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研究生:吳慧珍
研究生(外文):Hui-Chen Wu
論文名稱:植物熱休克反應之分子基礎研究-熱休克訊息傳遞相關分子之鑑定與氧化逆境交叉路徑之探討
論文名稱(外文):Molecular Bases of the Heat Shock Response in Plants- Identification of Elements Involved in Heat Shock Transduction Pathway and in the Cross Talk between Heat Shock and Oxidative Stress
指導教授:Florence Vignols靳宗洛靳宗洛引用關係
指導教授(外文):Florence VignolsTsung-Luo Jinn
口試委員:Christophe Brugidou林彩雲林秋榮常怡雍葉開溫林讚標
口試日期:2010-11-18
學位類別:博士
校院名稱:國立臺灣大學
系所名稱:植物科學研究所
學門:生命科學學門
學類:生物學類
論文種類:學術論文
論文出版年:2010
畢業學年度:99
語文別:英文
論文頁數:332
中文關鍵詞:細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶細胞壁果膠甲基酯酶
外文關鍵詞:CalciumChaperoneCalmodiumHeat shock proteinsOxidative stressPectin methylesteraseTetratricoredoxin
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植物生活史中常遭遇環境之脅迫,如熱、乾旱及鹽害等逆境,當其改變幅度超過適合植物正常生命活動範圍時,對其生命活動則造成不利之影響。尤其以溫度增加所引起之熱逆境,為普遍存在的農業問題,導致作物產量大幅的削減。另外,熱逆境會誘導活性氧大量產生,造成植物體內氧化逆境之形成;因此,活性氧之清除也是避免細胞在熱逆境下受到傷害之重要機制。探討逆境信號在植物體內傳導途徑及基因表達調控等分子層次上之調節,可提供具潛力發展之基因工程策略,以改進植物對逆境之耐性,在理論及生產上提供重要之研究基礎與實踐意義。
博士論文第一部分,主要以水稻及大豆為模式植物探討「熱逆境誘導外源鈣離子與細胞壁果膠甲基酯酶,參與植物細胞壁重建及訊息傳導之調控」。植物能大量累積低分子量熱休克蛋白質(small HSP, sHSP),扮演著抗熱逆境之重要角色;然本研究發現植物在熱休克 (heat shock, HS) 誘導下,藉由細胞壁果膠甲基酯酶 (pectin methylesterase, PME) 活性之調節,及激發細胞壁結構性鈣之移動,一面參與細胞壁之重建,增強細胞壁結構及細胞間之黏結作用;另一面,誘導外源鈣離子進入細胞質中,提高鈣訊號之震盪幅度及頻率,由鈣調蛋白 (calmodium, CaM) 接收並將信息傳達至下游,誘導低分子量熱休克蛋白質之表現,而提升植物抗熱逆境之能力。
論文第二部分以阿拉伯芥為模式植物,探討「硫氧還蛋白與分子伴護蛋白系統之功能性基因體與蛋白質體之交互作用」。植物中特有的類硫氧還蛋白(thioredoxin-like)稱Tetratricoredoxin (TDX),兼具氧化還原活性中心及分子伴護之特性。利用酵母菌雙雜交系統 (Y2H) 及雙分子螢光互補技術 (BiFC),在活细胞內證實TDX與阿拉伯芥高分子量熱休克蛋白質70 (HSP70) 發生交互作用,推測TDX能夠穩定HSP70與基質之結合,間接參與變性蛋白構型及活性之恢復。並且TDX受氧化逆境之誘導,轉移並累積至細胞核中,推測其功能與氧化逆境訊息之傳遞相關;藉由TDX基因缺失突變株,對氧化及熱逆境敏感性下降之外表型,並提高逆境相關基因之表現,推測TDX位於逆境訊號路徑之上游,扮演著訊號接受的角色,此過程可能與HSP70間之交互作用有關。此研究首次發現植物硫氧還蛋白在氧化與熱逆境中,同時參與訊息傳遞及伴護蛋白之功能,對於蛋白質在逆境間之交互作用有實質的貢獻。


While being unable to escape their lands, plants are continuously submitted to the modifications of their environment, and need to adjust proper physiological processes in response to various stimuli. During this work, I devoted my studies on two major stresses affecting plant development, heat shock (HS) and oxidative stresses (OS), focusing on key elements in these pathways (HS chaperons and HS-related thioredoxins) in order to bring news elements of knowledge and interconnexion of these pathways.
Using rice and soybean as mono- and dicotyledonous plant systems, I show how HS leads to calcium release from plant cell apoplast to the cytosol in a typical “calcium signature”, conferring cell wall rigidity and enhancing HS signaling pathway. I also identify pectin methylesterase (PME) as required in this pathway for cell wall remodeling and plasma membrane integrity. I further investigate how plant sense temperature increases and how they transmit the HS signal to downstream elements. Using systematic analyses of calmodulin (CaM) and small heat shock protein (sHSP) gene expression, I identify one CaM as a coordinator of HS response, which I characterize as involving specific cytosolic/nuclear isoforms of the sHSP family.
I latter perform the molecular analysis of TDX, a thioredoxin suspected to be involved in heat shock response. I show that TDX interacts with nucleo-cytoplasmic members of the HSP70 family in a redox dependent manner, both HS and OS inducing its nuclear relocation, and that TDX is required for both acquired thermotolerance and OS signaling.
I finally discuss the data brought by this work and propose models with cross-talks between HS and OS signaling.


ABSTRACT 1
摘要 1
Summary 2
Resume 3

I- Chapter 1: Literature Review 4
I.1- Introduction 4
I.2 Components of Induced-Stress Tolerance 5
I.2.1-The Versatile Role of Calcium Ions (Ca2+) 6
I.2.1.1-Ca2+ Signature 6
I.2.1.2-Ca2+, CaM, and Heat Stress 7
I.2.2-The Role of Ca2+/Pectate Interaction for Cell Wall Remodeling to Confer Thermotolerance in Plants 8
I.2.2.1-Elements of Plant Cell Wall 8
I.2.2.2-Ca2+/Pectate Network 9
I.2.2.3-Apoplastic Calcium 10
I.2.2.4-Pectin Methylesterases 10
I.2.3-Overview of Heat-Shock Response and Stress Proteins 15
I.2.3.1-Chaperone 15
I.2.3.2-Heat Shock Protein 70 16
I.2.3.3-Small Heat Shock Proteins 17
I.2.4- Reactive Oxygen Species and Oxidative Stress 25
I.2.4.1-Production of ROS 25
I.2.4.2-Hydrogen Peroxide (H2O2) 26
I.2.4.5-ROS Scavenging Mechanisms in Cells 27
I.3-Simultaneous Activation of Heat Shock Response and Oxidative Stress 30
I.4-Redox Regulation-Reduction/Oxidation (Redox) Status Regulates in Various Aspects of Cellular Function 32
I.4.1-Thioredoxins 33
I.4.2- Features of Plant Thioredoxin 33
I.5-New Perspectives on Heat Shock Response in Plant 38
I.5.1-Thioredoxin and Chaperone Regulation 38
I.5.2-Tetratricoredoxin (TDX) 39
I.6- Concluding Remarks 44
I.7-The Aim of Project 44
I.8-REFERENCES 48

II-Chapter 2: The Crosstalk between Extracellular and Intracellular Calcium Mobilization in Cell Wall Remodeling and Heat Shock Signaling 58
II-Chapter 2-Part 1: Heat Shock-Triggered Released Apoplastic Ca2+ Accompanied by Pectin Methylesterase Activity and Cytosolic Ca2+Oscillation Are Crucial for Plant Thermotolerance 58
II.1.1 ABSTRACT 58
II.1.2-RESULTS 59
II.1.2.1-Conditions for Lethal Treatment and Thermotolerance Establishment in Rice 59
II.1.2.2-Effect of EGTA Treatment on Plant Growth and Cellular Leakage 60
II.1.2.3-Effect of HS-Released Ca2+ Concentration and Its Recovery on the Development of Thermotolerance 61
II.1.2.4-Effect of EGTA on sHSP Accumulation and Organelle Localization in Vivo and Thermostabilization of Soluble Proteins in Vitro 70
II.1.2.5-Time-Course Study of the [Ca 2+]cyt Oscillation during Heat Shock Response in Rice Root 73
II.1.2.6-Effect of HS and EGTA Treatment on Pectin Methylesterase (PME) and Polygalacturonase (PG) Activity 73
II.1.2.7-Status of Demethylesterified Pectin in Response to HS and EGTA Treatment 74
II.1.2.8-The “egg box” Model Structure, Ca2+-Demethylated Homogalacturonan, in Response to HS and EGTA treatment 75
II.1.3-DISCUSSION 84
II.1.3.1-Effect of EGTA on Thermotolerance 84
II.1.3.2-Cytosolic Ca2+ Oscillation during HS and EGTA Treatment 84
II.1.3.3-Ca2+-Pectate Enriched the Structure and PME Physiological Functions during HS and EGTA Treatment 85
II.1.4- MATERIALS AND METHODS 90
II.1.4.1-Plant Growth and Cellular Leakage Analysis 90
II.1.4.2-Post-Ribosomal Supernatant (PRS) Preparation and Fractionation 90
II.1.4.3-Assay for Thermal Denaturation of Soluble Proteins 90
II.1.4.4-Quantitation of Class-I Small Heat Shock Protein (sHSP) Levels 90
II.1.4.5-Ion Analysis 91
II.1.4.6-Pectin Methylesterase (PME) Activity Analysed by Acidic Continuous Native-PAGE 91
II.1.4.7-Polygalacturonase (PG) Activity Assay 91
II.1.4.8-Histochemical Analysis of Pectin by Ruthenium Red (RR) Staining 92
II.1.4.9-Immunolocalization of Ca2+-Demethylated Homogalacturonan 92
II.1.4.10-Statistical Analysis 93
II.1.5- REFERANCES 94

II-Chapter 2-Part 2: Calcium/Calmodium Is Critical for Heat Shock Signal Transduction in Rice 97
II.2.1-ABSTRACT 97
II.2.2-RESULTS 97
II.2.2.1-Changes of Cytosolic Ca2+ Concentration Occur in Rice during Heat Shock 97
II.2.2.2-Apoplast Mediates Heat Shock-Induced Calcium Entry in Rice Cytosol .. 98
II.2.2.3-Rice Calmodulins Are Involved in Heat Shock-Induced Calcium Entry in the Cytosol 100
II.2.2.4-Rice Calmodulin Genes Differentially Respond to Heat Shock upon Time 107
II.2.2.5-Nucleo-Cytoplasmic Small HSP Gene Expression Differentially Accompanies Calmodulin Gene Induction during Early Heat Shock Response 108
II.2.2.6-Apoplastic Ca2+ as a Source for Rice Calmodulin and Nucleo-Cytoplasmic Small HSP Gene Induction under Early Heat Shock 113
II.2.2.7-Subcellular Redistribution of OsCaM1-1 in Response to Heat Shock 122
II.2.2.8-Overexpression of OsCaM1-1 Induces Heat Shock-Related Gene Expression and Enhances Thermotolerance in Arabidopsis 126
II.2.3-DISCUSSION 131
II.2.3.1-In Rice, Apoplast Mediates Heat Shock-Induced Calcium Entry into Cytosol Following Typical Ca2+ Signature Dynamics 131
II.2.3.2-The Spatio-Temporal Effects of [Ca 2+]cyt Oscillation on Calmodulin and Small HSP Genes Expression during HS 132
II.2.3.3-Subcellular Redistribution of OsCaM1-1 in Response to Heat Shock 136
II.2.3.4-Constitutive OsCaM1-1 Expression Enhances the Thermotolerance in Arabidopsis 137
II.2.4-MATERIALS AND METHODS 140
II.2.4.1-Plant Materials 140
II.2.4.2-Study of the Kinetic Changes in Ca2+ Oscillation 140
II.2.4.3-RNA Extraction and RT-PCR Analyses 140
II.2.4.4-Subcellular Localization of OsCaM1-1-GFP Fusion Protein 141
II.2.4.5-Production of OsCaM1-1 Overexpressing Line in Arabidopsis 141
II.2.4.6-Thermotolerance Tests 142
II.2.4.7-Cellular Ion Leakage Analysis 142
II.2.4.8-SDS-PAGE and Western Blot Analysis 142
II.2.4.9-Statistical Analysis 143
II.2.5-REFERENCES 144

III-Chapter 3: Redox and Chaperone Net Work in Arabidopsis-Search for the Function of Tetratricoredoxin (TDX) during Oxidative and Heat Stresses 150
III-SUMMARY 150
III-Chapter 3-Part 1: Tetratricoredoxin (TDX) and the Closely Related HSP70-Interacting Protein (HIP) Differentially Sense Oxidative Stress in Arabidopsis 151
III.1.1-ABSTRACT 151
III.1.2-RESULTS 151
Section I: Regulation of TDX Nuclear Relocalization in Response to Oxidative Sress 151
SI.1-TDX and HIP Preferentially Accumulate in Developing Arabidopsis Tissues 151
SI.2-TDX and HIP Genes Are Differently Expressed under Oxidative and Temperature stresses 152
SI.3-TDX and Hip Reside in the Cytosol and in the Nucleus in Vivo 152
SI.4-Oxidative Stress Induces Stable Relocation of TDX but Not HIP into the Nucleus. 153
SI.5-Validation of TDX Nuclear Relocation under Oxidative Stress by Immuno Blotting Sub-Cellular Fractions 153
SI.6-The Truncation of the Thioredoxin Active Site Specifically Attenuates TDX Nuclear Relocation under Oxidative Stress 154
Section II: TDX Plays a Specific Role in Oxidative Stress Signal Transduction 164
SII.1-The tdx Mutants Show Lower Sensitivity towards Oxidative Stress 164
SII.2-tdx-Deficient Plants Accumulate Less H2O2 under Oxidative Stress 165
SII.3-tdx-Deficient Plants Exhibit Alteration of H2O2 Detoxification Systems 165
SII.4-tdx-Deficient Plants are not Altered in Superoxide Production 166
SII.5-Search for Modification of Oxidative Stress-Related Gene expression in tdx Mutant 166
SII.6-A hip Mutant also Shows Lower Sensitivity towards H2O2 but Does Not Show Defect in H2O2 and O2‧– Accumulations 168
Section III: Search for TDX and HIP Functions in Additional Pathways 178
SIII.1-The tdx mutant but Not hip Is Insensitive to ABA 178
SIII.2-The hip.tdx Double Mutant Exhibit Enhanced Tolerance to Abiotic Stresses 178
SIII.3-A hip.tdx Double Mutant Is Sensitive to a Protein Synthesis Inhibitor 182
III.1.3-CONCLUSION AND PERSPECTIVES 184
III.1.4-MATERIAL AND METHODS 187
III.1.4.1-Plant Material and Growth Conditions 187
III.1.4.2-Identification of TDX and AtHIP Insertion Mutant Lines 187
III.1.4.3-RNA Extraction, RT-PCR and qPCR Analysis 188
III.1.4.4-Construction of Promoter TDX::GUS and HIP::GUS Fusion Genes 189
III.1.4.5-Fusion Constructs for Stable Expression in Arabidopsis 189
III.1.4.6-Histochemical GUS Staining 189
III.1.4.7-Gene Cloning and Subcellular Localization of GFP-Fusion Proteins 190
III.1.4.8-Preparation of the Cytosolic and Nuclear Proteins and Immunoblotting 191
III.1.4.9-Complementation Test 192
III.1.4.10-Stress Response Assays 193
III.1.4.11-Histochemical Detection of H2O2 and Superoxide Anions in Arabidopsis Leaves 193
III.1.4-REFERENCES 195

III.2-Chapter 3-Part 2: Tetratricoredoxin Is a HSP70-Interacting Protein Involved in Acquired Thermotolerance in Arabidopsis 199
III.2.1-ABSTRACT 200
III.2.2-RESULTS 200
Section I: The Partnership of TDX and HSP70s Family in Arabidopsis 200
SI.1-TDX Interacts Specifically with Arabidopsis HSP70sC/N Isoforms in Yeast Cells .200
SI.2-TDX-HSP70sC/N Interaction Efficiently Reports in Y2H Assay Involving Stress Responses 201
SI.3-TDX Interacts with HSP70sC/N in Planta ..202
SI.4-Search for Determinants in TDX Required for Interaction with HSP70C/N 213
SI.4.1- Both the TPR Motif and the Thioredoxin Domain of TDX Are Essential for Interacting with all HSP70sC/N 213
SI.4.2-The First Cys-304 of TDX Redox Center Is Involved in the Interaction with HSP70sC/N 213
SI.5-Both ATPase and Peptide Binding Domain of HSP70-1 Are Required for TDX Interaction 213
SI.6-Mutational Analysis of HSP70-1 214
Section II: HIP: another putative HSP70-interacting protein linked to TDX/HSP70s partnership 220
SII.1-HIP Interacts with HSP70sC/N in Yeast and Plant in Vivo Reporter Systems 220
SII.2-HIP Binds HSP70sC/N through Its N-terminal Domain, Displaying the Similar Pattern to TDX Binding 224
SII.3-Other Heat Shock Proteins Interact with TDX and HIP 227
SII.4-Dimerization Properties of TDX and HIP 229
Section III: TDX and HIP Are Components of Signaling Pathways with Similar Behaviors towards Heat Stress 231
SIII.1-Comparisons of HIP and TDX Gene Expression Patterns under Heat Stresses 231
SIII.2-Heat Shock Induces Transient Relocation of Both TDX and HIP into the Nucleus 232
SIII.3-The hip.tdx Double Mutant Exhibit Enhanced Tolerance to Heat Stress 232
SIII.4-The Transcript Level of Heat Related Gene Expression in TDX and HIP Mutant Background 233
III.2.3-DISCUSSION 238
III.2.3.1-TDX: An Atypical Thioredoxin Unifying Molecular Stress-Linked Chaperones Interactomes 238
III.2.3.2-TDX Interacts with Arabidopsis HSP70sC/N in Complex Chaperone Networks Probably Involving Several Classes of Heat Shock Proteins 239
III.2.3.3-Domain Mapping Highlights Specific Chaperone- and Redox-Linked Functions Required in TDX/HIP/HSP Networks 240
III.2.3.4-TDX and HIP Have Associated Function to Acquired Thermotolerance Process 241
III.2.4-MATERIALS AND METHODS 242
III.2.4-REFERENCES 243

III.3-Chapter 3-Part 3: Searching for TDX-Interacting Proteins: Characterization of a TDX-NAD Kinase Interaction 247
III.3.1-ABSTRACT 247
III.3.2-RESULTS 248
III.3.2.1-Identification of TDX Putative Targets by the Y2H Method 248
III.3.2.2-TDX Putative Target Proteins Are Involved in Distinct Pathways 248
III.3.2.3-TDX/NAD Kinase Interaction: a New Role of TDX in Regulating NADPH Pathway 253
III.3.2.3a-The NAD Kinase Family in Arabidopsis 253
III.3.2.3b-NADK1 and NADK2, but Not NADK3 Interact with TDX in a Y2H System.. 254
III.3.2.3c-TDX Interacts with NADK1 and NADK2 in Planta 254
III.3.2.3d-Are NADK Proteins Targeted by Other Redoxins or by HIP? 256
III.3.2.4-TDX Also Interacts with Distinct Proteins Involved in Different Pathways 265
III.3.3-CONCLUSIONS AND FUTURE PROSPECTS 270
III.3.4-MATERIALS AND METHODS (common to Chapter 3-Part 2+3) 274
III.3.4.1-Yeast Strains and Media 274
III.3.4.2-Two-Hybrid Experiments 274
III.3.4.3-DNA Cloning for Y2H Assay 275
III.3.4.4-Bimolecular Fluorescence Complementation (BiFC) Assay 275
III.3.4.5-RNA Extraction, RT-PCR and qPCR Analysis 276
III.3.4.6-Plant Material, Growth Conditions, and Mutants Identification 276
III.3.4.7-Thermotolerance Test 277
III.3.5-REFERENCES 278

IV-Chapter 4-Conclusions and Prospects 282
IV.1-Recovery of Heat Shock-Triggered Released Apoplastic Ca2+ Accompanied by Pectin Methylesterase Activity Is Required for Thermotolerance 282
IV.2-Early Heat Shock Signal Transduction Mechanisms: Newly Discovered Components Linked to Plant Thermotolerance 285
IV.3.3-The Hypothesis Model of TDX and HIP Function in Acquired Thermotolerance…. 290
IV.3.1-TDX May Serve as a Sensor/Transducer of Oxidative Stress Signals 290
IV.3.2-TDX/HSP70/HIP Interactome in Arabidopsis 292
IV.3.3-The Hypothesis Model of TDX and HIP Function in Acquired Thermotolerance 292
IV.4-Overall Comments 300


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