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JIN-DOCUMENT-2019.Pdf ABSTRACT Characterization of Oxidosqualene Cyclases in Brassicaceae: the ABCs (Arabidopsis, Brassica and Capsella) By Jing Jin One major class of plant secondary metabolites is the triterpenes, whose biosynthesis from oxidosqualene is catalyzed by oxidosqualene cyclases (OSCs). This thesis describes the characterization of OSCs from plants within the Brassicaceae family, which include the model species Arabidopsis thaliana and Capsella rubella as well as the crop species Brassica rapa and Brassica oleracea. Detailed product profiles of those cyclases are combined with phylogenetic analysis, synteny analysis, active-site prediction, plant tissue extraction and transcriptome analysis to explore enzyme mechanisms and evolutionary relationships within the OSC family. First, detailed product profiles are constructed for four Arabidopsis thaliana OSCs. Those cyclases exemplify the range of product specificity among OSCs, ranging from the 94% specific At PEN4 to the multi-functional cyclase At LUP5 which makes two major products at similar levels. Despite their varying product specificity, all those OSCs form many minor products. Next, the characterization of three OSCs from Brassica species is detailed. Bra032185 was determined to be an astertarone A synthase, which is the first reported OSC with 6/6/6/5 20R stereospecificity. Bra039929 is the first reported euphol synthase and is another 6/6/6/5 20R specific cyclase. In addition, Bol021540 was amplified from broccoli seedling RNAs and it was determined to be a mixed-amyrin synthase. Those results were combined with Brassica plant extraction results to explore the triterpene biosynthesis in this species. Lastly, the complete characterization of all Capsella rubella OSCs is described. The triterpene biosynthetic capability of this plant includes one cycloartenol synthase, five functional OSCs in the secondary metabolism and one pseudogene. The only secondary metabolic OSC conserved between A. thaliana and C. rubella is camelliol C synthase (LUP3). In addition, three C. rubella cyclases show similarity to their A. thaliana counterparts but different products are made. Overall, the comparison of OSCs across species illustrates the fast divergence of plant secondary metabolism and explores OSC evolution among the Brassicaceae family. The OSC family showcases rapid enzyme functional evolution as evident by neofunctionalization and convergent evolution, and thus it can be a valuable model for enzyme evolution studies. Acknowledgements I would like to thank my advisor, Professor Seiichi P. T. Matsuda, for his guidance and support throughout my graduate career. I would like to specially thank him for his patience while working with me and the freedom he gave me to pursue my research interests. I am grateful for the thought-provoking discussions we had and the encouragement I received from him. I would like to thank my committee members, Dr. Joff Silberg, Dr. Janet Braam and Dr. George Bennett. They have been on my committee since my first progress review, and they have always provided me with valuable guidance and support. I am grateful for the present and past members of the Matsuda Lab as wonderful co- workers and friends. I would like to thank Dr. Paul Bodager, Dr. Dorianne Castillo Rivera and Dr. Melisa Moreno Garcia for their mentorship, especially when I just joined the lab. I am grateful for my current lab mate Thasneem Banu Frousnoon for valuable scientific discussions. I would like to thank my undergraduate student Megan Moore for assisting me in many experiments. I would like to specially thank Dr. Bill Wilson for his help with NMR and for our collaboration on manuscripts. I am thankful for the incredible education that I have received at Rice University and Goshen College. I feel fortunate to have learned from so many wonderful professors and through many courses. They have provided me a solid foundation for future scientific endeavors. Finally and most importantly, I would like to thank my family for their love and support throughout everything. My parents, Yan Miao and Weiguo Jin, have always believed in me and supported me unconditionally. Jason Lai has been the greatest friend who is always tremendously supportive. Cadi and Cali Lai have always reminded me to rest well and to stress less, especially during the preparation of this thesis. Table of Contents Chapter 1. Introduction .................................................................................................... 1 Triterpenoids: important plant natural products .................................................... 1 Plant primary and secondary metabolism ............................................................. 2 Oxidosqualene cyclases (OSCs) in plants ............................................................. 3 Human lanosterol synthase.................................................................................... 4 OSCs as a system to study enzyme evolution ....................................................... 5 Brassicaceae family and model species ................................................................ 7 1.6.1 Arabidopsis thaliana ....................................................................................... 7 1.6.2 Arabidopsis lyrata ........................................................................................... 9 1.6.3 Capsella rubella .............................................................................................. 9 1.6.4 Brassica species ............................................................................................ 10 Heterologous expression in yeast ........................................................................ 11 Chapter 2. Materials and Methods ................................................................................. 13 Materials .............................................................................................................. 13 Method ................................................................................................................ 13 2.2.1 Genome mining and plasmid construction .................................................... 13 2.2.2 Common plasmid DNA protocols ................................................................. 14 2.2.3 E. coli protocols............................................................................................. 16 2.2.4 Yeast protocols .............................................................................................. 17 2.2.5 In vivo experimental scheme using EHY41 .................................................. 19 2.2.6 In vitro experimental scheme using RXY6 ................................................... 21 2.2.7 Extraction of triterpene alcohols from plant tissue ....................................... 23 2.2.8 mRNA extraction from plant tissue .............................................................. 24 2.2.9 Transcriptome search .................................................................................... 24 2.2.10 OSC product purification methods .............................................................. 24 2.2.11 Analytical tools for OSC products .............................................................. 26 Chapter 3. Detailed Characterization of A. thaliana OSCs: LUP4, LUP5, and PEN4 .. 27 Previous work ...................................................................................................... 27 LUP4 is a 74% accurate β-amyrin synthase ........................................................ 28 LUP5 produces tirucalla-7,24-dienol and isotirucallol at similar levels. ............ 29 PEN4 is an accurate thalianol synthase. .............................................................. 29 Insights from the product profiles ....................................................................... 31 Chapter 4. Characterization of OSCs from Brassica species ......................................... 33 Previous Work ..................................................................................................... 33 Bra032185: an astertarone A synthase from Brassica rapa ................................ 33 4.2.1 Phylogenetic analysis .................................................................................... 34 4.2.2 Experimental procedures for product determination ..................................... 35 4.2.3 Product profile of Bra032185 ........................................................................ 37 4.2.4 Detection and synthesis of 4-epiastertarone A .............................................. 39 4.2.5 Epimerization on 3-keto triterpenes .............................................................. 42 4.2.6 Product profile and enzyme active-site discussion ....................................... 44 4.2.7 Homology modeling ...................................................................................... 45 4.2.8 Conclusion and discussion ............................................................................ 49 Bra039929: an euphol synthase from Brassica rapa .......................................... 50 4.3.1 Phylogenetic analysis .................................................................................... 50 4.3.2 Experimental procedures for product determination ..................................... 50 4.3.3 Product profile of Bra039929 ........................................................................ 51 Characterization of B. oleracea OSC: Bol021540 .............................................. 55 4.4.1 Experimental procedures
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