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The Role of Primary Carbohydrate Metabolism in Wheat Grain Dormancy and Germination

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The Role of Primary Carbohydrate Metabolism in Wheat Grain Dormancy and Germination The role of primary carbohydrate metabolism in wheat grain dormancy and germination Author: Supervisors: Ross Dennis Professor Robert Furbank Doctor Jean-Philippe Ral A thesis submitted for the degree of Doctor of Philosophy to The Australian National University. Submitted May 2019 ii Declaration This thesis is an original work. None of this work has been submitted by me for the purposes of obtaining a degree or diploma in any university or tertiary institution. To the best of my knowledge this thesis does not contain material previously published by another person, except where due reference has been made. ………………………………………………. Ross J Dennis iii iv From little things big things grow Paul Kelly (b. 1966) v Dedication For Maddie vi Acknowledgments First and foremost I thank my supervisors Prof. Robert Furbank and Dr Jean-Philippe Ral for their guidance and support during this PhD. In particular, I would like to thank JP for his day-to- day discussions, enthusiasm to pursue ideas, navigation of the CSIRO bureaucracy, and initiation of this project to welcome me to Canberra. Thanks to Bob for being a source of cool, calm collectedness, our discussions of ideas and concepts, and regaling me with stories from the range and depth of his research experience. Thank you to my examiners for taking the time to provide constructive advice and positive feedback to make this thesis even stronger. Thank you to all the members of the two labs I was associated with both at CSIRO and ANU. In particular, I would like to thank Jeni Pritchard, Dr Jos Mieog, Dr Ron Yu, Dr Anna Flis, Dr Alex Ivakov, Lily Chen, and Peng Zhang for their technical wisdom and assistance. Thanks to Prof. Michelle Colgrave, Dr Utpal Bose, and Keren Byrne, for their advice and analysis of the SWATH samples for proteomic investigation of A3OE dormancy and germination. Thanks to Dr Frank Gubler, Dr Jose Barrero, Trijntje Hughes, Jasmine Rajamony, Dr Thy Truong and Dr Peter Chandler for sharing their knowledge and for discussions and help with dormancy and germination studies and ABA analysis. Thank you also to Dr Greg Rebetzke for discussion of coleoptile growth and to Dr Filomena Pettolino for discussions regarding cell wall biosynthesis. Thanks also to Dr Adam Carroll for his assistance trouble shooting a number of methods. Dr Andrew Bowerman, as my predecessor, was a fountain of wisdom on all things starch- and wheat-related and a valuable sounding board of ideas and trouble shooting. I would like to extend a warm thanks to Dr John Lunn, Regina Feil, Prof. Mark Stitt, and Franzi Fichtner for their hospitality and welcoming me to the Max Planck Institute of Molecular Plant vii Physiology, teaching me extraction of T6P, many discussions regarding T6P, metabolic analyses and our ongoing collaboration. I want to acknowledge and thank the ANU for my PhD scholarship and the Centre of Excellence for Translational Photosynthesis for top-up funding. I also would like to acknowledge CSIRO, the Society for Experimental Biology, the Grains Research and Development Corporation, the Crawford Fund and Australian Society for Plant Scientists for additional funds for research and travel. And a big thank you to my family and all my friends from the CSIRO W.A.C, CSIRO Social Club, CSIRO Crop Adaptation lab chat crew, CSIRO RP3, ANU Plant Sciences/RSB happy hour, Coffee Grounds and from further afield for their support, discussions, encouragement, friendship, and kindness. I want to express my gratitude to friends and mentors Associate Prof. Kat Dziegielewska, Prof. Norman Saunders, Doctor Paul Gibson-Roy whose experienced words of encouragement were a great support. A special thanks to Matthias Nachtschatt and Ross Deans for the many coffees, beers, discussions, and writing sessions. To Dr Andrew Hoskins and Holly Lourie: thanks for keeping me active and encouraging some competitive gardening and cathartic venting. And finally, I would like to thank my friend, wife and colleague, Dr Madeline Mitchell, without whom I would not have begun, continued or finished this PhD. I am grateful for her support, wisdom, thesis editing, technical advice, love and tolerance (of the beard and existential angst, the various procrasta-hobbies, the natural disasters and ill health, the coffees, the lunches, the highs and the lows). viii Précis Germination is the first step in a plant’s life history, critical to giving plants the best chance of surviving and prospering. Germination involves a suit of processes that culminate in the emergence of the seedling from the seed coat and requires considerable amounts of energy, particularly in the form of sugar. Dormancy prevents germination under appropriate conditions in an otherwise viable seed and is the strategy plants use to regulate the timing of germination. Domestication has caused dormancy to decline in crop species such as wheat as reduced dormancy leads to more uniform crop establishment. However, too little dormancy can have detrimental consequences for crop production. The aim of this study was to investigate the role of sugar metabolism and signalling during germination and dormancy in wheat seeds. This thesis will present three different analyses of germination and dormancy and a fourth analysis of these effects on seedling establishment in a transgenic wheat line with modified carbohydrate metabolism. First, a series of germination assays revealed the striking, and at times contradictory, interaction between sugar metabolism and hormone signalling during wheat dormancy and germination. The elevated sugars in the transgenic seeds appeared to overcome normal dormancy processes and cause precocious germination. Second, a proteomics approach identified differential abundance of proteins involved in key metabolic and signalling pathways, suggesting that dormancy processes were present concurrently with processes to initiate germination in precociously germinated seeds. Third, the correlation between sucrose and the sucrose sensing metabolite Trehalose-6-Phosphate (T6P) was found to be disrupted in precociously germinated grain, indicating a possible role for T6P in dormancy and germination. This prompted the development of novel transgenic wheat lines with altered expression of genes regulating T6P in the grain in order to further investigate T6P’s role in germination. Fourth, a novel method was developed to monitor plant establishment in the dark, which revealed that perturbations in dormancy and germination processes negatively affected seedling growth. Overall, this work highlights the importance of sugar signalling and metabolism in germination, dormancy and seedling establishment and challenges elements of the pre-existing model of these processes. ix Table of contents ACKNOWLEDGMENTS .......................................................................................................................... VII PRÉCIS .................................................................................................................................................. IX TABLE OF CONTENTS ............................................................................................................................. X LIST OF FIGURES .................................................................................................................................XIV LIST OF TABLES ...................................................................................................................................XVI ABBREVIATIONS ................................................................................................................................XVII 1. THE ROLE OF PRIMARY CARBOHYDRATE METABOLISM DURING WHEAT GRAIN DORMANCY AND GERMINATION ....................................................................................................................................... 1 WHEAT IS A NUTRITIONALLY AND ECONOMICALLY IMPORTANT CROP WORLDWIDE ................................................... 1 DORMANCY IS REDUCED IN WHEAT AND OTHER DOMESTICATED CROPS ................................................................. 2 Natural variation in dormancy mechanisms .................................................................................... 3 Wheat seeds have physiological dormancy ................................................................................................ 3 PLANT PROSPERITY, DEPENDS ON CORRECT GERMINATION ................................................................................. 6 Germination involves a suite of biological processes acting in concert ............................................. 7 DORMANCY AND GERMINATION PROCESSES CONTRIBUTE TO PRE-HARVEST SPROUTING AND LOSS OF GRAIN QUALITY ....... 9 Current tests for PHS are inaccurate ............................................................................................. 10 Transgenic wheat with high α-amylase as a system to explore PHS and LMA ................................ 11 SUCROSE SIGNALLING AFFECTS DORMANCY AND GERMINATION AND PHS ........................................................... 11 GENERAL AIMS OF THIS STUDY .................................................................................................................. 13 2. GERMINATION AND DORMANCY IN A3OE GRAINS WITH ALTERED CARBOHYDRATE RESERVES .. 15 INTRODUCTION .................................................................................................................................... 15 MATERIALS AND METHODS ....................................................................................................................
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