C4 Photosynthesis and Related CO2 Concentrating Mechanisms (eBook)

From the Series Editor 6
The Founding Series Editor 12
Series Editor 13
Contents 14
Preface 20
The Editors 24
Contributors 26
Author Index 28
Part ITributes & Introduction
Chapter 1: Sir Jagadish Chandra Bose (1858–1937): A Pioneer in Photosynthesis Research and Discoverer of Unique Carbon Assimilation in Hydrilla 31
I. Introduction 32
II. Life of Sir J.C. Bose 32
III. Out of Box Concepts and Innovative Instruments for Biological Experiments 33
IV. Classic and Comprehensive Monographs on Physiology of Plants 34
V. Work on Photosynthesis and Focus on Hydrilla 34
VI. Importance of Malate and Operation of C4-like Pathway 35
VII. Contemporary View of his Observations on Hydrilla 35
VIII. Observations on Inhibitors/Stimulants on Photosynthesis in Hydrilla 36
IX. Concluding Remarks: Inspiration for Biology Research in India and a Pioneer of Photosynthesis Research on Hydrilla 37
References 38
Chapter 2: Constance Endicott Hartt (1900–1984) and the Path of Carbon in the Sugarcane Leaf 40
I. Biography of Constance Hartt: Early Period and Her Move into Hawaii 41
II. Work at Hawaiin Sugar Planters’ Association: Focus on Biosynthesis and Transport of Sugar in Sugarcane 41
III. Discovery of the Role of Malate in Carbon Assimilation and Sucrose Biosynthesis 41
IV. Concluding Remarks 42
References 43
Chapter 3: Introduction 44
I. Introduction 45
II. New Physiological and Developmental Perspectives 47
III. Molecular Basis of the C4 Pathway 49
IV. Systematics, Diversity and Evolution 50
V. New Uses of C4 Photosynthesis 51
VI. Conclusions 51
References 51
Part II New Physiological and Developmental Perspectives 53
Chapter 4: C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants 54
I. Introduction 55
A. What Does It Take to Be C4? 55
B. Occurrence of C4 Among Terrestrial Plants 55
II. Structural and Biochemical Diversity in Kranz Type Anatomy 56
A. Structural Diversity 56
1. Poaceae 56
Classical NADP-ME Type Anatomy 57
Classical NAD-ME Type Anatomy 57
Classical PEP-CK Type Anatomy 59
Arundinelloid: Biochemical Subtype NADP-ME 59
Aristidoid: Biochemical Subtype NADP-ME 60
Stipagrostoid: Biochemical Subtype NADP-ME 60
Eriachneoid: Biochemical Subtype NADP-ME 60
Neurachneoid: Biochemical Subtypes NADP-ME and PEP-CK 61
Other Forms of NAD-ME Type Anatomy 61
2. Family Cyperaceae 62
Fimbristyloid: Biochemical Subtypes NADP-ME and NAD-ME 62
Chlorocyperoid: Biochemical Subtype NADP-ME 62
Rhynchosporoid: Biochemical Subtype NADP-ME 64
Eleocharoid: Biochemical Subtype NAD-ME 64
3. Dicotyledons 64
Atriplicoid: Biochemical Subtypes NAD-ME and NADP-ME 65
Kochioid: Biochemical Subtypes NAD-ME and NADP-ME 66
Salsoloid: Biochemical Subtypes NAD-ME and NADP-ME 66
Salsinoid: Biochemical Subtype NAD-ME 67
Schoberioid: Biochemical Subtype NAD-ME 67
Kranz-Tecticornioid: Biochemical Subtype NAD-ME 68
Pilosoid: Biochemical Subtype NADP-ME 68
Portulacelloid: Biochemical Subtype NADP-ME 68
Glossocardioid: Biochemical Subtype NAD-ME and NADP-ME 68
Simplicifolioid: Biochemical Subtype NADP-ME 70
Isostigmoid: Biochemical Subtype unknown 70
Angustifolioid: Biochemical Subtype NAD-ME 70
B. Biochemical Diversity: C4 Cycles and Energy Requirements for C4 Subtypes 70
1. Chloroplasts and Mitochondria 70
2. Illustration of Energetics for NADP-ME Type Species 71
3. Illustration of Energetics for NAD-ME Type Species 73
4. Illustration of Energetics for PEP-CK Type Species 73
5. Additional Energy Requirements in C4 Photosynthesis 73
III. Single-Cell C4 Photosynthesis in Terrestrial Plants 73
A. Occurrence (Family and Phylogeny) 74
B. Biogeography of Single-Cell C4 Species 74
C. Overview of Two Types of Single-CellC4 Photosynthesis in Terrestrial Plants 75
D. Biochemical Evidence for Function of C4 Photosynthesis in Single-Cell C4 Plants 76
1. General Features Characteristic of C4 76
Western Blots and Analysis of C4 Enzymes 76
C4 Type Carbon Isotope Composition 76
Physiological Response 77
Resistance to CO2 Loss 78
2. Spatial Compartmentation Enabling Function of NAD-ME Type C4 Photosynthesis 78
Dimorphic Chloroplasts (Structure, Enzymes and Starch) 78
Mitochondria and Peroxisomes 79
E. Development of Spatial Compartmentation and Dimorphic Chloroplasts 79
F. Form of Photosynthesis in Different Photosynthetic Organs in Single-Cell C4 Species 79
G. How Did Single-Cell C4 Evolve? 80
IV. Future Perspectives 80
References 81
Chapter 5: Single-Cell C4 Photosynthesis in Aquatic Plants 87
I. Introduction 88
II. Unraveling the Single-Cell C4 System 88
A. Some Early Intriguing Observations 88
B. Single-Cell C4 Photosynthesis in Hydrilla 89
C. Other Submersed Single-Cell C4 Species 95
D. Which Originated First: Aquatic or Terrestrial C4 Photosynthesis? 99
III. HCO3 -Use Mimics C4 Photosynthetic Gas Exchange Characteristics 100
IV. Concluding Thoughts 100
References 101
Chapter 6: Photorespiration: The Bridge to C4 Photosynthesis 105
I. Introduction 106
II. Biochemistry and Genetics of the C2 Cycle 108
A. Chloroplasts Produce 2-Phosphoglycolate by Oxygenation of RubP 109
B. 2-Phosphoglycolate Becomes Dephosphorylated to Glycolate 109
C. Glycolate Becomes Oxidized to Glyoxylate and H2O2 in the Peroxisomes 110
D. At Least Two Peroxisomal Transaminases Convert Glyoxylate to Gly 111
E. Mitochondrial Reactions of Gly Yield Ser, CO2, NH3, and NADH 112
1. Gly decarboxylase 112
A. P-Protein 113
B. H-Protein 113
C. T-Protein 114
D. L-Protein 114
2. Ser hydroxymethyltransferase 115
F. Hydroxypyruvate Is Produced from Ser and Becomes Reduced to Glycerate 115
G. Glycerate Becomes Phosphorylated and 3PGA Re-enters the Calvin Cycle 116
H. Transcriptional Regulation of Photorespiratory C2 Cycle Genes 117
III. Related Reactions and Interactions with Other Metabolic Pathways 117
A. Reassimilation of Photorespiratory NH3 117
B. Regulatory Interaction with Respiration 118
C. One-Carbon Metabolism 118
D. Alternative Sources and Destinies of C2 Cycle Metabolites 119
IV. Measurement of Photorespiration 119
A. Post-illumination Burst of CO2 (PIB) 119
B. Measurement of 14CO2 Evolution 120
C. Extrapolation from CO2 Response (A/ci) Curves 120
D. Estimation from Rubisco Kinetics and Gas Exchange Measurements 120
V. The Role of Photorespiration for the Evolution of C4 Photosynthesis 121
VI. Future Prospects 125
References 127
Chapter 7: Nitrogen and Sulfur Metabolism in C4 Plants 133
I. Introduction 134
II. Nitrogen Assimilation 134
A. Plant Nitrate Assimilation 134
B. Regulation of Nitrate Assimilation 135
C. Nitrate Assimilation in C4 Plants 137
III. Sulfate Assimilation 138
A. Plant Sulfate Assimilation 138
B. Regulation of Sulfate Assimilation 139
C. Sulfate Assimilation in C4 Plants 140
IV. Glutathione Synthesis and Reduction 141
A. Regulation of GSH Synthesis 141
B. Localization of GSH and GSH Synthesis 142
C. GSH Synthesis in C4 Plants 143
V. Physiological Significance of the Distribution of Nitrate and Sulfate Assimilation 144
A. Open Questions on Nitrate Assimilation in C4 Plants 144
B. Significance of BSC Localization of Sulfate Assimilation 145
C. Consequences of BSC Localization of Sulfate Assimilation 146
VI. Conclusions 146
References 147
Chapter 8: Nitrogen and Water Use Efficiency of C4 Plants 153
I. Introduction 154
II. Nitrogen Use Efficiency 155
A. Nitrogen Use Efficiency of C4 Grasses 155
B. CO2 Assimilation Rate, Leaf N and Leaf Mass per Area 156
C. C4 Species and the Global Plant Trait Network 157
D. Leaf N Budget 158
E. Rubisco and Nitrogen Use Efficiency of C4 Species 160
III. Water Use Efficiency 162
A. Water Use Efficiency of C4 Grasses 162
B. Water Use Efficiency and Carbon Isotope Discrimination in C4 Species 163
C. Effects of Environmental Conditions on Water Use Efficiency of C4 Grasses 165
IV. Conclusions 167
References 167
Chapter 9: Development of Leaves in C4 Plants: Anatomical Features That Support C4 Metabolism 171
I. Introduction 172
II. Overview of C4 Biology and Leaf Anatomy 172
III. Quantitative Variation in Leaf Traits 173
A. Venation 173
1. Organizing Role of Venation 173
2. Formation of the Leaf Venation Pattern 173
3. Polar Auxin Transport and Vein Ontogeny in Arabidopsis 174
4. Vein Ontogeny in Other Species 175
5. Theoretical Relationships Between PAT, Leaf Cell Proliferation and Vein Pattern 175
6. Regulation of Density of Leaf Venation 175
B. Downstream from Vein Formation: Patterns of Cell Proliferation, Expansion and Differentiation for C4 Cells 176
C. Barriers and Connections: Suberin Lamellae and Plasmodesmata 177
D. Environmental and Developmental Plasticity 178
IV. Complex Traits and Systems Analysis 178
References 179
Chapter 10: C4 Photosynthesis and Temperature 184
I. Introduction 185
II. The Temperature Responses of C4 Photosynthesis and Growth 186
A. Net CO2 Assimilation Rate 186
B. Interactions with CO2 and Light Intensity 189
C. Growth 189
III. The Biogeography of C4 Photosynthesis 191
A. Global Patterns 191
B. Cold-Adapted C4 Species 193
C. Evolutionary and Ecological Perspectives 193
D. Synopsis 198
IV. The Temperature Response of C4 Photosynthesis: Biochemical Controls 198
A. The Response of C4 Photosynthesis to Intercellular CO2 Partial Pressure 199
B. Photorespiration in C3 and C4 Plants 200
C. Quantum Yield 200
D. Rubisco Limitations 202
E. Rubisco Activase Limitations 203
F. C4 Cycle Limitations 204
1. Pyruvate-Pi-Dikinase 204
2. PEP Carboxylase 205
3. Other Enzymes 205
G. Electron Transport Limitations 206
V. Fluorescence at Low Temperature 207
VI. Stomatal Limitations 208
VII. Thermal Acclimation of C4 Photosynthesis 208
VIII. Conclusion: Are C4 Plants Inherently More Sensitive to Low Temperature Than C3 Plants? 210
References 211
Part III Molecular Basis of C4 Pathway 219
Chapter 11: Transport Processes: Connecting the Reactions of C4 Photosynthesis 220
I. Introduction 221
II. Intercellular Fluxes 224
III. Transport Processes in the NADP-Malic Enzyme Type 224
A. PEP Export from PCA Type Chloroplasts 225
B. Oxaloacetate and Malate Exchange in PCA Type Chloroplasts 226
C. Malate Import into PCR Chloroplasts 227
D. Pyruvate Export from PCR chloroplasts 228
E. Pyruvate Import into PCA Type Chloroplasts 228
F. Auxiliary Transport Processes 229
IV. Transport Processes in the NAD-Malic Enzyme Type 230
A. PEP Export from PCA Chloroplasts 231
B. Dicarboxylate Transport in PCR Mitochondria 231
C. Pyruvate Export from PCR Mito chondria 231
D. Pyruvate Import into PCA Chloroplasts 232
V. Transport Processes in the PEP Carboxykinase (PEP-CK) Type 232
A. PEP Export from PCA Chloroplasts 233
B. Oxaloacetate Malate Exchange in PCA Chloroplasts 233
C. Malate Import into PCR Mitochondria 233
D. ATP/ADP Translocation to Supply PEP-CK with ATP 233
VI. Transport Processes in Single Cell C4 Metabolism 233
VII. Future Prospects 234
A. Discovering the Molecular Identity of C4-Adapted-Transport Proteins 234
B. Prospects for Engineering C4 Photosynthesis into C3 Crop Species 235
References 236
Chapter 12: C4 Gene Expression in Mesophyll and Bundle Sheath Cells 241
I. Introduction and Overview 242
II. C4 Gene Expression in Bundle Sheath Cells 245
A. Rubisco 245
1. Rubisco Gene Expression and C4 Leaf Development 246
2. Rubisco Gene Expression Patterns in a C4 Dicot 246
3. Rubisco Gene Expression Patterns in a C4 Monocot 249
4. Rubisco Gene Expression in Different C4 Species 250
B. Malic Enzyme Genes 251
1. NAD-Dependent Malic Enzyme 251
2. NADP-Dependent Malic Enzyme 252
C. Genes Encoding Other BS Cell-Specific Proteins 254
III. C4 Gene Expression in Mesophyll Cells 255
A. PEPC and PPdK 255
1. Amaranth PEPC and PPdK Gene Expression 255
2. Flaveria PEPC and PPdK Gene Expression 256
3. Maize PEPC and PPdK Gene Expression 258
B. Genes Encoding Other MP Cell-Specific Proteins 258
IV. C4 Gene Expression in Organelles 260
V. Factors Affecting C4 Gene Expression in BS and MP Cells 260
A. Photosynthetic Metabolism 261
B. Cell Position and Lineage 262
C. Other Factors That Affect C4 Gene Expression 262
VI. Levels of C4 Gene Regulation 263
A. Transcriptional Control of C4 Gene Expression 263
B. Post-transcriptional Control C4 Gene Expression 265
VII. Conclusions, Future Directions, and Molecular Engineering of C4 Capability 268
References 270
Chapter 13: C4-Phosphoenolpyruvate Carboxylase 277
I. Phosphoenolpyruvate Carboxylase: An Overview 278
A. Origin of Plant PEPCs 278
B. Genes and Gene Families 278
C. The Enzyme: Biochemistry and Regulation 280
D. Differences Between C4 and Non-photosynthetic ppc Genes 283
II. Evolutionary Origin of C4 PEPCs 283
III. Molecular Evolution of C4 PEPCs 286
A. Protein Properties 286
B. Changes in Gene Expression 289
IV. Outlook 292
References 292
Chapter 14: C4 Decarboxylases: Different Solutions for the Same Biochemical Problem, the Provision of CO2 to Rubisco in the Bundle Sheath Cells 296
I. Introduction 297
II. NADP-Malic Enzyme, the Most Studied C4 Decarboxylase 299
A. The Photosynthetic Chloroplastic C4-NADP-ME 300
B. Non-photosynthetic Plastidic and Cytosolic Isoforms in C4-NADP-ME Plants 302
C. Non-photosynthetic Plastidic and Cytosolic NADP-ME Isoforms in C3 Plants 304
D. Phylogenetic Relationships Among Plant NADP-ME Sequences 305
III. Plant Mitochondrial NAD-E, a Hetero-Oligomeric Malic Enzyme 305
A. Photosynthetic Mitochondrial C4 Plant NAD-ME 307
B. NAD-ME from Non-photosynthetic Tissues of C4 Plants 307
C. Non-photosynthetic NAD-ME from C3 Plants 308
D. Phylogenetic Relationship Among Plant NAD-ME Sequences 308
IV. Plant PEPCK: the Cytosolic Gluconeogenic Enzyme Involved in C4 Photosynthesis 309
A. The Photosynthetic PEPCK Isoform 310
B. Non-photosynthetic PEPCK Isoforms from C4 Plants 311
C. Non-photosynthetic PEPCK Isoforms from C3 Species 311
D. Phylogenetic Relationship Among Plant PEPCK Sequences 312
V. Future Perspectives 314
References 314
Chapter 15: Structure, Function, and Post-translational Regulation of C4 Pyruvate Orthophosphate Dikinase 320
I. Introduction 321
A. Role of PPDK in C4 Plants 321
B. PPDK Enzyme Properties 321
1. Catalysis as Related to Structure 321
2. Oligomeric Structure and Tetramer Dissociation at Cool Temperatures 323
3. Substrate Kms for C4 PPDK 323
C. PPDK as a Rate-Limiting Enzyme of the C4 Pathway 323
II. Post-translational Regulation of C4 PPDK 324
A. Light/Dark Regulation of C4 PPDK Activity by Reversible Phosphorylation 324
1. Discovery of the PPDK Regulatory Protein, RP 324
2. PPDK RP: Enzyme Properties 324
3. The PPDK Phosphoryl-Inactivation Mechanism 325
4. Regulation of RP’s Opposing Activities 326
Putative Regulation by Adenylates: Stromal ADP as an Attenuator of RP Bifunctional Activity 326
Lack of Evidence for Post-translational Regulation of RP 329
B. Other Post-translational Components Governing PPDK Activity In Vivo 329
III. Functional and Bioinformatic Analysis of Cloned Maize C4 and Arabidopsis C4-Like PPDK-Regulatory Protein 329
A. Cloning of RP from Maize and Arabidopsis 329
B. Functional Properties of Recombinant Maize C4- and Arabidopsis C4-Like RP 330
C. Bioinformatic Analysis of RP Primary Amino Acid Sequence 331
1. RP Is Highly Conserved in C3 and C4 Plants 331
2. RP Represents a Fundamentally New Structural Class of Regulatory Protein Kinase 331
IV. Future Directions 332
References 332
Part IV Diversity and Evolution 335
Chapter 16: C4 Photosynthesis Origins in the Monocots: A Review and Reanalysis 336
I. Introduction 337
II. Alismatales 337
II. Cyperaceae 340
A. Rhynchosporeae C4 Diversification 340
B. Abildgaardieae C4 Diversification 342
C. Eleocharidae C4 Diversification 342
D. Cypereae C4 Diversification 342
IV. Poaceae 343
A. Chloridoideae C4 Diversification 344
B. Panicoideae C4 Diversification 344
V. Conclusions 349
References 352
Chapter 17: The Geologic History of C4 Plants 356
I. Introduction 357
II. Geologic Evidence 357
A. Geochemical Approach and Interpretation 357
B. Geochemical Signals in the Fossil Record 359
C. Macrofossils 360
D. Microfossils 360
III. Origin of C4 Photosynthesis 362
A. Oligocene 362
B. Earlier Origins for C4 Photosynthesis? 363
IV. Expansion of C4 Grasslands 364
A. CO2 Starvation Hypothesis 364
B. Palaeoclimate Hypotheses 365
C. Grass-grazer Co-evolution Hypothesis 367
D. Fire Hypothesis 368
E. Fire-Climate Feedbacks 368
F. An Evolutionary Link Between Fire and Grazing? 369
V. Conclusions 370
References 371
Part V C4 Engineering and Bioenergy 375
Chapter 18: Hurdles to Engineering Greater Photosynthetic Rates in Crop Plants: C4 Rice 376
I. Introduction 377
II. Why Try to Engineer a C4 Crop Plant? 377
III. How Can Crop Productivity Be Increased by C4 Photosynthesis? 378
IV. The Requirements for C4 Photosynthesis 378
V. Which Plant Should We Transform? 381
VI. Which Mechanism of C4 Photosynthesis Should Be Used and Why? 382
A. The Single-Cell Model 382
B. The Two-Cell Model 383
C. How Many Changes Are Required in the Two-Cell Model? 384
VII. Early Attempts at Transferring C4-Traits into C3 Plants 384
VIII. Alternate Approaches to Improving Photosynthetic Rates 387
A. Recycling Photorespiratory Products 387
B. Introduction of an Alternate Carbon Concentrating Mechanism 387
IX. Hurdles to Engineering C4 Crops 388
X. Assessment of C4-ness 389
XI. Conclusions 389
References 390
Chapter 19: C4 Species as Energy Crops 394
I. Introduction 395
II. What Are the Qualities of an ‘Ideal’ Energy Crop? 396
A. Light Use Efficiency 396
B. Water Use Efficiency 398
C. Nitrogen Use Efficiency 398
III. C4 Species as Energy Crops in Cool-Temperate Climates 398
IV. Examples of C4 Species as Biofuel Feedstock 400
V. Prospects for Energy Crop Improvement 403
VI. The Environmental Debate and Bioenergy Crops 404
VII. Economic and Energetic Costs and Benefits 406
VIII. Conclusions and Perspectives 407
References 407
Index 413