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The Evolution of a Gene Cluster Containing a Plant-Like Protein In EVOLUTION OF A PLANT-LIKE GENE ANCIENTLY ACQUIRED AS PART OF A GENOMIC ISLAND IN XANTHOMONAS A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI‘I AT MᾹNOA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN MOLECULAR BIOSCIENCES AND BIOENGINEERING May 2012 BY KEVIN SCHNEIDER DISSERTATION COMMITTEE GERNOT PRESTING, CHAIRPERSON ANNE ALVAREZ YANGRAE CHO GUYLAINE POISSON SEAN CALLAHAN Dedicated to my Parents! i Acknowledgments I want to give my biggest thanks to Dr Gernot Presting for providing me with so many opportunities during my career at UH Manoa. The teaching assistantship I received on an unexpected short notice that began my PhD to working and publishing on exciting and interesting topics from corn centromeres to bacterial genomes. I am forever grateful for the time, patience, and energy he has spent mentoring me. This work would not have been possible without Dr Anne Alvarez. She has provided not only her knowledge of plant pathology, but also her collection of bacterial strains that the majority of my research required. Also, I thank Asoka Da Silva whom has provided his expertise and skills to culture and purify the hundreds of strains used in this study. The analysis in this work would not have begun without the initial phylogenomic analysis of Arabidopsis completed by Aren Ewing. His work laid the foundation to stick with studying bacterial genomic evolution in light of all of the wonderful work to study the genomic evolution of the centromeres of Zea mays in our lab. I also thank all of my lab mates Anupma Sharma, Thomas Wolfgruber, Jamie Allison, Jeffrey Lai, Megan Nakashima, Ronghui Xu, Zidian Xie, Grace Kwan, Margaret Ruzicka, Krystle Salazar and Erin Mitsunaga from the past and the present for their advice, help, discussions and their friendship and casual chit-chat. The work presented in this dissertation was supported by USDA #2005-34135-15972. My special thanks go to my supportive father Bruce, mother Judy, brother Robbie and sister Carrie who have been there throughout my career as a graduate student. I also thank the many friends and colleagues that have provided an unforgettable graduate school experience. ii Abstract In this thesis, I determine that XAC3314, a plant-like gene, was anciently transferred to Xanthomonas axonopodis pv. citri strain 306 (Xac_306). An XAC3314 homolog has also been reported in the sequenced strain Xanthomonas axonopodis pv. vesicatoria strain 85-10, but is absent from three sequenced strains of X. campestris and three sequenced strains of X. oryzae. XAC3314 may have been lost in these species. The genetic diversity of XAC3314 and the evolution of this gene in Xanthomonas were characterized. Furthermore, I show that XAC3314 was acquired by an ancestral genome and transferred to Xanthomonas as part of a genomic island. Anciently acquired genes are expected to have ameliorated to the native genome; therefore, these genes cannot be identified using characteristics common to a horizontal transfer event. I compared Xac_306 to other sequenced genomes to identify potential gene clusters in the vicinity of XAC3314. Analysis of these genomes revealed that XAC3314 was likely acquired as a small gene cluster, which inserted in Xanthomonas after the split of X. albilineans. Xanthomonas albilineans and Stenotrophomonas have unique gene clusters inserted at the same region as those in X. axonopodis. XAC3314 homologs were also identified in the sequenced strains of X. vasicola and X. gardneri. The diversity of XAC3314 was analyzed in Xanthomonas strains from the Pacific Bacterial Collection. A total of 307 Xanthomonas strains were classified with the RIF marker. Trees constructed from Xanthomonas RIF sequences are similar in structure to a completed multi-locus analysis of the genus [Young et al., 2008]. XAC3314 homologs are present in 98 of the 307 strains in the Pacific Bacterial Collection. The XAC3314 sequences revealed that HGT may have occurred among some strains of X. axonoodis. This work expands our understanding of bacterial genome evolution and anciently acquired gene clusters. iii Table of Contents Acknowledgments ............................................................................................................................ ii Abstract ............................................................................................................................................. iii List of Tables ..................................................................................................................................... v List of Figures................................................................................................................................... vi Chapter 1: General Introduction ............................................................................................... 1 Chapter 2: Literature Review ..................................................................................................... 2 Chapter 3: Analysis of XAC3314 within sequenced genomes .......................................... 22 3.1 Introduction ............................................................................................................................ 22 3.2 Hypothesis .............................................................................................................................. 23 3.3 Methods .................................................................................................................................. 24 3.4 Results .................................................................................................................................... 26 3.5 Discussion .............................................................................................................................. 46 3.5 Conclusion .............................................................................................................................. 49 Chapter 4: Classification of Xanthomonas strains using RIF, a computationally derived DNA marker 50 4.1 Introduction ............................................................................................................................ 50 4.2 Hypothesis .............................................................................................................................. 51 4.3 Methods .................................................................................................................................. 52 4.4 Results .................................................................................................................................... 57 4.5 Discussion .............................................................................................................................. 71 4.5 Conclusion .............................................................................................................................. 75 Chapter 5: XAC3314 diversity in the PBC ............................................................................. 76 5.1 Introduction ............................................................................................................................ 76 5.3 Methods .................................................................................................................................. 78 5.4 Results .................................................................................................................................... 80 5.5 Discussion .............................................................................................................................. 88 5.5 Conclusion .............................................................................................................................. 90 Chapter 6: Summary ................................................................................................................. 91 Appendix A: Design of RIF primers for other plant associated bacteria ........................ 92 Appendix B: Identification of Clavibacter with RIF ............................................................. 96 Appendix C: Identification of Ralstonia with RIF ................................................................ 99 Appendix D: Identification of Enterobacteriaceae with RIF ............................................ 103 Appendix E: Supplemental Figures ..................................................................................... 108 Appendix F: Supplemental Tables....................................................................................... 113 References ..................................................................................................................................... 194 iv List of Tables Table 2.1. Sequenced strains used in this study ...................................................................... 16 Table 3.1. The gene cluster in Xac_306 that includes XAC3314 ............................................. 30 Table 4.1. Genes in Xoo_311018 and Xcc_33913 containing regions that match criteria for potential markers ...................................................................................................... 60 Table 4.2. In silico comparison of Xanthomonas with the RIF marker resolves one pair of closely related strains that is unresolved with four other housekeeping genes and the ITS ................................................................................................................ 64 Table 4.3. Abbreviations for Xanthomonas
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