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Phd Thesis Chapter 1 The Regulation of Stress-Induced Proanthocyanidin Metabolism in Poplar by Robin D. Mellway B. Sc., University of Victoria, 2003 A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY in the Department of Biology Robin D. Mellway, 2009 University of Victoria All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. Library and Archives Bibliothèque et Canada Archives Canada Published Heritage Direction du Branch Patrimoine de l’édition 395 Wellington Street 395, rue Wellington Ottawa ON K1A 0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre référence ISBN: 978-0-494-66841-2 Our file Notre référence ISBN: 978-0-494-66841-2 NOTICE: AVIS: The author has granted a non- L’auteur a accordé une licence non exclusive exclusive license allowing Library and permettant à la Bibliothèque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par télécommunication ou par l’Internet, prêter, telecommunication or on the Internet, distribuer et vendre des thèses partout dans le loan, distribute and sell theses monde, à des fins commerciales ou autres, sur worldwide, for commercial or non- support microforme, papier, électronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L’auteur conserve la propriété du droit d’auteur ownership and moral rights in this et des droits moraux qui protège cette thèse. Ni thesis. Neither the thesis nor la thèse ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent être imprimés ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author’s permission. In compliance with the Canadian Conformément à la loi canadienne sur la Privacy Act some supporting forms protection de la vie privée, quelques may have been removed from this formulaires secondaires ont été enlevés de thesis. cette thèse. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n’y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. ii Supervisory Committee The Regulation of Stress-Induced Proanthocyanidin Metabolism in Poplar by Robin D. Mellway B. Sc., University of Victoria, 2003 Supervisory Committee Dr. Peter Constabel, Department of Biology Supervisor Dr. Perry Howard, Department of Biochemistry and Microbiology and Department of Biology Departmental Member Dr. William Hintz, Department of Biology Departmental Member Dr. Chris Upton, Department of Biochemistry and Microbiology Outside Member Dr. Armand Séguin, Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre Additional Member iii Abstract Supervisory Committee Dr. Peter Constabel, Department of Biology Supervisor Dr. Perry Howard, Department of Biochemistry and Microbiology and Department of Biology Departmental Member Dr. William Hintz, Department of Biology Departmental Member Dr. Chris Upton, Department of Biochemistry Outside Member Dr. Armand Séguin, Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre Additional Member Proanthocyanidins (PAs) are polymeric phenolic chemicals produced by many plant species that may contribute to protection of tissues against biotic and abiotic stress conditions. In poplar (Populus spp.) leaves, PA biosynthesis is rapidly activated by insect herbivore damage, indicating that PAs may be an inducible chemical defence. In this study, the expression of PA biosynthetic genes was monitored in poplar leaves exposed to several stress stimuli. The PA pathway was shown to be rapidly activated at the level of gene transcription by stresses such as elevated light, UV-B irradiation and infection of leaves by a biotrophic fungal parasite. A transcription factor gene of the R2R3 MYB type, MYB134, was found to be co-activated with PA biosynthetic genes under these stress conditions. When overexpressed in transgenic poplar, this gene induced a strong, specific activation of the PA pathway, indicating that it might function as a regulator of stress-induced PA metabolism in poplar. MYB134 was shown to bind to promoter fragments of PA biosynthetic genes which contained a conserved DNA cis-element found in the promoter regions of many other phenylpropanoid genes including putative MYB134-regulated genes. A global transcriptome analysis of leaves of the MYB134- overexpressing poplar plants confirmed that the PA pathway activation was complete and specific, and led to the identification of a number of putative novel PA biosynthetic and regulatory genes. These results indicate that stress-responsive PA and flavonoid metabolism in poplar may be regulated by a complex system involving both positive and iv negative regulation. Preliminary results are also presented related to analysis of PA functions in transgenic plants, and the use of MYB134 to engineer PA metabolism in plants other than poplar. This study provides insight into the regulatory mechanisms controlling stress-induced PA metabolism, and expands our understanding of roles that this biological response may play in poplar. v Table of Contents Supervisory Committee ...................................................................................................... ii Abstract.............................................................................................................................. iii Table of Contents................................................................................................................ v List of Tables ................................................................................................................... viii List of Figures.................................................................................................................... ix List of Abbreviations ....................................................................................................... xiii Acknowledgments............................................................................................................. xv Frontispiece...................................................................................................................... xvi Chapter 1: Introduction....................................................................................................... 1 1.1 General introduction ................................................................................................. 1 1.2 Overview of flavonoid and PA biosynthesis ............................................................ 3 1.2.1 The biosynthesis of flavonoids .......................................................................... 3 1.2.2 The biosynthesis of PAs..................................................................................... 9 1.3 Investigation of the PA pathway in poplar ............................................................. 16 1.3.1 Poplar as a model system for investigating defence phenylpropanoid metabolism................................................................................................................ 16 1.3.2 PAs and other soluble phenolics in poplar....................................................... 18 1.4 Stress-protective functions of flavonoids and PAs ................................................. 23 1.4.1 Stress-induced flavonoid metabolism.............................................................. 23 1.4.2 Stress-protective functions of PAs................................................................... 27 1.4.3 Herbivore-induced PA metabolism in poplar and other trees.......................... 33 Alternative functions for stress-induced PAs in poplar ................................... 36 1.4.5 Transcriptional activation of PA biosynthetic genes in poplar........................ 39 1.5 The regulation of flavonoid and PA metabolism.................................................... 42 1.5.1 A conserved regulatory protein complex is involved in the regulation of anthocyanin and PA biosynthesis ............................................................................. 42 1.5.2 Regulation of the anthocyanin and flavonol pathways.................................... 53 1.5.3 Regulation of the PA pathway ......................................................................... 60 1.5.4 Negative regulators of flavonoid metabolism.................................................. 62 1.5.6 Phenylpropanoid and flavonoid gene promoters ............................................. 65 1.5.7 Regulation of the regulators and upstream signalling...................................... 68 1.6 Metabolic engineering of flavonoid and PA metabolism ....................................... 70 1.6.1 Metabolic engineering of plant secondary metabolism ................................... 70 1.6.2 Applications of flavonoid pathway engineering .............................................. 71 1.6.3 Metabolic engineering of flavonoid and PA metabolism ................................ 73 1.6.4 Candidate gene identification using transcription factor overexpression ........ 75 1.7 Hypotheses, objectives and summary of key findings............................................ 79 Chapter 2: Molecular Analysis of Stress-Induced PA Metabolism in Poplar .................
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