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JOHNSON-DISSERTATION.Pdf (13.16Mb) IN VIVO ANALYSIS OF THE ROLE OF FTSZ1 AND FTSZ2 PROTEINS IN CHLOROPLAST DIVISION IN ARABIDOPSIS THALIANA A Dissertation by CAROL BEATRICE JOHNSON Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY May 2012 Major Subject: Biology In Vivo Analysis of the Role of FtsZ1 and FtsZ2 Proteins in Chloroplast Division in Arabidopsis thaliana Copyright 2012 Carol Beatrice Johnson IN VIVO ANALYSIS OF THE ROLE OF FTSZ1 AND FTSZ2 PROTEINS IN CHLOROPLAST DIVISON IN ARABIDOPSIS THALIANA A Dissertation by CAROL BEATRICE JOHNSON Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Approved by: Chair of Committee, Andreas Holzenburg Committee Members, Karl Aufderheide David Stelly Alan Pepper Head of Department, U. Jack McMahan May 2012 Major Subject: Biology iii ABSTRACT In Vivo Analysis of the Role of FtsZ1 and FtsZ2 Proteins in Chloroplast Division in Arabidopsis thaliana. (May 2012) Carol Beatrice Johnson, B.S., Texas Southern University; M.A., Sam Houston State University Chair of Advisory Committee: Dr. Andreas Holzenburg Chloroplasts divide by a constrictive fission process that is regulated by FtsZ proteins. Given the importance of photosynthesis and chloroplasts in general, it is important to understand the mechanisms and molecular biology of chloroplast division. An FtsZ gene is known to be of prokaryotic origin and to have been transferred from a symbiont’s genome to host genome via lateral transfer. Subsequent duplication of the initial FtsZ gene gave rise to the FtsZ1 and FtsZ2 genes and protein families in eukaryotes. These proteins co-localize mid-chloroplast to form the Z-ring. Z-ring assembly initiates chloroplast division, and it serves as a scaffold for other chloroplast division proteins. Little is known, however, about the FtsZ protein subunit turnover within the Z-ring, the effects of accessory proteins on Z-ring turnover assemblies, as well as the in vivo ultrastructure of the Z-ring in plants. To investigate the Arabidopsis thaliana FtsZ subunit turnover rate within the Z-ring, a section of the Z-ring in the chloroplasts of living plants expressing fluorescently tagged FtsZ1 or FtsZ2 proteins was photobleached and the recovery rate was monitored. The results show that the iv fluorescence recovery half times for the FtsZ1 and FtsZ2 proteins are 117s and 325s, respectively. This is significant as these data mirror their differences in GTP hydrolysis rates. To elucidate in vivo structure and ultrastructure of the Z-ring, a protocol was established that maintained fluorescence during high pressure freezing, freeze substitution and low temperature embedding. Afterwards, a correlative microscopy approach was employed to visualize and identify fluorescently labeled puncta, circular structures, at the light microscopy level. These puncta were further resolved as mini- rings using optical microscopy eXperimental (OMX) superresolution microscopy. Electron microscopy (EM) analysis imaged mini-rings and filament assemblies comprised of dense subunits. Electron tomography (ET) showed mini-rings composed of protofilaments. v DEDICATION To my parents, Uriah and Jessie, for their guidance, support, and encouragement. To my grandmother, Willie B., for her wisdom and for the joy that she has brought to my life. To my Uncle T.L. for encouragement, support and mentoring. To my siblings, nieces, and nephews for their support throughout this journey. To my best friends, Stephanie Maeweather and Lilly Nguyen, who I thank for being there and for listening. To Ashton and Auston Johnson, thank you for making me a better person. To those family members who paved the way for me. vi ACKNOWLEDGEMENTS I would like to thank my advisor, Dr. Andreas Holzenburg for the opportunity to work in his lab and to contribute to the research; for his advice, support, encouragement, and guidance throughout my studies. I also thank Dr. Stanislav Vitha for teaching and advising me throughout my studies and for his patience. Special thanks to my committee members, Dr. Alan Pepper, Dr. Karl Aufderheide, and Dr. David Stelly for their insight, time, and encouragement. I thank Dr. Jack McMahan for his recommendations, support and guidance and for the use of his laboratory equipment and other lab resources, he was instrumental in the completion of this project. I thank Robert Marshall for his time, guidance, and patience. I thank the staff of Microscopy and Imaging Center for all of their help. Thank you to my past and current lab members: Dr. Christos Savva, Dr. Aaron Smith and Alvin Tang. In addition, I thank Ginger Stuessy for her help with the plants and their maintenance and all of the laboratories and persons who supported me throughout this research with their resources. vii NOMENCLATURE ARC3 Accumulation and replication of chloroplast 3 ARC5 Accumulation and replication of chloroplast 5 ARC6 Accumulation and replication of chloroplast 6 arc Accumulation and replication of chloroplast mutants At Arabidopsis thaliana C-terminus carboxyl terminus of a protein Col-0 Columbia ECL Chemiluminescent detection EM Electron microscopy ET Electron tomography FEG Field emission gun FRAP Fluorescence recovery after photobleaching FRET Fluorescence resonance energy transfer FP Fluorescent protein FS Freeze Substitution FtsZ Filamentation temperature sensitive Z protein FtsZ1 Filamentation temperature sensitive Z1 protein FtsZ2 Filamentation temperature sensitive Z2 protein ftsZ2-1 FtsZ 2-1 null mutant ftsZ2-2 FtsZ 2-2 null mutant viii GFP Green fluorescent protein GTP Guanosine triphosphate HAADF High angle annular dark field HPF High pressure freezing KO Knockout KD Knockdown Ler-0 Landsberg erecta LM Confocal laser scanning microscope mCFP Monomeric cyan fluorescent protein MEMK6.5 Protein assembly buffer Min minute MOLSCRIPT A program for displaying 3D molecular structure µm micrometer mYFP Monomeric yellow fluorescent protein nm namometer N-terminus amino terminus of a protein OMX Optical microscope eXperimental PAGE polyacrylamide gel electrophoresis PARC6 paralog of ARC6 Pb Lead PBS Phosphate buffered saline PDV1 PLASTID DIVISION 1 ix PDV2 PLASTID DIVISION 2 PPD paraphenylenediamine QFS Quick freeze substitution SDS Sodium dodecyl sulfate STEM scanning transmission electron microscope T1 Transgenic line one t1/2 Half time to fluorescence recovery TBST Tris buffered saline plus tween 20 TEM Transmission electron microscope UA Uranyl acetate vol Volume wt Weight WS-0 Wassilewskija WT Wild-type x TABLE OF CONTENTS Page ABSTRACT .............................................................................................................. iii DEDICATION .......................................................................................................... v ACKNOWLEDGEMENTS ...................................................................................... vi NOMENCLATURE .................................................................................................. vii TABLE OF CONTENTS .......................................................................................... x LIST OF FIGURES ................................................................................................... xii LIST OF TABLES .................................................................................................... xiv CHAPTER I INTRODUCTION ................................................................................ 1 Chloroplasts .................................................................................... 1 Chloroplast Division ...................................................................... 2 FtsZ ................................................................................................. 3 Chloroplast Division Proteins ........................................................ 7 Arabidopsis thaliana ...................................................................... 14 Fluorescence ................................................................................... 16 II DIFFERENTIAL TURNOVER DYNAMICS OF CHLOROPLAST DIVISION PROTEINS FTSZ1-1 AND FTSZ2-1 IN ARABIDOPSIS THALIANA ........................................................................................... 19 Introduction .................................................................................... 19 Results ............................................................................................ 22 Discussion ...................................................................................... 37 Material and Methods ..................................................................... 43 xi CHAPTER Page III MAINTAINING SPECIFIC FLUORESCENCE IN ARABIDOPSIS THALIANA AFTER HIGH PRESSURE FREEZING, FREEZE SUBSTITUTION AND EMBEDDING............................................... 49 Introduction .................................................................................... 49 Results ............................................................................................ 54 Discussion ...................................................................................... 60 Materials and Methods................................................................... 65 IV USING CORRELATIVE MICROSCOPY TO EXPLORE FTSZ ASSEMBLY STRUCTURE ............................................................... 73 Introduction ...................................................................................
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