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Combinatorial Biochemistry of Triterpene Saponins in Plants Jacob Pollier

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Combinatorial Biochemistry of Triterpene Saponins in Plants Jacob Pollier Combinatorial Biochemistry of Triterpene Saponins in Plants Jacob Pollier Ghent University - Faculty of Sciences Department of Plant Biotechnology and Bioinformatics VIB - Department of Plant Systems Biology Combinatorial Biochemistry of Triterpene Saponins in Plants Jacob Pollier Thesis submitted in partial fulfillment of the requirements for the degree of Doctor (PhD) in Sciences: Biotechnology Academic year: 2010-2011 Promotor: Prof. Dr. Alain Goossens Dit onderzoek werd uitgevoerd in het departement Planten Systeembiologie van het Vlaams Instituut voor Biotechnologie (VIB) en de Universiteit Gent. This work was conducted in the department of Plant Systems Biology of the Flanders Institute for Biotechnology (VIB) and the Ghent University. Dit onderzoek werd gefinancierd door het agentschap voor Innovatie door Wetenschap en Technologie in Vlaanderen (IWT-Vlaanderen, Strategisch Basisonderzoek project SBO040093). This work was supported by the Agency for Innovation by Science and Technology in Flanders (IWT-Vlaanderen, Strategisch Basisonderzoek project SBO040093). ii Board of Examiners Promotor Prof. Dr. Alain Goossens* VIB Department of Plant Systems Biology Department of Plant Biotechnology and Bioinformatics Faculty of Sciences Ghent University Examination Committee Prof. Dr. Ann Depicker (Chair) VIB Department of Plant Systems Biology Department of Plant Biotechnology and Bioinformatics Faculty of Sciences Ghent University Prof. Dr. Danny Geelen* Department of Plant Production Faculty of Bioscience Engineering Ghent University Prof. Dr. Jan Van Bocxlaer* Department of Bio-analysis Faculty of Pharmaceutical Sciences Ghent University Prof. Dr. Luc Pieters* Department of Pharmaceutical Sciences Faculty of Pharmaceutical, Biomedical and Veterinary Sciences University of Antwerp Dr. Kris Morreel* VIB Department of Plant Systems Biology Department of Plant Biotechnology and Bioinformatics Faculty of Sciences Ghent University iii Prof. Dr. Dirk Inzé VIB Department of Plant Systems Biology Department of Plant Biotechnology and Bioinformatics Faculty of Sciences Ghent University Prof. Dr. Sofie Goormachtig VIB Department of Plant Systems Biology Department of Plant Biotechnology and Bioinformatics Faculty of Sciences Ghent University * Members of the Reading Committee iv Table of Contents List of Abbreviations vi Abstract 1 Chapter 1 Combinatorial biochemistry in plants: A (p)review on its 3 potential and future exploitation Chapter 2 A functional genomics approach to discover genes involved in 49 triterpene saponin biosynthesis in five different plants Chapter 3 An integrated PCR colony hybridization approach to screen 83 cDNA libraries for full-length coding sequences Chapter 4 Metabolite profiling of triterpene saponins in Medicago 99 truncatula hairy roots by liquid chromatography Fourier transform ion cyclotron resonance mass spectrometry Chapter 5 Combinatorial biochemistry of triterpene saponins in plants 127 Chapter 6 The RING E3 ubiquitin ligase MAKIBISHI1 regulates triterpene 151 saponin biosynthesis in Medicago truncatula Chapter 7 Perspectives 191 Summary 201 Samenvatting 203 Acknowledgements 205 Appendix Additional publications 207 Curriculum vitae 213 Supplementary data 215 v List of Abbreviations ACN Acetonitrile AFLP Amplified Fragment Length Polymorphism BAS β-Amyrin Synthase BEH Bridged Ethyl Hybrid BLAST Basic Local Alignment Search Tool bp base pair BY-2 Bright Yellow 2 CAS Cycloartenol Synthase CHX Cycloheximide CID Collision-induced Dissociation CKD Chronic Kidney Disease CV Coefficient of Variation CytP450 Cytochrome P450 DDS Dammarenediol Synthase E-DMNT 4,8-dimethyl-1,3(E),7-nonatriene ERAD Endoplasmic Reticulum-associated Degradation ESI Electrospray Ionization EST Expressed Sequence Tag FL Full-length FPS Farnesyl Pyrophosphate Synthase FT-ICR MS Fourier Transform Ion Cyclotron Resonance Mass Spectrometry HMGR 3-hydroxy-3-methylglutaryl-CoA reductase HPLC High-performance Liquid Chromatography hpRNAi Hairpin RNA-mediated Interference HRD1 HMGR DEGRADATION 1 vi HTS High-throughput Screening ICH International Conference on Harmonisation of Technical Requirements for Registration of Pharmaceuticals for Human Use IgG Immunoglobulin G IPP Isopentenyl Pyrophosphate ISCOM Immunostimulating Complex IT Ion Trap JA Jasmonic Acid JA-Ile Jasmonoyl-isoleucine JAZ Jasmonate ZIM-domain LC Liquid Chromatography LOF Lack of Fit LUS Lupeol Synthase MeJA Methyl Jasmonate MEP 2-C-methyl-D-erythritol 4-phosphate MKB1 MAKIBISHI1 MS Mass Spectrometry MTGI Medicago truncatula Gene Index MVA Mevalonate NF-κB Nuclear Factor kappa-light-chain-enhancer of activated B cells NMR Nuclear Magnetic Resonance ORF Open Reading Frame OSC Oxidosqualene Cyclase PCS Pentaketide Chromone Synthase PDB Precursor-Directed Biosynthesis PPD Protopanaxadiol PPT Protopanaxatriol vii qRT-PCR Quantitative Real-time Polymerase Chain Reaction RACE Rapid Amplification of cDNA Ends RSD Relative Standard Deviation QTL Quantitative Trait Locus RIL Recombinant Inbred Line RING Really Interesting New Gene RMA1 RING-FINGER PROTEIN WITH MEMBRANE ANCHOR 1 RT-PCR Reverse Transcription Polymerase Chain Reaction SD Standard Deviation SEM Scanning Electron Microscopy SLIP Self-Ligation of Inverse PCR Products SPE Solid-phase Extraction SQE Squalene Epoxidase SQS Squalene Synthase STL Sesquiterpene Lactone TC Tentative Consensus TEM Transmission Electron Microscopy THAS Thalianol Synthase TIA Terpenoid Indole Alkaloid TIC Total Ion Current TIGR The Institute for Genomic Research UPLC Ultra Performance Liquid Chromatography UTR untranslated region viii Abstract Plants are capable of synthesizing an overwhelming variety of secondary metabolites, many of which possess biological activities relevant for the pharmaceutical and chemical industries. Furthermore, there is an ever increasing demand for novel compounds, due to, among others, the growing drug tolerance and resistance in microorganisms and newly emerging diseases. In microorganisms, combinatorial biochemistry is a widely used tool to increase structural variation in several classes of (microbial) natural products. Despite the potential importance of plant secondary metabolites, only a limited fraction of these molecules is currently used, mostly due to their complex structure and the low production levels in planta. Metabolic engineering of plants has offered limited help because the molecular mechanisms steering plant secondary metabolism remain poorly characterized. Here, we used a functional genomics approach to identify candidate genes involved in the saponin biosynthesis of five different plants. After targeted metabolite profiling confirmed the induction of triterpene saponin biosynthesis by methyl jasmonate treatment, a genome-wide cDNA-AFLP transcript profiling was carried out for the five plants. Taking into account the putative functional annotation and the expression pattern of the visualized transcript tags, a set of 259 candidate genes potentially involved in saponin biosynthesis and its regulation were identified. The generated gene list provided the basis for a combinatorial biochemistry platform that targets triterpene saponins in plants. Proof of concept of combinatorial biochemistry was achieved by heterologous expression of the candidate saponin biosynthesis genes in M. truncatula hairy roots. Three of the generated transgenic hairy root lines were found to accumulate novel molecules, two of which were shown to be novel triterpene saponins, whereas the third line produced a set of novel, non-saponin compounds. Furthermore, the identified transcription factors and other regulators were lead candidates for studies investigating the control of the saponin biosynthesis in planta. This led to the identification of a RING membrane-anchor E3 ubiquitin ligase, MAKIBISHI1 (MKB1), that targets 3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), the enzyme catalyzing the rate-limiting step in the mevalonate pathway, for ubiquitin-mediated proteasomal degradation, thereby controlling saponin biosynthesis. 1 2 Chapter 1 Combinatorial biochemistry in plants: A (p)review on its potential and future exploitation Jacob Pollier*, Tessa Moses, and Alain Goossens * Author contribution: writing of the (review) manuscript. 3 Publication status: A synopsis was accepted by the editorial board of Natural Product Reports (IF: 9.202). The full manuscript is under review. 4 Abstract Combinatorial biochemistry, also called combinatorial biosynthesis, comprises a series of methods that establish novel enzyme-substrate combinations in vivo, which in turn lead to the biosynthesis of new, natural product-derived compounds that can be used in drug discovery programs. Plants are an extremely rich source of bioactive natural products and continue to possess a huge potential for drug discovery. In this review, we discuss the state-of-the-art in combinatorial biosynthesis methods to generate novel molecules from plants. We debate on the progress and potential in biotransformation, mutasynthesis, combinatorial metabolism in hybrids, activation of silent plant metabolism and synthetic biology in plants and microbes to create opportunities for combinatorial biosynthesis of plant-derived natural products, and, ultimately, for drug discovery. The therapeutic value of two classes of natural products, the terpenoid indole alkaloids and the triterpene saponins is particularly highlighted. 5 1. Introduction For already thousands of years, mankind has made use of plant-derived natural products to treat diseases and injuries (Ji et al.,
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