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The Role of Starch in the Day/Night Re-Programming of Stomata in Plants with Crassulacean Acid Metabolism Natalia Hurtado Castan

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The Role of Starch in the Day/Night Re-Programming of Stomata in Plants with Crassulacean Acid Metabolism Natalia Hurtado Castan The role of starch in the day/night re-programming of stomata in plants with Crassulacean Acid Metabolism Natalia Hurtado Castano Doctor of Philosophy School of Natural and Environmental Sciences February 2020 Declaration This thesis is submitted to Newcastle University for the degree of Doctor of Philosophy. The research detailed within was performed between the years 2015-2019 and it was supervised by Professor Anne Borland and Professor Jeremy Barnes. I certify that none of the material offered in this thesis has been previously submitted by me for a degree or any other qualification at this or any other university. Natalia Hurtado Castano ii Abstract Crassulacean acid metabolism (CAM) is a specialised type of photosynthesis characterised by the unique inverted stomatal rhythm, which increases water use efficiency (WUE) and enhances the potential for sustainable biomass production in warmer and drier conditions. Starch turnover in the mesophyll of CAM species supports nocturnal CO2 assimilation and CAM activity. In C3 plants, starch metabolism has been reported to play an important role in determining stomatal behaviour; in this case, guard cell starch degradation is triggered by blue light, producing osmolytes that promotes stomatal opening. Based on the importance of starch and the little knowledge regarding CAM stomatal behaviour, this study tested the hypothesis that starch metabolism has been re-programmed in CAM plants to enable nocturnal stomatal opening, by using biochemical and genetic characterisation of wild type and RNAi lines with curtailed starch metabolism in the constitutive CAM species Kalanchoë fedtschenkoi. Measurements of guard cell starch content over 24 hours in wild type plants of K. fedtschenkoi indicated a day/night shift in starch turnover compared to C3, evidenced by an increment over the first hours of the day and a diminution at the beginning of the night. The characterisation of the RNAi lines confirmed that curtailed starch metabolism affected nocturnal CO2 fixation, besides the phosphorolytic starch degradation has a pivotal role for driving nocturnal CAM activity evidenced, in the same way, in both mesophyll and epidermis proteome datasets. Furthermore, higher levels of soluble sugars in the epidermis of the RNAi lines appeared to curtail completely stomatal closure during the day, indicating that guard cell starch biosynthesis is an important sink for carbohydrates, ensuring day-time stomatal closure. Finally, this thesis constituted an approach for the understanding of starch metabolism in CAM stomata and together with further studies lead to the potential engineering of CAM into C3 to enhance WUE. iii Acknowledgments I want to express my deeply gratitude to my supervisor Professor Anne Borland for her support, guidance and encouragement during this entire thesis. I really enjoyed all our discussions trying to understand the mysteries of CAM stomata. I also want to thank to my second supervisor Professor Jeremy Barnes for his support, guidance and for having always a funny story to share during our meetings. Besides my supervisors, I am very grateful with Helen Martin, the most patience laboratory technician I have ever met, for her time, immense help and explanations. My sincere thanks to Dr Vasilios Andriotis for his help and guidance with the proteins native PAGE and for his valuable advises during the postdoc application process. I also want to thank to the School of Natural and Environmental Sciences for the opportunity of working as a demonstrator, it was a great experience and a personal challenge teaching in an international environment. Thanks to Dr Alex Laude and Dr Rolando Berlinguer-Palmini in the Bio-Imaging Unit at Medical School for the valuable help in the conduction of the fluorescence microscopy. Also, thanks to Dr Simon Kometa at NUIT for his assistance with statistical analysis. I want to thank to all the members of Plant and Microbial Research Group for sharing every week their interesting projects and contributing with important discussions about our research, as well as for the nice conversations during our coffee breaks and the delicious cooking off competitions, making this time very enjoyable. I am very grateful with Dr James Hartwell, Dr Susanna Boxall, Dr Louisa Dever and Nina Pugh at University of Liverpool for providing the RNA sequence datasets, and for giving me the opportunity of joining their research group for training in Real time-qPCR. I want to thank to Sabrina Fluetsch at University of Zurich for performing the staining and confocal microscopy of the epidermal samples, the resulting data were a valuable resource for this thesis. Also my deepest gratitude with Dr Paul Abraham in Oak Ridge National Laboratory (USA) for conducting the proteomics experiment and providing the data. I want to thank to all the people I have met during the last four years and made life enjoyable in Newcastle. First, to all my Latin American friends, who made me feel at home and enriched our culture with all the diverse food, talks, trips and great moments we spent together. I want to thank specially to Alidi Kusuma, Joshua Loh and Jui Chanapan for being the best support during this process, for their valuable friendship, for sharing their amazing culture, for all the delicious meals we shared together and for encouraged me to finish this iv thesis. Also, I am very grateful with all the people I worked with in Geneius – Synlab for their time, help and for making all the hard work enjoyable with nice conversations Finally, I want to thank to the most important people, who made this thesis possible, my parents Luz Stella and Manuel, my sister Sofia and my beautiful niece Julieta, for their love and support through the distance, for being part of this process and encourage me to continue following my dreams. This thesis was funded by the Government of Colombia through the Administrative Department of Science, Technology and Innovation – Colciencias and the Newton-Caldas fund partnership. v Table of Contents Chapter 1. General introduction ................................................................................................. 1 1.1. Crassulacean acid metabolism ......................................................................................... 1 1.2. Crassulacean acid metabolism for sustainable agriculture in a warmer drier world ....... 2 1.3. Evolution of crassulacean acid metabolism..................................................................... 5 1.4. Stomatal regulation .......................................................................................................... 7 1.4.1. Signalling in stomatal guard cells ............................................................................. 8 1.4.2. Starch turnover influences guard cells metabolism .................................................. 9 1.5. Starch turnover in mesophyll ......................................................................................... 11 1.5.1. Synthesis of starch .................................................................................................. 11 1.5.2. Degradation of starch.............................................................................................. 12 1.6. Aims and Hypothesis ..................................................................................................... 15 Chapter 2. Materials and Methods............................................................................................ 17 2.1. Plant Material ................................................................................................................ 17 2.2. Determination of starch in mesophyll and stomatal guard cells .................................... 18 2.3. Soluble sugar content in mesophyll and guard cell-enriched epidermis ....................... 19 2.4. Quantification of malate in mesophyll and guard cell-enriched epidermis ................... 20 2.5. Gas exchange analysis ................................................................................................... 20 2.6. Protein isolation and quantification ............................................................................... 21 2.7. Identification of protein isoforms using Native polyacrylamide gels ........................... 22 2.8. RNA isolation and cDNA synthesis .............................................................................. 23 2.9. Transcript abundance of genes using Real Time q-PCR ............................................... 23 2.10. Statistical analysis ....................................................................................................... 24 Chapter 3. Identification of genes related to starch and sugar metabolism and a potential role in CAM stomatal regulation ..................................................................................................... 26 3.1. Introduction ................................................................................................................... 26 3.2. Materials and Methods .................................................................................................. 29 3.3. Results ........................................................................................................................... 30 vi 3.4. Discussion ...................................................................................................................... 44 3.4.1. Identification of genes to be further evaluated using Real Time qPCR ................. 45 3.4.2. CAM-related
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