The Leaf: A Platform for Performing Photosynthesis (eBook)

William W. Adams III, a Professor at the University of Colorado, has pursued a lifelong passion for leaves. An investigation of the heterophyllous leaves (trichome-covered, atmospheric juvenile versus glabrous, tank-forming adult leaves) of an epiphytic bromeliad was followed by PhD research on photosynthesis and photoinhibition of plants with crassulacean acid metabolism. After postdoctoral work into leaf senescence, pollution impacts on leaves, and photosynthesis and photoprotection in leaves, cladodes, and lichens, he moved to Colorado in 1989.  During the intervening years, he, his wife and colleague (Prof. Barbara Demmig-Adams), and their students explored the regulation and ecophysiology of photosynthesis, photoprotection, and photoinhibition of numerous species under controlled conditions and in many habitats including the understory of sunfleck-dappled forests, arid and desert landscapes, grasslands, and montane and subalpine forests.  More recently, they discovered significant relationships between foliar phloem and xylem architecture (underlying capacities to load and export sugars and distribute water within the leaf), photosynthesis, and transpiration that vary among species and exhibit acclimatory adjustment to environmental growth conditions. The Leaf represents the renewal of ties between William and Ichiro that were initiated during their PhD and postdoctoral work, respectively, at the Australian National University in the mid-1980s.  Ichiro Terashima began his study on the light environment within individual leaves and its effect on leaf photosynthesis with Prof. Toshiro Saeki, miniaturizing his supervisor’s study at the leaf canopy scale to the individual leaf scale. He subsequently conducted an eco-devo study examining effects of light direction on differentiation of palisade and spongy tissues in bifacial leaves with Prof. Noboru Hara, a plant anatomist. He then moved to the Australian National University and studied effects of light and nitrogen nutrition on leaf photosynthesis, patchy leaf photosynthesis in abscisic acid-treated leaves, and photoinhibition, followed by a position in Prof. Sakae Katoh’s laboratory at the University of Tokyo.  He became a full professor at Osaka University in 1997, and moved back to the University of Tokyo in 2006. With his colleagues and students, he has studied the influences of 1) green light in leaf photosynthesis, 2) mesophyll tissue in stomatal responses to environmental conditions, 3) soil dryness, high CO2 and ABA application on mesophyll conductance, 4) fluctuating light on photosynthesis, and 5) systemic signals such as sugars, hormones, peptides etc. on leaf development and senescence.

From the Series Editors 6
Advances in Photosynthesis and Respiration Including Bioenergy and Related Processes 6
Volume 44: The Leaf: A Platform for Performing Photosynthesis 6
Authors of Volume 44 7
Our Books 7
Future Advances in Photosynthesis and Respiration and Other Related Books 11
Series Editors 13
Contents 18
Preface: The Importance of Leaves to Life and Humanity 25
References 31
The Editors 33
A Fascination with Leaves 33
References 35
Contributors 40
The Life of a Leaf by William W. Adams III 44
Author Index 47
Chapter 1: A Consideration of Leaf Shape Evolution in the Context of the Primary Function of the Leaf as a Photosynthetic Organ 48
I. Introduction: Basic Mechanisms of Leaf Blade Formation 49
A. Basic, Common Mechanisms 49
B. Mechanisms for Compound Leaf Formation and Others 52
II. Natural Variation in Leaf Width 54
III. Genetic Factors Underlying Leaf Index Variation 57
IV. Diversity in Compound Leaves and Leaves with Serrated Margins 59
V. Proximal-Distal Pattern Variation 60
VI. Pitcher Leaves 63
VII. Unifacial Leaves – Terete and Ensiform Types 63
VIII. Indeterminate Leaves – Intermediate Form of a Shoot and a Leaf 65
IX. Cladodes and Other Leaf-Like Organs 66
X. Conclusions 68
References 68
Chapter 2: Leaf Vasculature and the Upper Limit of Photosynthesis 74
I. Introduction 75
II. Foliar Venation as a Structural Scaffold 78
III. Flux Capacity of Foliar Veins 80
A. Vein Density 80
B. Vascular Pipelines: Tracheary and Sieve Elements 81
C. Phloem Loading 81
IV. Foliar Hydraulic Conductance, Minor Vein Xylem Features, and Photosynthesis 83
V. Minor Vein Phloem Features and Photosynthetic Capacity 85
VI. Phenotypic Plasticity Underlying Photosynthetic Acclimation of Ecotypes from Varying Climatic Conditions 88
A. Response to Growth Light Intensity 88
B. Response to Growth Temperature 91
C. Extent of Plasticity Linked to Habitat Environment 92
VII. Conclusions 95
References 95
Chapter 3: Export of Photosynthates from the Leaf 102
I. Introduction 103
II. Phloem Loading Mechanisms 106
III. Apoplastic Loading 107
IV. Symplastic Loading 109
V. Passive Symplastic Loading 110
VI. Active Symplastic Loading (Polymer Trapping) 112
VII. Heterogeneous Phloem Loading 114
VIII. Control Mechanisms for Loading and Transport 115
IX. Integration of Whole-Plant Carbon Partitioning 118
X. Conclusions 119
References 121
Chapter 4: Leaf Water Transport: A Core System in the Evolution and Physiology of Photosynthesis 127
I. Transporting Water for Carbon – Principles of Cohesion-Tension Theory and the Link Between Water Transport and Photosynthetic Capacity in Leaves 128
A. Linking Hydraulics and Photosynthesis 130
II. Measuring and Modeling Kleaf 131
III. Adaptation and Regulation of Kleaf 133
A. Vein Density 133
B. Vein Xylem and Leaf Anatomy 133
C. Xylem-Stomatal Tissue Coordination 134
D. Regulation of Kleaf 134
IV. Evolution of Modern Vein Networks 135
V. Stress and Failure in the Leaf Hydraulic System 136
VI. Conclusions 138
References 138
Chapter 5: Leaf Anatomy and Function 143
I. Introduction 144
II. Types of Leaves and Their Anatomy 145
III. Leaf Anatomy and Its Major Functions 150
A. Light Absorption – Leaf Optics 150
B. CO2 Diffusion and Assimilation 153
1. Diffusion Through Intercellular Airspaces 154
2. Diffusion Through the Mesophyll Cells 158
C. Temperature Modulation 158
D. Anatomy and Water Transport 160
E. Mechanical Function 162
F. Functions of the Leaf Surface – The Role of Trichomes 165
1. Trichome Morphology 165
2. Trichome Functions 165
IV. Acclimation and Adaptation 167
A. Responses of Leaf Anatomy to Light 167
B. Responses of Leaf Anatomy to Temperature 170
C. Responses of Leaf Anatomy to Water Stress 171
V. Conclusions 171
References 174
Chapter 6: Coordination Between Photosynthesis and Stomatal Behavior 186
I. Introduction 187
II. Anatomical Features and Physiological Responses Determine Stomatal Conductance 188
III. Stomatal Behavior Correlates with Mesophyll Demands for Photosynthesis 189
IV. Co-ordination of Stomatal Behavior and Mesophyll Photosynthesis 191
V. A Role for Guard Cell Chloroplasts and Photosynthesis in Co-ordinating Mesophyll Photosynthesis and Stomatal Behavior 192
VI. Evidence for a Mesophyll Driven Signal: A Comparison between Stomatal Responses in Intact Leaves and in Epidermal Peels 193
VII. Characteristics of Apoplastic Mesophyll Signals: Is the Production of a Mesophyll Signal Dependent on Mesophyll Photosynthesis? 195
VIII. Mesophyll Signals Move from the Mesophyll to the Epidermis via the Apoplast 196
IX. Possible Mesophyll Signals 196
X. Adaxial and Abaxial Stomatal Responses to Light 197
XI. Effects of Growth Light Environment on Adaxial and Abaxial Stomatal Light Responses 199
XII. Conclusions 201
References 201
Chapter 7: CO2 Diffusion Inside Photosynthetic Organs 207
I. Introduction 208
II. How to Estimate Internal CO2 Diffusion Conductance? 211
A. The Isotopic Methods 212
B. The Chlorophyll Fluorescence Method 216
III. The CO2 Pathway 218
A. Sources and Sinks of CO2 Inside Photosynthetic Organs 218
1. Sinks of CO2 Inside Photosynthetic Organs 219
2. Sources of CO2 Inside Photosynthetic Organs 219
3. CO2 Diffusion Inside Photosynthetic Organs 220
B. Models for CO2 Diffusion 221
C. The CO2 Fluxes Inside Photosynthesizing Cells 222
IV. Mesophyll Conductance to CO2 in Different Plant Groups and Its Co-Regulation with Leaf Hydraulics 225
A. Mesophyll Conductance to CO2 in Different Plant Groups 225
B. Co-Regulation of Mesophyll Conductance with Leaf Hydraulics 227
1. Leaf Hydraulic Conductance (Kleaf) 227
2. Stomatal Conductance (gs) 228
V. Structural Determinants of Mesophyll Conductance 228
VI. Biochemical Determinants of Mesophyll Conductance 232
A. The Role of Aquaporins (COO-porins) 232
B. The Role of Carbonic Anhydrase (CAs) 234
C. The Potential Role of Other Biochemical Processes 234
VII. Environmental Responses of Mesophyll Conductance 235
VIII. Conclusions 237
References 240
Chapter 8: Molecular Mechanisms Affecting Cell Wall Properties and Leaf Architecture 253
I. Introduction 256
A. Leaf Growth and Architecture 256
B. Alterations in Leaf Growth and Architecture Mediated by CAMTA/SA, PHYB/GA/PIF, and JAZ/JA Upstream Molecular Signaling Pathways 257
II. Regulation of Cell Wall Composition 260
A. Alterations in Cellulose Synthase Gene Expression 262
B. Potential PIF Mediated Effects on CESA and CESL Expression 265
III. Regulation of Cortical Microtubule and Microfilament Organization 265
A. Genes That Regulate Microtubule Alignment 266
B. Regulation of F-Actin Formation and Abundance 268
C. Potential PIF Mediated Effects on Fine F-Actin Network and Microtubule Bundle Formation 272
IV. Cross-Linkages Between Different Cell Wall Constituents 274
A. Xyloglucan Endotransglucosylase/Hydrolase 275
1. XTH as a Key Downstream Point of Execution of Leaf Architectural Changes, and Its Modulation by CAMTA/SA, JAZ/JA and PHYB/GA/PIF 276
B. Regulation of Ca2+ Mediated Cross-Linking of Pectin 279
1. Pectin Methylesterase and Pectin Methylesterase Inhibitor 279
2. Pectin Methyltransferase 279
3. PMT/PME/PMEI System as a Key Downstream Execution Point of Leaf Architectural Changes and Its Modulation by CAMTA/SA, JAZ/JA, and PHYB/GA/PIF 280
V. Broader Implications of Understanding Genes and Molecular Mechanisms That Affect Cell Wall Properties and Leaf Architecture 284
A. Mesophyll Architecture and Its Impact on CO2 Availability at Rubisco and Area-Based Photosynthesis 284
B. Mesophyll Architecture and Its Impact on Area-Based Respiration and Daily C Gain 285
C. Leaf Architecture and Its Impact on Light Capture, Whole-Plant Photosynthesis, and Growth 286
D. Genes Such as CGR2 and CGR3 That Alter Cell Wall Properties Can Modulate the Relationship Between Photosynthesis and Growth 288
VI. Conclusions 290
References 291
Chapter 9: Significance of C4 Leaf Structure at the Tissue and Cellular Levels 298
I. Introduction 299
II. The C4 Leaf 300
A. Leaf Structures in Kranz-Type C4 Plants 300
B. Leaf Structure of Single-Cell C4 Plants 300
III. Evolution of C4 Leaf Structure 302
A. Leaf Anatomical Traits: Preconditions for C4 Evolution 302
1. Low Interveinal Distance 303
2. Decrease in Mesophyll to Bundle Sheath Cell Area 304
B. Sub-cellular Changes During Evolutionary Transition from C3 to C4 Leaf Anatomy 304
1. Preconditional Sub-cellular Anatomy in C3 Plants 304
2. Proto-Kranz Anatomy 305
3. Sub-cellular Structure of C2 Photosynthetic Plants 305
4. Sub-cellular Structure of C4-like Plants 306
IV. Tissue Structure and Function 307
A. Leaf Structural Influence on Gas and Metabolite Movement within a C4 Leaf 307
1. Mesophyll CO2 Conductance 307
2. Leakiness and Metabolite Flux 309
3. Plasmodesmata and Metabolite Flux 310
V. Cell 311
A. Differential Positioning of Organelles in M and BS Cells of C4 Plants 311
1. Mesophyll Chloroplasts 311
2. Bundle Sheath Chloroplasts 312
3. Bundle Sheath Mitochondria 312
B. Maintenance Mechanism for the Localization of BS Chloroplasts 313
1. In Case of Kranz-Type C4 Plants 313
2. In Case of Single-Cell C4 Plants 314
C. Aggregative Movement of C4 Mesophyll Chloroplasts 314
VI. Conclusions 316
References 317
Chapter 10: Functional Anatomical Traits of the Photosynthetic Organs of Plants with Crassulacean Acid Metabolism 323
I. Introduction 324
II. Convergence of CAM Across Diverse Phylogenies 326
III. Succulence and Diversity in Anatomy and Morphology of CAM Species 327
A. The Succulence Syndrome 327
B. Succulent Traits Have Been Incorporated into a Variety of Different Leaf Anatomies Across CAM Lineages 329
C. CAM Is Found in Specific Cell Types Within the Leaf 329
D. CAM in Photosynthetic Stems 332
E. CAM in Other Photosynthetic Organs 332
IV. Physiological Consequences of Succulence 333
A. Water Use 333
B. Division of Labor Between Hydrenchyma and Chlorenchyma: Implications for CAM and Water Use 334
C. CO2 Uptake and Carbon Gain 335
V. Vasculature and Hydraulic Traits of Photosynthetic Organs of CAM Plants 336
A. Venation Patterns 336
B. Hydraulic Traits 337
VI. Stomatal Traits in CAM Plants 338
A. Stomatal Patterning 338
B. Physiological Implications of Stomatal Patterning 339
VII. Engineering Anatomical Traits That Are Conducive to CAM 340
VIII. Conclusions 342
References 342
Chapter 11: Trade-offs and Synergies in the Structural and Functional Characteristics of Leaves Photosynthesizing in Aquatic Environments 348
I. Introduction 349
II. Adaptation of Aquatic Plants to the Environmental Challenges and Opportunities in Water 350
A. Evolution of Aquatic Embryophytes 350
B. Comparison of Air and Water as Environments for Photosynthesis and Growth 351
III. Response of Leaf Morphology, Structure, and Composition to Aquatic Environments 355
A. Leaf Morphology 355
B. Leaf Structure 355
C. Leaf Composition 360
1. Nitrogen and Phosphorus 360
2. Cell Walls 361
3. Storage Compounds 361
4. Regulation of Leaf Form and Structure 362
IV. Resource Acquisition and Responses to Aquatic Environments 363
A. Light Acquisition 363
B. Carbon Acquisition 364
1. C3 Metabolism 364
2. Avoidance Strategies 366
3. Exploitation Strategies 366
4. Amelioration Strategies 366
C4 Metabolism 366
CAM 369
Bicarbonate Use 370
V. Trade-Offs, Synergies, and Future Prospects 372
A. Trade-Offs 372
B. Synergies 373
C. Future Prospects 374
VI. Conclusions 375
References 375
Chapter 12: Leaf Photosynthesis of Upland and Lowland Crops Grown under Moisture-Rich Conditions 385
I. Introduction 386
A. Plant Responses to Water Stress 386
B. Water Uptake and Transport by Plants 387
C. Individual-Leaf Photosynthesis 388
II. Rice 389
A. Characteristics of Rice-Water Relationships 389
B. Photosynthetic Characteristics of High-Yielding Rice 390
1. Photosynthetic Capacity 393
2. Midday and Afternoon Depression of Photosynthesis 393
3. Depression of Photosynthesis During Senescence 394
C. Quantitative Trait Loci (QTLs) That Increase Photosynthesis, and Their Functions 395
1. Detecting QTLs That Increase the Rate of Photosynthesis by Using Rice Cultivars with a High Photosynthetic Rate 395
2. Introgression of QTLs to Enhance Photosynthesis 397
III. Upland Crops 398
A. Distribution of Seasonal Precipitation and Water Relations of Upland Crops 398
B. Growth Response of Soybeans 400
1. Growth and Photosynthesis of Plants in the Irrigated and Water-Deficient Plots Before Flowering 402
2. Growth and Photosynthesis of Plants in Irrigated and Water-Deficient Plots After Flowering 402
C. Growth Response of Wheat 403
1. Growth of Plants in Irrigated and Water-­Deficient Plots Before Flowering 403
2. Growth and Photosynthesis of Plants in Irrigated and Water-Deficient Plots After Flowering 403
IV. Conclusions 405
References 405
Chapter 13: Photosynthesis in Poor Nutrient Soils, in Compacted Soils, and under Drought 410
I. Limiting Nutrients 411
A. Photosynthesis and Nitrogen Deficiency 411
B. Photosynthesis and Phosphorous Deficiency 413
C. Photosynthesis and Potassium Deficiency 415
D. Photosynthesis and Iron Deficiency 416
E. Photosynthesis and Manganese Deficiency 417
F. Photosynthesis and Copper Deficiency 418
G. Photosynthesis and Zinc Deficiency 419
II. Photosynthesis in Compacted Soils 419
III. Photosynthesis Under Drought 422
IV. The Case of Carnivorous Plants 423
V. Conclusions 428
References 430
Chapter 14: The Role of Leaf Movements for Optimizing Photosynthesis in Relation to Environmental Variation 439
I. Introduction and Overview 440
II. A Classification of Leaf Movements 441
A. Leaf Movements as a Consequence of Differential Cell Growth 441
1. Phototropism 443
2. Gravitropism 443
3. Hydrotropism 444
4. Thigmotropism 444
5. Epinastic Growth 444
6. Compass Plants 444
B. Movements Due to Cell Physiological Changes 445
1. Tropic Movements Toward or Away from a Stimulus – Heliotropism 445
2. Nastic Movements in Response to a Stimulus 446
Thermonastic 446
Nyctinastic 446
Hyponastic 446
Thigmonastic 447
3. Movements Due to Anatomical Structure 447
Leaf Fluttering 447
Hydronastic 447
III. Relationships Between Leaf Photosynthesis and Leaf Movements 447
A. Effects of Leaf Movements on Diurnal Patterns of Leaf Photosynthesis 449
B. Avoiding Stress on Photosynthetic Performance 450
1. Avoiding over Excitation of the Photosystems 450
2. Avoiding Overheating or Nocturnal Freezing 453
3. Avoiding Low Water Potential, Conserving Water, and Maintaining WUE 454
IV. Conclusions 455
References 457
Chapter 15: Photosynthetic and Photosynthesis-Related Responses of Japanese Native Trees to CO2: Results from Phytotrons, Open-Top Chambers, Natural CO2 Springs, and Free-Air CO2 Enrichment 462
I. Introduction 464
II. Sensitivity of Japanese White Birch Leaves Grown under Elevated CO2 and Long-Term Drought to PS II Photoinactivation 464
A. Introduction 464
B. Leaf Physiological Acclimation to Long-Term Drought 465
C. Excess Energy in Plants Grown Under Long-Term Drought and Elevated CO2 465
D. Impacts of Drought and Elevated CO2 466
III. Effects of Long-Term Exposure to High CO2 Springs in Japan 467
A. Introduction: CO2 Springs 467
B. In situ Ecophysiological Traits in CO2 Spring Plants 469
C. Genetic Variation in Plant Traits Between High and Normal CO2 Plants 470
D. Implications 472
IV. Photosynthesis and Other Processes in Young Deciduous Trees Grown under Elevated CO2 473
A. Introduction 473
B. Photosynthetic Responses of Trees to Elevated CO2 473
C. Allocation of Photosynthates to Roots 474
D. Plant Defense: Disease and Insect Herbivores 475
E. Roles of Symbionts 476
F. Change in Forest Structure Through Changes in Leaf Area Index 477
G. Stand Structure and Regeneration Success 477
H. Methane Emission from Forests at Elevated CO2 478
I. Further Considerations 478
V. Conclusion 479
References 480
Chapter 16: The Leaf Economics Spectrum and its Underlying Physiological and Anatomical Principles 487
I. Introduction 488
II. Leaf Economics Spectrum 489
A. Mass-Based Traits 489
B. Area-Based Traits 492
C. Photosynthetic N Use Efficiency 494
III. Physiological and Structural Basis Underlying LES 494
A. Cell Walls 496
B. Leaf N Allocation 497
C. Mesophyll Diffusion Conductance 499
D. Relative Influence 502
IV. Conclusions 503
References 504
Chapter 17: Leaf Photosynthesis Integrated over Time 508
I. Introduction 509
II. Leaf Longevity – Optimizing Model for Carbon Gain 509
A. Parameter a and Mean Labor Time 510
B. Instantaneous Photosynthetic Rate per Unit Leaf Area, Aarea 510
C. Potential Leaf Longevity or Parameter b 511
D. Construction Costs and Parameter C 512
E. Leaf Mass per Area (LMA) 513
F. Leaf Economic Spectrum (LES) 515
III. Extension of the Model to Seasonal Environments 515
A. Favorable Period (f) 515
B. Functional Leaf Longevity (Lf) 516
C. Leaf Lifetime Performance 516
IV. Plant Size, Plant Performance and L 519
A. Normalization Constant of Allometry 519
B. Relative Growth Rate 519
V. Ecosystems 520
A. Productivity of a Stand 520
B. Longevity of Fallen Leaves in Ecosystems 521
C. Comparison of Ecosystems 522
VI. Biogeographical Patterns 522
VII. Conclusions 524
References 525
Chapter 18: Photosynthetic Modulation in Response to Plant Activity and Environment 528
I. Introduction 530
II. Photosynthesis in the Context of Whole Plant Source and Sink Strength 532
A. Alteration of Source Strength 533
1. Partial Shading, Defoliation, or Girdling 533
2. Continuous Light 533
3. Sugar Feeding 534
4. Elevated Level of Carbon Dioxide 534
5. Decreased Light Harvesting 535
B. Alteration of Sink Strength 535
1. Root Activity 535
2. Synthesis of Leaf-Localized Molecules 537
3. Sink Removal 538
4. Shoot, Branch, or Petiole Girdling 539
5. Genetic Engineering Approaches 539
6. Pruning and Fire 540
III. Adjustment of Photosynthesis in Response to the Abiotic Environment 540
A. Light 541
B. Temperature 544
C. Water Availability 550
D. Salinity 551
E. Nutrients 552
F. Pollution 552
G. Herbicides 552
IV. Adjustment of Photosynthesis in Response to the Biotic Environment 553
A. Competition 553
B. Herbivory 554
C. Pathogens 556
D. Induced Galls and Tumors 557
E. Tapping of Vascular Tissues by Insects and Parasitic Plants 557
F. Witches’ Brooms 560
G. Symbioses with Fungi and Bacteria 560
V. Conclusions 561
References 562
Subject Index 599