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Exploiting the Potential of Agave for Bioenergy in Marginal Lands Dalal Exploiting the Potential of Agave for Bioenergy in Marginal Lands Dalal Bader Al Baijan A Thesis submitted for the Degree of Doctor of Philosophy School of Biology Newcastle University July 2015 Declaration I hereby certify that this thesis is the result of my own investigations and that no part of it has been submitted for any degree other than Doctor of Philosophy at the Newcastle University. All references to the work of others have been duly acknowledged. Dalal B. Al Baijan ii “It is not the strongest of the species that survives, nor the most intelligent, but the one most responsive to change” Charles Darwin Origin of Species, 1859 iii Abstract Drylands cover approximately 40% of the global land area, with minimum rainfall levels, high temperatures in the summer months, and they are prone to degradation and desertification. Drought is one of the prime abiotic stresses limiting crop production. Agave plants are known to be well adapted to dry, arid conditions, producing comparable amounts of biomass to the most water-use efficient C3 and C4 crops but only require 20% of water for cultivation, making them good candidates for bioenergy production from marginal lands. Agave plants have high sugar contents, along with high biomass yield. More importantly, Agave is an extremely water-use efficient (WUE) plant due to its use of Crassulacean acid metabolism. Most of the research conducted on Agave has centered on A. tequilana due to its economic importance in the tequila production industry. However, there are other species of Agave that display higher biomass yields compared to A. tequilana. These include A. mapisaga and A. salmiana and A. fourcroydes Lem has been reported to possess high fructan content making it a promising plant for biofuel feedstock. Also, fructans act as osmo-protectants by stabilizing membranes during drought and other abiotic stress. This project set out to examine several hypotheses. In the first experimental chapter (Chapter 2), the central aim was to start identifying traits for the improvement of Agave species for biomass production on arid lands by first examining if the capacity of CAM, and fructan accumulation are linked traits. To address this question 3 species of Agave varying in succulence were compared under different water regimes. Measurements were made of leaf, gas exchange and titratable acidities as markers of CAM and of soluble sugar and fructan content using high performance liquid chromatography (HPLC). High leaf succulence is associated with increased magnitude of CAM, manifested as + higher H and nocturnal CO2 uptake and fructan accumulation also increased with leaf succulence in Agave. Sucrose provided most, if not all of the substrate required for dark CO2 uptake. At the leaf level, highest CAM activity was found in the tip region whilst most fructan accumulation occurred in the base of the leaf. These results indicate that CAM and fructan accumulation are subject to contrasting anatomical and physiological control processes. iv In Chapter 3, the aim was to test 4 hypotheses relating to succulence and biochemical capacity for C3 and C4 carboxylation in Agave. The first hypothesis tested the abundance of PEPC and its variation between species in relation to leaf succulence and age and will vary along the leaf, in line with differences in CAM activity. The second hypothesis looked into the abundance of Rubisco and Rubisco activase and its variation between species in relation to leaf succulence and age and will vary along the leaf, in line with differences in CAM activity. The third hypothesis the more succulent Agave species, drought will have less impact on the abundance of PEPC, Rubisco and Rubisco activase compared to the less succulent species. And the abundance of Rubisco activase will vary over the diel cycle, particularly in leaves of more succulent species of Agave. Results showed that leaf succulence influenced the abundance of PEPC. Thus, the optimal anatomy for nocturnal malic acid accumulation is accompanied by high PEPC abundance in leaves with higher vacuolar storage capacity. In contrast, the abundances of Rubisco and Rubisco activase showed an inverse relationship to succulence and CAM activity. The aim of Chapter 4, was to identify other species of Agave that could be exploited as sources of biofuel from semi-arid marginal lands. Some 14 different species of Agave that showed varying levels of succulence were compared, evaluating the capacity for CAM, fructan content, carbohydrate composition, osmotic pressure and the relationship with succulence. Results demonstrated that Inter-specific variations in the magnitude of expression of CAM in Agave are dependent on leaf succulence. Also, Agave displays flexibility in the use of carbohydrate source pools to sustain dark CO2 uptake. Some species appear to use fructans and others sucrose as substrate for dark CO2 uptake. The final experimental Chapter’s aim was to develop a method to identify vacuolar sugar transporters in Agave related to sucrose turnover and fructan accumulation. First, identifying the tonoplast by testing activity of ATPase and PPiase of leaf vesicles of Agave Americana marginata, and its sensitivity to inhibition by known ATPase inhibitors. Second, was to use a proteomics approach, analysing of the purified tonoplast involved fractionation of the proteins by SDS-PAGE and analysis by LC-MS/MS, to identify vacuolar sugar transporter proteins which are hypothesized to play a key regulatory role in determining sucrose turnover for CAM and fructan accumulation and as such, v could represent future targets for genetic engineering of increased sugar content for plants grown for bioenergy. The capacity of the vacuole as a sink for carbohydrate maybe an important determinant of CAM expression and has important implications for plant growth and productivity. Combining tonoplast proteomics with the interrogation of diel transcriptome data is a potentially powerful approach to identify candidate vacuolar sugar transporters in Agave. vi Acknowledgements The process of giving credit to all the people who have contributed to my research is essential to the completion of this thesis. The effort to put it in written form is always filled with a certain apprehension that someone will be inadvertently be left out. Sometimes historical quotations can provide the needed inspiration. There is a saying attributed to the Prophet Muhammed that says, "He has not thanked Allah who has not thanked people ". There are many people and institutions that I should like to thank for making it possible to complete my thesis. I am truly thankful for their kind support and thoughtful assistance. First and foremost, I would like to thank my supervisor Prof Anne M Borland and Prof Jeremy Barnes for their encouragement, technical expertise, enthusiasm and development throughout my study in the past 4 years. I’m very grateful for their guidance and they never hesitated to provide me with their help in academic and personal matters. Within the School of Biology I have received encouragement, friendship and support from many people, which contributed to an enjoyable experience and friendly environment in Newcastle University. In particular, I would like to thank Dr Taybi, Dr Aayush Sharma, Gillian Davis, Dr Eileen Power, Helen Martin and Dr Matthew Peake for their advice. A mention must also be given to people who inspired me and contributed to help me develop new skills and knowledge and who collaborated with me in this thesis; Dr Achim Treumann and Samantha Baker from NUPPA. My acknowledgement would not be complete without mentioning Shreya and Aysha. Thank you for your friendship, and sharing with me the ups and downs of this PhD, and being my gym buddies. This thesis wouldn't be possible without the love, support and blessings of my parents Sandra and Bader, my twin sister Dina, my aunt Marye and my nephews Mohammed and Bader Jr; I dedicate this achievement to them. I’m very thankful to my husband Suhail for his love, patience and constant support through the distance. Thank you for being a positive force in my life. I would wish to thank Judy for her visits to Newcastle. My sincere thank you goes to HE Sheikha Hussah Sabah al-Salim Al-Sabah, Director-General of Dar al-Athar al-Islamiyyah (Islamic Art Museum, Kuwait) not only for her support and constant encouragement but also for being an impressive role-model This thesis was funded by Kuwait Institute for Scientific Research. vii Table of Contents Declaration .......................................................................................................... ii Abstract .............................................................................................................. iv Acknowledgements ........................................................................................... vii Table of Contents ............................................................................................. viii List of Figures .................................................................................................. xiii List of Tables....................................................................................................xxii Abbreviations .................................................................................................. xxiii Chapter 1 General Introduction ..................................................................... 1 1. Introduction ....................................................................................................
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