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Characterization of Axenic Immune Deficiency in Arabidopsis Thaliana CHARACTERIZATION OF AXENIC IMMUNE DEFICIENCY IN ARABIDOPSIS THALIANA By James Michael Kremer A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of Microbiology and Molecular Genetics – Doctor of Philosophy 2017 ABSTRACT CHARACTERIZATION OF AXENIC IMMUNE DEFICIENCY IN ARABIDOPSIS THALIANA By James Michael Kremer Evolution of land plants began and has since occurred, in concert with complex communities of microorganisms, giving rise to a vast spectrum of plant-microbe relationships. Over the past decade, plant molecular biologists and microbial ecologists have worked together to identify drivers of microbiome composition that inspire hypotheses about microbiome functional potential, but many fall short of offering empirical evidence of microbiome-mediated influence on host phenotypes. Herein, I introduce a new suite of tools to explore microbiome function and report that many facets of plant immunocompetence are microbiome-dependent. Chapter One summarizes the current understanding of plant innate immunity and notable progress of plant microbiome research, including: (1) detection and response to microbe-associated molecular patterns, (2) hormone signaling during biotic interactions, (3) technology for exploration of plant microbiome ecology, (4) factors that influence microbiome community structure, and (5) a review of relevant model systems and gnotobiotic growth platforms. Chapter Two describes the development of a novel “FlowPot” growth system: a peat-based platform conducive to axenic (microbe-free), gnotobiotic (defined microbiota), and holoxenic (undefined, complex microbiota) Arabidopsis thaliana growth. This system provides the ability to maintain control of abiotic parameters and exogenous microbiota, thus providing a valuable platform for discovery for plant microbiome research. The FlowPot system and offers a substantial improvement over alternative growth systems regarding plant health, tractability to greenhouse conditions, and maintenance of bacterial alpha diversity upon inoculation with soil-derived microbiota. An implementation of the growth system is detailed in Chapter Three, featuring a comparative analysis of the axenic vs. holoxenic Arabidopsis transcriptome, metabolome, and immunocompetence. Axenic Arabidopsis has a reduced level of defense- and immunity-associated gene expression and the defense hormone salicylic acid (SA). We report that axenic Arabidopsis is compromised in defense against the foliar pathogen Pseudomonas syringae pv. tomato DC3000 (Pst). Immune elicitation experiments revealed that axenic Arabidopsis is also compromised in the ability to recognize and/or mount normal defense responses to the microbe-associated molecular pattern flg22. Axenic susceptibility to Pst is partially explained by defective innate immunity. Finally, we report the identity of differentially abundant metabolites and transcripts in axenic and holoxenic Arabidopsis that may be involved in microbiome-influenced host phenotypes. Collectively, research described in this dissertation provides new tools and a discovery platform to empirically characterize function of plant microbiota, as well as detailed characterization of axenic phenotypes and axenic immune deficiency. Copyright by JAMES MICHAEL KREMER 2017 This dissertation is dedicated to you, the reader. I hope that this will inspire new hypotheses and future experiments. v ACKNOWLEDGEMENTS First and foremost, I must acknowledge my mentors, Dr. Sheng Yang He and Dr. Jim Tiedje. Without your support and guidance, none of this work would have been possible. I was originally drawn to Michigan State University because of your respective expertise in microbial suppression of plant innate immunity and the ecology of root-associated microbiota. Over time, as I rotated in your respective laboratories and eventually began to focus my dissertation research, I realized how unique and incredible an opportunity it was to be at a place like Michigan State University; nowhere else in the world could I have such brilliant advisors with different but complementary perspectives. Both of you identify and cultivate passion in your students towards the pursuit of areas of research that inspire us individually. When the inevitable roadblocks and experimental setbacks arise, you inspire tenacity. Sheng Yang, you were incredibly patient when I was resistant to attempt certain experiments, and likewise, you trusted me to conduct many experiments that did not necessarily coincide with the primary objectives of this dissertation. By doing so, you have provided me with the incredible opportunity to make mistakes and retrospectively evaluate depth versus breadth of research, and that has taught me more than you can imagine. Jim, you inspire me to think globally, and taught me the importance of creativity and communication in science. Your academic legacy and success of past students are inspirational, and I cannot understate how honored and fortunate I am to receive your mentorship. Both of you have provided me with numerous opportunities to present at vi academic conferences and build a network of collaborators, and for this, I thank you. I also must acknowledge Dr. Paul Schulze-Lefert. You extended an invitation to visit your group in Cologne, and immediately embraced me as one of your own students. I learned a tremendous amount from your pragmatic approach to tackle highly complex scientific questions. Drs. Amine Hassani, Sergio de los Santos, JP Jerome and Brian Kvitko, you have all been incredible scientific collaborators and lifelong friends. To Kevin Nehil, Alec Bonifer, Kristin Drumheller, Alan Mundakkal, David Rhodes, Caleigh Griffin, and all of the other undergraduate researchers I have had the pleasure of advising, you have taught me more than you can realize and I cannot wait to see where life takes you. I also want to acknowledge Brad Paasch for being a great colleague and friend in our mutual pursuit to characterize microbiome function. To the many members of the He and Tiedje lab groups, you have been tremendous colleagues and thank you for all the discussions and input. It has been a pleasure to work with many of you, and I look forward to crossing paths again in the future. Finally, I must acknowledge my family. Without the tremendous unwavering love and support from my parents, I never would have finished this dissertation. To my aunt Dr. Margaret McLaughlin, your help and wisdom during the “final push” made this all possible. And to my grandmother Bernice Neuberg, your creativity and love for plants no doubt inspired me to pursue this Ph.D. vii TABLE OF CONTENTS LIST OF TABLES x LIST OF FIGURES xi Chapter 1 History and review of plant microbiome research 1 Introduction 2 Early plant pathology 5 Microbial ecology of plant and soil environments 9 The Arabidopsis thaliana model 12 Arabidopsis innate immunity 14 Defense hormone signaling 18 Systemic acquired resistance and induced systemic resistance 21 Chapter 2 Construction and optimization of a soil-based growth system conducive to axenic, gnotobiotic, and holoxenic Arabidopsis growth 23 Abstract 24 Introduction 26 Materials and Methods 31 Sterilization of the FlowPot peat-based substrate 31 FlowPot growth system assembly 31 Calcined clay system assembly 34 Soil collection 34 Preparation of input community microbiota 35 Growth system inoculation 35 Arabidopsis growth conditions 36 Protein extraction and quantification of photosynthesis-associated proteins 36 Sample collection and DNA extraction 37 16S rRNA gene fragment amplification and MiSeq Library preparation 38 Preprocessing of 16S rRNA gene fragment amplicons 39 Results 40 Arabidopsis growth in axenic FlowPots 40 Beta-diversity 43 Alpha-diversity 45 Bacterial community differentiation at the Phylum level 48 Bacterial community differentiation at the OTU level 54 Discussion 62 viii Chapter 3 Characterization of axenic Arabidopsis thaliana 76 Abstract 77 Introduction 78 Materials and Methods 84 Soil collection and biochemical analysis 84 Arabidopsis seeds and growth conditions 84 DNA extractions 85 ITS and 16S rRNA gene targeted amplification 86 Bioinformatic analysis of ITS1 and 16S rRNA gene fragment amplicons 87 RNA extraction and quantitative PCR 88 RNA seq library preparation and analysis 89 Tissue collection flg22 elicitation experiments 90 Protein extraction 91 Phytohormone quantification by UPLC/MS 91 Metabolite quantification by GC/MS 93 Bacterial growth conditions, sources, and strain construction 93 Infiltration of rosettes with bacterial suspensions 94 Bacterial multiplication in planta protocol 95 Oxidative burst assay 96 Callose deposition assay 98 Results 99 Bacterial and fungal compositions of input soil communities are distinct 99 Fungal and bacterial community differentiation 107 Axenic plants lack normal basal expression of immune-associated genes 120 Basal: metabolite analysis (GC/MS) 138 Basal: Salicylic acid quantification (UPLC/MS) 144 Transcriptional response to immune elicitation is defective in axenic plants 146 Compromised axenic posttranslational immune response 148 Oxidative burst and callose deposition are compromised in axenic plants 150 Defective priming and defense against pathogens in axenic plants 152 Discussion 156 Chapter 4 Discussion and future directions for plant microbiota research 177 Development of model host-microbiome systems with associated microbial culture collections and reference genomes 180 Define core microbiomes and metagenomes 182 Rules of synthetic,
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