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Elucidation of Functional and Regulatory Aspects of Sulfate Transport in Chlamydomonas Reinhardtii

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Elucidation of Functional and Regulatory Aspects of Sulfate Transport in Chlamydomonas Reinhardtii ELUCIDATION OF FUNCTIONAL AND REGULATORY ASPECTS OF SULFATE TRANSPORT IN CHLAMYDOMONAS REINHARDTII A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGY AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Wirulda Pootakham July 2010 © 2010 by Wirulda Pootakham. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/jq238dx7130 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Arthur Grossman, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Martha Cyert, Co-Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Mary Mudgett I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Zhiyong Wang Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii ABSTRACT Chlamydomonas reinhardtii (Chlamydomonas) exhibits a suite of responses to 2- sulfur (S) deprivation, including an elevation of sulfate (SO4 ) uptake, synthesis of extracellular arylsulfatase, down-regulation of photosynthesis and cessation of growth and cell division. One of the earliest responses to S starvation is an increase in the 2- 2- SO4 transport rate. Aspects of SO4 transport during S-replete and S-depleted 2- conditions were previously studied, although the SO4 transporters had not been functionally identified. In this study, both forward and reverse genetic approaches 2- were employed to identify SO4 transporters in Chlamydomonas. SULTR2, SLT1, and SLT2 transcripts and polypeptides increased markedly in S-starved wild-type cells, 2- suggesting that these genes encode high-affinity SO4 transporters that function when the cells experience S limitation. Mutant strains defective for acclimation to S starvation, sac1 and snrk2.1, exhibited much less of an increase in the level of SULTR2, SLT1, and SLT2 transcripts and their encoded proteins during S deprivation compared to wild-type cells. Consequently, these two strains were unable to induce 2- SO4 uptake to the same extent as in the wild-type strain. The SULTR2, SLT1 and SLT2 polypeptides were localized to the plasma membrane and their rates of turnover were significantly impacted by S availability; the turnover for SLT1 and SLT2 (but not for SULTR2) was demonstrated to be dependent on proteasome function. Mutants identified for each of the S-deprivation-responsive transporters were used to establish 2- their critical role in the transport of SO4 into S-starved cells. I have also discovered a sequential, temporal regulation of the S-starvation 2- responsive genes. The primary responses (e.g. the induction of high-affinity SO4 iv transporters) are not dependent on protein synthesis occurring on 80S ribosomes. In contrast, the secondary responses (the induction of ARS, ECP76 and ECP88) require de novo protein synthesis. ARS73a, a putative transcriptional activator, is directly or indirectly involved in the regulation of the expression of the second tier genes, most of which encode proteins associated with the scavenging of extracellular S or the redistribution of internal S. Genetic analysis has shown that ARS73a and SAC3 kinase act in the same pathway; ARS73a is epistatic to SAC3. These new discoveries are incorporated into a model that describes S-deprivation elicited regulation in Chlamydomonas. v ACKNOWLEDGEMENTS My PhD project was like a roller coaster ride. There were lots of ups and downs, and I cherished every moment of it. There was a rush of joy, self-satisfaction, and excitement when I got fascinating data. There were also times when my scientific world was filled with disappointment and frustration from failed experiments. I would like to thank a number of people who’ve helped me throughout my graduate career. First and foremost, I want to thank my advisor, Arthur Grossman. You are a great scientist and a wonderful teacher. Thank you so much for your support and encouragement. You always gave me great advice and never told me what to do. That’s one of the greatest qualities any advisor could have. You’ve given me freedom to make my own decisions about the project, and I’m very grateful for that. Most importantly, thank you for encouraging me during tough times. If you hadn’t convinced me that this project would turn out to be a beautiful story, I might have given up halfway through. There are three very important people without whom I couldn’t have completed this PhD: Nakako Shibagaki, Jeffrey Moseley and David Gonzalez- Ballester. Nakako, you are one of the most amazing people I’ve ever met. I remember doing my first rotation project with you, and I didn’t know a lot about molecular biology. You were kind and very patient with me. You taught me a lot of techniques and little tricks that turned out to be really useful. Thanks for all the great discussions we had about my project and keeping me company on the weekends. vi Jeff, you rock! You are my personal “Chlamydomonas sourcebook,” really. Pretty much everything I know about Chlamy, I learned from you. Thanks for letting me share my scientific passion with you. It’s good to know that there is another person who cares about sulfate transporters as much as I do. I miss all the discussions we had – you always motivated me. David, lab would not be as fun without you. Thank you for helping me set up the mutant screen. I couldn’t have done it without you. I also want to thank you for cheering me up when I had bad days. I enjoyed making spaghetti noodles from TAP medium and washing glassware with you! I also want to thank other Grossman/Bhaya lab members, past and present: Devaki Bhaya, Florence Mus, Anne Steunou, Fariba Fazeli, Claudia Catalanotti, Leonardo Magneschi, Matt Prior, Ariana Afshar, Blaise Hamel, Mark Heinnickel, Wenqiang Yang, Sussi Wisén, Eva Nowack, Michelle Davidson, David Dewez, Rosario Gomez, Mine Berg, Kate Mackey, Shaun Bailey, Chao-Jung Tu, and Chungsoon Im. You guys create such a fun working environment. Thanks for your friendship and intellectual scientific discussions. Thanks to my committee members: Martha Cyert, Mary Beth Mudgett and Zhiyong Wang, for their support, encouragement and most importantly for their helpful suggestions. I would also like to thank my undergraduate advisor, David Stern, for jump-starting my research career. Last but certainly not least, I want to thank my family: Mom, Dad, Thanyakarn (my brother), and my partner and best friend, Metha Jeeradit. Mom and Dad, I couldn’t have done this without you. I don’t think I could ever thank you enough for vii your endless love and support. I’m incredibly lucky to have you both and I would like to dedicate this thesis to you. Thanyakarn, you’ve always been a great friend and a wonderful brother. Thanks for keeping me sane while I was in graduate school. Metha, thanks for being with me every step of the way. You are nothing but supportive, and I would never get this far without you. I’m really grateful for the love and support you’ve shown me. Thanks for enduring my relentless complaints about my experiments. Finally, thanks for being an amazing hiking/rock- climbing/bouldering partner. Those activities really helped maintain my sanity during my graduate career. ☺ viii TABLE OF CONTENTS ABSTRACT iv ACKNOWLEDGEMENTS vi TABLE OF CONTENTS ix LIST OF TABLES xi LIST OF FIGURES xii CHAPTER 1: Introduction 1 Sulfur in the environment 2 Chlamydomonas as a model organism 3 Sulfate acquisition and assimilation 5 Sulfate transport in Chlamydomonas 5 Arabidopsis sulfate transporters 7 Putative sulfate transporters in Chlamydomonas 10 Sulfate assimilation 11 Synthesis of cysteine and methionine 13 Synthesis of glutathione 14 Recycling of sulfur compounds 15 Sulfur starvation responses in Chlamydomonas 16 General and specific responses 16 Genes responsive to sulfur deprivation 18 Identification of genes controlling sulfur deprivation responses 20 Model for acclimation of Chlamydomonas to sulfur starvation 23 Thesis aims 25 References 37 CHAPTER 2: Selenate resistant mutant selection in Chlamydomonas 44 reinhardtii Abstract 45 ix Introduction 46 Results 50 Discussion 52 Materials and methods 56 References 67 CHAPTER 3: The sulfate transporters of Chlamydomonas reinhardtii; 69 From regulation to functionality Abstract 70 Introduction 72 Results 76 Discussion 91 Materials and methods 101 Acknowledgements 112 References 146 CHAPTER 4: ARS73a is involved in a tiered regulation of sulfur 151 starvation responses Abstract 152 Introduction 154 Results 159 Discussion 165 Future directions 169 Materials and methods 171 References 192 CHAPTER 5: Concluding remarks and future directions 195 References 206 x LIST OF TABLES CHAPTER 1 2- Table 1-1. Arabidopsis SO4 transporters: their subcellular 34 locations, expression patterns, and functions. 2- Table 1-2. Genes involved in SO4 assimilation in Chlamydomonas. 36 CHAPTER 2 2- Table 2-1. Characteristics of SO4 transport in wild-type cells (D66) 66 and sr mutants in S-depleted conditions.
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