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UNIVERSITY of CALIFORNIA RIVERSIDE Metabolic Novelties In UNIVERSITY OF CALIFORNIA RIVERSIDE Metabolic Novelties in the Oomycete Phytopathogen, Phytophthora infestans A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Microbiology by Melania Abrahamian December 2017 Dissertation Committee: Howard S. Judelson, Chairperson Katherine A. Borkovich Linda L. Walling Copyright by Melania Abrahamian 2017 The Dissertation of Melania Abrahamian is approved: Committee Chairperson University of California, Riverside Acknowledgments I would like to express my deepest appreciation to my advisor Dr. Howard Judelson for his support, guidance and patience. I have gained valuable experiences at Dr. Judelson’s lab, and because of his amazing mentorship and support for my independence I have been able to thrive as a young scientist. I am grateful for the Ph.D. training opportunity that Dr. Howard Judelson gave me in his laboratory. I would also like to thank my dissertation committee members Dr. Katherine Borkovich and Dr. Linda Walling for their strong support, valuable scientific advice, and encouragement as they made my dissertation possible. My appreciation also extends to Dr. Judelson’s laboratory current and past members, for their encouragement and help. It was a great experience working in a multicultural lab, where we could share our experiences. Finally, my huge thanks are to my parents and my husband for their limitless love, support, encouragement and guidance, without them none of this would be possible. I dedicate this work to my husband for his sacrifices and unlimited love. iv ABSTRACT OF THE DISSERTATION Metabolic Novelties in the Oomycete Phytopathogen, Phytophthora infestans by Melania Abrahamian Doctor of Philosophy, Graduate Program in Microbiology University of California, Riverside, December 2017 Dr. Howard Judelson, Chairperson Phytophthora infestans, the causal agent of potato late blight, is a significant threat to global food security. Little is known about the metabolism of this oomycete, including how it adapts to different growth and nutrient conditions, while such aspects are one key to understanding host-pathogen interactions. To identify nutrient transporter and metabolic genes involved in pathogenicity, genome and RNA-seq data were mined. One of the major findings was the identification of nitrate assimilation genes that were strongly upregulated at mid time-point tomato leaf tissues compared to late time-point. Mutants silenced for these genes were then generated, which showed a reduction in virulence. This v confirmed involvement of the nitrate assimilation genes in pathogenicity. Even though P. infestans can not grow using nitrate as the sole nitrogen source, enzyme assays and isotopic labeling studies indicated that its nitrate assimilation pathway is functional. Enzyme assays revealed few biochemical differences in the activity of nitrate reductase from P. infestans and the enzyme from Phytophthora mirabilis and Pythium ultimum, which are two oomycetes that can grow on nitrate. Isotopic labelling studies indicated that P. infestans and P. mirabilis assimilated little nitrate into amino acids in young cultures, but incorporated substantial nitrate in older cultures. In contrast, Py. ultimum utilized nitrate at both early and late growth stages. Studies of other metabolic pathways revealed the presence of mitochondrial glycolytic pay-off phase in addition to the canonical cytosolic one, and a mitochondrial serine biosynthesis pathway, which is cytoplasmic in other species; both pathways are linked through the intermediate, 3-phosphoglycerate. These novel mitochondrial genes are restricted to stramenopiles. Such novel enzymes could be used as targets for the vi chemical control of oomycetes. I purpose that manipulation of metabolism is a promising approach for control of P. infestans, one of the most devastating phytopathogens. vii TABLE OF CONTENTS INTRODUCTION .................................................................................................. 1 REFERENCES ............................................................................................... 15 CHAPTER I ........................................................................................................ 21 Gene expression and silencing studies in Phytophthora infestans reveal infection-specific nutrient transporters and a role for the nitrate reductase pathway in plant pathogenesis ABSTRACT ..................................................................................................... 21 INTRODUCTION ............................................................................................ 22 RESULTS ....................................................................................................... 25 DISCUSSION .................................................................................................. 67 METHODS ...................................................................................................... 74 ACKNOWLEDGEMENTS ............................................................................... 79 REFERENCES ............................................................................................... 81 CHAPTER II ....................................................................................................... 90 Uncovering differences in nitrogen source utilization in hemibiotrophic and necrotrophic oomycetes ABSTRACT ..................................................................................................... 90 INTRODUCTION ............................................................................................ 91 RESULTS ....................................................................................................... 94 viii DISCUSSION ................................................................................................ 135 METHODS .................................................................................................... 143 ACKNOWLEDGEMENTS ............................................................................. 149 REFERENCES ............................................................................................. 151 CHAPTER III .................................................................................................... 159 Rethinking the evolution of eukaryotic metabolism: Novel cellular partitioning of enzymes in stramenopiles links serine biosynthesis to glycolysis in mitochondria ABSTRACT ................................................................................................... 159 INTRODUCTION .......................................................................................... 160 RESULTS ..................................................................................................... 163 DISCUSSION ................................................................................................ 194 METHODS .................................................................................................... 199 REFERENCES ............................................................................................. 207 CHAPTER IV .................................................................................................... 217 Phytophthora infestans possesses active mitochondrial and cytosolic 3- phosphoglycerate kinases ABSTRACT ................................................................................................... 217 INTRODUCTION .......................................................................................... 218 RESULTS ..................................................................................................... 219 DISCUSSION ................................................................................................ 227 ix METHODS .................................................................................................... 229 ACKNOWLEDGEMENTS ............................................................................. 232 REFERENCES ............................................................................................. 233 CONCLUSION ................................................................................................. 236 REFERENCES ............................................................................................. 245 x List of Figures INTRODUCTION Fig 1………………………………………………………………………………………7 CHAPTER I Gene expression and silencing studies in Phytophthora infestans reveal infection-specific nutrient transporters and a role for the nitrate reductase pathway in plant pathogenesis. Fig 1……………………………………………………………………………………..26 Fig 2……………………………………………………………………………………..33 Fig 3……………………………………………………………………………………..35 Fig 4……………………………………………………………………………………..38 Fig 5……………………………………………………………………………………..41 Fig 6……………………………………………………………………………………..44 Fig 7……………………………………………………………………………………..50 Fig 8……………………………………………………………………………………..54 Fig 9……………………………………………………………………………………..56 Fig 10……………………………………………………………………………………59 Fig 11……………………………………………………………………………………62 Fig 12……………………………………………………………………………………65 xi CHAPTER II Uncovering differences in nitrogen source utilization in hemibiotrophic and necrotrophic oomycetes Fig 1……………………………………………………………………………………..95 Fig 2……………………………………………………………………………………..97 Fig 3……………………………………………………………………………………..99 Fig 4…………………………………………………………………………………...102 Fig 5……………………………………………………………………………………105 Fig 6……………………………………………………………………………………110 Fig 7……………………………………………………………………………………113 Fig 8……………………………………………………………………………………116 Fig 9……………………………………………………………………………………119
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