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Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor

Abstract

Jasmonates are a family of plant hormones that regulate plant growth, development and responses to stress. The F-box protein CORONATINE INSENSITIVE 1 (COI1) mediates jasmonate signalling by promoting hormone-dependent ubiquitylation and degradation of transcriptional repressor JAZ proteins. Despite its importance, the mechanism of jasmonate perception remains unclear. Here we present structural and pharmacological data to show that the true Arabidopsis jasmonate receptor is a complex of both COI1 and JAZ. COI1 contains an open pocket that recognizes the bioactive hormone (3R,7S)-jasmonoyl-l-isoleucine (JA-Ile) with high specificity. High-affinity hormone binding requires a bipartite JAZ degron sequence consisting of a conserved α-helix for COI1 docking and a loop region to trap the hormone in its binding pocket. In addition, we identify a third critical component of the jasmonate co-receptor complex, inositol pentakisphosphate, which interacts with both COI1 and JAZ adjacent to the ligand. Our results unravel the mechanism of jasmonate perception and highlight the ability of F-box proteins to evolve as multi-component signalling hubs.

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Figure 1: COI1–ASK1 and JAZ proteins form a high-affinity jasmonate co-receptor.
Figure 2: Crystal structure of the COI1–ASK1 complex with JA-Ile and the JAZ degron peptide.
Figure 3: The bi-partite JAZ degron peptide.
Figure 4: Identification of an inositol pentakisphosphate cofactor in COI1.
Figure 5: Inositol phosphate is an essential component of the COI1–JAZ co-receptor.

Accession codes

Primary accessions

Protein Data Bank

Data deposits

Structural coordinates and structural factors have been deposited in the Protein Data Bank under accession numbers 3OGK, 3OGL and 3OGM.

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Acknowledgements

We thank the beamline staff of the Advanced Light Source at the University of California at Berkeley and the Advanced Photon Source at Argonne National Laboratory for help with data collection. We also thank P. Rajagopal and R. Klevit for 31P NMR analysis, M. Sadilek for mass spectrometry analysis, L. Katsir, C. Hague and J. Lyssand for radioligand binding assay assistance, and C. Mecey and M. Melotto for initial cloning of coi1(sdm) mutants. We also thank members of the Zheng laboratory and W. Xu laboratory and R. Gardner for discussion and help. This work is supported by the Howard Hughes Medical Institute and grants from the National Institutes of Health (R01 CA107134 to N.Z., T32 GM07270 to L.B.S., R01GM57795 to G.A.H., R01AI068718 to S.Y.H.), National Science Foundation (0929100 to N.Z.), US Department of Energy (DE-FG02-99ER20323 to J.B. and DE-FG02-91ER20021 to G.A.H. and S.Y.H.), Michigan State University Plant Science Fellowship (J.W.), the Welch Foundation (I-1304 to J.R.) and the European Research Council (ERC) under the European Community’s Seventh Framework Program (FP7/2007-2013)/ ERC Grant agreement no. 239679 (G.B.-N. and M.S.).

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L.B.S., G.A.H. and N.Z. conceived and L.B.S. conducted radioligand binding and additional functional experiments. X.T., H.M. and L.B.S. purified the COI1–ASK1 complex and conducted crystallographic experiments. X.T. crystallized and determined the structures of the COI1–ASK1–JAZ1 hormone complexes. L.B.S., X.T. and N.Z. analysed crystallographic data. J.W. and S.Y.H. conceived and J.W. conducted yeast two-hybrid experiments. G.B.-N. and M.S. conducted and interpreted the structural mass spectrometry experiments. L.B.S., H.M., T.R.H., F.-F.H., J.R. and N.Z. conceived and conducted experiments for inositol phosphate purification and identification. Y.K. synthesized jasmonate stereoisomers. L.B.S. and N.Z. wrote the manuscript with comments from all authors.

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Correspondence to Ning Zheng.

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Sheard, L., Tan, X., Mao, H. et al. Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor. Nature 468, 400–405 (2010). https://doi.org/10.1038/nature09430

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