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The Role of Brown Algal Cell Walls in Morphogenesis and Development

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The Role of Brown Algal Cell Walls in Morphogenesis and Development The role of brown algal cell walls in morphogenesis and development Marina Linardić Downing College April 2018 This dissertation is submitted for the degree of Doctor of Philosophy Summary Name: Marina Linardić Thesis title: The role of brown algal cell walls in morphogenesis and development Morphogenesis in walled organisms represents a highly controlled process by which the variability of shapes arises through changes in the structure and mechanics of the cell wall. Despite taking different evolutionary paths, land plants and some brown algae exhibit great developmental and morphological similarities. In two brown algal model systems: the Sargassum muticum apex and the Fucus serratus embryo, I have used a combination of imaging techniques, growth analyses, surgical and pharmacological treatments, as well as molecular, biochemical and mechanical approaches to characterise the growth patterns and the cell wall contribution to shape change. To understand how the adult algal body is formed, I examined the branching strategy (phyllotaxis) in S. muticum. My results suggest that in S. muticum the spiral phyllotactic pattern and the apical cell division pattern are not linked. The phytohormone auxin and the biochemical changes of the cell wall do not seem to be correlated with the bud outgrowth, contrary to observations in plants. In summary, these results suggest Sargassum convergently developed a distinct growth mechanism with similar shape outcome as observed in plants. This dissertation is one of the first attempts to explore cell wall mechanics in brown algal development and its correlation with underlying cell wall biochemistry utilising the Fucus embryo as a known system. The results suggest a correlation between the wall mechanics and alginate biochemistry with the growing and non-growing regions of the embryo. In addition, altering cell wall deposition or composition has a strong effect on embryo rhizoid elongation and is, in certain cases, accompanied by significant increase in cell wall stiffness and reduction of alginate epitopes. Furthermore, preliminary results exploring ii transcriptomic changes during development indicate differential expression of particular alginate biosynthesis enzymes (mannuronan C5 epimerases) during development, suggesting alginate conformational modifications might be stage specific. These results contribute to the current knowledge addressing the importance of cell walls in brown algal development using novel tools and approaches. Understanding developmental processes in brown algae will provide a better insight how similar morphogenetic traits are established using different body-building mechanisms. iii This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text. I further state that no substantial part of my dissertation has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution except as declared in the Preface and specified in the text. It does not exceed the length limit of 60,000 words set by the Degree Committee for the Faculty of Biology. - Marina Linardić, 2018 iv Acknowledgments Firstly, a big thank you to my supervisor Dr Siobhan Braybrook – for giving me the opportunity to explore the interesting developmental side of brown algae and for all the support through the ups and downs during this three-year long process. To Prof Alison Smith – thank you for all the useful discussions and your support in the final moments of my PhD. Thank you to the whole Braybrook group: Louis, Giulia, JJ, Rozi, Firas, Marco, Tom, Joanna and Adi – for all the valuable discussions (scientific and non- scientific), help in the lab and always-needed short coffee breaks. Science is best made in collaboration – I would like to thank the Phycomorph members for all the valuable discussions, advice and suggestions during workshops and conferences I attended. To Anna – thank you for all the help with the RNA sequencing analysis. To Downing College – thank you for all the financial support during my studies. It was a great honour to be a recipient of a studentship that honours two great minds in the field of algal research, Ralph Lewin and Felix E Fritsch. To the Cambridge bunch: Nadine, Claire, Tessa, Thomas, João, Fabricio, Chris, Clément and Tom – thank you for the amazing three years I have shared with you in this beautiful place, all the many adventures we had (and will have!), all the tears and laughter along the way. You all hold a special place in my heart. To my Biokolektiva: Petra, Zrinka, Maja, Sanya and Franka – this is what all those all-nighters were leading to. Thank you for being here for me along the way. To Mateja, Stela and Karmen – thank you for such a genuine friendship and support in every aspect of my life. And finally, to my family, Zoran, Nikica and Ivana – these past three years, and all the moments that led me to where I am today, would not have been possible if it weren’t for your unconditional love and support. v Table of Contents CHAPTER 1. INTRODUCTION ....................................................................... - 1 - 1.1. Brown algae – independent evolution of multicellularity .................... - 1 - 1.2. Shape formation in brown algal lineage ................................................ - 3 - 1.3. Brown algal cell walls - architecture ...................................................... - 6 - 1.3.1. Alginate .......................................................................................................................... - 8 - 1.3.1.1. Structure ................................................................................................................. - 8 - 1.3.1.2. Alginate biosynthesis .............................................................................................. - 9 - 1.3.1.3. Biological role of alginates.................................................................................... - 11 - 1.3.1.4. Application of brown algal alginates ..................................................................... - 12 - 1.3.2. Sulphated fucans ......................................................................................................... - 12 - 1.3.2.1. Structure ............................................................................................................... - 12 - 1.3.2.2. Biosynthesis of sulphated fucans ......................................................................... - 13 - 1.3.2.3. Biological role of sulphated fucans ....................................................................... - 13 - 1.3.3. Cellulose ...................................................................................................................... - 14 - 1.3.3.1. Structure of cellulose ............................................................................................ - 14 - 1.3.3.2. Biosynthesis ......................................................................................................... - 14 - 1.3.4. Phlorotannins ............................................................................................................... - 15 - 1.3.5. Cell walls in brown algae and plants – a mechanical role in shape formation ............ - 16 - 1.4. Investigating properties of cell walls ................................................... - 17 - 1.4.1. Mechanical characterisation of cell walls ..................................................................... - 18 - 1.4.2. Spatial distribution of brown algal wall components .................................................... - 20 - 1.5. Studying brown algal cell walls and morphogenesis – step towards understanding different evolutionary paths to shape formation ............. - 20 - 1.6. Aim of the study .................................................................................... - 21 - CHAPTER 2. TOWARDS AN UNDERSTANDING OF SPIRAL PATTERNING IN THE SARGASSUM MUTICUM SHOOT APEX ............................................. - 23 - 2.1. Summary ................................................................................................ - 23 - 2.2. Introduction ........................................................................................... - 24 - vi 2.3. Materials and Methods .......................................................................... - 26 - 2.3.1 Sample collection and processing ................................................................................ - 26 - 2.3.2. Imaging of the apices for divergence angle measurements ........................................ - 27 - 2.3.3. Histology ....................................................................................................................... - 27 - 2.3.4. Cell division pattern quantification................................................................................ - 27 - 2.3.5. Apex ablation................................................................................................................ - 28 - 2.3.6. Alginate immunolocalisation ......................................................................................... - 29 - 2.3.7. Auxin immunolocalisation ............................................................................................. - 30 - 2.3.8. *Atomic force microscopy (AFM).................................................................................. - 31 - 2.3.9.
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