Amino Acids in Higher Plants

Amino Acids in Higher Plants

Amino Acids in Higher Plants

Edited by

J.P.F. D’Mello

Formerly of SAC, University of Edinburgh King’s

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Library of Congress Cataloging-in-Publication Data

Amino acids in higher plants / edited by J.P.F. D’Mello.

pages cm

Includes bibliographical references and index.

ISBN 978-1-78064-263-5 (alk. paper)

1.  Amino acids. 2.  Plants--Metabolism.  I. D’Mello, J.P. Felix.

QK898.A5A56 2015

572′.65--dc23

2014033212

ISBN-13: 978 1 78064 263 5

Commissioning editor: Rachel Cutts

Assistant editor: Alexandra Lainsbury

Production editor: James Bishop

Typeset by SPi, Pondicherry, India

Printed and bound in the UK by CPI Group (UK) Ltd, Croydon, CR0 4YY

v

Contents

Contributors xix

Preface xxiii

Glossary xxvii

PART I ENZYMES AND METABOLISM

1 Glutamate Dehydrogenase 1

G.O. Osuji and W.C. Madu

1.1 Abstract 1

1.2 Introduction 2

1.3 Glutamate Dehydrogenase Structure and Localization 2

1.4 Control Plants and Control Glutamate Dehydrogenase 3

1.5 Availability of Ammonium Ions 4

1.5.1 Ammonium ion contents of experimental tissues and plants 4

1.5.2 Glutamate deamination in mitochondria 5

1.6 Glutamate Dehydrogenase-Linked Schiff Base Amination Complex 5

1.6.1 Pesticide treatment and ammonium ion fertilization 5

1.6.2 Pesticide treatment, ammonium ion fertilization and protein contents 6

1.7 Protect the Glutamine Synthetase-Glutamate Synthase Cycle in

Glutamate Dehydrogenase Research 7

1.8 Molecular Biology of Glutamate Dehydrogenase 8

1.8.1 The supply of a-ketoglutarate from the citric acid cycle

to glutamate dehydrogenase and glutamate synthase 8

1.8.2 Aminating and deaminating activities 16

1.8.3 Amination-based crop yield doubling biotechnology 19

1.8.4 The aminating cassette of glutamate dehydrogenase isoenzymes 19

1.9 Food Security 20

1.10 Conclusions 23

Acknowledgements 24

References 24

vi Contents

2 Alanine Aminotransferase: Amino Acid Metabolism in Higher Plants 30

A. Raychaudhuri

2.1 Abstract 30

2.2 Introduction 30

2.3 Structure and Functions of Alanine 31

2.3.1 Structure of alanine 31

2.3.2 Functions of alanine 31

2.4 Alanine Metabolism 32

2.4.1 Alanine metabolism by alanine aminotransferase 33

2.5 Specific Cellular and Sub-cellular Functions of Alanine

Aminotransferase 33

2.5.1 Homologues and tissue localization 34

2.5.2 Sub-cellular localization 35

2.6 A Phylogenetic Analysis of Alanine Aminotransferase 35

2.7 Purification of Alanine Aminotransferase 36

2.8 Protein Characterization of Alanine Aminotransferase 36

2.8.1 Subunits and substrate specificities 36

2.8.2 Kinetics and reaction mechanism 38

2.8.3 Inhibitors of the enzyme 43

2.8.4 Crystal structure 44

2.9 Diverse Roles of Alanine Aminotransferase in Plants 45

2.9.1 Roles in metabolism 45

2.9.1.1 Roles in carbon metabolism 45

2.9.1.2 Roles in photorespiration 47

2.9.1.3 Role in nitrogen use efficiency 48

2.9.2 Role in stress biology 48

2.9.2.1 Roles in hypoxia 49

2.9.2.2 Other abiotic and biotic stresses 50

2.10 Conclusions 50

References 52

3 Aspartate Aminotransferase 57

C.D. Leasure and Z-H. He

3.1 Abstract 57

3.2 Introduction 57

3.3 The Vitamin B6 Cofactor 58

3.4 Enzyme Function 58

3.4.1 The reaction mechanism 60

3.4.2 Enzyme properties 61

3.5 Enzyme Structure 61

3.5.1 K258 61

3.5.2 R292* 61

3.5.3 R386 61

3.5.4 D222 62

3.5.5 Y225 62

3.6 Enzyme Genetics 62

3.7 The Enzyme during Plant Development 63

3.8 The Role of Aspartate in Plants 63

3.8.1 C4 metabolism 64

3.9 Other Roles of Aspartate Aminotransferase 64

3.9.1 Moonlighting 64

3.9.2 Genetic engineering with aspartate aminotransferases 64

Contents vii

3.10 Future Research 65

3.11 Conclusions 65

References 65

4 Tyrosine Aminotransferase 68

A.O. Hudson

4.1 Abstract 68

4.2 Introduction 68

4.2.1 Aminotransferases: a brief introduction 68

4.2.2 A brief history of aminotransferase activity in plants 69

4.2.3 Oligomeric state, cofactor requirement and mechanism

of action of action of aminotransferases 69

4.3 Aminotransferases from the Model Organism Arabidopsis thaliana 70

4.4 The Anabolism of Tyrosine and Phenylalanine in Plants and Bacteria 71

4.4.1 The anabolism of tyrosine and phenylalanine in bacteria 71

4.4.2 A second pathway for the synthesis of tyrosine and

phenylalanine in plants 73

4.5 Properties of Tyrosine Aminotransferase Annotated

by the Locus Tag At5g36160 from Arabidopsis thaliana 74

4.5.1 Kinetic and physical properties 74

4.5.2 Substrate specificity 76

4.5.3 In vivo analysis of tyrosine aminotransferase 76

4.6 The Role of Tyrosine Aminotransferase in Plants 77

4.7 Conclusions 79

Acknowledgement 79

References 79

5 An insight Into the Role and Regulation of Glutamine Synthetase in Plants 82

C. Sengupta-Gopalan and J.L. Ortega

5.1 Abstract 82

5.2 Introduction 82

5.3 Classification of Glutamine Synthetase 83

5.4 Glutamine Synthetase in Plants 83

5.4.1 Chloroplastic glutamine synthetase 84

5.4.2 Cytosolic glutamine synthetase 84

5.5 Modulation of Glutamine Synthetase Expression in Transgenic Plants 86

5.6 Regulation of Glutamine Synthetase Gene Expression in Plants 88

5.6.1 Transcriptional regulation 88

5.6.2 Post-transcriptional regulation 89

5.6.3 Translational regulation 91

5.6.4 Post-translational regulation 91

5.7 Concluding Remarks 93

Acknowledgements 94

References 94

6 Asparagine Synthetase 100

S.M.G. Duff

6.1 Abstract 100

6.2 Introduction: the Role of Asparagine and Asparagine

Synthetase in Nitrogen Metabolism 100

6.3 Asparagine: History, Chemical Properties and Role in Plants 101

6.4 Asparagine Synthetase: an Early History of Research in Humans,

Microbes and Plants 102

6.5 The Occurrence of Asparagine Synthetase in Nature 104

6.6 The Expression and Function of Asparagine Synthetase in Plants 105

6.6.1 Nutritional and mineral deficiency 105

6.6.2 Seed germination 105

6.6.3 Light signalling 106

6.6.4 Developmental stage and tissue specificity 106

6.6.5 Environmental stress and carbohydrate depletion 107

6.6.6 Senescence and nitrogen remobilization 108

6.6.7 Seed maturation 108

6.6.8 Photorespiration 109

6.6.9 Nitrogen signalling and glutamine:asparagine ratio 109

6.6.10 Asparagine: a nitrogen carrier, storage compound,

detoxification mechanism and signal 110

6.7 Phylogeny, Subunit Structure and Enzymatic Activity

of Asparagine Synthetase 110

6.7.1 Phylogeny 110

6.7.2 Subunit structure 112

6.7.3 The enzymatic activities of asparagine synthesis 112

6.8 Kinetics, Reaction Mechanism and Crystal Structure

of B-type Asparagine Synthetases 112

6.8.1 Kinetics of plant asparagine synthetase 112

6.8.2 The crystal structure and reaction mechanism

of asparagine synthetase 114

6.9 Other Routes of Asparagine Synthesis in Plants 116

6.10 Asparagine Catabolism 116

6.11 Asparagine Synthetase and Agriculture 117

6.11.1 Seed protein content and crop yield 117

6.11.2 The impact of plant nutrition 118

6.11.3 Metabolic engineering and transgenic studies 118

6.12 Conclusions 120

Acknowledgements 120

References 120

7 Glutamate Decarboxylase 129

J.J. Molina-Rueda, A. Garrido-Aranda and F. Gallardo

7.1 Abstract 129

7.2 Introduction 129

7.3 Characteristics of Glutamate Decarboxylase in Plants 130

7.4 Glutamate Decarboxylase Gene Family 131

7.5 Expression of Glutamate Decarboxylase Genes 131

7.6 g-Aminobutyric Acid Synthesis and its Metabolic Context 135

7.6.1 The g-aminobutyric acid shunt pathway and stress 135

7.6.2 Alternative sources of g-aminobutyric acid

in plant tissues and transport 137

7.7 Classical and Recent Evidence Supporting the Functions

of Glutamate Decarboxylase and g-Aminobutyric Acid 137

7.8 Future Research 139

Acknowledgement 139

References 139

viii Contents

8 l-Arginine-Dependent Nitric Oxide Synthase Activity 142

F.J. Corpas, L.A. del Río, J.M. Palma and J.B. Barroso

8.1 Abstract 142

8.2 Introduction 142

8.3 Arginine Catabolism in Plants: Urea, Polyamines and Nitric Oxide 143

8.3.1 Urea metabolism 144

8.3.2 l-Arginine modulates polyamine and nitric oxide biosynthesis 144

8.3.3 Arginine and nitric oxide synthesis in higher plants 145

8.4 Modulation of l-arginine-dependent Nitric Oxide Synthase

Activity During Plant Development and Under Stress Conditions 147

8.4.1 Nitric oxide synthase activity during plant development 147

8.4.2 Nitric oxide synthase activity in plants under stress conditions 149

8.5 A Genetic Engineering Approach to Study of the Relevance

of Nitric Oxide Synthase Activity in Plants 150

8.6 Conclusions 150

Acknowledgements 151

References 151

9 Ornithine: At the Crossroads of Multiple Paths to

Amino Acids and Polyamines 156

R. Majumdar, R. Minocha and S.C. Minocha

9.1 Abstract 156

9.2 Introduction 156

9.3 Ornithine Biosynthesis and Utilization 158

9.4 Cellular Contents 159

9.5 Mutants of Ornithine Biosynthesis 160

9.6 Genetic Manipulation of Ornithine Metabolism and its

Impact on Amino Acids and Other Related Compounds 164

9.7 Ornithine Biosynthesis and Functions in Animals 168

9.8 Exogenous Supply of d- and l-Ornithine 169

9.9 Modelling of Ornithine Metabolism and Associated Flux:

Ornithine as a Regulatory Molecule 170

9.10 Conclusions 171

Acknowledgements 172

References 172

10 Polyamines in Plants: Biosynthesis From Arginine, and Metabolic,

Physiological and Stress-response Roles 177

A.K. Mattoo, T. Fatima, R.K. Upadhyay and A.K. Handa

10.1 Abstract 177

10.2 Introduction 177

10.3 Substrates and Enzymes Catalysing Polyamine Biosynthesis 178

10.3.1 The route to the diamine putrescine 178

10.3.2 The route to higher polyamines, spermidine and

spermine/thermospermine 180

10.3.3 S-Adenosylmethionine decarboxylase 180

10.3.4 Spermidine synthase 181

10.3.5 Spermine/thermospermine synthases 181

10.4 Substrate Flux into the Polyamine Versus Ethylene Pathway 182

10.5 Back Conversion of Polyamines and Reactive Oxygen Species Signalling 183

10.6 Polyamines have an Impact on Metabolism 184

Contents ix

10.7 Polyamines and Plant Growth Processes 185

10.8 Polyamines in Plant Responses to Abiotic Stress 186

10.9 Conclusions 186

References 188

11 Serine Acetyltransferase 195

M. Watanabe, H-M. Hubberten, K. Saito and R Hoefgen

11.1 Abstract 195

11.2 Introduction 195

11.3 Biochemical Properties and Sub-cellular Localization

of Serine Acetyltransferases 197

11.4 The Serine Acetyltransferase-O-Acetylserine(Thiol)Lyase Complex 199

11.5 Expression Patterns of Serine Acetyltransferase Genes 202

11.6 In Vivo functions of Serine Acetyltransferases 204

11.7 Serine Acetyltransferase Overexpressors 206

11.8 O-Acetylserine Signalling 207

11.8.1 Identification of O-acetylserine cluster genes 207

11.8.2 Regulation of O-acetylserine cluster genes 209

11.8.3 Functions of O-acetylserine cluster genes 210

11.9 Conclusions 211

References 212

12 Cysteine Homeostasis 219

I. García, L.C. Romero and C. Gotor

12.1 Abstract 219

12.2 Introduction 219

12.3 Photosynthetic Assimilation of Sulfate in Plants 220

12.3.1 Sulfate transport 220

12.3.2 Sulfate reduction 221

12.3.3 Cysteine biosynthesis 222

12.4 The Cysteine Synthase Complex: Regulation of Cysteine Biosynthesis 222

12.5 Cysteine Synthesis in Cellular Compartments 224

12.6 Other Members of the O-Acetylserine(Thiol)Lyase Gene Family 224

12.6.1 CS26 225

12.6.2 CYS-C1 226

12.6.3 DES1 227

12.7 Conclusions 229

Acknowledgements 229

References 229

13 Lysine Metabolism 234

L.O. Medici, A.C. Nazareno, S.A. Gaziola, D. Schmidt and R.A. Azevedo

13.1 Abstract 234

13.2 Introduction 234

13.3 Aspartate Kinase and Homoserine Dehydrogenase 236

13.4 Aspartate Semialdehyde Dehydrogenase 237

13.5 Homoserine Kinase 237

13.6 Dihydrodipicolinate Synthase 238

13.7 Lysine Catabolism 240

13.8 What Next? 243

13.9 Conclusions 245

References 245

x Contents

14 Histidine 251

R.A. Ingle

14.1 Abstract 251

14.2 Introduction 251

14.3 Histidine Biosynthesis in Plants 252

14.4 Links Between Histidine Biosynthesis and Other

Metabolic Pathways in Plants 256

14.5 Sub-cellular Localization and Evolution of

Plant Histidine Biosynthetic Enzymes 256

14.6 Regulation of Histidine Biosynthesis in Plants 256

14.7 Role of Histidine in Nickel Hyperaccumulation in Plants 258

14.8 Conclusions 258

References 258

15 Amino Acid Synthesis Under Abiotic Stress 262

E. Planchet and A.M. Limami

15.1 Abstract 262

15.2 Introduction 262

15.3 The Glutamate Family Pathway 264

15.3.1 Proline accumulation and adaptive responses to stress 264

15.3.2 The regulation of proline metabolism during stress 266

15.3.3 Accumulation of g-aminobutyric acid (GABA)

in response to plant stresses 267

15.4 The Pyruvate Family Pathway 267

15.4.1 Alanine accumulation: a universal phenomenon under stress 268

15.4.2 Leucine and valine: the importance of branched-chain

amino acid accumulation in response to stress 270

15.5 The Aspartate Family Pathway 270

15.5.1 Stress-induced asparagine accumulation 271

15.5.2 Aspartate-derived amino acids in response to stress 272

15.6 Conclusions 272

References 273

16 The Central Role of Glutamate and Aspartate in the

Post-translational Control of Respiration and Nitrogen

Assimilation in Plant Cells 277

B. O’Leary and W.C. Plaxton

16.1 Abstract 277

16.2 Introduction: The Metabolic Organization of N Assimilation 277

16.2.1 The pivotal role of phospoenolpyruvate metabolism

in the control of plant glycolysis and respiration 280

16.3 Metabolic Effects of N Resupply in Unicellular Green Algae

and Vascular Plants 282

16.3.1 The response of primary C metabolism to

N resupply in N-starved green microalgae 282

16.3.2 The response of primary C metabolism to

N resupply in vascular plants 283

16.4 The Post-translational Control of Plant Phosphoenolpyruvate Carboxylase

and Cytosolic Pyruvate Kinase is Often Geared to NH4

+ Assimilation 284

16.4.1 The functional diversity of plant phosphoenolpyruvate

carboxylase isoenzymes reflects their complex mechanisms

of post-translational control 284

Contents xi

16.4.2 The allosteric features of plant cytosolic pyruvate

kinase isoenzymes help to synchronize C/N

interactions in different tissues 288

16.4.3 Glutamate and aspartate play a central role in the coordinate

allosteric control of phosphoenolpyruvate carboxylase and

cytosolic pyruvate kinase during NH4

+ assimilation 289

16.5 Transgenic Plants with Altered Phospoenolpyruvate or

Glutamate Metabolism Display an Altered C/N Balance 290

16.5.1 Mutants with phosphoenolpyruvate metabolism

perturbed by cytosolic pyruvate kinase or

phosphoenolpyruvate carboxylase 290

16.5.2 Effect of mutations that perturb glutamate levels 291

16.6 Conclusions and Future Directions 292

Acknowledgements 292

References 293

PART II DYNAMICS

17 Amino Acid Export in Plants 298

M.B. Price and S. Okumoto

17.1 Abstract 298

17.2 Introduction 298

17.3 Physiology of Amino Acid Export 299

17.3.1 Amino acid export from the seed coat 300

17.3.2 Amino acid export into the xylem 300

17.3.3 Amino acid exchange with the rhizosphere 301

17.3.4 Vascular amino acid transport 302

17.4 Amino Acid Export Proteins in Plants and Other Systems 302

17.4.1 The drug/metabolite transporter (DMT) superfamily 302

17.4.2 The amino acid-polyamine-organocation (APC) superfamily 303

17.4.3 The ATP-binding cassette (ABC) transporter superfamily 304

17.4.4 The major facilitator superfamily (MFS) 305

17.5 Regulation of Amino Acid Export 305

17.6 Amino Acids in Inter-organism Interactions 306

17.6.1 Amino acid secretion into the rhizosphere 306

17.6.2 Amino acid transport during nodulation 306

17.6.3 Amino acids in plant–pathogen interactions 307

17.7 Conclusions 307

References 307

18 Uptake, Transport and Redistribution of Amino

Nitrogen in Woody Plants 315

S. Pfautsch, T.L. Bell and A. Gessler

18.1 Abstract 315

18.2 Introduction 315

18.3 Uptake of Amino-N by Plant Roots 317

18.3.1 Principles of N uptake 317

18.3.2 Capacity and importance of uptake of amino-N 319

18.3.3 Uptake involving mycorrhizal associations 321

18.3.4 ‘Uptake’ involving an N2-fixing association 323

18.3.5 ‘Double-dipping’ or how root hemiparasites access amino-N 324

xii Contents

18.4 Transporting Amino-N in the Xylem 325

18.4.1 Transpiration – the upward ‘conveyor belt’ for amino-N 325

18.4.2 Loading amino-N into the xylem 326

18.4.3 Amino-N composition of xylem sap 326

18.5 Exchange of Amino Acids Between Xylem and Phloem

and Integration of N Transport and Plant N Metabolism 328

18.6 Future Research Directions 329

18.7 Conclusions 330

References 331

PART III CHEMICAL ECOLOGY

19 Auxin Biosynthesis 340

J.W Chandler

19.1 Abstract 340

19.2 Introduction 341

19.3 Sites of Auxin Synthesis in Plants and Cells 342

19.4 Pathways of Auxin Synthesis 342

19.4.1 The indole-3-pyruvate (IPA) pathway 343

19.4.2 Alternative biosynthetic routes 345

19.4.3 The indole-3-acetaldoxime (IAOx) pathway 346

19.4.4 The indole-3-acetamide (IAM) pathway 346

19.4.5 The tryptamine (TAM) pathway 347

19.5 Endogenous Auxins 348

19.6 Auxin Synthesis via the IPA Pathway is Transcriptionally

and Spatio-temporally Regulated 349

19.7 Environmental Regulation of Auxin Synthesis 350

19.8 Hormonal Regulation of Auxin Biosynthesis 351

19.9 Conjugation Contributes to Auxin Homeostasis 352

19.10 The Evolution of Auxin Synthesis in Plants 352

19.11 Conclusions 354

Acknowledgement 354

References 354

20 Involvement of Tryptophan-pathway-derived Secondary

Metabolism in the Defence Responses of Grasses 362

A. Ishihara, T. Matsukawa, T. Nomura, M. Sue, A. Oikawa, Y. Okazaki and S. Tebayashi

20.1 Abstract 362

20.2 General Introduction to Secondary Metabolism Derived

From the Tryptophan Pathway 362

20.3 The Biosynthesis and Functions of Benzoxazinones in Wheat,

Rye and Maize 364

20.3.1 Molecular genetics of the benzoxazinone pathway 364

20.3.2 Detoxification and reactivation of benzoxazinones 368

20.3.3 Inducible defence response associated with benzoxazinones 371

20.4 Significance of the Metabolic Processes of Avenanthramides

in the Defence Response of Oats 372

20.4.1 Biosynthesis of avenanthramide phytoalexins in oats 372

20.4.2 Metabolism of avenanthramides in elicitor-treated oat leaves 374

20.5 Accumulation of Serotonin in Rice in Response to Biological Stimuli 375

20.5.1 Occurrence of serotonin and its putative ecological

roles in plants 375

Contents xiii

20.5.2 Critical role of serotonin accumulation in the interaction

between rice and its pathogens 377

20.6 Concluding Remarks 380

References 381

21 Melatonin: Synthesis From Tryptophan and its Role in Higher Plants 390

M.B. Arnao and J. Hernández-Ruiz

21.1 Abstract 390

21.2 Introduction 390

21.2.1 Discovery of melatonin 391

21.2.2 Physiological roles of melatonin 391

21.2.3 1995: a critical year for plants 395

21.3 Biosynthesis of Melatonin 396

21.3.1 Melatonin-related enzymes and their regulation 396

21.3.1.1 Tryptophan 5-hydroxylase (T5H) 396

21.3.1.2 Tryptophan decarboxylase (TDC) 401

21.3.1.3 Serotonin N-acetyltransferase (SNAT) 402

21.3.1.4 Hydroxyindole O-methyltransferase (HIOMT) 403

21.3.2 Characteristic features of melatonin-related enzymes in plants 404

21.3.2.1 Tryptophan 5-hydroxylase (T5H) 404

21.3.2.2 Tryptophan decarboxylase (TDC) 405

21.3.2.3 Serotonin N-acetyltransferase (SNAT) 406

21.3.2.4 Hydroxyindole O-methyltransferase (HIOMT) 407

21.4 Catabolism of Melatonin: Enzymatic and Non-enzymatic Pathways 407

21.5 Physiological Actions of Melatonin in Plants 409

21.5.1 Searching for roles of melatonin in plants similar to those

observed in animals 410

21.5.2 Searching for specific roles of melatonin in plants 413

21.6 Future Perspectives and Concluding Remarks 415

References 416

22 Glucosinolate Biosynthesis From Amino Acids 436

H.U. Stotz, P.D. Brown and J. Tokuhisa

22.1 Abstract 436

22.2 Introduction: Evolution of Glucosinolate Biosynthesis 436

22.3 Cellular and Tissue Distribution of Glucosinolate Metabolism 438

22.4 Connections of Glucosinolate Metabolism to Amino Acid Biosynthesis 440

22.5 Regulation of Glucosinolate Biosynthesis 441

22.6 Biological Activities of Glucosinolate Metabolites 441

22.7 Conclusions 443

References 444

23 Natural Toxins that Affect Plant Amino Acid Metabolism 448

S.O. Duke and F.E. Dayan

23.1 Abstract 448

23.2 Introduction 448

23.3 Approaches to the Discovery of Phytotoxin Mode of Action 449

23.4 Inhibitors of Aminotransferases 449

23.5 An Inhibitor of b-Cystathionase (Cystathionine b-lyase) 450

23.6 Inhibitors of Glutamate Synthase and Asparagine Synthetase 450

23.7 Inhibitors of Glutamine Synthetase 451

xiv Contents