate, but not other jasmonate-derivatives such as jasmonate, 12-oxo-phytodienoic acid, or methyl-jasmonate, promotes physical interaction between COI1 and JAZ1 proteins in the absence of other plant proteins. Our results suggest a model in which jasmonate ligands promote the binding of the SCFCOI1 ubiquitin ligase to and subsequent degradation of the JAZ1 repressor protein, and implicate the SCFCOI1–JAZ1 protein complex as a site of perception of the plant hormone JA–Ile.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Genome-wide analysis of the JAZ subfamily of transcription factors and functional verification of BnC08.JAZ1-1 in Brassica napus
Biotechnology for Biofuels and Bioproducts Open Access 12 September 2022
-
The Musa troglodytarum L. genome provides insights into the mechanism of non-climacteric behaviour and enrichment of carotenoids
BMC Biology Open Access 24 August 2022
-
Jasmonates and Histone deacetylase 6 activate Arabidopsis genome-wide histone acetylation and methylation during the early acute stress response
BMC Biology Open Access 11 April 2022
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout





References
Mandaokar, A. et al. Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J. 46, 984–1008 (2006)
Farmer, E. E. & Ryan, C. A. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl Acad. Sci. USA 87, 7713–7716 (1990)
Vijayan, P., Shockey, J., Lévesque, C. A., Cook, R. J. & Browse, J. A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7209–7214 (1998)
Kessler, A., Halitschke, R. & Baldwin, I. T. Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305, 665–668 (2004)
Farmer, E. E. Surface-to-air signals. Nature 411, 854–856 (2001)
Reymond, P. et al. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132–3147 (2004)
Conconi, A., Smerdon, M. J., Howe, G. A. & Ryan, C. A. The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation. Nature 383, 826–829 (1996)
Browse, J. in Vitamins and Hormones (ed. Litwack, G.) 431–456 (AP-Elsevier, New York, 2005)
Feys, B., Benedetti, C. E., Penfold, C. N. & Turner, J. G. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751–759 (1994)
Xie, D. X., Feys, B. F., James, S., Nieto-Rostro, M. & Turner, J. G. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094 (1998)
Xiao, S. et al. COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell 16, 1132–1142 (2004)
Staswick, P. E. & Tiryaki, I. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16, 2117–2127 (2004)
Turner, J. G., Ellis, C. & Devoto, A. The jasmonate signal pathway. Plant Cell 14 (Suppl.). S153–S164 (2002)
Li, L. et al. The tomato homolog of CORONATINE INSENSITIVE1 is required for maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16, 126–143 (2004)
Funk, C. D. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871–1875 (2001)
Deshaies, R. J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15, 435–467 (1999)
Moon, J., Parry, G. & Estelle, M. The ubiquitin-proteasome pathway and plant development. Plant Cell 16, 3181–3195 (2004)
Lorenzo, O. & Solano, R. Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8, 532–540 (2005)
Xu, L. et al. The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919–1935 (2002)
Jensen, A. B., Raventos, D. & Mundy, J. Fusion genetic analysis of jasmonate-signalling mutants in Arabidopsis. Plant J. 29, 595–606 (2002)
Lorenzo, O., Chico, J. M., Sanchez-Serrano, J. J. & Solano, R. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16, 1938–1950 (2004)
Ellis, C. & Turner, J. G. The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13, 1025–1033 (2001)
Devoto, A. et al. COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J. 32, 457–466 (2002)
Devoto, A. et al. Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol. Biol. 58, 497–513 (2005)
Shikata, M. et al. Characterization of Arabidopsis ZIM, a member of a novel plant-specific GATA factor gene family. J. Exp. Bot. 55, 631–639 (2004)
Schmid, M. et al. A gene expression map of Arabidopsis thaliana development. Nature Genet. 37, 501–506 (2005)
Stintzi, A. & Browse, J. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl Acad. Sci. USA 97, 10625–10630 (2000)
Katagiri, F., Thilmony, R. & He, S. Y. in The Arabidopsis Book (eds Somerville, C. R. & Meyerowitz, E.M.) doi:10.1199-tab.0039 (American Society of Plant Biologists, Rockville, Maryland, 2002)
McConn, M., Creelman, R. A., Bell, E., Mullet, J. E. & Browse, J. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl Acad. Sci. USA 94, 5473–5477 (1997)
Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001)
Sasaki, A. et al. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299, 1896–1898 (2003)
Chini, A. et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature doi: 10.1038/nature06006 (this issue).
Kramell, R. et al. Amino acid conjugates of jasmonic acid induce jasmonate-responsive gene expression in barley (Hordeum vulgare L.). FEBS Lett. 414, 197–202 (1997)
Seo, H. S. et al. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc. Natl Acad. Sci. USA 98, 4788–4793 (2001)
Stintzi, A., Weber, H., Reymond, P., Browse, J. & Farmer, E. E. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl Acad. Sci. USA 98, 12837–12842 (2001)
Tan, X. et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640–645 (2007)
Li, C. et al. Role of β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17, 971–986 (2005)
Schilmiller, A. L., Koo, A. J. K. & Howe, G. A. Functional diversification of acyl-CoA oxidases in jasmonic acid biosynthesis. Plant Physiol. 143, 812–824 (2007)
Acknowledgements
We are particularly grateful to Y. Shimada and members of his laboratory for the publicly available data in Fig. 1b, J. Turner for coi1-1, R. Kramell and P. Staswick for providing jasmonate–amino-acid conjugates, and M. Garavito for pRMG-nMAL. We thank C. Skidmore for help preparing the figures, B. Ryan and C. Somerville for discussions and critical reading of the manuscript. Arabidopsis T-DNA mutants were from the Arabidopsis Biological Resource Center, Ohio State University. This work was supported by funding from the US Department of Energy (J.B., S.Y.H., G.A.H.), the National Institutes of Health (S.Y.H., G.A.H.) and the Agricultural Research Center at WSU (J.B.).
Author Contributions B.T., L.K., M.M., S.Y.H., G.A.H. and J.B. planned experiments and analyses. B.T., L.K., M.M., Y.N., A.M., G.L. and K.N. performed experiments and analysed the results. B.T., S.Y.H., G.A.H. and J.B. wrote the manuscript. All authors discussed the results and commented on the manuscript.
The GenBank accession number for the tomato JAZ1 nucleotide sequence is EF591123. The GEO accession number for microarray data is GDS2133.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The GenBank accession number for the tomato JAZ1 nucleotide sequence is EF591123. The GEO accession number for microarray data is GDS2133. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Methods and Results, Supplementary Figures S1 - S5 with Legends and additional references. (PDF 792 kb)
Rights and permissions
About this article
Cite this article
Thines, B., Katsir, L., Melotto, M. et al. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665 (2007). https://doi.org/10.1038/nature05960
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature05960
This article is cited by
-
Long-lasting memory of jasmonic acid-dependent immunity requires DNA demethylation and ARGONAUTE1
Nature Plants (2023)
-
Plant Immunity: A Plastic System Operated Through Cell-Fate Transition
Journal of Plant Biology (2023)
-
Histone deacetylase gene SlHDA3 is involved in drought and salt response in tomato
Plant Growth Regulation (2023)
-
Identification of TIFY gene family in walnut and analysis of its expression under abiotic stresses
BMC Genomics (2022)
-
Genome-wide identification and characterization of the TIFY gene family in kiwifruit
BMC Genomics (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.