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(Pisum Sativum) Seed Coat University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2014-02-07 Comparative transcriptomics and proanthocyanidin metabolism in pea (Pisum sativum) seed coat Ferraro, Kiva Ferraro, K. (2014). Comparative transcriptomics and proanthocyanidin metabolism in pea (Pisum sativum) seed coat (Unpublished doctoral thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/25368 http://hdl.handle.net/11023/1373 doctoral thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Comparative transcriptomics and proanthocyanidin metabolism in pea (Pisum sativum) seed coat by Kiva Sage Ferraro A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES CALGARY, ALBERTA JANUARY, 2014 © Kiva Ferraro 2014 Abstract Plants produce a vast array of specialized compounds known as secondary metabolites, which were originally thought to be non-essential for plant survival. However, we now know that secondary metabolites play integral roles in plant defense, signalling, reproduction and more. Proanthocyanidins (PAs) are a class of flavonoid polymers derived from the phenylpropanoid pathway. PAs accumulate in the seed coat, bark, and leaves of many plants and are believed to play a role in plant defense. Recent evidence of health benefits associated with PA consumption has spurred new research interests in PA biosynthesis. Many of the studies of seed coat PA biosynthesis have been conducted in non-crop species that produce a limited variety of PAs. Pea (Pisum sativum) offers a number of unique advantages for PA research. Peas produce large seed coats, which are easy to isolate. Dry peas are an important source of nutrition for both humans and livestock, enabling research integration into the human diet and commercial agriculture. Finally, centuries of breeding have produced a wide variety of pea cultivars, making pea a valuable phenotypic and genetic resource for plant research. Despite these advantages, PA biosynthesis in pea has not been well characterized. This work presents the seed coat PA chemical profile of three pea cultivars and the biochemical characterization of two PA branch point enzymes, anthocyanidin reductase and leucoanthocyanidin reductase, from pea. In addition, the seed coat transcriptomes of these three varieties were compared to those of two varieties lacking PAs in an effort to elucidate novel genetic mechanisms relating to PA biosynthesis. This comparative transcriptomic analysis was expanded to study general seed phenotypic differences between pea cultivars. Two target genes were identified; one related to seed weight and another to PAs, the latter of which was further characterized. ii Acknowledgements Scientific inquiry is not an individual endeavour. This work would not have been possible without the personal and academic support I have received from many people. I would like to thank my supervisor, Dr. Dae-Kyun Ro, for his advice and support in designing this project and mentoring me throughout the past six years. His guidance and enthusiasm for research have been an inspiration to me. I would also like to thank my supervisory committee members, Dr. Douglas Muench and Dr. Peter Facchini, for their advice and support. Parts of this work were done in collaboration with Dr. Jocelyn Ozga (University of Alberta), Dr. Alena L. Jin and Dr. Mark Wildung (Washington State University). Their contributions and expertise were invaluable. Science has a steep learning curve and I would also like to thank all of the past and present members of the Ro Lab who have taught me much and helped with the inevitable troubleshooting, including Gillian MacNevin, Dr. Vince Yang Qu, Dr. T. Don Nguyen, Rod Mitchell, Dr. Hue Tran, Dr. Romit Chakrabarty, and Dr. Benjamin Pickel. I wish to also extend my gratitude to the many friends with whom I have shared coffee walks and science talks, including Dr. Glen Urhig, Scott Farrow, Guillaume Beaudoin, and Donald Dinsmore. During my studies I was fortunate to receive financial support from the Province of Alberta (Queen Elizabeth II Scholarships) and from the University of Calgary. Without the personal support of close friends and especially my family, I would not be writing this today. Thank you Annie, Phil, Nancy, Dave, Calina and Shaman for all your love and encouragement. And to my wife, Natasha, who has been with me every step of this journey, you have my eternal gratitude for all your love, sacrifice and support. iii Dedication To the giants of knowledge whose shoulders I stand upon, And to all of those who helped lift me up. iv Table of Contents Abstract ............................................................................................................................... ii Acknowledgements ............................................................................................................ iii Dedication .......................................................................................................................... iv Table of Contents .................................................................................................................v List of Tables ..................................................................................................................... ix List of Figures ......................................................................................................................x List of Abbreviations ........................................................................................................ xii Epigraph ........................................................................................................................... xiv CHAPTER ONE: INTRODUCTION ..................................................................................1 1.1 Plant secondary metabolism ......................................................................................1 1.2 Phenylpropanoid metabolism ....................................................................................2 1.2.1 Plant polyphenols ..............................................................................................2 1.2.2 Biosynthesis of phenylpropanoid precursors: phenylalanine and tyrosine .......3 1.2.3 Core phenylpropanoid metabolism (PAL, C4H and 4CL) ................................4 1.2.4 Flavonoid biosynthesis ......................................................................................6 1.2.4.1 Isoflavonoids ............................................................................................7 1.2.4.2 Flavanols, dihydroflavanols and flavanones ............................................8 1.2.4.3 Anthocyanin and proanthocyanidin branch point ..................................10 1.3 Proanthocyanidins ....................................................................................................11 1.3.1 Proanthocyanidin biosynthesis ........................................................................11 1.3.2 Trans-flavan-3-ol biosynthesis by LAR ..........................................................13 1.3.3 Cis-flavan-3-ol biosynthesis by ANR .............................................................15 1.3.4 Cis- to trans-flavan-3-ol epimerization by ANR .............................................16 1.3.5 Substrate channelling in the PA biosynthetic pathway ...................................17 1.3.6 Intracellular transport of PA precursors ..........................................................18 1.3.6.1 Glutathione S-transferase (GST) in PA metabolism ..............................19 1.3.6.2 Transporters in PA metabolism .............................................................21 1.3.6.3 Proton (H+)-antiporter in PA metabolism .............................................22 1.3.6.4 Glycosylation of PA monomers .............................................................22 1.3.6.5 Vesicle-mediated transport of PA monomers ........................................23 1.3.7 PA structures ...................................................................................................25 1.3.8 Condensation of PA monomers .......................................................................26 1.3.9 Transcriptional regulation of PA biosynthesis ................................................28 1.3.9.1 Transcriptional regulation of PA metabolism in Arabidopsis ...............30 1.3.9.2 Hormonal regulation of Arabidopsis PA biosynthesis ..........................34 1.3.9.3 Feedback and RNAi-mediated regulation of flavonoid biosynthesis ....35 1.4 Pea: Pisum sativum L. ..............................................................................................36 1.5 Next generation sequencing (NGS) technology ......................................................38 1.5.1 Roche/454-pyrosequencing .............................................................................39 1.5.2 Illumina Hi-Seq 2000 sequencing ...................................................................39 1.5.3 NGS data processing and analysis ...................................................................40
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