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The Characterisation of Low Temperature Tolerance in Legumes

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The Characterisation of Low Temperature Tolerance in Legumes The characterisation of low temperature tolerance in legumes. James William Cooper Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Biology Centre for Plant Sciences August 2016 Declaration and Publications The candidate confirms that the work submitted is their own, except where work which has formed part of jointly authored publications has been included. The contribution of the candidate to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given with the thesis where reference has been made to the work of others. Chapter 1: Foyer, C. H., Lam, H-M., Nguyen, H. T., Siddique, K. H. M., Varshney, R. K., Colmer, T. D., Cowling, W., Bramley, H., Mori, T. A., Hodgson, J. M., Cooper, J. W., Miller, A. J., Kunert, K. J., Vorster, J., Cullis, C., Ozga, J. A., Wahlqvist, M. L., Liang, Y., Shou, H., Shi, K., Yu, J., Fodor, N., Kaiser, B. N., Wong, F. L., Valliyodan, B., Considine, M. J. (2016). Neglecting legumes has compromised human health and sustainable food production. Nature Plants, 2. DOI:10.1038/nplants.2016.112 The candidate was responsible for the generation of figure 3 and contributed to the body of the review text. Quain M. D., Makgopa, E. M., Cooper, J. W., Kunert, K. J., Foyer, C. H. (2015). Ectopic phytocystatin expression increases nodule numbers and influences the responses of soybean (Glycine max) to nitrogen deficiency. Phytochemistry, 112, 179-187. DOI:10.1016/j.phytochem.2014.12.027 The candidate was responsible for the generation of the graphical abstract and contributed to the writing of the text. Page | ii Chapter 3: Marquez-Garcia, B., Shaw, D., Cooper, J. W., Karpinska, B., Quain, M. D., Makgopa, E. M., Kunert., K. J., Foyer, C. H. (2015). Redox markers for drought-induced nodule senescence, a process occurring after drought-induced senescence of the lowest leaves in soybean (Glycine max). Annals of botany,116(4). 497-510. DOI:10.1093/aob/mcv030 The candidate was responsible for the extraction of RNA and the generation of figures pertaining to the regulation of redox-related transcripts in drought exposed soybean crown root nodules. Chapter 5: Cooper, J. W., Dasgan, H. Y., Foyer, C. H. (2015). Understanding chilling tolerance in legumes. Aspects of Applied Biology, 124. 117-121. The candidate was responsible for the generation of all data and figures within this publication. Chapter 6: Cooper, J. W., Wilson, M., Derk, M., Smit, S., Kunert, K. J., Cullis, C., Foyer, C. H. (2016). Application of short sequence reads provides improved genomic resources in faba bean (Vicia faba L.). Journal of Experimental Botany – submitted. The candidate was responsible for the sequencing and assembly and interpretation and representation of all data. © 2016 The University of Leeds and James William Cooper Page | iii Acknowledgments Firstly I wish to thank my supervisor, Professor Christine Foyer, whose guidance and support have helped me to become a better scientist. I would also like to give a special thanks to Professor Karl Kunert, for helping to pioneer this project and for providing stimulating discussions over the past 4 years. Many thanks go to my industrial partner, Wherry and Sons Ltd, and to the BBSRC for funding this project. Thanks also to Peter Smith, whose foresight laid the foundation for this research. I thank my Mother, Deirdre, and my Father, Graeme, for their love and support throughout my studies. They have always been available to provide advice on life, the universe and everything. I couldn’t ask for better parents. I would also like to thank Adam Churchman, for his patience, understanding and unwavering support. I thank Barbara Karpinska for helping me take my first steps in the lab. She taught me that with enough coffee and willpower you can master anything. I would also like to thank the other members of the Foyer lab, both past and present, for providing such a wonderfully diverse environment to work in. In particular I should mention my fellow PhD Students, Daniel Shaw and Ambra de Simone. My PhD journey would have been infinitely blander without them. Special thanks go to Dr Mary O’Connell, Dr Sandra Smit and Martijn Derks for helping me to take my first fledgling steps into bioinformatics. Perhaps my biggest mention of gratitude goes to Dr Michael Wilson, who has been a friend, mentor and a general source of peace and knowledge. My understanding of bioinformatics has been due to his guidance and assistance. May the force be with you! I thank my collaborators: Dr Jeremy Harbinson for his assistance in constructing the freezing chamber, Professor Christopher Cullis for his help with genomic sequencing, Dr Stefan van Wyk for his knowledge of legumes and Professor Yildiz Dasgan, who guided me through the subtleties of plant growth. I also thank Masters Student, Leila Beyouddh, who taught me how to be a better teacher and whose efforts have been so greatly appreciated. Finally I wish to thank Grace Hoysted and the rest of the PhD group, as well as the Leeds University Union Sub-Aqua Club and my pub quiz group. Without them life would have been very boring indeed. Special thanks go to Jamie Bojko and Jack Goode for their limitless moral support. Page | iv Dedicated to my Nan, Doreen Cooper, who was never too old to be young. Page | v Abstract Legumes underpin the global food network, providing the majority of the world’s dietary protein. However, global productivity of grain legumes is limited by environmental stresses, particularly chilling and freezing. For example, chilling temperatures (0-15 ºC) limit the production of soybean (Glycine max; a tropical legume), while extreme freezing temperatures (<0 ºC) limit use of temperate legumes such as faba bean (Vicia faba L). The following studies were performed to gain new insights into chilling and freezing tolerance in these two important legumes. Transgenic soybean lines, overexpressing the rice cysteine protease inhibitor, oryzacystatin I (OCI), showed decreased chilling- induced inhibition of photosynthesis compared to wild type (Wt). These lines also showed an increased abundance of transcripts encoding the strigolactone (SL) biosynthesis enzymes: carotenoid cleavage dioxygenases 7 and 8 (CCD7, CCD8). Pea (rms3, rms4, rms5) and Arabidopsis thaliana (max2-1, max3-9, max4-1) mutants, deficient in SL synthesis and signalling, showed enhanced sensitivity to dark-chilling. Differences in chilling and freezing sensitivity were also identified in 5 faba bean cultivars. Transcriptome profiling comparisons were performed on the most chilling sensitive (Wizard) and most chilling tolerant (Hiverna) cultivars to identify specific differences in gene expression, underpinning stress tolerance. Moreover, genome sequencing of the Wizard cultivar enabled the assembly and annotation of the mitochondrial and chloroplast genomes. Single nucleotide polymorphisms (SNP) were found in several organelle genes, when comparing read sequences to published references. Furthermore, based on published SNP orientated linkage maps, contiguous read sequences could be mapped to chromosomal loci, leading to the identification of 8 putative nuclear gene sequences and an increase in sequence length data at 147 loci. Together with these new genomic resources, the discovery that cysteine proteases, phytocystatins and SL are important in legume low temperature tolerance will enable the development of stress tolerance markers, for use in faba bean selective breeding programs. Page | vi Table of Contents Acknowledgments ............................................................................................................................ iv Table of Contents............................................................................................................................. vii List of Abbreviations ........................................................................................................................ xi List of tables ................................................................................................................................... xiii List of figures....................................................................................................................................xv 1. Introduction..................................................................................................................................... 2 1.1. Low temperature stress ................................................................................................................... 2 1.2. Low temperature stress: damage, perception and transduction ...................................................... 3 1.3. Low temperature gene induction: acclimation and vernalization ................................................... 6 1.4. Cold associated hormone signalling ............................................................................................... 9 1.5. Mechanisms of protection from low temperature stress ............................................................... 12 1.6. Stress induced protein turnover .................................................................................................... 14 1.7. Legumes........................................................................................................................................ 16 1.8. Legume responses to low temperature exposure .......................................................................... 19 1.9. Genetic resources for grain legumes............................................................................................
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