Evolution of Plant Physiology (eBook)

Cover 1
Contents 6
List of contributors 8
Preface 12
The origins of plant physiology 12
Evolution of plant physiology from the molecular level 12
Evolution of anatomical physiology 13
Evolution of environmental and ecosystem physiology 13
Part I The Origins of Plant Physiology 16
1 Turning the land green: inferring photosynthetic physiology and diffusive limitations in early bryophytes 18
Introduction 18
Phylogeny of bryophytes 19
Rubisco: a discriminating marker for photosynthetic metabolism 20
Life on land: caught in a compromising situation 23
Why is there no biophysical CCM in terrestrial plants other than hornworts? 23
Comparative physiology of bryophyte photosynthesis 24
Conclusions 27
Acknowledgements 28
References 28
2 Physiological evolution of lower embryophytes: adaptations to the terrestrial environment 32
Introduction 32
The ancestors of embryophytes 33
Water, carbon dioxide and energetics of land plants 34
Desiccation tolerance, desiccation intolerance, poikilohydry and homoiohydry 37
Poikilohydry of algae and early-evolving embryophytes 37
Desiccation tolerance and intolerance 42
Evolution of homoiohydry 43
History of physiological interpretations of early embryophytes 46
Introduction 46
Transpiration rate and endodermal function in regulating nutrient supply to the shoot 48
Mechanism of endohydric water movement 49
Role of stomata in determining the rate of photosynthesis and the water cost of photosynthesis 50
Conclusions 52
Acknowledgements 52
References 53
3 Origin, function and development of the spore wall in early land plants 58
Introduction 58
Origin of the spore wall 59
Function of the spore wall 60
Spore wall development 61
Basic mechanisms of spore wall formation 61
Substructural organization of spore walls 63
Spore wall formation in extant plants 63
Spore wall formation in early land plants 67
Molecular genetics of spore wall development 70
Conclusions 74
Acknowledgements 75
References 75
Part II Evolution of Plant Physiology from the Molecular Level 80
4 The evolution of plant biochemistry and the implications for physiology 82
Introduction 83
Molecular evolution, biochemical evolution and metabolic evolution – hierarchical terms 83
Metabolic evolution – what determines whether a new enzyme is retained? 84
Biomolecular activity – the evolution of ‘secondary metabolism’ 84
Molecules retained because of their physicochemical properties 85
Primary metabolism – canalized metabolism, each step depending on other pre-existing metabolic capabilities 86
Selection for different molecular properties has consequences for metabolic evolution 86
Biochemical evolution and physiology 87
The interaction of plants with other organisms 88
The human experience 88
Plant/microbe and plant/insect interactions 89
The evolution of regulatory systems for secondary metabolism 91
A speculative scenario for the evolution of the control of pathways leading to compounds retained because they possess biomolecular activity 92
Signalling molecules within plants 93
The link between secondary metabolism and hormonal control 93
Are plant hormones ‘secondary metabolites’? 93
Gibberellin synthesis – generating diversity? 95
Plant hormone degradation – another role? 96
Summary 96
Acknowledgements 97
References 97
5 Did auxin play a crucial role in the evolution of novel body plans during the Late Silurian–Early Devonian radiation of land plants? 100
Introduction 100
Brief overview of Cambrian radiation of bilateral animals 101
Rapid diversification of animal phyla 101
Characteristic body plan of each phylum 101
Early establishment of body plan 102
Altered expression of embryonic genes resulting in new body plans 102
Silurian–Devonian radiation of land plants 103
Did early land plants diverge in a rapid evolutionary radiation? 103
Are the characteristic body plans of land plants established during embryonic development? 105
What developmental mechanisms act to generate plant body plans? 111
Did major changes in auxin regulation occur prior to the Silurian–Devonian radiation? 114
Conclusions 116
Acknowledgements 117
References 117
6 Aquaporins: structure, function and phylogenetic analysis 124
Introduction 124
Transport of water across cell membranes 125
Discovery of aquaporins and the MIP-family 126
Structure and function of MIPs 127
MIPs of bacteria, fungi and animals 128
Plant MIPs 130
Phylogenetic analysis 132
Acknowledgement 133
References 133
7 Evolutionary origin of the ethylene biosynthesis pathway in angiosperms 136
Introduction 136
Evolution of the angiosperm ethylene biosynthesis pathway 137
Early responses to stress conditions 137
The role of ACC 138
The acquisition of ACC oxidase 138
How ACC oxidase originated 140
ACC oxidase as a 2-oxoacid-dependent dioxygenase 140
Molecular changes 141
The enzyme ancestral to ACC oxidase 143
When did the ethylene biosynthesis pathway arise? 143
Palaeoclimatic considerations 143
Acknowledgements 144
References 145
8 Structural biomacromolecules in plants: what can be learnt from the fossil record? 148
Introduction 148
Characterizing resistant biomacromolecules 149
Resistant biomacromolecules in outer coverings 151
Algal cell walls 151
Pollen and spore walls 153
Higher land plant leaf and stem cuticles 158
Inner structural entities 161
Water-conducting and strengthening tissues 161
Conclusions 165
References 165
9 Early land plant adaptations to terrestrial stress: a focus on phenolics 170
Introduction 170
Materials and techniques 171
Trait mapping 171
Thioacidolysis 171
Qualitative and quantitative assessment of acid hydrolysis-resistant biomass 172
Fluorescence, scanning and transmission electron microscopy 173
Global estimates of early Palaeozoic resistant and sequestered carbon 173
Results 174
Discussion 177
Conclusions 180
Acknowledgements 180
References 180
Appendix 9.1 Physiological traits related to early stress adaptation in land plants 183
10 Plant cuticles: multifunctional interfaces between plant and environment 186
Introduction 186
The multifunctional interface 189
Transport properties of plant cuticles 190
Organic non-electrolytes 190
Water 191
Ions 193
Wax movement: a simple solution? 193
‘Pores’ or ‘microchannels’ 193
Lipid transfer proteins 194
Wax transport via diffusion 194
Interactions with the biotic and abiotic environment 195
Water repellency and self-cleaning property 196
Water repellency 196
Influence of biotic and non-biotic factors on water repellency 196
Self-cleaning property: the ‘lotus-effect’ 197
Biomechanical properties 200
Acknowledgements 202
References 202
Part III Evolution of Anatomical Physiology 210
11 Falling atmospheric CO2 – the key to megaphyll leaf origins 212
Introduction 212
A mechanism coupling Devonian megaphyll evolution with falling CO[sub(2)]2 214
Early evolution of the megaphyll leaf 217
Quantifying the trends in early megaphyll leaf evolution 223
Discussion 225
Acknowledgements 226
References 226
12 Stomatal function and physiology 232
Introduction 232
Stomatal control of leaf gas exchange 233
Role of stomata in leaf gas exchange 237
Heterogeneity in stomatal characters 239
Effect of environmental variables on stomata and photosynthesis 240
Stomatal response to CO[sub(2)] 241
Stomatal response to humidity 243
Stomatal response to light 245
Environmental interactions and stomatal responses 248
Modern techniques for ecophysiological stomatal research 250
Evolutionary context 251
Conclusion 252
Acknowledgements 253
References 253
13 The photosynthesis.transpiration compromise and other aspects of leaf morphology and leaf functioning within an evolutionary and ecological context of changes inƒ 258
Introduction 259
‘Trade-off’ between photosynthesis and transpiration 259
Desert plants 259
Stomatal response to atmospheric CO[sub(2)] 260
Analysis of the ‘trade-off’ response within a broader context 261
Modern Mediterranean ecosystems 261
Dry season 261
Wet season 262
Prevention of wetting of leaves by rain and facilitation of drying 262
Dripping tip of leaves and position of the leaf 262
Wettability of leaves 263
Avoidance of direct contact between water film and stomata: effect of a hair layer and stomatal wax plugs 263
Further ecological consequences: effect of fungal leaf pathogens and ion leaching 264
Drying of wet leaves by evaporation 264
Formulation of the rate of drying of a wet surface 264
Ecological consequences of leaf morphology on the rate of drying of wet leaves 268
Adaptive changes in leaf morphology in relation to the ‘trade-off’ between photosynthesis and transpiration 269
Final remarks 270
Acknowledgements 270
References 271
14 Xylem hydraulics and angiosperm success: a test using broad-leafed species 274
Introduction 274
Materials and methods 276
Choice of species 276
Physiological studies 276
Water relations 276
Photosynthesis studies 277
Results 278
Discussion 281
References 285
15 Evolution of xylem physiology 288
Introduction 288
‘Trade-off’ triangle 289
Early beginnings 289
Distribution of wood anatomical features 290
Vessel element perforations 290
Diameter, density and length of vessels 292
Ecological preferences in modern woods 292
Type 1 292
Type 2 292
Type 3 293
Type 4 294
Type 5 294
Geological record 295
Experimental work 298
Conductive efficiency versus vulnerability to embolism 298
Conductive efficiency versus mechanical strength 302
Cohesion–tension theory and sap ascent 304
Mechanical strength, implosion resistance and resistance to embolism 304
Roots versus stems 305
Parenchyma 305
Towards a synthesis: the evolution of hydraulic structure and function 305
Acknowledgements 306
References 306
16 Hydraulics and mechanics of plants: novelty, innovation and evolution 312
Introduction 312
Terminology and evolution 313
Turgor 315
The hypodermal sterome 316
Secondary growth 319
Does the appearance of the bifacial vascular cambium represent a key innovation? 324
Lignification and biomechanics of the plant cell wall 325
Reaction wood 327
Hydraulics, mechanics and evolution of the climbing habit 329
Types of climbing strategy 329
Appearance of the lianoid habit 329
Vessels and the climbing habit 330
What is special about lianas? 333
Conclusions 333
Acknowledgements 336
References 336
17 Becoming fruitful and diversifying: DNA sequence phylogenetics and reproductive physiology of land plants 342
Introduction 342
Reproductive ‘Physiology’ 344
Sexual incompatibility systems 347
Self-incompatibility (SI) as a defining angiosperm characteristic 347
SI acting at the stigma 348
SI acting in the style 349
SI in euasterid I 350
Alternative kinds of SI 351
Heteromorphic SI 351
Self-compatibility 352
Conclusion 352
References 353
18 Evolution of angiosperm fruit and seed dispersal biology and ecophysiology: morphological, anatomical and chemical evidence from fossils 358
Introduction 359
Dispersal biology 359
Abiotic – plumes 359
Abiotic – wings 359
Abiotic – dust and microseeds 361
Abiotic – flotation 362
Biotic – dry fruits and seeds 362
Biotic – spines 363
Biotic – fleshy tissues 363
Germination and establishment 364
Embryo and endosperm 364
Radicle emergence 364
Embryo and endosperm development, dormancy and establishment 364
Embryo and endosperm in the order Myrtales 366
Embryo, endosperm and seed internal organization in the order Zingiberales 367
Seedlings 367
Vivipary in Rhizophoraceae 367
Vivipary in Nypa 368
Other seedlings 369
Dormancy versus germination 369
Chemical composition of resistant layers 371
Conclusions 376
Acknowledgements 378
References 378
Appendix 18.1 Palaeogene Plumed Disseminules 387
Apocynospermum-like plumes 387
Other plumes 387
Appendix 18.2 Palaeogene Winged Disseminules 387
Betulaceae (see review in Chen et al., 1999 and also Takhtajan, 1982) 388
Juglandaceae (see Manchester, 1987, 1989a Budantsev, 1994)
Oleaceae 389
Tiliaceae and Tilioideae 389
Ulmaceae 389
Aceraceae/Sapindaceae 389
Caprifoliaceae 390
Other winged disseminules 390
One-sided lateral wings 390
Encircling wings 390
Bilateral wings 391
Multiple wings (‘helicopters/propellers’) 392
Multiple wings (longitudinally arranged) 392
Part IV Evolution of Environmental and Ecosystem Physiology 394
19 The rise and fall of the Podocarpaceae in Australia – a physiological explanation 396
Introduction 396
A physiological approach to the interpretation of the fossil record 397
The fossil record of the Podocarpaceae 397
Podocarpaceae diversity through time 398
Adaptation to low light 401
Cretaceous forest structure at high southern latitudes 404
Constraints on extant Podocarpaceae distributions 404
Synthesis 409
Acknowledgements 411
References 411
20 The adaptive physiology of Metasequoia to Eocene high-latitude environments 416
Introduction 416
Background 417
The Eocene lowland forests of Axel Heiberg Island 417
Metasequoia: fossil and living 421
Physiological challenges of a high-latitude, continuous-light environment 422
Adaptations to Arctic light regimes 422
Carbon balance physiology 423
Site dominance 424
Photoprotection 425
Water balance 425
Comparative ecophysiology of Metasequoia glyptostroboides 425
Foliar morphology and crown architecture 426
Photosynthetic light-response 430
Water-use efficiency: direct measurements and stable isotope data 432
Photosynthetic and accessory pigments 434
Summary: a conceptual model for the success of Metasequoia in Eocene high-Arctic forests 435
Acknowledgements 436
References 436
21 Experimental evaluation of photosystem parameters and their role in the evolution of stand structure and deciduousness in response to palaeoclimate seasonality inƒ 442
Introduction 442
Materials and methods 446
Gas-exchange measurements 446
Stand structure 447
Fossil evidence 448
Light measurements 449
Seedling germination study 449
Results 450
Light environment 450
Gas exchange 450
Stand structure 453
Seedling germination 454
Discussion 454
Acknowledgements 458
References 458
22 Adaptive ancientness of vascular plants to exploitation of low-nutrient substrates – a neobotanical overview 462
Introduction 462
The modern array of low-nutrient habitats 463
The modern diversity of ALVP colonists of low-nutrient habitats 465
Taxonomic distribution 465
Habitat distribution 465
Responses to cultivation 469
Discussion 471
Advantages of low-nutrient toleration for survival of ALVPs 472
Ancientness of low-nutrient toleration 473
Theoretical perspectives 475
Conclusions 476
Acknowledgements 476
References 476
23 The evolution of aluminium accumulation in angiosperms 482
Aluminium in the environment and its toxicity for plants 482
What are Al accumulators? 483
The distribution of Al accumulators in flowering plants 484
Al accumulation: a useful character in plant systematics 485
The ecology of Al accumulators 487
The evolution of heavy metal accumulation 489
The wider relevance of studies on Al accumulation 490
General conclusion 490
Acknowledgements 491
References 491
Index 496
A 496
B 497
C 497
D 499
E 499
F 500
G 500
H 500
I 501
J 501
K 501
L 501
M 502
N 503
O 503
P 503
Q 505
R 505
S 505
T 506
U 507
V 507
W 507
X 507
Y 507
Z 507
Colour Plates 508