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Use of Whole Genome Sequence Data to Characterize Mating and Rna USE OF WHOLE GENOME SEQUENCE DATA TO CHARACTERIZE MATING AND RNA SILENCING GENES IN TILLETIA SPECIES By SEAN WESLEY MCCOTTER A thesis submitted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE IN PLANT PATHOLOGY WASHINGTON STATE UNIVERSITY Department of Plant Pathology DECEMBER 2014 © Copyright by SEAN WESLEY MCCOTTER, 2014 All Rights Reserved © Copyright by SEAN WESLEY MCCOTTER, 2014 All Rights Reserved To the Faculty of Washington State University: The members of the Committee appointed to examine the thesis of SEAN WESLEY MCCOTTER find it satisfactory and recommend that it be accepted. Lori M. Carris, Ph.D., Chair Dorrie Main, Ph.D. Patricia Okubara, Ph.D. Lisa A. Castlebury, Ph. D. ii ACKNOWLEDGMENTS The research presented in this thesis could not have been carried out without the expertise and cooperation of others in the scientific community. Significant contributions were made by colleagues here at Washington State University, at the United States Department of Agriculture and at Agriculture and Agri-Food Canada. I would like to start by thanking my committee members Dr. Lori Carris, Dr. Lisa Castlebury, Dr. Pat Okubara and Dr. Dorrie Main, who provided guidance on procedure, feedback on my research as well as contacts and laboratory resources. Dr. André Lévesque of AAFC initially alerted me to the prospect of collaboration with other AAFC Tilletia researchers and placed me in contact with Dr. Sarah Hambleton, whose lab sequenced four out of five strains of Tilletia used in this study (CSSP CRTI 09-462RD). Dr. Prasad Kesanakurti and Jeff Cullis coordinated my access to AAFC’s genome and transcriptome data for these species. Separately, Dr. Guus Bakkeren, also of AAFC, provided technical advice on cloning and sequencing smut fungal mating loci. Dr. Jodi Humann was an invaluable source of technical advice and the key individual responsible for the PacBio+454 hybrid genome assembly. Crucially, Dr. Ping Zheng developed Perl scripts which saved me weeks of work. Mark Wildung and Derek Pouchnik at the WSU Laboratory for Biotechnology and Bioanalysis were responsible for next generation sequencing on both PacBio RS and Roche 454 platforms. Dr. Tobin Peever at WSU graciously allowed me bench space in his laboratory where my lab-mate, Dr. Lydia Tymon, provided a great partner-in- a-pinch for impromptu dance parties and rarely criticized my controversial tastes in music. iii USE OF WHOLE GENOME SEQUENCE DATA TO CHARACTERIZE MATING AND RNA-SILENCING GENES IN TILLETIA SPECIES Abstract by Sean Wesley McCotter, M.S. Washington State University December 2014 Chair: Lori M. Carris Tilletia species (Ustilaginomycotina, Basidiomycota), the bunt fungi, are pathogens of grasses (Poaceae) such as wheat (Triticum aestivum) and ryegrass (Lolium spp.) and represent a molecularly underexplored branch of the fungal tree of life. Most Tilletia species must mate prior to infecting their hosts, highlighting the importance of sex in their life cycles. Mating loci identified in related smut fungi consist of a pheromone precursor, G-protein-coupled pheromone receptor and two divergently transcribed homeodomain transcription factors. The primary objective of this study was to annotate mating and RNA-silencing genes in available genomes of the systemically infecting bunts T. caries and T. contraversa, and non-systemically infecting bunts T. indica and T. walkeri. Phylogenetic comparisons of homeodomain proteins in Tilletia species reveal four clades with more than two mating-type homeodomain proteins present in T. caries and T. controversa. Mating genes identified in each species in single copy include putative pheromone precursors and G-protein-coupled-pheromone-receptors. A high level of protein- sequence homology is seen in comparisons of mating-type genes between T. caries and T. contraversa, as well as between T. walkeri and T. indica, however lower homology is present in iv comparisons between the two groups. Comparisons of RNA-silencing protein copy numbers in T. caries 517 with those of other basidiomycetes reveal an expansion of some RNA-silencing- related gene families in T. caries. Preliminary genome annotation was carried out using AUGUSTUS. Predicted proteins were clustered by similarity. Putative mating and RNA- silencing-related genes were identified in each species by homology to genes previously identified in Ustilaginomycotina. Transcript evidence for all mating-genes identified was obtained from cDNA. This work is the first to identify mating genes in T. caries, T. contraversa, T. indica and, T. walkeri. While it demonstrates conservation of the mating type genes found in Ustilago spp., it also shows that mating-type homeodomain proteins in T. caries and T. controversa are present in multiple copies, rather than just a divergently transcribed pair. This work provides an informative first look into the genomes of these economically and historically important plant pathogens, and highlights unique molecular features of their mating and RNA- silencing mechanisms, which distinguish them from other fungi. v TABLE OF CONTENTS Page ACKNOWLEDGMENTS .......................................................................................................... iii ABSTRACT ................................................................................................................................ iv LIST OF TABLES ........................................................................................................................x LIST OF FIGURES ................................................................................................................... xii CHAPTER ONE 1. INTRODUCTION TO COMMON BUNT .......................................................................1 Common Bunt Biology .....................................................................................................1 Brief History of Common Bunt ........................................................................................2 Common Bunt in Organic Wheat .....................................................................................4 The Phylogenetic Placement of the Bunt Fungi ...............................................................5 2. MATING IN BASIDIOMYCETES ...............................................................................10 Introduction .....................................................................................................................10 The Molecular Basis of Mating in Ustilago maydis and its Close Relatives..................11 The Organization of Tetrapolar Versus Bipolar Mating Loci and the Generation of non- Parental Mating Types by Recombination between Mating Loci ......................14 Multiallelic Mating Systems ...........................................................................................15 Mating in Agaricomycotina: Molecular Basis and Manifestations in phenotype ...........16 Mating in Pucciniomycotina ...........................................................................................20 Cryptic Sex in Basidiomycetes .......................................................................................21 Observations on Mating in Tilletia Species ....................................................................22 vi 3. CHAPTER ONE REFERENCES ...................................................................................26 CHAPTER TWO 1. INTRODUCTION ..........................................................................................................36 2. METHODS .....................................................................................................................39 Strains and Culture Conditions .......................................................................................39 Nucleic Acids Extraction ................................................................................................40 Whole Genome Sequencing ............................................................................................40 cDNA Preparation ...........................................................................................................41 Polymerase Chain Reaction and Sanger Sequencing......................................................41 Genome Annotation and Protein Family Clustering .......................................................42 Annotation of the Mating Loci .......................................................................................43 Phylogenetic Analyses ....................................................................................................44 3. RESULTS .......................................................................................................................44 Homeodomain Proteins ...................................................................................................44 Putative b-East mating type HDPs .....................................................................49 Putative b-West mating type HDPs.....................................................................51 Other HDPs ........................................................................................................56 Putative GPCR (STE3 Orthologs) and Pheromone Precursors ......................................59 Synteny Analyses ............................................................................................................62 4. DISCUSSION .................................................................................................................66
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