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I Jasmonate Perception by Inositol-Phosphate-Potentiated COI1 Jasmonate Perception by Inositol-phosphate-potentiated COI1- JAZ Co-receptor Laura B. Sheard A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Washington 2012 Program Authorized to Offer Degree: Pharmacology i University of Washington Graduate School This is to certify that I have examined this copy of a doctoral dissertation by Laura B. Sheard and have found that it is complete and satisfactory in all respects and that any and all revisions required by the final examining committee have been made. Chair of the Supervisory Committee: _______________________________________________________________ Ning Zheng Reading Committee: _______________________________________________________________ Ning Zheng _______________________________________________________________ Chris Hague _______________________________________________________________ Richard Gardner Date: _____________________________________ ii In presenting this dissertation in partial fulfillment of the requirements for the doctoral degree at the University of Washington, I agree that the Library shall make its copies freely available for inspection. I further agree that extensive copying of the dissertation is allowable only for scholarly purposes, consistent with “fair use” as prescribed in the U.S. Copyright Law. Requests for copying or reproduction of this dissertation may be referred to Proquest Information and Learning, 300 North Zeeb Road, Ann Arbor, MI 48106-1346, 1-800-521-0600, to whom the author has granted “the right to reproduce and sell (a) copies of the manuscript in microform and/or (b) printed copies of the manuscript made from microform.” Signature ___________________________ Date ___________________________ iii University of Washington Abstract Jasmonate Perception by Inositol-phosphate-potentiated COI1-JAZ Co-receptor Laura B. Sheard Chair of the Supervisory Committee: Professor Ning Zheng Department of Pharmacology Jasmonates (JAs) are a family of plant hormones that regulate plant growth, development, and responses to stress. The F-box protein CORONATINE-INSENSITIVE 1 (COI1) mediates JA signaling by promoting hormone-dependent ubiquitination and degradation of transcriptional repressor JAZ proteins. Despite its importance, the mechanism of JA perception remains unclear. Here we present structural and pharmacological data to show that the true JA 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 a-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 JA co-receptor complex, inositol iv pentakisphosphate, which interacts with both COI1 and JAZ adjacent to the ligand. Our results unravel the mechanism of JA perception and highlight the ability of F-box proteins to evolve as multi-component signaling hubs. v TABLE OF CONTENTS Page List of Figures........................................................................................................vii List of Tables........................................................................................................viii Chapter 1: Introduction to plant hormones and their receptors ............................11 1.1 Auxin and TIR1...................................................................................12 1.2 Abscisic acid and PYR/PYL/RCAR ...................................................23 1.3 Strigolactone and MAX2.....................................................................29 1.4 Jasmonate and COI1............................................................................39 Chapter 2: COI1-JAZ complex as a jasmonate co-receptor .................................41 2.1 Results .................................................................................................41 2.2 Materials and Methods ........................................................................46 Chapter 3: Jasmonate-binding pocket on COI1 ....................................................49 3.1 Results .................................................................................................49 3.2 Materials and Methods ........................................................................58 Chapter 4: Structural roles of the bipartite JAZ degron .......................................60 4.1 Results .................................................................................................60 Chapter 5: Inositol pentakiphosphate as a cofactor of COI1 to potentiate jasmonate perception by COI1-JAZ1.............................65 5.1 Results .................................................................................................65 5.2 Materials and Methods ........................................................................67 Chapter 6: InsP5 potentiates jasmonate perception by COI1-JAZ1......................78 6.1 Results .................................................................................................78 6.2 Materials and Methods ........................................................................85 Chapter 7: Discussions ..........................................................................................88 Bibliography..........................................................................................................90 vi LIST OF FIGURES Figure Number................................................................................................... Page 1. Figure 1.1 Auxin signaling pathway ................................................................21 2. Figure 1.2 Abscisis acid (ABA) signalling pathway.........................................27 3. Figure 1.3 Strigolactone structural backbone ...................................................38 4. Figure 2.1 COI1-ASK1 and JAZ proteins form a high-affinity JA co-receptor ..............................................................................42 5. Figure 2.2 Radioligand binding and pull-down analysis of COI1-JAZ interaction......................................................................44 6. Figure 3.1 Crystal structure of the COI1-ASK1 complex with JA-Ile and the JAZ degron peptide............................................................52 7. Figure 3.2. Sequence allignment and structural annotation of COI1 orthologues ........................................................................54 8. Figure 3.3 Residues within the JA-Ile binding pocket of COI1 are critical for ligand-induced COI1-JAZ1 interaction ...........56 9.Figure 3.4 Hydrophobic binding pockets for JA-Ile on COI1 .................................................................................................57 10.Figure 4.1 The bi-partite JAZ degron peptide..................................................63 11.Figure 5.1 Identification of an inositol pentakisphosphate cofactor in COI1...............................................................................................70 12.Figure 5.2 Structural mass spectrometry analysis of the COI1-ASK1 complex.............................................................................72 13.Figure 5.3. Mass spectrometry analysis of Ins(1,2,4,5,6)P5 purified from recombinant COI1-ASK1 ................................74 14.Figure 5.4 Surface conservation mapping of COI1..........................................77 15.Figure 6.1 Inositol phosphate is an essential component of the COI1-JAZ co-receptor......................................................................................81 16.Figure 6.2 Mutational studies of COI1 residues in the putative InsP5 binding site.......................................................83 vii LIST OF TABLES Table Number.................................................................................................... Page 1. Crystallographic data collection and refinement statistics ................................51 viii ACKNOWLEDGEMENTS This work would not have been possible without the help from all members of the Zheng Laboratory and the generous support from the Cellular and Molecular Biology Training Grant from National Institutes of Health, T32 GM07270. ix DEDICATION For My Family x CHAPTER 1 Introduction to plant hormones and their receptors For much of the Kingdom Plantae, life and developmental choices are regulated almost exclusively by a handful of small organic molecules, the phytohormones. Many of these hormones are produced locally in the plant and transported to target tissues within the plant either from cell to cell transport or through the vasculature. Other hormones are volatilized and are sensed by distal portions of the same plant, or by other nearby plants. The first five “classic phytohormones” identified were auxin, gibberellin, cytokinin, ethylene, and abscisic acid. Since then, a number of other hormones have been isolated, including salicylic acid, jasmonates, brassinosteroids, and strigolactones. The receptors for phytohormones are diverse. Ethylene and cytokinins are sensed by transmembrane receptors, which resemble the two-component systems in prokaryotes. Brassinosteroids activate their signal transduction cascades through leucine-rich repeat receptor kinases (LRR-RKs), which are also transmembrane proteins commonly utilized by other eukaryotes including mammals. Recent studies have shown that auxin, jasmonate,
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