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Study of Heavy Metal Tolerance, Accumulation and Recovery in Hyperaccumulator Plant Species

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Study of Heavy Metal Tolerance, Accumulation and Recovery in Hyperaccumulator Plant Species STUDY OF HEAVY METAL TOLERANCE, ACCUMULATION AND RECOVERY IN HYPERACCUMULATOR PLANT SPECIES By RENGASAMY BOOMINATHAN A thesis submitted for the degree of Doctor of Philosophy School of Biotechnology and Biomolecular Science The University of New South Wales June,2002 Dedicated To My Mother TABLE OF CONTENTS Page Table of Contents List of Figures vm List of Tables 11 L- .. XXl L~ 6\- Abb'£evfaa c.-J.Ot !$, List of Appendices xxn Abstract xxm Acknowledgments XXVI CHAPTER 1 - INTRODUCTION 1. 1 Heavy Metals In The Environment 1 1. 1. 1 Cadmium 1 1. 1. 2 Nickel 2 1. 2 Phytoremediation 3 1. 3 Phytomining 4 1. 4 Hyperaccumulators 6 1. 5 Mechanisms of Heavy Metal Accumulation and Tolerance 8 1. 5. 1 Compartmentation 9 1. 5. 1. 1 Distribution Between Organs 9 1. 5. 1. 2 Intraorgan and Intracellular Distribution 12 1. 5. 2 Complexation With Organic Acids 14 1. 6 Oxidative Stress 16 1. 6. 1 Superoxide Dismutase 18 1. 6. 2 Catalase 20 1. 6. 3 Ascorbate Peroxidase 21 11 1. 6. 4 Hydrogen Peroxide 23 1. 6. 5 Lipid Peroxidation 24 1. 6. 6 Glutathione 26 1. 6. 6. 1 Effect of Heavy Metal 27 1. 6. 6. 2 Glutathione and Hydrogen Peroxide 28 1. 6. 7 Sulfhydryl Groups 29 1. 7 Phytochelatins 31 1. 8 Hairy Root Cultures 33 1. 9 Aims of This Study 35 CHAPTER 2 - MATERIALS AND METHODS 2. 1 Hairy Root Cultures 36 2. 1. 1 Nickel Hyperaccumulator (A. bertolonii) and Non-hyperaccumulator (N. tabacum) 38 2. 1. 1. 1 Short-term Ni Uptake by Live and Dead Biomass 38 2. 1. 1. 2 Culture Experiments 38 2. 1. 1. 3 Effect ofH+-ATPase Inhibitor 38 2. 1. 2 Cadmium Hyperaccumulator (T. caerulescens) and Non-hyperaccumulator (N. tabacum) 39 2. 1. 2. 1 Short-term Cd Uptake by Live and Dead Biomass 39 2. 1. 2. 2 Culture Experiments 39 2. 1. 2. 3 Effect ofH+-ATPase Inhibitor 39 2. 1. 2. 4 Effect of Glutathione Synthesis Inhibitor 39 2. 1. 2. 5 Effect of Free Radical Generators 40 2. 1. 2. 6 Effect of Free Radical Scavenger 40 2.2 Nickel Recovery 41 lll 2.2. 1 Hairy Root Cultures 41 2.2.2 Whole Plant Cultivation 41 2.2.3 Nickel Recovery by Furnace Treatment 42 2. 3 Analytical Procedures 43 2. 3. 1 Biomass Fresh and Dry Weight 43 2.3.2 Heavy Metal Concentrations 43 2.3.3 Distribution of Cd or Ni in Hairy Roots 44 2. 3. 3. 1 Apoplasm and Symplasm 44 2.3.3.2 Microscope Analysis 44 2.3.4 Organic Acids 45 2.3.4. 1 Extraction 45 2.3.4.2 Gel Filtration 46 2.3.4.3 HPLC Measurements 46 2.3.5 Superoxide Dismutase Assay 47 2.3.6 Catalase Assay 47 2.3. 7 Ascorbate Peroxidase Assay 48 2.3. 8 Hydrogen Peroxide Assay 48 2.3.9 Estimation of Malondialdehyde 49 2. 3. 10 Total Glutathione Assay 49 2. 3. 11 Estimation of Free -SH groups on Root Cell Surfaces 50 2.3. 12 Field Emission Scanning Electron Microscope (FESEM) Analysis 51 2. 3. 13 X-ray Diffraction Analysis 51 2.3. 14 Inductively Coupled Plasma-Atomic Emission Spectrometry (ICP-AES) Analysis 51 2.3. 15 Statistical Analysis 52 lV CHAPTER 3 - RESULTS 3. 1 Growth of Hairy Roots 53 3. 1. 1 Nickel Hyperaccumulator (A. bertolonii) and Non-hyperaccumulator 53 (N. tabacum) 3. 1. 1. 1 Effect of Ni 53 3. 1. 1. 2 Effect of Ni and H+-ATPase Inhibitor 56 3. 1. 2 Cadmium Hyperaccumulator (T. caerulescens) and Non-hyperaccumulator (N. tabacum) 57 p• I. 2-• la_ [ 1=tel: o:f. In.4, ol f"·le.d-iu r • , 'p I--\ 3. 1. 2. 1b Effect of Cd and Zn 57 3. 1. 2. 2 Effect of Cd and H+-ATPase Inhibitor 60 3. 1. 2. 3 Effect of Cd and Glutathione Synthesis Inhibitor 62 3. 1. 2. 4 Effect of Cd and Free Radical Generators 63 3. 1. 2. 5 Effect ofCd and Free Radical Scavenger 65 3. 2 Heavy Metal Uptake 66 3. 2. 1 Nickel Accumulation in A. bertolonii and N. tabacum Hairy Roots 66 3. 2. 1. 1 Live and Dead Biomass 66 3. 2. 1. 2 Effect ofH+-ATPase Inhibitor 68 3. 2. 2 Cadmium Accumulation in T. caerulescens and N. tabacum Hairy Roots 69 3. 2. 2. 1 Live and Dead Biomass 69 3.2.2.2 EffectofZn 71 3. 2. 2. 3 Effect ofH+-ATPase Inhibitor 72 3. 2. 2. 4 Effect of Glutathione Synthesis Inhibitor 74 3. 2. 2. 5 Effect of Free Radical Generator 75 3. 2. 2. 6 Effect of Free Radical Scavenger 75 3. 3 Heavy Metal Distribution 77 3. 3. 1 Nickel Distribution in A. bertolonii and N. tabacum Hairy Roots 77 V 3. 3. 1. 1 Effect of Solvent Incubation Time and Agitation 77 3. 3. 1. 2 Effect ofH+-ATPase Inhibitor 78 3. 3. 1. 3 Microscope Analysis 81 3. 3. 2 Cadmium Distribution in T. caerulescens and N tabacum Hairy Roots 84 3. 3. 2. 1 Effect of Solvent Incubation Time and Agitation 84 3.3.2.2 EffectofZn 84 3. 3. 2. 3 Effect ofH+-ATPase Inhibitor 87 3. 3. 2. 4 Effect of Glutathione Synthesis Inhibitor 88 3. 3. 2. 5 Microscope Analysis 90 3. 4 Organic Acids 93 3. 4. 1 Concentration of Organic Acids in A. bertolonii and T. caerulescens Hairy Roots 93 3.4.2 Association of Ni and Cd with Organic Acids 97 3.5 Oxidative Stress Parameters 102 3. 5. 1 Nickel Hyperaccumulator and Non-hyperaccumulator 102 3. 5. 1. 1 Superoxide Dismutase 102 3. 5. 1. 2 Catalase 104 3. 5. 1. 3 Ascorbate Peroxidase 105 3. 5. 1. 4 Hydrogen Peroxide 107 3. 5. 1. 5 Malondialdehyde 108 3. 5. 1. 6 Sulphydryl Groups on Root Cell Surfaces 110 3.5.2 Cadmium Hyperaccumulator and Non-hyperaccumulator 111 3. 5. 2. 1 Superoxide Dismutase 111 3.5.2.2 Catalase 113 3.5.2.3 Ascorbate Peroxidase 114 3. 5.2.4 Hydrogen Peroxide 116 Vl 3. 5. 2. 5 Malondialdehyde 117 3. 5. 2. 6 Total Glutathione 119 3. 5. 2. 7 Sulphydryl Groups on Root Cell Surfaces 120 3. 6 Nickel Recovery 124 3. 6. 1 Alyssum bertolonii Hairy Roots 124 3. 6. 1. 1 Inductively Coupled Plasma-Atomic Emission Spectrometry (ICP-AES) Analysis 124 3. 6. 1. 2 Furnace Treatment 125 3. 6. 1. 2a Effect of Time 125 3. 6. 1. 2b Effect oflnitial Concentration of Ni 126 3. 6. 1. 2c Effect of Nitrogen 131 3. 6. 2 Berkheya coddii Plants 134 3. 6. 2. 1 Biomass Dry Weight and Ni Uptake 134 3. 6. 2. 2 ICP-AES Analysis 135 3. 6. 2. 3 Furnace Study 136 CHAPTER 4 - DISCUSSION 4. 1 Growth Analyses 141 4. 2 Nickel Uptake and Distribution 143 4. 3 Cadmium Uptake and Distribution 146 4. 4 Organic Acid Complexation 148 4. 5 Oxidative Stress in Ni-hyperaccumulator and Non-hyperaccumulator 150 4. 6 Oxidative Stress in Cd-hyperaccumulator and Non-hyperaccumulator 154 4. 7 Nickel Recovery 160 4. 7. 1 Alyssum bertolonii Hairy Roots 160 4. 7. 2 Berkheya coddii Plants 161 Vll CHAPTER 5 - CONCLUSIONS 5. 1 Nickel-hyperaccumulator and Non-hyperaccumulator 164 5. 2 Cadmium-hyperaccumulator and Non-hyperaccumulator 165 5. 3 Nickel Recovery 166 REFERENCES APPENDIX Vlll LIST OF FIGURES Figure 1.1 Possible mechanisms of metal tolerance in plants. Figure 1.2 Interactions between the reduced and oxidised forms of glutathione and ascorbate in removal ofH2O2. Figure 3.1 Growth of hairy roots of A. bertolonii without and with 25 ppm Ni. Figure 3.2 A. bertolonii hairy roots in B5 medium without Ni after 21 days and with 25 ppm Ni after 28 days. Figure 3.3 Growth of hairy roots of N. tabacum without and with 25 ppm Ni. Figure 3.4 N tabacum hairy roots in B5 medium without Ni and with 25 ppm Ni after 21 days. Figure 3.5 Growth of hairy roots of A. bertolonii without Ni and DES with 100 µM DES and 25 ppm Ni+ 100 µM DES. Figure 3.6 Growth of hairy roots of N. tabacum without Ni and DES with 100 µM DES and 25 ppm Ni + 100 µM DES. Figure 3.7 Hairy roots of T caerulescens cultured without Cd and with 20 ppm Cd after 21 days. Figure 3.8 Growth of hairy roots of T caerulescens without Cd and Zn with 20 ppm Cd and 20 ppm Cd + 33 ppm Zn. lX Figure 3.9 Growth of hairy roots of N. tabacum without Cd and Zn with 20 ppm Cd and 20 ppm Cd + 33 ppmZn. Figure 3.10 Hairy roots of N. tabacum cultured without Cd and with 20 ppm Cd after 21 days. Figure 3.11 Growth of hairy roots of T caerulescens without Cd and DES, with 100 µM DES and 20 ppm Cd + 100 µM DES. Figure 3.12 Growth of hairy roots of N. tabacum without Cd and DES, with 100 µM DES and 20 ppm Cd + 100 µM DES. Figure 3.13 Growth of hairy roots of T caeru/escens without Cd and BSO, with 100 µM BSO and 20 ppm Cd + 100 µM BSO. Figure 3.14 Growth of hairy roots of N. tabacum without Cd and BSO, with 100 µM BSO and 20 ppm Cd + 100 µM BSO. Figure 3.15 Growth of hairy roots of T caerulescens without Cd and CHP, with 33 µM CHP and 20 ppm Cd + 100 µM CHP.
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