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STRUCTURAL, PHYSIOLOGICAL AND MOLECULAR CHARACTERISATION OF THE AUSTRALIAN NATIVE RESURRECTION GRASS TRIPOGON LOLIIFORMIS (F.MUELL.) C.E.HUBB. DURING DEHYDRATION AND REHYDRATION Mohammad Reza Karbaschi Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Centre for Tropical Crops and Biocommodities Science and Engineering Faculty Queensland University of Technology November 2015 Keywords Arabidopsis thaliana; Agrobacterium-mediated transformation; Anatomy; Anti-apoptotic proteins; BAG4; Escherichia coli; Bulliform cells; C4 photosynthesis; Cell wall folding; Cell membrane integrity; Chaperone-mediated autophagy; Chlorophyll fluorescence; Hsc70/Hsp70; Desiccation tolerance, Dehydration; Drought; Electrolyte leakage; Freehand sectioning; Homoiochlorophyllous; Leaf structure; Leaf folding; Reactive oxygen species (ROS); Resurrection plant; Morphology; Monocotyledon; Nicotiana benthamiana; Photosynthesis; Physiology; Plant tissue; Programed cell death (PCD); Propidium iodide staining; Protein microarray chip; Sclerenchymatous tissue; Stress; Structure; Tripogon loliiformis; Ubiquitin; Vacuole fragmentation; Kranz anatomy; XyMS+; Structural, physiological and molecular characterisation of the Australian native resurrection grass Tripogon loliiformis (F.Muell.) C.E.Hubb. during dehydration and rehydration i Abstract Plants, as sessile organisms must continually adapt to environmental changes. Water deficit is one of the major environmental stresses that affects plants. While most plants can tolerate moderate dehydration (leaf water potential from -5 to -10 MPa) a small group of vascular plants can tolerate desiccation to an air-dry state (- 100 MPa) and beyond. Since the initial discovery of desiccation-tolerance in plants in 1912 by Irmscher, scientists and plant botanists world-wide have been fascinated by these unique plants, particularly how these land-plants can tolerate desiccation and resurrect. Tripogon loliiformis is a largely uncharacterised Australian desiccation-tolerant grass that resurrects from the desiccated state within 72 hours. The work performed in this thesis involved a combination of structural, physiological and molecular techniques to investigate the unique structural, physiological and molecular features that enable T. loliiformis, and potentially other resurrection plants, to tolerate desiccation. The molecular studies were performed using high-throughput protein microarray technology which provided a platform for comparative analysis of potential protein-protein interacting partners with the pro-survival/anti-apoptotic protein, Bcl-2 associated athanogene 4 (BAG4). In addition to analysis of the BAG4 protein from Arabidopsis, a novel orthologue of AtBAG4 was isolated from T. loliiformis and expressed, thus allowing an investigation of the roles of this protein between desiccation sensitive (A. thaliana) and tolerant (T. loliiformis) plants. Key observations included; i) a myriad of structural changes such as leaf folding, cell wall folding and vacuole fragmentation that mitigate desiccation stress, ii) potential role of sclerenchymatous tissue within rapid leaf folding and light protection, iii) retention of approximately 70 % chlorophyll in the desiccated state, iv) early shutdown of photosynthesis, 50 % at 80 % relative water content (RWC) and ceasing completely at 70 % RWC, v) the possible contribution of bulliform cells in leaf folding, water reserve and a key role in photosynthesis shut down by dehydration, vi) a sharp increase in electrolyte leakage during dehydration, vii) confirmation of membrane integrity by propidium iodide staining throughout dehydration, desiccation and rehydration, and viii) the molecular demonstration of a large number of proteins that possibly interact with BAG4 which mostly are related ii Structural, physiological and molecular characterisation of the Australian native resurrection grass Tripogon loliiformis (F.Muell.) C.E.Hubb. during dehydration and rehydration to carbohydrate pathways involved in autophagy. Taken together, these results demonstrate that T. loliiformis implements a range of structural and physiological mechanisms, both early on and throughout the drying, that protect tissues from mechanical, oxidative and irradiation stress. These results confirm that resurrection plants actively participate in stress tolerance and provide insights into tolerance mechanisms utilized by these unique land-plants for potential utilization in enhancement of stress-tolerance in crop plants. The protein results from protein microarray chip demonstrated that BAG4 has anti-apoptotic properties due to its interaction with a large number of proteins involved in autophagy (particularly carbohydrates). Detoxification and recycling of damaged and unwanted proteins result in recovery of the cells and prevent apoptosis. More proteins interacted with the TlBAG4 compared with AtBAG4 which might suggest that the more binding sites exist on BAG4 from this resurrection plant which in return might contribute in desiccation-tolerance. Although the exact involvement of BAG4 protein with other proteins and its true involvement in autophagy remained to be explored, this project for the first time suggested a potential role for BAG4 in plant autophagy pathways. Furthermore, the data generated from the protein-protein interaction of BAG4 using high-density protein microarrays provided a valuable resource for uncovering the mechanisms/pathways that this protein influences for future research. Structural, physiological and molecular characterisation of the Australian native resurrection grass Tripogon loliiformis (F.Muell.) C.E.Hubb. during dehydration and rehydration iii Table of Contents Keywords ................................................................................................................................................. i Abstract ................................................................................................................................................... ii Table of Contents ................................................................................................................................... iv List of Figures ....................................................................................................................................... vii List of Tables ......................................................................................................................................... ix List of Abbreviations .............................................................................................................................. x Statement of Original Authorship ........................................................................................................ xiv Acknowledgements ............................................................................................................................... xv CHAPTER 1: INTRODUCTION AND LITERATURE REVIEW ................................................. 1 1.1 Introduction.................................................................................................................................. 1 1.2 Classification of land Plants based on their tolerance toward water deficit ................................. 2 1.3 Desiccation tolerance in plants .................................................................................................... 3 1.3.1 Evolutionary aspects ......................................................................................................... 3 1.3.2 Geographic distribution and ecology ................................................................................ 3 1.3.3 Desiccation-tolerant plants types ...................................................................................... 6 1.4 Impacts of water deficit on plants .............................................................................................. 11 1.4.1 Plant responses to water deficit ...................................................................................... 11 1.4.2 Water deficit response characteristics common among all plants .................................. 12 1.5 Structural aspects ....................................................................................................................... 12 1.5.1 Leaf surface structures .................................................................................................... 12 1.5.2 Reducing leaf surface area .............................................................................................. 13 1.5.3 Xylem tissue (in stem and root) ...................................................................................... 15 1.6 Physiological aspects ................................................................................................................. 16 1.6.1 Reactive oxygen species ................................................................................................. 16 1.6.2 Photosynthesis ................................................................................................................ 17 1.6.3 Respiration ...................................................................................................................... 18 1.7 Molecular responses to water deficit in plants ........................................................................... 19 1.7.1 Molecular responses to water deficit in desiccation-tolerant plants ............................... 19 1.7.2 Regulatory .....................................................................................................................
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