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University of Florida Thesis Or Dissertation Formatting EVOLUTION OF PLANT PATHOGENICITY IN STREPTOMYCES By YUCHENG ZHANG A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2016 © 2016 Yucheng Zhang To my family for their unconditional love and support ACKNOWLEDGMENTS I would like to express my gratitude to Dr. Rosemary Loria, my advisor, for her guidance in my research. She always encouraged me to be a passionate and independent researcher and gave me freedom to explore new research fields. During the last three years in Dr. Loria’s lab, I have learned microbiology and biotechnology skills, have developed the habits of logical thinking and proper questioning. From Dr. Loria, I also learned the importance of networking and collaboration for a successful career in academia. I would like to thank Drs. Valerie de Crecy-Lagard, Jeffrey B. Jones, and G. Shad Ali for serving on my committee, and for providing their time and expertise. Their advice and recommendations are valuable resources for my projects, and for the improvement of my dissertation. I am grateful to the past members of the Loria lab. Your friendship and support let me feel very happy in this international family. I would like to express my special thanks to Drs. Isolde Francis and Jose C. Huguet Tapia for kindly teaching me Streptomyces techniques and bioinformatics. I would like to thank Dr. Yousong Ding and his student Mr. Ran Zuo for helpful collaborations, particularly HPLC and LC-MS analysis. Last but most importantly, I deeply thank my parents (Zhongle Zhang and Tongling Liu), my parents-in-law (Yingshun Qiu and Shuqin Zhao), my wife Sai Qiu, and my adorable daughter Flora Zhang for their unconditional support and encouragement. They are the most important motivation for pursuing my academic and career goals. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................4 LIST OF TABLES ...........................................................................................................................8 LIST OF FIGURES .........................................................................................................................9 ABSTRACT ...................................................................................................................................11 CHAPTER 1 GENERAL INTRODUCTION ..............................................................................................13 The Streptomyces Genus .........................................................................................................13 Streptomyces Genomes ...........................................................................................................13 Plant Pathogenic Streptomyces Species ..................................................................................14 Streptomyces scabiei (syn. S. scabies) ............................................................................15 Streptomyces acidiscabies ...............................................................................................15 Streptomyces turgidiscabies ............................................................................................16 Streptomyces ipomoeae ...................................................................................................16 Streptomyces europaeiscabiei .........................................................................................16 Streptomyces stelliscabiei ................................................................................................16 Streptomyces reticuliscabiei ............................................................................................17 Streptomyces caviscabies ................................................................................................17 Streptomyces luridiscabiei, Streptomyces puniciscabiei, and Streptomyces niveiscabiei ..................................................................................................................17 Pathogenicity and Virulence Factors ......................................................................................17 Thaxtomins ......................................................................................................................17 Nec1 .................................................................................................................................19 TomA ...............................................................................................................................20 Fas Operon .......................................................................................................................21 Coronafacic Acid .............................................................................................................21 Concanamycins ................................................................................................................22 FD-891 .............................................................................................................................22 Borrelidin .........................................................................................................................23 Other Unknown Pathogenicity/virulence Factors ...........................................................23 Integrative and Conjugative Elements ....................................................................................23 Pathogenicity Islands of Streptomyces ...................................................................................26 The PAI in S. turgidiscabies Car8 ...................................................................................26 The Toxicogenic Region and Colonization Region in Other Pathogenic Species ..........26 Goals and Objectives of This Study .......................................................................................27 2 PHYLOGENY OF THE STREPTOMYCES GENUS ............................................................29 Introduction .............................................................................................................................29 5 Materials and methods ............................................................................................................31 Bacterial Strains, Culture Conditions and DNA Extraction ............................................31 Virulence Bioassays ........................................................................................................32 Analysis of Thaxtomin A Production ..............................................................................32 Genome Sequencing and Assembly ................................................................................32 Ortholog Retrieval and Single-copy Cluster Search .......................................................33 Gene Alignment and Filtering Criteria ............................................................................33 Maximum Likelihood (ML) Phylogeny Estimation ........................................................33 Average Nucleotide Identity and in silico DNA-DNA Hybridization Estimation ..........34 Results.....................................................................................................................................34 Characterization of Pathogenic Streptomyces Isolates ....................................................34 Two Copies of Selected Housekeeping Genes Were Detected in Some Streptomyces Genomes ................................................................................................35 Phylogenomic Analysis of the Streptomyces Genus .......................................................36 isDDH and ANI Comparison of Plant Pathogenic Streptomyces Isolates ......................38 Discussion ...............................................................................................................................39 3 PROMISCUOUS PATHOGENICITY ISLANDS OF STREPTOMYCES SPP. ....................51 Materials and Methods ...........................................................................................................53 Phylogeny of the Thaxtomin Biosynthetic Cluster .........................................................53 Insertion of Antibiotic Resistance Markers in the PAI ...................................................53 Selection of Transconjugant Strains ................................................................................54 Virulence Bioassays ........................................................................................................55 Analysis of Thaxtomin A Production ..............................................................................55 Results.....................................................................................................................................56 Streptomyces Pathogens Contained Different Versions of PAIs .....................................56 ThxA-phylogeny Contradicts the Core-genome Phylogeny ...........................................57 The S. scabiei PAI was Site-specifically Mobilized into the Chromosome of Non- pathogenic Species .......................................................................................................57 PAI Acquisition Conferred a Pathogenic Phenotype in S. diastatochromogenes Transconjugants ...........................................................................................................59
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