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The Role of Water Stress in Plant Disease Resistance and the Impact Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations 2009 The oler of water stress in plant disease resistance and the impact of water stress on the global transcriptome and survival mechanisms of the phytopathogen Pseudomonas syringae Brian Carl Freeman Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/etd Part of the Plant Pathology Commons Recommended Citation Freeman, Brian Carl, "The or le of water stress in plant disease resistance and the impact of water stress on the global transcriptome and survival mechanisms of the phytopathogen Pseudomonas syringae" (2009). Graduate Theses and Dissertations. 10537. https://lib.dr.iastate.edu/etd/10537 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. iii The role of water stress in plant disease resistance and the impact of water stress on the global transcriptome and survival mechanisms of the phytopathogen Pseudomonas syringae by Brian C. Freeman A dissertation submitted to the graduate faculty in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Major: Plant Pathology Program of Study Committee: Gwyn A. Beattie, Major Professor Larry J. Halverson Edward J. Braun Thomas J. Baum Lynn G. Clark Iowa State University Ames, Iowa 2009 Copyright © Brian C. Freeman, 2009. All rights reserved. ii Dedication To my parents, who inspired me to dream about the stars, and to my wife, who helped me reach them. iii Table of Contents Abstract .......................................................................................................................................................................iv General Introduction ................................................................................................................................................... 1 Dissertation organization ......................................................................................................................................... 2 Chapter 1. Literature Review ..................................................................................................................................... 3 The leaf as a habitat for bacterial colonization ........................................................................................................ 3 Cellular water movement and bacterial adaptation to water stress ......................................................................... 5 Disease mechanisms of Pseudomonas syringae ....................................................................................................... 8 Plant defenses against bacterial pathogens ............................................................................................................ 12 References ............................................................................................................................................................... 16 Chapter 2. Bacterial growth restriction during Arabidopsis thaliana resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity .......................................................... 25 Abstract ................................................................................................................................................................... 25 Introduction ............................................................................................................................................................ 26 Materials and Methods ........................................................................................................................................... 29 Results ..................................................................................................................................................................... 31 Discussion ............................................................................................................................................................... 47 Acknowledgements .................................................................................................................................................. 52 References ............................................................................................................................................................... 53 Chapter 3. Whole-genome transcript responses of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000 to osmotic stress........................................................................................................................................... 57 Abstract ................................................................................................................................................................... 57 Introduction ............................................................................................................................................................ 58 Materials and Methods ........................................................................................................................................... 59 Results ..................................................................................................................................................................... 62 Discussion ............................................................................................................................................................... 75 Acknowledgements .................................................................................................................................................. 80 References ............................................................................................................................................................... 80 Chapter 4. Identification of the trehalose biosynthetic loci in Pseudomonas syringae pv. tomato and their contribution to osmotolerance and phyllosphere fitness ........................................................................................ 86 Abstract ................................................................................................................................................................... 86 Introduction ............................................................................................................................................................ 87 Materials and Methods ........................................................................................................................................... 89 Results ..................................................................................................................................................................... 93 Discussion ............................................................................................................................................................. 102 Acknowledgements ................................................................................................................................................ 104 References ............................................................................................................................................................. 105 Chapter 5. Conclusions and future directions ....................................................................................................... 107 References ............................................................................................................................................................. 110 iv Abstract Leaf water status may play a significant role in determining the outcome of bacterial- plant interactions based on changes in leaf hydration as well as the molecular and physiological changes that occur in bacterial cells when responding to such stresses. In this study, we characterized localized changes in leaf hydration of Arabidopsis thaliana that occurred in response to challenge with the ubiquitous bacterial plant pathogen Pseudomonas syringae. We found that A. thaliana resistance to P. syringae pv. tomato DC3000 cells expressing avrRpm1 involved virtually complete cessation of vascular water movement into the infection site coupled with water loss through the stomata. Interestingly, suppression of bacterial growth during AvrRpm1-mediated resistance was prevented by physically blocking leaf water loss through the stomata or by incubating plants at high relative humidity. Collectively, these results indicate that gene-for-gene resistance in A. thaliana requires at least a localized loss of water for effective suppression of P. syringe growth, suggesting that this water loss either directly starves the invading bacteria of water or induces other components of the hypersensitive response that suppress bacterial growth. To understand the responses of P. syringae to low water availability and if these responses vary among strains, we performed a transcriptome analysis of the closely related strains P. syringae pv. tomato DC3000 and pv. syringae B728a exposed to water stress. We found significant differences in gene expression between the two strains. For example, certain osmoadaptation
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