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Regulation of Photosynthesis in Plants Under Abiotic Stress a Thesis Regulation of Photosynthesis in plants under abiotic stress A thesis submitted to the University of Manchester for the degree of PhD in the Faculty of Life Sciences 2014 Sashila Abeykoon Walawwe 1 Table of contents List of Figures 5 List of Tables 9 Abbreviations 10 Abstract 12 Declaration 13 Copyright Statement 13 Acknowledgements 14 Chapter 1- General Introduction 15 1.1. Introduction 16 1.2. Photosynthesis 18 1.2.1. Light capture and electron transport chain 18 1.2.2. Cyclic electron transport 31 1.2.3. The Calvin-Benson-Bassham cycle 39 1.3. Effects of abiotic or environmental stress on plants 43 1.3.1. Salt stress 43 1.3.1.1. Effects of salt stress on plants 45 1) Effects of salt on plant growth 45 2) Effects of salt on photosynthesis 46 3) Effects of salt on water relations and ion balance in plants 47 4) Effects of salt on photosynthetic pigments, proteins and lipid 48 composition 5) Effects of salt on leaf anatomy and the structure of chloroplast 49 6) Effects of salt on the nitrate and malate metabolism 50 1.3.1.2. Sensing and signal transduction in salt stress tolerance 51 1.3.1.3. Transcriptomics and proteomics of salt tolerance 55 1.3.1.4. Salt tolerance mechanisms in plants 59 1) Ion regulation and compartmentalization 59 2) Accumulation of compatible solutes 64 3) Involvement of the antioxidant enzymes 65 4) Involvement of plant hormones 67 1.3.1.5. Effects of salt stress on other photosynthetic organisms 69 2 1) Cyanobacteria 69 2) Algae 73 1.3.2. Drought stress 75 1.3.3. Heat stress 76 1.3.4. Low temperature stress 77 1.4. Effects of Environmental stress on the electron transport of photosynthesis 80 1.4.1. Effects on energy use in photosynthesis 81 1.4.1.1. Reactive oxygen species (ROS) formation 82 1.4.2. Effects on components of the electron transport 85 1.5. Regulation of electron transport chain of photosynthesis under stress conditions 89 1.5.1. State-transitions (qT) 89 1.5.2. High-energy state Quenching (qE) 92 1.5.3. Other electron transport pathways involved in regulatory process 98 1.5.3.1. Mehler Reaction 98 1.5.3.2. Chlororespiration 100 1.6. Involvement of Plastid terminal oxidase (PTOX) in alternative electron transport 103 in the electron transport chain of Thellungiella salsuginea 1.7. Aims and Objectives 110 Chapter 2- Effect of salt stress on the regulation of photosynthesis in barley 112 (Hordeum vulgare L.) Preface 113 2.1. Abstract 114 2.2. Introduction 115 2.3. Materials and Methods 119 2.4. Results 130 2.5. Discussion 140 Chapter 3- Physiological evaluation of salinity stress in two rice varieties from Sri Lanka 149 Preface 150 3.1. Abstract 151 3.2. Introduction 152 3.3. Materials and Methods 157 3 3.4. Results 169 3.5. Discussion 187 Chapter 4- Regulation of photosynthesis in Thellungiella salsuginea under abiotic stress 197 Preface 198 4.1. Abstract 199 4.2. Introduction 200 4.3. Materials and Methods 206 4.4. Results 215 4.5. Discussion 231 Chapter 5- General Discussion 239 Bibliography 247 Word Count: 59755 4 List of Figures Chapter 1- Introduction Figure 1.1. Schematic model of the major protein complexes involved in electron transport 20 chain in photosynthesis Figure 1.2. Schematic model representing the proteins of light harvesting complex II 23 (LHCII) and reaction centre core (RCII) of photosystem II (PSII) Figure 1.3. The model of Q cycle representing the electron and proton transport in the 26 cytochrome b6f Figure 1.4. Schematic model representing the proteins of light harvesting complex I (LHCI) 28 and reaction centre core (RCI) of photosystem I (PSI) Figure 1.5. Schematic model representing the chloroplast ATP synthase 30 Figure 1.6. Possible pathways of cyclic electron transport around PSI 38 Figure 1.7. A diagram representing the major steps in the Calvin cycle or the light-independent 42 reactions Figure 1.8. Cellular Na+ transport mechanisms and important components of the salt 54 stress responses in plant root cells Figure 1.9. Regulation of electron transport through qE 97 Chapter 2 Figure 2.1. Far-red light induced signal giving the 100% of P700 122 Figure 2.2. Typical fluorescence signal showing all the reference points 123 Figure 2.3. P700 oxidation of which is induced by the actinic light was measured during 126 a 100 milliseconds period of darkness Figure 2.4. The relative concentration of 'active' PSI centres (centres that can be oxidized by 127 light and are then rapidly re-reduced during a period of darkness) 2 Figure 2.5. The first leaf of barley plant showing the section of approximately 2.1 cm 128 (length 3 cm x width 0.7 cm between 4 cm and 7 cm from the leaf tip of each leaf) area Figure 2.6. Gas exchange parameters of barley plants subjected to varying degrees 132 of salinity 5 Figure 2.7. Maximum quantum yield (Fv/Fm) of control and salt-treated barley plants 133 Figure 2.8. The effect of salt treatment on the efficiency of PSII (ΦPSII), relative 135 electron transport of PSII (PSII ETR) and non-photochemical quenching (NPQ) of barley plants Figure 2.9. The effect of salt treatment on redox state of P700, relative proportion of the 138 active PSI centres, rate constant for P700 reduction and electron transport rate of PSI (PSI ETR) of barley plants Figure 2.10. The effect of salt treatment on the leaf chlorophyll content per leaf area and 139 chlorophyll a/b ratio in barley Chapter 3 Figure 3.1. Far-red light induced signal giving 100% of P700 161 Figure 3.2. Typical fluorescence signal showing all the reference points 162 Figure 3.3. P700 oxidation induced by the actinic light was measured during a 164 100 milliseconds period of darkness Figure 3.4. The relative concentration of 'active' PSI centres (centres that can be oxidized by 165 light and are then rapidly re-reduced during a period of darkness) Figure 3.5. Fluorescence signal showing the relaxation kinetics 167 Figure 3.6. 34 days old At-354 and Bg-352 control and salt treated plants at the early 170 vegetative stage Figure 3.7. Change in leaf area of two rice varieties At-354 and Bg-352 at the early 171 vegetative stage and at the flowering stage when exposed to 50 and 100 mM of NaCl Figure 3.8. The effect of salinity on leaf chlorophyll content per leaf area and chlorophyll 173 a/b ratio in two varieties of rice, At-354 and Bg-352 Figure 3.9. Gas exchange parameters measured in rice plants at the early vegetative stage 175 and the flowering stage of Bg-352 and At-354 exposed to: 0, 50 and 100 mM 6 of NaCl Figure 3.10. CO2 assimilation rate (A) as a function of internal CO2 concentration (Ci) in 176 plants at the tillering stage and flowering stage of Bg-352 and At-354 exposed to: 0, 50 and 100 mM of NaCl Figure 3.11. Maximum quantum yield (Fv/Fm) of salt stressed (50 or 100 mM) and control 177 plants at early vegetative stage and at flowering stage of At-354 and Bg-352 Figure 3.12. Photochemical efficiency (ΦPSII) and relative linear electron transport rate of 179 PSII (PSII ETR) plants at the early vegetative stage and the flowering stage of Bg-352 and At-354 exposed to: 0, 50 and 100 mM of NaCl Figure 3.13. Non Photochemical Quenching (NPQ) plants at the early vegetative stage and 181 the flowering stage of Bg-352 and At-354 exposed to: 0, 50 and 100 mM of NaCl Figure 3.14. Chlorophyll fluorescence relaxation kinetics of control and salt treated plants at 182 the flowering stage recorded using the PAM 101 fluorometer. Figure 3.15. Redox state of P700 and the proportion of 'active' PSI centres of two rice 184 varieties subjected to different salt concentrations plants at the early vegetative stage and the flowering stage Figure 3.16. The rate constant of P700 reduction and PSI electron transport rate (PSI ETR) of 186 plants at the early vegetative stage and the flowering stage of Bg-352 and At-354 exposed to: 0, 50 and 100 mM of NaCl. Chapter 4 Figure 4.1. Images showing the physical changes of leaves of 7-week old T. salsuginea 216 when exposed to stresses. Figure 4.2. Immunoblots and relative band intensity of PTOX, cytochrome f (Cyt f) and 218 PsbA from control, salt-treated, droughted and plants exposed to different growth 7 irradiance Figure 4.3. PTOX gene expression along with actin and the relative expression level of 220 PTOX mRNA in control and salt-treated plants. Figure 4.4. Change in the efficiency of PSII (ΦPSII) measured in control and stressed 222 -1 plants at the different light intensities and CO2 concentration of >1200 μL L Figure 4.5. Change in the electron transport rate of PSII (ETR of PSII) measured in control 223 plants and stressed plants at the different light intensities and CO2 concentration of >1200 μLL-1 Figure 4.6. Blue-native PAGE showing the separated complexes of isolated thylakoids of T. 225 salsuginea Figure 4.7. PTOX genomic sequence of T. salsuginea including exons, introns and 229 untranslated regions (UTRs) coding sequence of PTOX which indicates the annealing sites of primers used in rt-PCR analysis. Figure 4.8. The schematic representation of the genomic structure of PTOX contains exons, 230 introns and transcription start site (ATG) and stop codon (TAA) Chapter 5- General Discussion 8 List of Tables Chapter 1 Table 1.1.
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