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Annual Plant Reviews, Volume 48, Phosphorus Metabolism in Plants

William Plaxton (Editor), Hans Lambers (Editor)
ISBN: 978-1-118-95885-8
480 pages
June 2015, Wiley-Blackwell
Annual Plant Reviews, Volume 48, Phosphorus Metabolism in Plants (1118958853) cover image

Description

The development of phosphorus (P)-efficient crop varieties is urgently needed to reduce agriculture's current over-reliance on expensive, environmentally destructive, non-renewable and inefficient P-containing fertilizers. The sustainable management of P in agriculture necessitates an exploitation of P-adaptive traits that will enhance the P-acquisition and P-use efficiency of crop plants. Action in this area is crucial to ensure sufficient food production for the world’s ever-expanding population, and the overall economic success of agriculture in the 21st century.

This informative and up-to-date volume presents pivotal research directions that will facilitate the development of effective strategies for bioengineering P-efficient crop species. The 14 chapters reflect the expertise of an international team of leading authorities in the field, who review information from current literature, develop novel hypotheses, and outline key areas for future research. By evaluating aspects of vascular plant and green algal P uptake and metabolism, this book provides insights as to how plants sense, acquire, recycle, scavenge and use P, particularly under the naturally occurring condition of soluble inorganic phosphate deficiency that characterises the vast majority of unfertilised soils, worldwide. The reader is provided with a full appreciation of the diverse information concerning plant P-starvation responses, as well as the crucial role that plant–microbe interactions play in plant P acquisition.

Annual Plant Reviews, Volume 48: Phosphorus Metabolism in Plants is an important resource for plant geneticists, biochemists and physiologists, as well as horticultural and environmental research workers, advanced students of plant science and university lecturers in related disciplines. It is an essential addition to the shelves of university and research institute libraries and agricultural and ecological institutions teaching and researching plant science.

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Table of Contents

List of Contributors xvii

Preface xxiii

Section I Introduction

1 Phosphorus: Back to the Roots 3
Hans Lambers and William C. Plaxton

1.1 Introduction 3

1.2 Phosphorus or phosphorous? 4

1.3 Phosphorus on a geological time scale 6

1.4 Phosphorus as an essential, but frequently limiting, soil nutrient for plant productivity 7

1.5 Soil phosphorus pools 9

1.6 Soil phosphorus mobility 10

1.7 Factors determining rates of phosphorus uptake by roots 11

1.8 Phosphorus-starvation responses: does phosphorus homeostasis exist? 13

1.9 Concluding remarks 14

Acknowledgements 15

References 15

Section II P-Sensing, Transport, and Metabolism

2 Sensing, Signalling, and Control of Phosphate Starvation in Plants: Molecular Players and Applications 25
Wolf-Rüdiger Scheible and Monica Rojas-Triana

2.1 Introduction 25

2.2 The plant phosphate-starvation response 26

2.3 Sensing of phosphate and other macronutrient limitations in plants 29

2.3.1 Nutrient transporters as sensors/receptors 29

2.3.2 Local Pi sensing and signalling at the root tip by PDR2/LPR1 31

2.3.3 Phosphite, a tool to investigate P-sensing/signalling 31

2.4 Signalling of phosphate limitation 32

2.4.1 The role of phytohormones 33

2.4.2 Systemic signalling during P-starvation 37

2.4.3 Transcriptional regulators involved in P-signalling and affecting P-starvation responses 39

2.4.4 The role of microRNAs and targeted protein degradation in P-signalling 41

2.4.5 Additional regulators of P-signalling 43

2.5 Improving plant P-acquisition and -utilization efficiency: approaches and targets 44

2.6 Concluding remarks 48

References 49

3 ‘Omics’ Approaches Towards Understanding Plant Phosphorus Acquisition and Use 65
Ping Lan, Wenfeng Li and Wolfgang Schmidt

3.1 Introduction 66

3.2 Towards a transcriptomics-derived ‘phosphatome’ 67

3.3 Pi deficiency-induced alterations in the proteome 77

3.4 Core PSR proteins 80

3.5 Membrane lipid remodelling: insights from the transcriptome, the proteome, and the lipidome 83

3.6 Genome-wide histone modifications in Pi-deficient plants 86

3.7 Conclusions and outlook 89

3.8 Acknowledgements 90

References 90

4 The Role of Post-Translational Enzyme Modifications in the Metabolic Adaptations of Phosphorus-Deprived Plants 99
William C. Plaxton and Michael W. Shane

4.1 Introduction 100

4.2 In the beginning there was protein phosphorylation 101

4.3 Monoubiquitination has emerged as a crucial PTM that interacts with phosphorylation to control the function of diverse proteins 104

4.4 Post-translational modification of plant phosphoenolpyruvate carboxylase by phosphorylation versus
monoubiquitination 107

4.4.1 Activation of PEP carboxylase by in-vivo phosphorylation appears to be a universal aspect of
the plant P-starvation response 107

4.4.2 PEP carboxylase monoubiquitination: an old dog learns new tricks 109

4.4.3 Reciprocal control of PEP carboxylase by in-vivo monoubiquitination and phosphorylation in
developing proteoid roots of P-deficient harsh hakea 111

4.5 Glycosylation is a sweet PTM of glycoproteins 114

4.5.1 A pair of AtPAP26 glycoforms is upregulated and secreted by P-deprived Arabidopsis 115

4.5.2 The AtPAP26-S2 glycoform copurifies with, and appears to interact with, a curculin-like lectin 116

4.6 Concluding remarks 117

Acknowledgements 118

References 119

5 Phosphate Transporters 125
Yves Poirier and Ji-Yul Jung

5.1 Introduction 125

5.2 The PHT1 transporters 126

5.2.1 PHT1 structure, activity, and expression patterns 126

5.3 Control of PHT1 activity 130

5.3.1 Control of PHT1 transcript levels 130

5.3.2 Post-transcriptional control of PHT1 133

5.4 PHO1 and phosphate export 136

5.4.1 PHO1 structure, activity, and expression patterns 136

5.4.2 Transcriptional control of PHO1 expression 139

5.4.3 Post-transcriptional control of PHO1 139

5.5 Phosphate transporters of organelles 140

5.5.1 Mitochondrial phosphate transporters 140

5.5.2 Plastidial phosphate transporters 141

5.5.3 The role of PHT2 in plastid phosphate transport 143

5.5.4 The role of PHT4 in plastid phosphate transport 143

5.6 Phosphate transporters of other organelles 145

5.6.1 Golgi phosphate transporters 145

5.6.2 Peroxisomal phosphate transporters 146

5.6.3 Vacuolar (tonoplast) phosphate transporters 146

5.7 Concluding remarks 146

Acknowledgements 147

References 147

6 Molecular Components that Drive Phosphorus-Remobilisation During Leaf Senescence 159
Aaron P. Smith, Elena B. Fontenot, Sara Zahraeifard and Sandra Feuer DiTusa

6.1 Introduction 159

6.2 Transcriptomes of senescence and phosphate-deficiency 160

6.3 Major biochemical components that mediate P-remobilisation during leaf senescence 162

6.3.1 Nucleases 163

6.3.2 Phosphatases 166

6.3.3 Lipid-remodelling enzymes 168

6.3.4 Pi transporters 169

6.4 Regulatory and signalling components of senescing leaves 170

6.4.1 Transcription factors 170

6.4.2 The SPX superfamily 173

6.4.3 Ubiquitination components and miRNAs 174

6.5 Role of hormones during leaf senescence 175

6.5.1 Ethylene and strigolactones 175

6.5.2 Abscisic acid 176

6.5.3 Cytokinins 176

6.6 Concluding remarks 176

Acknowledgements 177

References 177

7 Interactions Between Nitrogen and Phosphorus Metabolism 187
John A. Raven

7.1 Introduction 188

7.2 Roles of N and P in plants and the extent to which compounds containing N or P can be substituted by compounds lacking N or P 188

7.3 Variability in the N:P ratio in plants and its metabolic and ecological significance 195

7.3.1 Fixed N:P ratios: the role of compounds containing both N and P 195

7.3.2 Protein:RNA ratio, organism N:P ratio, the Growth Rate Hypothesis 197

7.3.3 Organism N and P concentration as a function of external supply of N and P 200

7.3.4 Conclusions 201

7.4 Interactions in N and P acquisition and assimilation 201

7.4.1 Structures involved in acquisition of N and P 202

7.4.2 Secretion of enzymes and organic anions facilitates root N and P acquisition 204

7.5 Protein synthesis and protein degradation during P-deprivation: significance for N–P interaction 207

7.6 General conclusions 207

Acknowledgements 208

References 208

Section III P-deprivation Responses

8 Metabolomics of Plant Phosphorus-Starvation Response 217
Chris Jones, Jean-Hugues Hatier, Mingshu Cao, Karl Fraser and Susanne Rasmussen

8.1 Introduction 218

8.2 Metabolomic approaches 219

8.3 Metabolomic analysis platforms 220

8.4 Data analysis 222

8.5 Metabolomics strategies directed at dissecting responses to P starvation 223

8.6 Opportunities for metabolomics to contribute to the development of P-efficient crops 229

8.7 Future prospects 230

Acknowledgements 231

References 231

9 Membrane Remodelling in Phosphorus-Deficient Plants 237
Meike Siebers, Peter Dörmann and Georg Hölzl

9.1 Introduction 237

9.2 Membrane lipid remodelling during phosphate deprivation 238

9.3 Monogalactosyldiacylglycerol (MGDG) 242

9.4 Digalactosyldiacylglycerol (DGDG) 243

9.5 Sulfolipid (SQDG) and glucuronosyldiacylglycerol (GlcADG) 247

9.6 Phospholipid degradation by phospholipase D and phosphatidate phosphatase 248

9.7 Phospholipase C (PLC) 249

9.8 Acyl hydrolases 250

9.9 Lipid trafficking under phosphate starvation 250

9.10 Glucosylceramide, sterol glucoside, and acylated sterol glucoside 253

9.11 The role of auxin in remodelling of membrane lipid composition 254

9.12 Improved Pi status by symbiosis with arbuscular mycorrhizal fungi 255

9.13 Outlook 255

References 256

10 The Role of Intracellular and Secreted Purple Acid Phosphatases in Plant Phosphorus Scavenging and Recycling 265
Jiang Tian and Hong Liao

10.1 Introduction 266

10.2 Bioinformatics and structural analysis of plant PAPs 266

10.2.1 PAP bioinformatics 266

10.2.2 Structural biochemistry of plant PAPs 269

10.3 Biochemical characterisation of plant PAPs 269

10.4 Diverse subcellular localisation of plant PAPs 271

10.5 Transcriptional and post-transcriptional regulation of PAP expression by P availability 275

10.5.1 Complex signal transduction pathways integrate nutritional P status with PAP expression 276

10.5.2 Post-translational PAP modification 277

10.6 Functional analysis of PAPs involved in P mobilization and utilisation 278

10.7 Perspectives 281

Acknowledgements 282

References 282

11 Metabolic Adaptations of the Non-Mycotrophic Proteaceae to Soils With Low Phosphorus Availability 289
Hans Lambers, Peta L. Clode, Heidi-Jayne Hawkins, Etienne Laliberté, Rafael S. Oliveira, Paul Reddell, Michael W. Shane, Mark Stitt and Peter Weston

11.1 Introduction 290

11.2 Phosphorus nutrition of Proteaceae, with a focus on south-western Australia 291

11.2.1 Phosphorus acquisition by non-mycorrhizal roots: cluster roots 291

11.2.2 Proteaceae species that do not produce cluster roots 298

11.2.3 Phosphorus toxicity 299

11.2.4 High rates of photosynthesis despite low leaf P concentrations 300

11.2.5 Leaf longevity 307

11.2.6 Delayed greening 308

11.2.7 Efficient and proficient P remobilisation from senescing organs 310

11.2.8 Seed Preserves 311

11.3 Comparison of species of Proteaceae in south-western Australia with species elsewhere 312

11.3.1 The Cape Floristic Region in South Africa 312

11.3.2 Eastern Australia 314

11.3.3 Southern South America 316

11.3.4 Brazil 317

11.4 Perspectives 318

Acknowledgements 323

References 323

12 Algae in a Phosphorus-Limited Landscape 337
Arthur R. Grossman and Munevver Aksoy

12.1 Introduction 338

12.2 P-deprivation responses of green algae and vascular plants 339

12.2.1 Phosphatases 342

12.2.2 Nucleases 346

12.2.3 Pi transport 348

12.2.4 Polyphosphates 350

12.2.5 Phospholipids 351

12.3 Control of P deprivation responses 353

12.3.1 PSR1-dependent gene expression in P-starved algae 356

12.3.2 Low-phosphate bleaching mutants 358

12.4 Future prospects 359

Acknowledgements 360

References 360

Section IV Significance of Plant–Microbe Interactions for P-Acquisition and Metabolism

13 Impact of Roots, Microorganisms and Microfauna on the Fate of Soil Phosphorus in the Rhizosphere 377
Philippe Hinsinger, Laetitia Herrmann, Didier Lesueur, Agnès Robin, Jean Trap, Kittima Waithaisong and Claude Plassard

13.1 Introduction 378

13.2 Spatial extension of the rhizosphere 378

13.2.1 Root architecture and growth 379

13.2.2 Root hairs and mycorrhizas 380

13.2.3 Root growth-promoting effect of rhizosphere biota 381

13.3 Mobilisation of inorganic P in the rhizosphere 385

13.3.1 Effect of rhizosphere pH changes 385

13.3.2 Effect of exudation of carboxylates 387

13.4 Mobilisation of organic P in the rhizosphere 389

13.4.1 Effects of phosphatases 390

13.4.2 Effects of phytases 391

13.5 Microbial P, microbial loop, and P recycling in the rhizosphere 393

13.5.1 Abiotic processes 393

13.5.2 Biotic processes 394

13.6 Conclusions and future prospects 397

References 398

14 Mycorrhizal Associations and Phosphorus Acquisition: From Cells to Ecosystems 409
Sally E. Smith, Ian C. Anderson and F. Andrew Smith

14.1 Introduction 410

14.2 Arbuscular mycorrhizas 413

14.2.1 Establishment of the symbiosis 413

14.2.2 Specialised AM interfaces in soil and roots are critical for P uptake 413

14.2.3 The AM pathway in plant P nutrition 416

14.2.4 The ‘mutualism–parasitism’ continuum 417

14.2.5 Some higher-scale issues in AM symbiosis 418

14.2.6 Significance of AM symbioses in agriculture and horticulture 419

14.3 Ectomycorrhizas 421

14.3.1 Establishment of the symbiosis 421

14.3.2 Roles of ectomycorrhizas in plant P nutrition 422

14.3.3 ECM phosphate transporters 423

14.3.4 Solubilisation of inorganic phosphates by ECM fungi 425

14.3.5 Mobilisation of organic-P sources by ECM fungi 426

14.3.6 ECM symbioses and forest tree P nutrition: future challenges 428

14.4 Conclusions 429

References 430

Index 441

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Author Information

About the Editors

William Plaxton is currently a Full Professor and Queen’s Research Chair in the Department of Biology at Queen’s University, Kingston, Canada. Hans Lambers is Professor of Plant Physiological Ecology in the School of Plant Biology at the University of Western Australia, Perth, Australia.

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