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Exploring Caffeyl-Lignin Biosynthesis in Cleome Hassleriana and Polymerization of Caffeyl Alcohol in Arabidopsis Thaliana

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Exploring Caffeyl-Lignin Biosynthesis in Cleome Hassleriana and Polymerization of Caffeyl Alcohol in Arabidopsis Thaliana EXPLORING CAFFEYL-LIGNIN BIOSYNTHESIS IN Cleome hassleriana AND POLYMERIZATION OF CAFFEYL ALCOHOL IN Arabidopsis thaliana Aaron D. Harkleroad Thesis Prepared for the Degree of MASTER OF SCIENCE UNIVERSITY OF NORTH TEXAS December 201 9 APPROVED: Richard A. Dixon, Major Professor Brian Ayre, Committee Member Rajeev Azad, Committee Member Jyoti Shah, Chair of the Department of Biological Sciences Su Gao, Dean of the College of Science Victor Prybutok, Dean of the Toulouse Graduate School Harkleroad, Aaron D. Exploring Caffeyl-Lignin Biosynthesis in Cleome hassleriana and Polymerization of Caffeyl Alcohol in Arabidopsis thaliana. Master of Science (Biochemistry and Molecular Biology), December 2019, 47 pp., 2 tables, 15 figures, references, 43 titles. C-lignin (caffeyl-lignin) is a novel linear lignin polymer found in the seed coats of several non-crop plants, notably Vanilla planifolia (Vanilla), Jatropha curcas (Jatropha), and Cleome hassleriana (Cleome). C-lignin has several advantages over normal G/S- lignin, found in the majority of lignocellulosic biomass, for valorization in the context of bioprocessing: less cross-linking to cell wall polysaccharides (less recalcitrant biomass), ordered linkages between monomers (homogeneous polymer), and no branching points (linear polymer). These properties make C-lignin an attractive replacement for native lignin in lignocellulosic biomass crops. The seed coats of Cleome hassleriana (Cleome) synthesize G-lignin during early seed maturation, then switch to synthesis of C-lignin during late maturation. This switch to C-lignin in Cleome seed coats is accompanied by loss of caffeoyl-CoA 3-O- methyltransferase (CCoAOMT) and caffeic acid 3-O-methyltransferase (COMT) activities, along with changes in transcript abundance of several lignin related genes. The focus of this research thesis is to understand the biochemical changes leading to C-lignin deposition in Cleome hassleriana seed coats, and to explore the ability of Arabidopsis thaliana seedlings to polymerize caffeyl alcohol to C-lignin. In this thesis, candidate transcripts were implicated in C-lignin biosynthesis by differential gene expression analysis of transcripts in seed coat tissues at 8-18 days after pollination (DAP) and in non-seed coat tissues. Three candidate genes were selected for recombinant expression and their in vitro kinetic properties were measured with potential substrates. Of the three candidates, a cinnamyl alcohol dehydrogenase (ChCAD5) was found to have high transcript levels during C-lignin formation and have a novel preference for converting caffealdehyde to caffeyl alcohol, the precursor of C- lignin. To determine if accumulation of caffeyl alcohol is sufficient for polymerization of C-lignin, Arabidopsis seedlings grown in a xylem induction system were supplied caffeyl alcohol. Polymerization of caffeyl alcohol was not found to occur in this Arabidopsis system, suggesting the need for a C-lignin specific polymerization mechanism. Copyright 2019 by Aaron D. Harkleroad ii ACKNOWLEDGMENTS I would like to acknowledge the support and funding by UNT start-up funds, provided to the Dixon Laboratory, along with grant #1456286 from the National Science Foundation, Integrated Organismal Systems. This thesis is dedicated to my family and friends who provided support and encouragement throughout my graduate work. I would like to thank my wife, Jagruti Harkleroad, for her confidence in my scholastic abilities and for providing inspiration during challenging times. To my mom and dad, thank you for believing in me and supporting my educational journey. Thanks to my friends for listening to my esoteric “biology talk” with earnest interest and good humor; you have all been a great source of emotional support. Thanks to all my graduate student cohorts in the UNT biology program for their comradery and stimulating conversations, I will truly miss them. I would like to extend my greatest appreciation to my major professor, Dr. Richard Dixon, for his amazing patience and encouragement during my graduate work. His critical thinking and openness to hypotheses has been instrumental in my research. I also thank the members of my graduate committee for their critical analysis and feedback. I thank the many researchers who have assisted me in my research by providing materials and expertise- there are too many to name here, but I appreciate you all. I specifically thank Chunliu Zhuo and Fang Chen for supplying substrates, Chan Man Ha for supplying Arabidopsis seeds, Xiaolan Rao for her RNA sequencing work, and Xiaoqiang Wang for his protein modeling work. iii TABLE OF CONTENTS Page ACKNOWLEDGMENTS .................................................................................................. iii LIST OF TABLES ............................................................................................................vi LIST OF FIGURES ......................................................................................................... vii CHAPTER 1. INTRODUCTION ....................................................................................... 1 Biosynthesis of Monolignols ....................................................................... 3 Polymerization of Lignin ............................................................................. 7 Engineering Lignin Subunits ...................................................................... 8 Hypothesis and Objectives ........................................................................ 9 Methods Overview ................................................................................... 10 1.5.1 Candidate Gene Discovery by RNA Sequencing .......................... 10 1.5.2 Recombinant Expression and Characterization of Target Proteins10 1.5.3 In vitro Polymerization Systems and Induction of Lignification in vivo ................................................................................................ 12 1.5.4 Analysis of Lignin Presence, Amount and Composition ................ 14 CHAPTER 2. DISCOVERY OF CANDIDATE GENES RELATED TO C-LIGNIN BIOSYNTHESIS IN Cleome SEED COATS .................................................................. 15 Objectives ................................................................................................ 15 Methods ................................................................................................... 15 2.2.1 RNA Sequencing and Assembly ................................................... 15 2.2.2 Analysis of Differential Gene Expression ...................................... 15 2.2.3 Homology Mapping to Arabidopsis ................................................ 16 2.2.4 Protein Modeling ........................................................................... 16 Results and Discussion ............................................................................ 16 2.3.1 RNA Sequencing ........................................................................... 16 2.3.2 Differential Gene Expression ........................................................ 16 2.3.3 Comparison of Candidate Cleome Transcripts to Arabidopsis Homologs ...................................................................................... 19 2.3.4 Protein Modeling of ChCAD5 ........................................................ 19 Conclusion ............................................................................................... 21 iv CHAPTER 3. IN VITRO CHARACTERIZATION OF RECOMBINANT CANDIDATE ENZYMES ..................................................................................................................... 22 Objectives ................................................................................................ 22 Methods ................................................................................................... 22 3.2.1 Cloning, Recombinant Protein Expression, and Enzyme Purification ...................................................................................................... 22 3.2.2 Kinetic Assays ............................................................................... 23 3.2.3 Mixed Reactions ............................................................................ 24 3.2.4 HPLC Analysis .............................................................................. 24 Results and Discussion ............................................................................ 25 3.3.1 Expression of Recombinant Proteins ............................................ 25 3.3.2 Kinetic Properties of ChCCR and ChCAD4 and 5 ......................... 25 3.3.3 Mixed Reactions with ChCCR and ChCAD 4 or 5 ......................... 29 Conclusions ............................................................................................. 32 CHAPTER 4. POLYMERIZATION OF CAFFEYL ALCOHOL AND OTHER MONOLIGNOLS IN Arabidopsis SEEDLINGS .............................................................. 33 Objectives ................................................................................................ 33 Methods ................................................................................................... 33 4.2.1 Xylem Induction in Arabidopsis Seedlings and Feeding of Monolignols ................................................................................... 33 4.2.2 Staining and Microscopic Observation of Seedlings ..................... 34 4.2.3 Harvesting of Shoot Tissue and Preparation of Cell Wall Residues .....................................................................................................
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