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Development of a Metabolomics Strategy for Novel Natural Product Discovery Development of a Metabolomics Strategy for Novel Natural Product Discovery and its Application to the Study of Soybean Defense Responses Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Jiye Cheng, M.A.S. Graduate Program in Plant Pathology The Ohio State University 2011 Dissertation Committee: Terrence Lee Graham, Advisor A. Douglas Kinghorn Laurence Vincent Madden Pierluigi Bonello Copyright by Jiye Cheng 2011 ii Abstract Plant secondary product metabolic pathways produce an astonishing wealth of metabolites with important biological functions. These secondary metabolites play critical roles in plant defense responses, including defense against herbivores, pests and pathogens. Also, plant natural product compounds are the source of numerous pharmaceuticals. In the areas of cancer and infectious disease, 60 and 75%, respectively, of new drugs originate from plants. Metabolomics, with the aim at qualitative and quantitative analysis of the full complement of metabolites in biological samples, has truly established itself as a valuable tool for plant functional genomics and studies of plant biochemical composition. However, its potential to find new natural products remains untapped due to the diversity and complexity of natural products. Optimized metabolomics strategies for the discovery of new natural products are needed. Therefore, we proposed a series of simple operations for new natural products discovery based on metabolomic studies. The main steps include (1) LC-ESI-MS profiling analysis, (2) peak detection, supervised retention time alignment and peak matching for multiple groups of samples, (3) selection of the metabolites that are unknown induced natural products, (4) purification of target metabolites by preparative HPLC and finally, (5) structure elucidation based on NMR. This strategy was applied to the metabolite profiling and systematic identification of defense- response-induced secondary metabolites in soybean cotyledons. We were able to simultaneously detect and identify 13 isoflavones, 2 coumestans and 6 ii pterocarpans. Totally, 5 compounds were discovered as natural products for the first time in soybean. Comparative metabolite profiling of soybean cultivars resistant and susceptible to Phytophthora sojae (Kauf. and Gerde.) was performed. Principal component analysis clearly demonstrated a separation of elicitor-activated resistant and susceptible soybean cultivars. 3’- prenylisoafrormosin, glyceocarpin, glyceofuran, 3'-prenylgenistein and phaseol were identified as the key secondary metabolites accounting for the separation. The metabolite profiling results present the most complete analysis of soybean induced secondary metabolites to date, which can be further utilized to evaluate chemical components of soybean samples for plant biology, food science and pharmaceutical studies. Our results also provide additional knowledge of the soybean secondary metabolite pathways involved in defense. Moreover, the proposed strategy demonstrates a promising future approach for novel compound discovery even in relatively well studied plants. In soybean, phenylpropanoids play critical roles in defense responses. They regulate certain aspects of oxidative stress and hypersensitive cell death and act as phytoalexins, which directly inhibit pathogen growth. Interestingly, some of phenylpropanoids from soybean also have many reported activities in animal cells. In particular, genistein is one of the most potent phytoestrogens and glyceollin has been reported a good lead for anticancer activity. Due to these important activities, an in depth study of how phenylpropanoid pathways are regulated was conducted. Over 25 compounds were examined, including exogenous elicitors, signal molecules iii and signal transduction regulators for their effects on wound-, light- and glucan defense elicitor-induced phenylpropanoid responses in soybean. As for exogenous elicitors, many of the Pathogen Associated Molecular Patterns (PAMPs) tested (chitin oligomers, LPS, wall glucan elicitor, mycolaminaran) induce the production of glyceollin as expected. Interestingly, all chemicals that are H+ and/or K+ ion effectors (vanadate, monensin, valinomycin, nigericin and fusicoccin) cause a massive accumulation of inducible secondary metabolites. Additionally, 2-methoxy-3,9-dihydroxycoumestone, 1- methoxy-3,9-dihydroxy coumestone, 8-methoxy-3,9-dihydroxycoumestone, and 7,4’-dihydroxy-5’-methoxycoumaronochromone were discovered as natural products for the first time in soybean in this study. Overall, the results of this study suggest that phenylpropanoid metabolism may be controlled by manipulating the transmembrane potential. iv Dedication This thesis is dedicated to my parents. They are the reason of my success, the reason of my life. I love you. v Acknowledgements My foremost gratitude goes to my adviser Dr. Terrence Lee Graham whose guidance and support were crucial for me to accomplish this thesis. I thank him for his patience, encouragement, and consideration that carried me on through difficult times, and for his insights and suggestions on my research. I gratefully acknowledge my student advisory committee members, Dr. A. Douglas Kinghorn, Dr. Laurence Vincent Madden and Dr. Pierluigi Bonello, who advised me and helped me in various aspects of my thesis. It has been a precious experience to work with Madge Graham, Michelle Sinden and Kara Riggs and I thank them for their valuable suggestions for my research, collegiality and technical support in lab. I would like to thank Kyle Benzle and Chunxue Cao for their assistance in collection and treatment of soybean cotyledons for my study. Also, I want to give my special thanks to Dr. Chunhua Yuan and Dr. Stephen Opiyo. Dr. Yuan provided me exceptional NMR training and metabolite structure elucidation support. Dr. Opiyo has done a tremendous job in organizing and maintaining the use of LC/MS instrument which was critical for me to complete my project in time. Finally, I am forever indebted to my parents and my fiancée for their understanding, endless patience and encouragement when it was most required. vi Vita 2006 ................................. B.S. Pharmacy, Shanghai Jiaotong University 2010 ................................. M.A.S. Statistics, The Ohio State University 2006 to present................. Graduate Research Associate, Department of Plant Pathology, The Ohio State University Fields of Study Major Field: Plant Pathology vii Table of Contents Abstract .....................................................................................................ii Dedication..................................................................................................v Acknowledgments .....................................................................................vi Vita ............................................................................................................vii Table of Contents ......................................................................................viii List of Tables .............................................................................................x List of Figures ............................................................................................xii List of Abbreviations ..................................................................................xvi Chapter 1: Introduction ..............................................................................1 Chapter 2: Potential defense-related prenylated isoflavones in lactofen- induced soybean .......................................................................................17 Introduction .....................................................................................18 Materials and methods....................................................................20 Results and discussion ...................................................................28 Conclusion ......................................................................................40 Chapter 3: Systematic identification and comparative metabolite profiling of soybean (Glycine max) defense-related secondary metabolites in Phytophthora sojae resistant and susceptible cultivars .............................42 Introduction .....................................................................................43 Materials and methods....................................................................46 viii Results and discussion ...................................................................54 Conclusion ......................................................................................67 Chapter 4: A metabolomic strategy for new natural product discovery......69 Introduction .....................................................................................70 Results and discussion ...................................................................73 Materials and methods....................................................................90 Conclusion ......................................................................................96 References ................................................................................................98 ix List of Tables Table 1.1 Software and databases for LC-MS tentative compound identification................................................................................................. 13 Table 1.2 Known soybean defense-related metabolites
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