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University of Thessaly Department of Biochemistry and Biotechnology University of Thessaly Department of Biochemistry and Biotechnology Afrodite Krokida GENOME ORGANIZATION, FUNCTIONAL ANALYSIS OF BIOSYNTHETIC GENES AND METABOLIC DIVERSITY OF TRITERPENES IN LEGUMES 2013 i Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 ii Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 Genome Organization, Functional Analysis of Biosynthetic Genes and Metabolic Diversity of Triterpenes in Legumes iii Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 iv Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 Three member committee Papadopoulou Kalliope, Associate Professor, Department of Biochemistry & Biotechnology, University of Thessaly, Expertise: Plant Biotechnology Osbourn E. Anne, Professor/Head, Department of Metabolic Biology, University of East Anglia/John Innes Centre Karpouzas Dimitrios, Assistant Professor, Department of Biochemistry & Biotechnology, University of Thessaly, Expertise: Environmental Microbiology & Biotechnology Seven member committee Haralampidis Kosmas, Assistant Professor at University of Athens, Faculty of Biology, Department of Botany, Molecular Plant Development Laboratory Hatzopoulos Polydeukis, Professor at Agricultural University of Athens, Department of Biotechnology, Director at Laboratory of Molecular Biology Kanellis Angelos, Professor of Biotechnology of Pharmaceutical Plants, Laboratory of Pharmacognocy, Department of Pharmaceutical Sciences, Aristotle University of Thessaloniki Karpouzas Dimitrios, Assistant Professor, Department of Biochemistry & Biotechnology, University of Thessaly, Expertise: Environmental Microbiology & Biotechnology Osbourn E. Anne, Professor/Head, Department of Metabolic Biology, University of East Anglia/John Innes Centre Papadopoulou Kalliope, Associate Professor, Department of Biochemistry & Biotechnology, University of Thessaly, Expertise: Plant Biotechnology Psarra Anna-Maria, Assistant Professor, Biochemistry, Department of Biochemistry & Biotechnology, University of Thessaly v Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 vi Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 Afrodite Krokida Genome Organization, Functional Analysis of Biosynthetic Genes and Metabolic Diversity of Triterpenes in Legumes vii Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 viii Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 Afrodite Krokida 2013 “Genome Organization, Functional Analysis of Biosynthetic Genes and Metabolic Diversity of Triterpenes in Legumes” PhD Thesis University of Thessaly Abstract Triterpenes are plant natural products that are formed by cyclization of 2,3- oxidosqualene. The triterpene scaffolds formed by enzymes known as oxidosqualene cyclases (OSCs) may be subsequently modified by enzymes such as cytochrome P450s and glucosyltansferases. Genes for triterpene biosynthetic pathways exist as metabolic gene clusters in oat and Arabidopsis thaliana plants. Four loci of candidate metabolic gene clusters were identified in the genomes of the model legumes Lotus japonicus and Medicago truncatula, in regions flanking OSC genes. Amongst these was a L. japonicus cluster containing the AMY2 OSC gene along with genes for two different classes of cytochrome P450 and a reductase. This cluster represents a new pathway for triterpene biosynthesis in legumes. Expression of AMY2 cluster genes in Nicotiana benthamiana identified a novel triterpene structure, dihydrolupeol, produced by AMY2, and allowed the biochemical characterization of a new plant cytochrome P450, CYP71D353, which catalyses the formation of 20-hydroxybetulinic acid in a sequential three-step oxidation of 20-hydroxylupeol. The cluster genes are highly co-expressed during root and nodule development, in hormone-treated plants and under different environmental stresses. A possible role for the gene cluster in plant development was revealed by the production of RNA silencing lines. These experiments also revealed an unexpected mechanism for the regulation of cluster gene expression by long distance transcriptional gene silencing. The role of βAS gene of M. truncatula was identified. The expression pattern of βAS gene was studied under various developmental conditions. Knockout ix Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 experiments in which transgenic M. truncatula for βAS were generated through A. rhizogenes transformation. Furthermore, silenced plant lines shown an increased nodule number when compared with control plants, disclosing a possible involvement of βAS in nodulation. The role of lupeol synthase, encoded by OSC3, and its product, lupeol, was identified in developing roots and nodules of the model legume L. japonicus. The expression patterns of OSC3 in different developmental stages of uninfected roots and in roots infected with Mesorhizobium loti were determined. The tissue specificity of OSC3 expression was analyzed by in situ hybridization. Functional analysis, in which transgenic L. japonicus roots silenced for OSC3 were generated, was performed. The absence of lupeol in the silenced plant lines was determined by GC- MS. The expression of ENOD40, a marker gene for nodule primordia initiation, was increased significantly in the OSC3-silenced plant lines, suggesting that lupeol influences nodule formation. Silenced plants also showed a more rapid nodulation phenotype, consistent with this. Exogenous application of lupeol to M. loti-infected wild-type plants provided further evidence for a negative regulatory effect of lupeol on the expression of ENOD40. The synthesis of lupeol in L. japonicus roots and nodules can be solely attributed to OSC3. Taken together, our data suggest a role for lupeol biosynthesis in nodule formation through the regulation of ENOD40 gene expression. Number of Preliminary Pages: 17 Number of Pages of PhD Thesis: 213 Number of Tables: 11 Number of Figures: 70 Number of Photographs: 5 Number of Appendices: 2 Number of References: 629 x Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 Prologue This PhD thesis was conducted at the research group of Plant & Environmental Biotechnology, at Department of Biochemistry & Biotechnology, University of Thessaly. The functional analysis of AMY2 cluster genes in Nicotiana benthamiana and the GC-MS analysis of OSC3-silenced plant lines were carried out at John Innes Centre, Norwich, UK. George Lomonossoff provided the pM81-FSC1 plasmid vector, Thomas Ott the pUBI-GWS-GFP vector and Peter M. Waterhouse the pHannibal vector. The work has been supported by the ESF / NSRF programme Heracleitus II. Declaration I declare that the work contained in this thesis, submitted by me for the degree of Ph.D., is my own original work, except where due reference is made to other authors, and has not been submitted by me for a degree at this or any other university. xi Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 xii Institutional Repository - Library & Information Centre - University of Thessaly 09/12/2017 11:34:05 EET - 137.108.70.7 Acknowledgements I would like to thank my supervisor Papadopoulou Kalliope for all of her help and support over the last five years, through the good times and the bad. I would also like to thank Osbourn E. Anne and Karpouzas Dimitrios for their guidance and advice all of these years. I would like to thank the seven member committee, Haralampidis Cosmas, Hatzopoulos Polydeukis, Kanellis Angelos, Karpouzas Dimitrios, Osbourn E. Anne, Papadopoulou Kalliope and Psarra Anna-Maria, for their invaluable comments and remarks that improved the quality of this work. I would like to thank Dr Delis Costas and Dr Tsikou Daniela for their wise words and invaluable advice during the conduction of the experimental procedures. I would also like to thank Dr Luis M. Peña-Rodríguez for completing all the GC-MS analyses, Dr Katrin Geisler for her help in infiltration and metabolite extraction experiments and all the members of Osbourn E. Anne‘s laboratory. I would like to thank the present and past members of the research group of Plant & Environmental Biotechnology, PhD candidate Katsarou Dimitra, PhD candidate Roussidou Konstantina, PhD candidate Perruchon Chiara, MSc student Psarrakou Ioanna-Sofia, Dr Mirtziou Ioanna, Karagounis Constantine, PhD candidate at the University of Oxford and Koufogiannis Asterios, MSc student at the Aristotle University of Thessaloniki, for their help, excellent collaboration and enjoyable time in the lab. I would especially like to thank PhD candidate Karas Panagiotis for his help, support and friendship for all of these years. I would also like to thank anyone in the Department of Biochemistry & Biotechnology that contributed in any way to this work. I would like to thank my friends Chanika Eleni, Georgiadou Dafni, Kyriakopoulou Zacharoula and Tomatsidou Anastasia for their advice, long conversations and
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