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Waduwara-Jayabahu Chammika.Pdf Significance of Methylthioadenosine Metabolism to Plant Growth and Development by Chammika Ishari Waduwara-Jayabahu A thesis presented to the University of Waterloo in fulfillment of the thesis requirement for the degree of Doctor of Philosophy in Biology Waterloo, Ontario, Canada, 2011 ©Chammika Ishari Waduwara-Jayabahu 2011 Author’s Declaration I hereby declare that I am the sole author of this thesis. This is a true copy of the thesis, including any required final revisions, as accepted by my examiners. I understand that my thesis may be made electronically available to the public. ii Abstract Arabidopsis thaliana contains two genes annotated as methylthioadenosine nucleosidases (MTN): MTN1, At4g38800 and MTN2, At4g34840. This enzyme activity hydrolyzes the methylthioadenosine (MTA) produced by nicotianamine (NA), polyamine (PA), and ethylene biosynthesis to methylthioribose (MTR) within the Yang cycle. Comprehensive analysis of the mtn1-1mtn2-1 mutant line with 14 % residual MTN activity revealed a complex phenotype that includes male and female infertility and abnormal vascular development. Based on metabolite profiling, mtn1-1mtn2-1 has a reduced NA content, altered PA profiles with higher putrescine (Put) and lower spermidine (Spd) and spermine (Spm) levels, disrupted metal ion profiles, and abnormal auxin distribution. The modeling of Arabidopsis PA synthases developed by comparison with the crystal structures of human Spd and spermine synthases complexed with MTA suggests that Arabidopsis PA synthases are product inhibited by MTA. Thus, these pleiotropic mutant phenotypes possibly are the result of one metabolite directly inhibiting numerous pathways. By creating and analyzing a series of mutants and transgenic lines with moderate levels of MTN activity the complex phenotype of mtn1-1mtn2-1 was dissected in order to determine the fundamental trait associated with MTN deficiency. Two double mutants were identified by crossing single T-DNA mutants, and an artificial micro RNA (amiRNA) line was generated by transforming mtn1-1 with amiRNA specific to MTN2. The T-DNA double mutants, mtn1-4mtn2- 1, and mtn1-1mtn2-5 had 98 % and 28 % MTN activity, respectively, whereas the amiRNA line has 16 % MTN activity. The growth, development, and metabolite analysis of these mutants revealed that their delayed bolting, correlated with an increased number of leaves, was the common trait observed across all lines. Xylem proliferation defects and increased number of vascular bundles per unit area were shared in all lines except mtn1-4mtn2-1. Based on these iii results, auxin distribution is proposed as the key target of the accumulated MTA that results from MTN deficiency. The infertility related to MTN-deficiency was restored by supplying 100 µM of Spd to the mtn1- 1mtn2-1 seedlings over 14 days. The data presented in this thesis reveals two potential links that work synergistically to recover fertility in this mtn1-1mtn2-1 line. Based on a detailed analysis of the female gynoecia morphology, transcript, hormone and metabolite profiles, it is proposed that the Spd partially reverses the mutant phenotypes through the recovery of auxin distribution and /or vascular development. Interestingly, the Spd effect seems to be transgenerational: they give rise to plants that are genotypically mtn1-1mtn2-1 but phenotypically WT over generations. Taken together, all of the results suggest that MTN- deficient mutants provide the potential for unraveling the molecular mechanism associated with nicotianamine, polyamines, auxin, and vascular development with respect to enhancing the efficiency of nutrient use and yields in plants. iv Acknowledgements First, I would like to thank my supervisor, Prof. Barb Moffatt. Barb, I am without the words to express how thankful I am to you. You have stood by me, encouraged me, guided me, and helped me develop in to a confident scientist. I know that sometimes I was difficult to handle, but you always managed me with great patience. You have been a model for me in many ways and have also played many roles in my life, from tough master to comforting soul. For all of your contributions to the person I have become, not only in a scientific context but also in day- to-day life situations, I owe you the greatest possible gratitude. To my committee members, Dr. Susan Lolle, Dr Frederique Guinel, and Dr. Simon Chuong (not in a particular order), I am indebted to all three of you for the invaluable expertise, suggestions, and guidance you provided during the committee meetings what have made this project a success. I would also like to thank each of you individually for inspiring me in your own special ways: Susan, you always had an encouraging word for me even when I met you in the hallway for a quick question. I especially thank you for supervising my work during Barb’s sabbatical. Your suggestions were always valuable, but particularly in the case of my proposal for the NSERC-summer-Japan scholarship, they helped to make my application outstanding. Dr. Guinel, you have inspired me in many ways especially with respect to your meticulous method of editing scientific writing. You have been there to discuss scientific issues or how to focus on writing a paper, and you have gone even beyond expectations to lend me your literature collection when needed it. Simon, I feel very fortunate to have had your “gentle” criticism throughout my graduate career: you were there as a committee member when I defended my MSc thesis in 2007, and four years later you were in the same position at my PhD defense. It was v because of your advice, that I hold my basic knowledge of plant anatomy and physiology as a source of pride. I would also like to thank my external supervisors, Prof. Jim Mattson and Dr. Betsy Daub, for devoting their precious time to the reading of my thesis and for critically evaluating my current knowledge. I give special thanks to all who contributed toward the success of this project. I would certainly not have been able to progress as far as I have without all of your hard work. Our collaborators Prof. Rudiger Hell and Dr. Markus Wirtz from the University of Heidelberg, Germany; Prof. Margret Sauter and Yasmin Oppermann from Universität Kiel, Germany; Prof. Hitoshi Sakakibara and Dr. Nori Nakamichi from RIKEN Japan; and Prof. Taku Takahashi and Dr. Jun-ichi Kekahi, Okayama University, Japan. The undergraduate students of the Moffatt laboratory, who assisted me technically in conducting many parts of this project: Olga Kazberova, Andy Kong, Lilian Lee, Farah El-zarkout, Ahmed Elzahabi, Danielle Menezes, Shantel Menezes, Marie Leung, Roba Bdeir, Zachary, T. Hull, Natasha Peer, Kameisha Parkins. Sarah Schoor, former graduate student of Moffatt laboratory, who initiated the work presented in this thesis, and, Tzann-Wei Wang and Qifa Zheng, research associates of Thompson laboratory, who provided assistance with the two dimentional gel electrophoresis. The providers of greatly appreciated expert knowledge throughout this project: Prof. Jaideep Mathur, University of Guelph for microscopic analysis of the mutant; Prof. Sheila Macfee, University of Western Ontario, Canada, for ionomic analysis; and Dr. Alexander N. Plotnikov for MTA inhibition modelling. vi Yong Li, technician of Moffatt laboratory, who taught me technical skills, guided me in designing the cloning and RT-PCR experiments, and gave his fullest support during critical experiments for the project. The kind gifts of the seeds of the auxin reporter line DR5rev::GFP, the NA overproducing Arabidopsis K1 line, and tkv from J. Friml (Ghent University, Belgium), Pierre Czernic (Université Montpellier, France), and Timothy Nelson (Yale University, USA), respectively. Prof. W.D. Kruger, Fox Chase Cancer Center, Philadelphia who donated the hMTAP cDNA; and Prof. M. Niitsu of the Faculty of Pharmaceutical Sciences, Josai University, who provided Tspm. I would like to thank all the sources that provided funding during my PhD program: Ontario Graduate Student scholarships (OGS), the NSERC discovery grant, the NSERC summer Japan scholarship, travel and other bursaries from the Graduate Student Office, University of Waterloo; graduate student scholarships and research and teaching assistantships from the Department of Biology, University of Waterloo. My profound thanks to Prof. Carol Peterson and Dr. Arunika Gunewardana: Carol for giving me the opportunity to come to Canada, igniting the scientist in me and guiding me in the building of a firm foundation in plant knowledge, and Arunika for connecting me with Carol and making my dream of graduate studies in Canada a reality. To all my colleagues at the University of Waterloo, including Katja Engle, Sarah Schoor, Dr. Sanghyun Lee, Tony Facciuolo, Makoto Yanagisawa, and Terry (Shiu Cheung) Lung, and to those at RIKEN, Japan, I thank you for sharing your knowledge and expertise whenever I needed it and also for making the lab a fun place to work. vii I am extremely grateful for the faculty, staff, and students of the Department of Biology. Very special thanks go to Linda Zepf, for always lending me a shoulder to lean on when things were not going well at my end. And to Dr. Mungo Marsden and Dr. Simon Chuong, thank you for letting me use your microscopes. Lynn Hoyles was there to guide and advise me every time I encountered problems with my plants on chambers and even with totally unrelated other matters. Thank you Lynn, for always taking care of my problems right away. Dale Weber deserves special thanks for teaching me the fundamentals of confocal microscopy and helping me out in every possible way, whether related to microscopy or not. I also owe Jeannie Redpath-Erb and administrative staff, Gracia Murase, Karen Miinch, Daryl Enstone, and, Ron Socha, thanks for their assistance in a variety of ways during the last four years. I am grateful to Dragana Miskovic and Cheryl Duxbury for trusting in me during TA assignments. I would like to thank Barbara Trotter for editing this thesis and Erin Harvey for her assistance with the statistical analysis.
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