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Mortierellaceae Phylogenomics and Tripartite Plant-Fungal-Bacterial Symbiosis of Mortierella Elongata

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Mortierellaceae Phylogenomics and Tripartite Plant-Fungal-Bacterial Symbiosis of Mortierella Elongata MORTIERELLACEAE PHYLOGENOMICS AND TRIPARTITE PLANT-FUNGAL-BACTERIAL SYMBIOSIS OF MORTIERELLA ELONGATA By Natalie Vandepol A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of Microbiology & Molecular Genetics – Doctor of Philosophy 2020 ABSTRACT MORTIERELLACEAE PHYLOGENOMICS AND TRIPARTITE PLANT-FUNGAL-BACTERIAL SYMBIOSIS OF MORTIERELLA ELONGATA By Natalie Vandepol Microbial promotion of plant growth has great potential to improve agricultural yields and protect plants against pathogens and/or abiotic stresses. Soil fungi in Mortierellaceae are non- mycorrhizal plant associates that frequently harbor bacterial endosymbionts. My research focused on resolving the Mortierellaceae phylogeny and on characterizing the effect of Mortierella elongata and its bacterial symbionts on Arabidopsis thaliana growth and molecular functioning. Early efforts to classify Mortierellaceae were based on morphology, but phylogenetic studies with ribosomal DNA (rDNA) markers have demonstrated conflicting taxonomic groupings and polyphyletic genera. In this study, I applied two approaches: low coverage genome (LCG) sequencing and high-throughput targeted amplicon sequencing to generate multi-locus sequence data. I combined these datasets to generate a well-supported genome-based phylogeny having broad sampling depth from the amplicon dataset. Resolving the Mortierellaceae phylogeny into monophyletic groups led to the definition of 14 genera, 7 of which are newly proposed. Mortierellaceae are broadly considered plant associates, but the underlying mechanisms of association are not well understood. In this study, I focused on the symbiosis between M. elongata, its endobacteria, and A. thaliana. I measured aerial plant growth and seed production and used transcriptomics to characterize differentially expressed plant genes (DEGs) while varying fungal treatments. M. elongata was shown to promote aerial plant growth and affect seed production independent of endobacteria. A. thaliana DEGs were related to hormone signaling, immune responses, root development, abiotic stress, and metabolism. These data suggest that the mechanism of plant-fungal symbiosis involves fungal manipulation and stimulation of the auxin, ethylene, and ROS response pathways. Future experiments are proposed that could test these hypotheses and further characterize the fungal side of this symbiosis. ACKNOWLEDGEMENTS I would like to thank my supervisor and mentor, Dr. Gregory Bonito, for his guidance and support through this process. I would like to thank my committee, Dr. Ashley Shade, Dr. Hideki Takahashi, Dr. Frances Trail, and Dr. Sheng-Yang He, for their guidance, constructive criticism, and support throughout my research and professional development. I would like to thank my labmates for their time, support, community, and invaluable assistance in designing, conducting, and surviving my research, especially Dr. Nico Benucci, Dr. Pedro Beschoren, Abigail E Bryson, Julian Liber, Bryan Rennick, and Xinxin Wang. I am grateful to Amy McGovern and Gail Doehring for assistance in performing DNA extractions, the MLST library preparation and sequencing, and metadata collection in Chapter 2. I am grateful to Dr Marty Chilvers, Dr. Andrea Porras-Alfaro, Dr Matthew E Smith, Dr. Matt Kasson and the ZyGoLife project for contributing isolates that were used in my phylogenetic analyses. The collection of Modicella provided by Dr. M.E. Smith added significant value to my phylogenetic study. I thank Dr. Kevin Liu for advice on phylogenetic analyses, as well as Bryan Rennick and Alicja Okrasińska for proofreading Chapter 2 and helpful discussions. I would like to thank Abigail Bryson and Bryan Rennick for their extensive assistance with setting up plant-fungal interaction experiments, Xinxin Wang for her tireless and inexplicably enthusiastic assistance collecting Arabidopsis seeds from plant material, and Natalie Golematis for her help with antibiotic passaging to cure fungal strains and DNA extractions for qPCR analyses. I would like to thank Dr. Zsofia Szendrei for generously providing access to her lab microbalance for weighing seeds and plants. I am grateful to Dr. Pat Edger for his advice on RNA- seq experimental design and data analysis and to Keith Koonter and Dr. Matthew Greishop for sharing their automated image analysis pipeline. I am endlessly grateful to my friends and family for their love and understanding throughout my academic training, despite my preoccupation, stress, and distance, especially Diane iv Vandepol, Katherine Vandepol, Karen Matlock, and Dr. Amanda Lorenz. I would not have completed this dissertation research without the love, advice, and steadfast support of my partner, Dr. Jason Matlock. I would also like to acknowledge the companionship and unconditional love of Arthur Vandepol, who stayed by my side every day and through every all-nighter. v TABLE OF CONTENTS LIST OF TABLES ..................................................................................................................... viii LIST OF FIGURES .................................................................................................................... ix KEY TO ABBREVIATIONS ........................................................................................................ xi CHAPTER 1. INTRODUCTION .................................................................................................. 1 Problem Statement ................................................................................................................. 1 Background ............................................................................................................................ 2 Mortierellaceae Phylogeny .................................................................................................. 2 Plant-Fungal Symbiosis .....................................................................................................10 Mortierellaceae-Plant Symbiosis ........................................................................................18 Research Focus ....................................................................................................................23 Value of this research ........................................................................................................24 CHAPTER 2. RESOLVING THE MORTIERELLACEAE PHYLOGENY THROUGH SYNTHESIS OF MULTI-GENE PHYLOGENETICS AND PHYLOGENOMICS ..............................................25 Authors & Contributions .........................................................................................................25 Introduction ...........................................................................................................................25 Materials & Methods ..............................................................................................................28 Sampling, Isolation, & Culture Conditions ..........................................................................28 Preliminary Isolate Identification .........................................................................................30 Genomic DNA Extraction ...................................................................................................30 Low Coverage Genome (LCG) Library Preparation & Sequencing .....................................30 Low-Coverage Genome (LCG) Sequence Analysis ...........................................................31 PHYling methods for genome analysis ...............................................................................32 Multi-Gene Phylogenetic (MGP) Primer Design & Validation .............................................33 MGP Multiplex Amplification, Library Preparation, & Sequencing .......................................34 MGP Sequence Analysis ...................................................................................................34 Results ..................................................................................................................................36 Geographic and Biodiversity Sampling ...............................................................................36 The Low Coverage Genome Approach ..............................................................................38 The Multi-Gene Phylogenetics Approach ...........................................................................39 Taxonomy .............................................................................................................................44 Accepted Genera ...............................................................................................................45 Novel Genera .....................................................................................................................51 Discussion .............................................................................................................................61 Conclusions ...........................................................................................................................66 Figures & Tables ...................................................................................................................68 CHAPTER 3. MORTIERELLA ELONGATA STIMULATES AERIAL GROWTH, SEED PRODUCTION, AND RESPONSES TO AUXIN, ETHYLENE, AND REACTIVE OXYGEN SPECIES IN ARABIDOPSIS THALIANA................................................................................. 170 Authors & Contributions ......................................................................................................
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