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New Species and Phylogeny of the Genus Phytophthora Xiao Yang

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New Species and Phylogeny of the Genus Phytophthora Xiao Yang New Species and Phylogeny of the Genus Phytophthora Xiao Yang Dissertation submitted to the faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy In Plant Pathology, Physiology, and Weed Science Chuanxue Hong, Chair Anton B. Baudoin Warren E. Copes Erik L. Stromberg Brett M. Tyler December 9th, 2014 Blacksburg, VA Keywords: Phytophthora, aquatic species, novel species, morphology, taxonomy, phylogeny, systematics New Species and Phylogeny of the Genus Phytophthora Xiao Yang ABSTRACT The genus Phytophthora includes many agriculturally and ecologically important plant pathogens. Characterization of new Phytophthora species is the first and a most critical step to understanding their biology, ecology and economic importance. Six novel Phytophthora species recovered from irrigation systems at ornamental plant nurseries in Mississippi and Virginia were described based on morphological, physiological and molecular characters: 1. Phytophthora mississippiae sp. nov. produces a mix of non-papillate and semi- papillate sporangia, and catenulate hyphal swellings. It is a heterothallic species. All examined isolates of P. mississippiae are A1. When paired with A2 mating type testers, P. mississippiae produces ornamented oogonia and amphigynous antheridia. It is phylogenetically grouped in Phytophthora subclade 6b based on sequences of the rRNA internal transcribed spacer (ITS) region and the mitochondrially encoded cytochrome c oxidase 1 (cox 1) gene. 2. Phytophthora hydrogena sp. nov. is heterothallic. It produces non-caducous and non-papillate sporangia. It is characterized by frequently producing widening at the pedicel tip of sporangiophores or tapered sporangial based toward the point of attachment. This species is phylogenetically placed in a high-temperature tolerant cluster in Phytophthora clade 9. All members in this cluster grow well at 35℃. 3. Phytophthora virginiana sp. nov. is a self-sterile species. All examined isolates are silent A1. It produces non-caducous and non-papillate sporangia and is also placed in the high-temperature tolerant cluster in clade 9. Morphologically, it is characterized by producing abundant thin-walled, lateral chlamydospores in carrot agar and clarified V8 juice agar. 4. Phytophthora macilentosa sp. nov. is a heterothallic species. Only A1 isolates have been found. It produces characteristic elongated, non-papillate sporangia. It is also a member of the high-temperature cluster in clade 9. 5. Phytophthora stricta sp. nov. is a heterothallic species. It produces unique non- papillate and slightly caducous sporangia with one to three constrictions on its sporangiophore. Phylogenetically, P. stricta represents a new ITS clade within the genus. 6. Phytophthora ✕stagnum nothosp. nov. is a novel hybrid species with P. taxon PgChlamydo as its paternal parent and a P. mississippiae-like species as its maternal parent. This new hybrid produces intercalary chlamydospores and catenulate hyphal swellings, which are morphological characters of P. taxon. PgChlamydo and P. mississippiae, respectively. It also produces both smooth- walled and ornamented oogonia, which may be indicative of oogonial characters of its paternal and maternal parents, respectively. By incorporating new Phytophthora species, clusters and clades, phylogenies including approximately 128 Phytophthora taxa were constructed based on sequences of five genetic markers. Among the selected genetic markers, the beta-tubulin (B-tub) gene provided the highest phylogenetic resolution. General phylogenetic structure of the B-tub phylogeny was similar to that in previous multi-locus phylogenies, except that P. iii cinnamomi, P. parvispora, P. quercina, P. stricta, and a provisional species, P. sp. e1, were not clustered in any of the 10 known Phytophthora clades and represented new clades. The B-tub phylogeny was also used to study the correlations between phylogeny and morphological characteristics including sporangial papillation, caducity, homothallism, and antheridial configuration, as well as maximum growth temperature. The results indicated that the character of sporangial papillation was mostly consistent among species within individual subclades. Maximum growth temperature was also generally correlated with phylogenetic positions. Consistency in caducity, homothallism or antheridial configuration was not found. A new multi-locus phylogeny based on sequences of 11 genetic markers of more than 146 Phytophthora species was proposed to validate new clades and clusters, as well as investigate detailed phylogenetic relations among species in this quickly expanding, taxonomically complex group of plant pathogens. iv DEDICATION To my grandfather, Mr. Yuan. v ACKNOWLEDGEMENTS I would like thank my major advisor Dr. Chuanxue Hong for his continual guidance and encouragement. I would also like to extend my deepest gratitude to my graduate committee members, Dr. Anton Baudoin, Dr. Warren Copes, Dr. Erik Stromberg, and Dr. Brett Tyler. Drs. Baudoin and Stromberg provided me with lab space, equipment, and generous guidance for my PhD research from August 2011 to May 2012 when I was taking classes in Blacksburg, VA. Dr. Baudoin also provided me excellent guidance when I was a teaching assistant for one of his courses. Dr. Copes was the coauthor of two published manuscripts in this dissertation. He was a great person to work with and a knowledgeable plant pathologist who provided me lots of great guidance to my study and research. Dr. Tyler also provided me great guidance especially for the molecular aspect of my research. I also learned a lot in the 2012 Oomycete Bioinformatics Training Workshop he organized in Blacksburg. I would like to express my deepest appreciation to Dr. Giovanni Cafà, Dr. Ping Kong, Dr. Mrinalini Nikrad, Dr. Heather Olson, Mrs. Patti Richardson, Dr. Hao Wei, Dr. Haibo Zhang and other faculty and staff at the Hampton Roads Agricultural Research and Extension Center in Virginia Beach, VA and Department of Plant Pathology, Physiology and Weed Science in Blacksburg, VA, who supported and advised my research. vi Thank Dr. Mannon Gallegly of West Virginia University, Dr. Hon Ho of New York State University, Dr. Steve Jeffers of Clemson University for helpful discussions and comments on my chapter manuscripts. vii TABLE OF CONTENTS LIST OF FIGURES ......................................................................................................................... X LIST OF TABLES ....................................................................................................................... XV CHAPTER 1 INTRODUCTION ..................................................................................................... 1 THE GENUS ‘PLANT DESTROYER’ ............................................................................................... 1 PHYTOPHTHORA BIOLOGY ........................................................................................................... 2 DESCRIPTION OF NOVEL PHYTOPHTHORA SPECIES ..................................................................... 4 AQUATIC PHYTOPHTHORA SPECIES IN IRRIGATION SYSTEMS ..................................................... 5 PHYLOGENY OF THE GENUS PHYTOPHTHORA ............................................................................. 6 RESEARCH OBJECTIVES............................................................................................................... 8 LITERATURE CITED ..................................................................................................................... 8 CHAPTER 2 PHYTOPHTHORA MISSISSIPPIAE SP. NOV., A NEW SPECIES RECOVERED FROM IRRIGATION RESERVOIRS AT A PLANT NURSERY IN MISSISSIPPI .................. 16 ABSTRACT ................................................................................................................................. 16 INTRODUCTION .......................................................................................................................... 17 MATERIALS AND METHODS ...................................................................................................... 19 RESULTS .................................................................................................................................... 22 TAXONOMY ............................................................................................................................... 24 DISCUSSION ............................................................................................................................... 26 LITERATURE CITED ................................................................................................................... 28 CHAPTER 3 A HIGH-TEMPERATURE TOLERANT SPECIES IN CLADE 9 OF THE GENUS PHYTOPHTHORA: P. HYDROGENA SP. NOV. ......................................................................... 44 ABSTRACT ................................................................................................................................. 44 INTRODUCTION .......................................................................................................................... 45 MATERIALS AND METHODS ...................................................................................................... 47 RESULTS .................................................................................................................................... 51 TAXONOMY ..............................................................................................................................
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