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Basu, Debarati Dissertation 08-05-15 Identification and Characterization of Five Arabidopsis Hydroxyproline Galactosyltransferases and Their Functional Roles in Arabinogalactan-Protein Glycosylation, Growth, Development, and Cellular Signaling A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Debarati Basu August 2015 © 2015 Debarati Basu. All Rights Reserved. 2 This dissertation titled Identification and Characterization of Five Arabidopsis Hydroxyproline Galactosyltransferases and Their Functional Roles in Arabinogalactan-Protein Glycosylation, Growth, Development, and Cellular Signaling by DEBARATI BASU has been approved for the Department of Environmental and Plant Biology and the College of Arts and Sciences by Allan M. Showalter Professor of Environmental and Plant Biology Robert Frank Dean, College of Arts and Sciences 3 ABSTRACT BASU, DEBARATI, Ph.D., August 2015, Molecular and Cellular Biology Identification and Characterization of Five Arabidopsis Hydroxyproline Galactosyltransferases and Their Functional Roles in Arabinogalactan-Protein Glycosylation, Growth, Development, and Cellular Signaling Director of Dissertation: Allan M. Showalter Arabinogalactan-proteins (AGPs) are a class of highly glycosylated ubiquitous plant cell wall glycoproteins, implicated in diverse biological roles. Although plants contain substantial amounts of AGPs, enzymes responsible for glycosylation of AGPs are largely unknown. Given that sugar side chains account for about 90% of the molecular mass of AGPs, sugars likely define the interactive surface of the molecule and hence its function. Bioinformatic analysis indicated that hydroxyproline (Hyp)-O- galactosyltransferases (GALTs) for AGPs might belong to the Carbohydrate-Active enZYme (CAZY) glycosyltransferase 31-family, which includes β-GALTs involved in the synthesis of glycoproteins. Here, five GT 31 Hyp-O-GALTs, namely AtGALT2 (At4g21060), AtGALT3 (At3g06440), AtGALT4 (At1g27120), AtGALT5 (At1g74800) and AtGALT6 (At5g62620), were characterized. Detergent permeabilized microsomes obtained from Pichia pastoris expressing AtGALT2 and AtGALT5 and from tobacco epidermal cells expressing AtGALT2, AtGALT3, AtGALT4, AtGALT5 and AtGALT6 specifically catalyzed the transfer of [14C]Gal from UDP-[14C]Gal to Hyp in the chemically synthesized AGP peptide substrate acceptor, [AO]7. Furthermore, these Hyp- O-GALTs exhibited similar biochemical properties. Confocal microscopic analysis of 4 fluorescently tagged AtGALT2-6 indicated AtGALT2 was localized in the ER and Golgi, while the other four proteins were localized exclusively in Golgi vesicles. Additional support that these five GALTs encode AGP-specific Hyp-O-GALTs was provided by analysis of allelic knockout mutants of the five GALT genes. These mutants demonstrated significantly lower Hyp-O-GALT activities, reduced β-Yariv-precipitated AGPs and pleiotropic growth and developmental phenotypes compared to wild type plants with increasing severity in galt2galt5 double mutants. To varying degrees, all five Hyp-O-GALTs were essential for tip growth and involved in root development in response to salt stress. Interestingly, the galt2galt5 double mutant phenocopied the root swelling phenotypes as well as the seed coat mucilage and cellulose-deficient phenotypes of previously characterized mutants, namely sos5 (a GPI-anchored fasciclin- like AGP), fei1fei2 (a pair of leucine rich cell wall receptor-like kinases), and sos5fei1fei2. These findings indicated that the arabinogalactan (AG) polysaccharides of SOS5 are likely critical for cellular signaling and in stimulating cellulose biosynthesis. In summary, this dissertation contributes to an understanding of AGP biosynthesis, particularly with respect to Hyp-galactosylation, and to the functional roles which AG polysaccharides play in plants. 5 ACKNOWLEDGMENTS First and foremost, I am indebted to my supervisor, Dr. Allan Showalter, for granting me the opportunity to pursue my PhD, for his continued support, encouragement, financial assistance and guidance throughout my PhD study. I am very grateful for his patience, availability to discuss my coursework and thesis research, and to help answer the many questions that arose throughout my graduate studies. Most importantly he always encouraged me to develop independent scientific thinking and research skills. I am honored to have had the opportunity to learn from him and to grow as a scientist under his guidance. I am grateful to all my committee members for their invaluable suggestions and criticism relevant to my thesis. They were instrumental in developing my professional and research career with regular inputs and critical suggestions. I am thankful to them for allowing me to use their instruments and reagents for my research. I am very grateful to the past and present members of the Showalter lab who have made my time here such an enjoyable experience including Brian Keppler, Yan Liang, Wuda Wang, and Lu Tian. I am thankful to all the brilliant, enthusiastic, dedicated, diligent undergraduates for assisting me in the research including Shauni Bobbs, Hannah Fritts, Tayler DeBrosse, Emily Poirier, Eric Sokup, Kirk Emch, Megan Moore, Siyi Ma, Hayley Herock, Andrew Travers and Kiara Dillard. I sincerely appreciate the help of Connie Pollard and Jamie Dewey for their incessant co-ordination and unconditional help. 6 I am thankful to Vijay Nadella for his valuable suggestions on QPCR analysis. I also thank Dr. Micheal Held and Jeffrey Thuma for their insightful suggestions on confocal microscopy, especially for image acquisition and analysis. I am thankful all my friends including Claudia Lechler, Bailey Hunter, Hayley Shurr, Svetlana Bondareva, Conny Bartholmes, Proma Basu, Mohor Chatterjee, Sutapa Ghosh, Enakshi Ghosh, Laura Cristea, Aditi Vyas, Nilesh Khade, Aditya Kulkarni, and friends from the International Student Union for making my stay at Athens an enjoyable and memorable experience. I am also thankful to the Department of Environmental and Plant Biology, the Molecular and Cellular Biology Program, and the Ohio University Graduate College for providing me with financial assistance. I am also thankful to the Graduate Student Senate for providing me with funds to attend national scientific meetings. I also express my gratitude towards all my instructors in the University of Calcutta and Thakurpukur College, especially Prof. Sumita Jha, Moumita Banerjee Prof. Anita Mukherjee, Dr. Asim Bhadra, Dr. Silanjan Bhattacharya, Dr. Meenakshi Mukherjee, Dr. Kuntal Narayan Chaudhury and Dr. Sutapa Kumar who inspired me to embark upon my journey for a Ph.D. Lastly, none of this would have been possible without the unending love, encouragement, and support of my family. 7 TABLE OF CONTENTS Page Abstract ................................................................................................................................ 3 Acknowledgments ............................................................................................................... 5 List of Tables ..................................................................................................................... 17 List of Figures .................................................................................................................... 20 List of Abbreviations ......................................................................................................... 26 Chapter 1: Introduction ................................................................................................... 28 1.1. Plant Cell Walls .................................................................................................... 28 1.1.1. Overview ........................................................................................................ 28 1.1.2. Cell wall composition ..................................................................................... 29 1.1.3. Biosynthesis of cell wall polysaccharides ...................................................... 30 1.1.4. Plant cell wall proteins ................................................................................... 41 1.1.5. Structure of AGPs .......................................................................................... 46 1.1.6. Biosynthesis of AGPs ..................................................................................... 48 1.1.7. Function of AGPs ........................................................................................... 54 1.2. Objectives ............................................................................................................. 61 1.3. Organization of the Dissertation ........................................................................... 62 Chapter 2: Functional Identification of a Hydroxyproline-O-Galactosyltransferase Specific for Arabinogalactan-Protein Biosynthesis in Arabidopsis .................................. 64 2.1. Abstract ................................................................................................................. 64 2.2. Introduction .......................................................................................................... 65 8 2.3. Results .................................................................................................................. 68 2.3.1. Identification of putative AGP GALTs in Arabidopsis thaliana by in-silico analysis ....................................................................................................................
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