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Metabolic Responses to Potassium Availability and Waterlogging in Two Oil- Producing Species: Sunflower and Oil Palm

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Metabolic Responses to Potassium Availability and Waterlogging in Two Oil- Producing Species: Sunflower and Oil Palm Metabolic responses to potassium availability and waterlogging in two oil- producing species: sunflower and oil palm Jing Cui Supervisor: Prof. Guillaume Tcherkez A thesis submitted for the degree of Doctor of Philosophy The Australian National University Declaration Except where otherwise indicated, this thesis is my own original work. No portion of the work presented in this thesis has been submitted for another degree. Jing Cui Research School of Biology College of Medicine, Biology and Environment September, 2019 © Copyright by Jing Cui (2019). All Rights Reserved. 1 Acknowledgements Primarily my deepest thank goes to my principal supervisor Professor Guillaume Tcherkez (Research School of Biology, The Australian National University, Canberra), who has always given me help, advice and support throughout my PhD, Thank you very much for your enthusiasm, patience, efficience and guidance. One of the major motivations I committed to this PhD is your strong faith in me, I have been truly fortunate to work with you for the last three years. I thank my co-supervisor Dr. Emmanuelle Lamade (CIRAD, France), for your time, thoughtful comments and invaluable advice that they gave me along my project. Thank you also to my PhD committee members Dr. Adam Carroll (Research School of Chemistry and Biology Joint Mass Spectrometry Facility), Dr. Cyril Abadie, Dr. Hilary Stuart-Williams and Prof. Marilyn Ball (Research School of Biology, The Australian National University) for their help and guidance. I would like to thank Dr Thy Truong (Research School of Chemistry and Biology Joint Mass Spectrometry Facility) for taking the time to share with me her expertise in GC-MS, and look forward to working with her in LC/MSMS, also thank Dr.Marlène Davanture and Dr. Michel Zivy (PAPPSO, France) for their help in proteomics analysis. In particular, I would like to acknowledge the advice from Dr. Juan Chao de la Barca (University of Angers, France) for statistical analysis. I thank Les and Linda (Research School of Earth Science, ANU) for their assistance with ICP-OES analysis and for helpful discussions of digestion protocol. In addition I wish to thank Andrew Higgins (Fenner School, ANU) for welcoming me to do digestion experiment in his laboratory. I am also grateful for the invaluable advice on gas exchange matters offered by Dr. Florian Busch and Ross Dean (both of the Research School of Biology, ANU). I thank Dr Christina Spry and Professor Kevin Saliba (both of the Research School of Biology) for letting me work in their laboratory, so I can finish all my experiment before lab moving to Robertson Building. Many thanks go to the Plant Science HDR convenor, Professor Spencer Whitney for his encouragement and giving guidance of completing all PhD milestone. Also, I want to thank Professor Barry Pogson for giving me opponituty to involve in teaching, which is one of my favourite parts during study. I would like to thank Research School of Biology Plant Service Team (Steven Dempsey, Darren, Gavin, Steve Zabar, Jenny and Christine) for their kind help in the glasshouse. Thank you to Stephanie McCaffery, Ursula Hurley, 2 Dr. Farid Rahimi and Graham Hicks, for helping me solve different kinds of problems in their first time. Thank you to Gagan Bhardwaj and Helen Wong for their kind administrative help, I could not have finished all the headache paperwork without them. I also would like to say thank you to my group of friends and colleagues in the Tcherkez laboratory and Research School of Biology. It was an absolute luck to work with, especially, Dr. Camille Bathellier, Dr. Illa Tea, Sophie Blanchet, Jean-Baptiste Domergue, Cathleen Mirande-Ney, Sophie Renou, Haydon Siiteri, Peter Groeneveld, Dr. Charles Hocart, Dr. Suan Wong, Thomas Davis, Denis Hawkins, Dr. John Rivers, Dr. Kai Chan, Dr. Xin Hou, Kiran Javed, and Graeme Clemow. This project would not have been done without their friendship, encouragement and cheering me up. Additionally, I am thankful to receive the Australian postgraduate Scholarship (APA), without which I would not have been able to undertake this PhD. This whole project was partly funded by the Australian Research Council via a Future Fellowship awarded to my principal supervisor, under contract FT140100645. Also, I would like to acknowledge the support from the ANU Vice-Chancellor’s HDR Travel Grant and CSIRO Plant Nutrition Trust Travel Grant, under these grants support, I attended two international conferences and shared my PhD results with other scientists. Very big thank you to my family, thanks my parents and parents-in-law’ help, support and all of the sacrifices you have made for me, especially during the hard times. Last but not least goes to my beloved husband, Weihua, for everlasting support throughout this thesis, wherever possible, for patiently during my tantrums, for being such a wonderful husband in so many ways for the last twelve years of my life, and for your unconditional love, I will not be able to go through this amazing journey without you. 3 Abstract Oil palm and sunflower are important major oil-producing crops at the global scale, with 70 Mt oil produced each year. Although they have been studied for decades for their agronomical aspects, their metabolism is poorly documented, in particular situations such as low potassium. In fact, these species are strong potassium (K)-demanding species cultivated in regions where soil K availability is generally low and waterlogging caused by tropical heavy rains or poor drainage system can limit further nutrient absorption. That is, K deficiency and waterlogging are common stresses that can occur simultaneously and impact on crop development and yield. They are both known to impact on catabolism, with rather opposite effects: inhibition of glycolysis and higher glycolytic fermentative flux, respectively. However, the metabolic effects of K and waterlogging have never been assessed precisely. This is very surprising because most tropical or wet areas where rice, sunflower, oil palm and other important crops are cultivated combine these two environmental constraints. The aim of this study was to understand the overall impact of waterlogging and limited K availability on metabolism, and to understand how such advert environmental conditions reshape the carbon balance in two-oil producing species (sunflower and oil palm). Here, we examined the metabolic response of sunflower seedlings and oil palm saplings in the greenhouse under controlled conditions (nutrient composition with low or high K availability, with or without waterlogging) using gas exchange, metabolomics, proteomics, elemental quantitation, isotope and major flux analyses at different sampling times. While separate K deficiency and waterlogging caused well-known effects like polyamines production and sugar accumulation, respectively, waterlogging altered K- induced respiration enhancement and polyamine production, and K deficiency tended to suppress waterlogging-induced accumulation of Krebs cycle intermediates in leaves, stems and roots. Furthermore, the natural 15N/14N isotope composition (δ15N) in leaf, stem and root compounds shows that there was a change in nitrate circulation, with less nitrate influx to leaves and stems under low K availablity combined with waterlogging, and more isotopic dilution of lamina nitrates under high K. 4 Our results also show that both low K and waterlogging have a detrimental effect on photosynthesis but clearly stimulate leaf respiration, thereby impacting the carbon use efficiency. Omics analyses show differential accumulation of typical metabolic intermediates and enzymes not only of the Krebs cycle but also of alternative catabolic pathways. In addition, we found a strong relationship between metabolic composition and the rate of leaf dark respiration. Finally, based the results we have and from literature, in the last chapter of this thesis, we briefly describe potential roles of putrescine, and then review data that help defining the most likely specific role of putrescine under K deficiency. Overall, advert environmental conditions (here, low K and waterlogging) have an enormous impact on respiration in oil producing species (sunflower and oil palm here). Leaf metabolome and proteome appear to be good predictors not only of K availability but also of CO2 efflux, and this opens avenues for cultivation biomonitoring using functional genomics technologies. 5 Guide This thesis is structured in five chapters: Introduction, Materials and methods, two Results chapters based on experiments, General discussion and perspectives chapter and Appendix chapters. The Introduction focuses on the aims of this thesis and literature review. The two Results chapters can be read semi-individually, together with the relevant sections in the Materials and methods, since each presents data on separate experimental systems. The general discussion chapter aims to provide an integrated discussion and reviews the major outcomes of this thesis. Below is an overview: Chapter 1: Introduction - literature review on the topics investigated in this thesis. Chapter 2: Materials and methods - information on the experimental procedures performed. Chapter 3: Responses to K deficiency and waterlogging interact via respiratory and metabolism in sunflower seedlings: Results and Discussion. Chapter 4: Metabolic responses to potassium availability and waterlogging reshape respiration and carbon use efficiency in oil palm saplings: Result and Discussion. Chapter 5: General discussion and perspectives.
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