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HOST SPECIFICITY and PHYLOGENETIC RELATIONSHIPS AMONG TILLETIA SPECIES INFECTING WHEAT and OTHER COOL SEASON GRASSES by XIAODO

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HOST SPECIFICITY and PHYLOGENETIC RELATIONSHIPS AMONG TILLETIA SPECIES INFECTING WHEAT and OTHER COOL SEASON GRASSES by XIAODO HOST SPECIFICITY AND PHYLOGENETIC RELATIONSHIPS AMONG TILLETIA SPECIES INFECTING WHEAT AND OTHER COOL SEASON GRASSES By XIAODONG BAO A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY WASHINGTON STATE UNIVERSITY Department of Plant Pathology DECEMBER 2010 To the Faculty of Washington State University: The members of the Committee appointed to examine the dissertation of XIAODONG BAO find it satisfactory and recommend that it be accepted. Lori M. Carris, Ph.D., Chair Tobin L. Peever, Ph.D. Jack D. Rogers, Ph.D. Scot H. Hulbert, Ph.D. ii ACKNOWLEDGEMENTS I would like to express the deepest gratitude to my major advisor Dr. Lori M. Carris, for her persistent guidance, support and encouragement which make it possible to this dissertation. Her enthusiasm for research and excitement in teaching continuously provide inspiration and motivation for my academic goals. I would like to give the most sincere thanks to the members of my dissertation committee, Drs. Tobin L. Peever, Jack D. Rogers and Scot H. Hulbert, for their insightful suggestions to my research and critical review of the dissertation. I am heartily thankful to Dr. Lisa A. Castlebury (USDA-ARS, Baltimore, Maryland) for generously providing sequencing facilities and guidance for my research. I appreciate Mr. Blair J. Goates (USDA-ARS, Aberdeen, ID) for hosting our visit to National Small Grains Collections and providing a treasure of wheat bunt collections for my research. My thanks also go to Drs. Kálmán Vánky (Herbarium Ustilaginales Vánky, Germany), Lennart Johnsson (Plant Pathology and Biocontrol Unit, SLU, Sweden), Veronika Dumalasová (Research Institute of Crop Production, Czech Republic) and Denis A. Gaudet (Lethbridge Research Centre, Canada), for many of the collections used in the analyses. I would also like to thank Dr. Martin I. Chilvers, Dr. Hajime Akamatsu, Jane E. Stewart, Dr. Chuntao Yin, Janet G. Matanguihan and Jeremiah Dung, for their unselfish support on my research and writing. iii I’m thankful to the Department of Plant Pathology in Washington State University for providing great staff and facilities to support my Ph.D. program. I thank NSF grant 0542603 for providing financial support on my research. Special thanks to my family and all my friends for their love, understanding and support whenever I need it. iv HOST SPECIFICITY AND PHYLOGENETIC RELATIONSHIPS AMONG TILLETIA SPECIES INFECTING WHEAT AND OTHER COOL SEASON GRASSES Abstract by Xiaodong Bao, Ph. D. Washington State University December 2010 Chair: Lori M. Carris The 140 species of Tilletia (Ustilaginomycotina, Basidiomycota) are biotrophic pathogens that cause bunt and smut diseases of grasses (Poaceae). Among the most economically important species are the wheat bunt pathogens, T. caries, T. contraversa, and T. laevis. Most smut fungi infect relatively few hosts, but the host range of T. contraversa includes 65 species in 17 grass genera. The objective of this study was to incorporate sequence data from ITS rDNA, eukaryotic translation elongation factor 1-alpha (EF1-alpha), and the second largest subunit of RNA polymerase II (RPB2) with three anonymous loci (A13, A16 and P18) to elucidate relationships and test the host range of the wheat bunt fungi and related Tilletia species infecting cool-season grasses in the Pacific Northwestern U.S. Sorus shape and teliospore size of 60 dwarf and common bunt isolates analyzed with k-means clustering revealed two groups, one largely corresponding to common bunt and the second to dwarf bunt. Network analysis based on three anonymous loci and RBP2 region revealed three clades, but none of the clades contained isolates of all three species. Phylogenetic analyses of the three anonymous loci, EF1-alpha, ITS rDNA v and RPB2 were used to test the conspecific status of Eurasian and North American isolates of T. contraversa infecting species of nine grass genera. Phylogenetic trees were reconstructed independently for RPB2/ITS/EF1-alpha and A16/P18/ITS/EF1-alpha loci. NeighborNet networks were estimated from A16/P18/ITS/EF1-alpha loci and compared with the NeighborNet networks constructed with “gene-jackknifing” method. All phylogenetic trees and networks suggested a wide host range for T. contraversa. The analyses failed to support dwarf bunt pathogen as genetically distinct from the common bunt pathogens, but Eurasian isolates of T. contraversa on Elymus repens and Thinopyrum intermedium were consistently placed in a clade distinct from the majority of T. contraversa isolates, suggesting that substructure exists among isolates in this group. In contrast to the broad host range supported for T. contraversa, phylogenetic analysis of Tilletia species on cool-season grasses based on ITS, EF1-alpha and RPB2 revealed well-supported clades corresponding to host. A new species, T. puccinelliae, was proposed for a bunt infecting Puccinellia distans (alkaligrass) in Washington. vi TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ........................................................................................................... iii ABSTRACT .................................................................................................................................... v LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES ........................................................................................................................ x CHAPTER 1. GENERAL INTRODUCTION ......................................................................................... 1 Literature cited ................................................................................................................ 5 2. TILLETIA PUCCINELLIAE, A NEW SPECIES OF RETICULATE-SPORED BUNT FUNGUS INFECTING PUCCINELLIA DISTANS ....................................................... 8 Abstract ........................................................................................................................... 8 Introduction ..................................................................................................................... 8 Results ........................................................................................................................... 23 Taxonomy ..................................................................................................................... 27 Discussion ..................................................................................................................... 28 Acknowledgements ....................................................................................................... 32 Affiliation of Co-authors ............................................................................................... 33 Literature cited .............................................................................................................. 33 3. A MULTILOCUS PHYLOGENETIC APPROACH TO TESTING SPECIES LIMITS IN THE WHEAT BUNT FUNGI TILLETIA CARIES, T. CONTRAVERSA AND T. LAEVIS ............................................................................................................ 36 Abstract ......................................................................................................................... 36 vii Introduction ................................................................................................................... 37 Materials and Methods .................................................................................................. 41 Results ........................................................................................................................... 57 Discussion ..................................................................................................................... 69 Literature cited .............................................................................................................. 75 4. THE HOST RANGE AND SPECIES CONCEPT OF TILLETIA CONTRAVERSA ....... 83 Abstract ......................................................................................................................... 83 Introduction ................................................................................................................... 84 Materials and Methods .................................................................................................. 93 Results ........................................................................................................................... 99 Discussion ....................................................................................................................114 Literature cited .............................................................................................................118 ATTRIBUTION .......................................................................................................................... 125 APPENDIX ................................................................................................................................. 126 viii LIST OF TABLES CHAPTER 2 Table 2-1. Isolates and DNA sequences used in Chapter 2. .................................................. 10 Table 2-2. Host, infection type, morphology and germination of Tilletia species compared. ....................................................................................................................................... 16 CHAPTER 3 Table 3-1. Tilletia
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