Amino acids in higher plants

Tai Lieu Chat Luong


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
Buildings Campus, Edinburgh, UK


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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


Contents

Contributors

xix

Preface

xxiii

Glossary

xxvii

PART I  ENZYMES AND METABOLISM
1  Glutamate Dehydrogenase
G.O. Osuji and W.C. Madu

1

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
Acknowledgements24
References24

v

viContents

2  Alanine Aminotransferase: Amino Acid Metabolism in Higher Plants
A. Raychaudhuri

30

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
Aminotransferase33
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

References52
3  Aspartate Aminotransferase
C.D. Leasure and Z-H. He
3.1 Abstract
3.2 Introduction
3.3  The Vitamin B6 Cofactor
3.4  Enzyme Function
3.4.1  The reaction mechanism
3.4.2  Enzyme properties
3.5  Enzyme Structure
3.5.1 K258
3.5.2 R292*
3.5.3 R386
3.5.4 D222
3.5.5 Y225
3.6  Enzyme Genetics
3.7  The Enzyme during Plant Development
3.8  The Role of Aspartate in Plants
3.8.1 C4 metabolism
3.9  Other Roles of Aspartate Aminotransferase
3.9.1 Moonlighting
3.9.2  Genetic engineering with aspartate aminotransferases

57
57
57
58
58
60
61

61
61
61
61
62
62
62
63
63
64
64
64
64


Contentsvii

3.10  Future Research
65
3.11 Conclusions
65
References65
4  Tyrosine Aminotransferase
A.O. Hudson

68

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 thaliana70
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 thaliana74
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
Acknowledgement79
References79

5  An insight Into the Role and Regulation of Glutamine Synthetase in Plants
C. Sengupta-Gopalan and J.L. Ortega

82

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
Acknowledgements94
References94
6  Asparagine Synthetase
S.M.G. Duff
6.1 Abstract
6.2 Introduction: the Role of Asparagine and Asparagine
Synthetase in Nitrogen Metabolism
6.3  Asparagine: History, Chemical Properties and Role in Plants

100
100
100
101


viiiContents

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
Acknowledgements120
References120
7  Glutamate Decarboxylase
J.J. Molina-Rueda, A. Garrido-Aranda and F. Gallardo

129

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
Acknowledgement139
References139


Contentsix

8 

l-Arginine-Dependent Nitric Oxide Synthase Activity142
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
Acknowledgements151
References151
9 Ornithine: At the Crossroads of Multiple Paths to
Amino Acids and Polyamines
R. Majumdar, R. Minocha and S.C. Minocha

156

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-Ornithine169
9.9 Modelling of Ornithine Metabolism and Associated Flux:
Ornithine as a Regulatory Molecule
170
9.10 Conclusions
171
Acknowledgements172
References172
10 Polyamines in Plants: Biosynthesis From Arginine, and Metabolic,
Physiological and Stress-response Roles
A.K. Mattoo, T. Fatima, R.K. Upadhyay and A.K. Handa

177

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/thermospermine180
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


xContents

10.7  Polyamines and Plant Growth Processes
185
10.8  Polyamines in Plant Responses to Abiotic Stress
186
10.9 Conclusions
186

References188
11  Serine Acetyltransferase
M. Watanabe, H-M. Hubberten, K. Saito and R Hoefgen

195

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
References212
12  Cysteine Homeostasis
I. García, L.C. Romero and C. Gotor

219

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
Acknowledgements229
References229
13  Lysine Metabolism
L.O. Medici, A.C. Nazareno, S.A. Gaziola, D. Schmidt and R.A. Azevedo

234

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
References245

Contentsxi

14 Histidine
R.A. Ingle

251

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
References258
15  Amino Acid Synthesis Under Abiotic Stress
E. Planchet and A.M. Limami

262

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

References273
16 The Central Role of Glutamate and Aspartate in the
Post-translational Control of Respiration and Nitrogen
Assimilation in Plant Cells277
B. O’Leary and W.C. Plaxton
16.1 Abstract
16.2  Introduction: The Metabolic Organization of N Assimilation
16.2.1 The pivotal role of phospoenolpyruvate metabolism
in the control of plant glycolysis and respiration
16.3 Metabolic Effects of N Resupply in Unicellular Green Algae
and Vascular Plants
16.3.1 The response of primary C metabolism to
N resupply in N-starved green microalgae
16.3.2 The response of primary C metabolism to
N resupply in vascular plants
16.4 The Post-translational Control of Plant Phosphoenolpyruvate Carboxylase
and Cytosolic Pyruvate Kinase is Often Geared to NH4+ Assimilation
16.4.1 The functional diversity of plant phosphoenolpyruvate
carboxylase isoenzymes reflects their complex mechanisms
of post-translational control

277
277
280
282
282
283
284

284

xiiContents

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
Acknowledgements292
References293
PART II  DYNAMICS
17  Amino Acid Export in Plants
M.B. Price and S. Okumoto

298

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
References307
18 Uptake, Transport and Redistribution of Amino
Nitrogen in Woody Plants
S. Pfautsch, T.L. Bell and A. Gessler
18.1 Abstract
18.2 Introduction
18.3  Uptake of Amino-N by Plant Roots
18.3.1  Principles of N uptake
18.3.2  Capacity and importance of uptake of amino-N
18.3.3  Uptake involving mycorrhizal associations
18.3.4  ‘Uptake’ involving an N2-fixing association
18.3.5  ‘Double-dipping’ or how root hemiparasites access amino-N

315
315
315
317
317
319
321
323
324

Contentsxiii

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
References331
PART III  CHEMICAL ECOLOGY
19  Auxin Biosynthesis
J.W Chandler

340

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

Acknowledgement354
References354
20 Involvement of Tryptophan-pathway-derived Secondary
Metabolism in the Defence Responses of Grasses362
A. Ishihara, T. Matsukawa, T. Nomura, M. Sue, A. Oikawa, Y. Okazaki and S. Tebayashi
20.1 Abstract
20.2 General Introduction to Secondary Metabolism Derived
From the Tryptophan Pathway
20.3 The Biosynthesis and Functions of Benzoxazinones in Wheat,
Rye and Maize
20.3.1  Molecular genetics of the benzoxazinone pathway
20.3.2  Detoxification and reactivation of benzoxazinones
20.3.3  Inducible defence response associated with benzoxazinones
20.4 Significance of the Metabolic Processes of Avenanthramides
in the Defence Response of Oats
20.4.1  Biosynthesis of avenanthramide phytoalexins in oats
20.4.2  Metabolism of avenanthramides in elicitor-treated oat leaves
20.5  Accumulation of Serotonin in Rice in Response to Biological Stimuli
20.5.1 Occurrence of serotonin and its putative ecological
roles in plants

362
362
364
364
368
371
372
372
374

375
375


xivContents

20.5.2 Critical role of serotonin accumulation in the interaction
between rice and its pathogens
377
20.6  Concluding Remarks
380
References381
21  Melatonin: Synthesis From Tryptophan and its Role in Higher Plants
M.B. Arnao and J. Hernández-Ruiz

390

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

References416
22  Glucosinolate Biosynthesis From Amino Acids
H.U. Stotz, P.D. Brown and J. Tokuhisa

436

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
References444
23  Natural Toxins that Affect Plant Amino Acid Metabolism
S.O. Duke and F.E. Dayan

448

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


Contentsxv

23.8  Inhibitors of Ornithine Transcarbamoylase
453
23.9  Inhibitor of Dihydrodipicolinate Synthase
453
23.10  Potential Inhibitors of Amino Acid Metabolism
454
23.11 Ascaulitoxin Aglycone – A Potential Aminotransferase Inhibitor
454
23.12  Enhanced Photodegradation of l-Phenylalanine454
23.13  Final Thoughts
454
References456
24 Glyphosate: The Fate and Toxicology of a Herbicidal
Amino Acid Derivative
D.A. Saltmiras, D.R. Farmer, A. Mehrsheikh and M.S. Bleeke

461

24.1 Abstract
461
24.2 Introduction
461
24.3  History of Glyphosate
462
24.4  Herbicidal Mode of Action of Glyphosate
462
24.5 Physico-chemical Properties of Glyphosate
462
24.6  Glyphosate in the Environment
463
24.6.1  Uptake and metabolism in plants
463
24.6.2  Environmental fate
466
24.7  Glyphosate in Mammals
469
24.7.1 Mammalian absorption, distribution, metabolism
and excretion (ADME) studies
470
24.7.2 Toxicology
470
24.7.2.1  Acute toxicity
471
24.7.2.2  Repeat dose toxicity
471
24.7.2.3 Genotoxicity
472

24.7.2.4 Carcinogenicity
472
24.7.2.5  Developmental and reproductive toxicity
473
24.7.2.6  Endocrine disruption
474
24.7.2.7 Neurotoxicity
474
24.7.3  Human dietary exposures to glyphosate
474
24.7.4  Human health risk assessments
475
24.8 Conclusions
476
References476
PART IV  PLANT PRODUCTS: QUALITY AND SAFETY
25  Amino Acid Analysis of Plant Products
S.M. Rutherfurd
25.1 Abstract
25.2 Introduction
25.3  Sample Preparation
25.4  Amino Acid Analysis
25.4.1  The hydrolysis step
25.4.2  Least-squares non-linear regression
25.4.3  The chromatography step
25.4.4  Mass spectrometry and nuclear magnetic resonance
25.4.5  Determination of free amino acids
25.4.6  Presentation of amino acid composition data
25.4.7  Internal and external standards

481
481
481
482
482
482
484
486
486
487
488
488


xviContents

25.5  Determination of the Amino Acid Composition of Processed Plant Products
488
25.5.1 Lysine
489
25.5.2  Methionine and cysteine
490
25.5.3  Threonine and serine
491
25.5.4  Amino acid racemization
491
25.6 Conclusions
492
References492
26 Metabolic Amino Acid Availability in Foods of Plant Origin: Implications

for Human and Livestock Nutrition497
C.L. Levesque
26.1 Abstract
497
26.2 Introduction
497
26.3  Amino Acid Digestibility and its Limitations
498
26.4  Metabolic Availability of Amino Acids
499
26.4.1  Metabolic availability in protein sources
501
26.4.2  Advantages of the metabolic availability method
502
26.5  Future Research and Conclusions
503
References503
27  Toxicology of Non-protein Amino Acids
J.P.F. D’Mello

507

27.1 Abstract
507
27.2 Introduction
508
27.3 Classification
509
27.4 Distribution
511

27.5  Metabolic Fate
512
27.5.1 Canavanine
512
27.5.2  Analogues of sulfur amino acids
513
27.5.3 Mimosine
513
27.6  Adverse Effects
514
27.6.1  Anti-microbial activity
515
27.6.2 Phytotoxicity
515
27.6.3  Insecticidal activity
517
27.6.4  Manifestations in higher animals
518
27.6.5  Human health risks
520
27.7 Mechanisms
522
27.7.1  Biochemical basis of toxicity
522
27.7.2  Stress-resistance mechanisms
525
27.8 Detoxification
527
27.9  Potential Applications
528

27.10 Conclusions
529
References531
PART V  CONCLUSIONS
28 Delivering Innovative Solutions and Paradigms for a
Changing Environment
J.P.F. D’Mello
28.1 Abstract
28.2 Background

538
538
539




Contentsxvii

28.3 Approach
540
28.4 Glutamate
541
28.5 Proline
541
28.6 Arginine
542
28.7 Ornithine
542
28.8 Citrulline

542
28.9 Glycine
543
28.10  Sulfur Amino Acids
544
28.11 Branched-chain Amino Acids
545
28.12  Aromatic Amino Acids
547
28.13  Secondary Metabolism
549
28.14  Comparative Metabolism
550
28.15  Signal  Transduction
553
28.16  Molecular Interactions
554
28.16.1  Synergistic effects
556
28.16.2 Antagonisms
556
28.16.3 Integration
558
28.17  Biotic and Environmental Stress Responses
559
28.17.1  A general model
563
28.17.2  Specific examples
564
28.18  Plant Products

565
28.19 Summary
566
28.19.1  Enlightenment and debate in equal measure
566
28.19.2  Amino acids of ‘particular distinction’
569
28.19.3 Innovation
570
28.20 Outlook
572
References573
Index585



Contributors

Arnao, M.B., Department of Plant Physiology, Faculty of Biology, University of Murcia, 30100-Murcia,
Spain. E-mail:
Azevedo, R.A., Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”,
Universidade de São Paulo, Piracicaba, Brazil. E-mail:
Barroso, J.B., Departamento de Bioquímica, Biología Celular y Molecular de Plantas, Estacíon
­Experimental del Zaídin, Consejo Superior de Investigaciones Científicas (CSIC), Apartado 419,
E-18080 Granada, Spain. E-mail:
Bell, T.L., Faculty of Agriculture and Environment, University of Sydney, 1 Central Avenue, Eveleigh,
NSW 2015, Australia. E-mail:
Bleeke, M.S., Regulatory Product Safety Center, Monsanto, 800 North Lindberg Boulevard, St Louis,
MO 63167, USA. E-mail:
Brown, P.D., Departments of Chemistry, Biology and Environmental Studies, Trinity Western

University, 7600 Glover Road, Langley, BC V2Y 1Y1, Canada. E-mail:
Chandler, J.W., Institute of Developmental Biology, Cologne Biocenter, Cologne University, Zulpicher
Strasse 47b, D-50674 Cologne, Germany. E-mail:
Corpas, F.J., Departamento de Bioquímica, Biología Celular y Molecular de Plantas, Estacíon
Experimental del Zaídin, Consejo Superior de Investigaciones Científicas (CSIC), Apartado 419,
E-18080 Granada, Spain. E-mail:
Dayan, F.E., USDA Agricultural Research Service, Natural Products Utilization Research Unit,
­Oxford, MS 38677, USA. E-mail:
del Rio, L.A., Departamento de Bioquímica, Biología Celular y Molecular de Plantas, Estacíon
­Experimental del Zaídin, Consejo Superior de Investigaciones Científicas (CSIC), Apartado 419,
E-18080 Granada, Spain. E-mail:
D’Mello, J.P.F., Formerly of SAC (Scottish Agricultural College), University of Edinburgh King’s
Buildings Campus, West Mains Road, Edinburgh, EH9 3JG, UK. E-mail:
Duff, S.M.G., Monsanto, 700 Chesterfield Parkway West, Chesterfield, MO 63017, USA. E-mail:

Duke, S.O., USDA Agricultural Research Service, Natural Products Utilization Research Unit,
­Oxford, MS 38677, USA. E-mail:
Farmer, D.R., Regulatory Product Safety Center, Monsanto, 800 North Lindberg Boulevard, St Louis,
MO 63167, USA. E-mail:
Fatima, T., Sustainable Agricultural Systems Laboratory, USDA Agricultural Research Service,
Beltsville Agricultural Research Center, Beltsville, MD 20705-2350, USA. Present address:
xix


xxContributors

­ epartment of Physiology and Pharmacology, University of Western Ontario, London, ON N6A
D
5C1, Canada. E-mail:
Gallardo, F., Departamento de Biología Molecular y Bioquímica, Facultad de Ciencias, Universidad

de Málaga, E-29071 Malaga, Spain. E-mail:
Garcia, I., Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas
(CSIC) and Universidad de Sevilla, Sevilla, Spain. E-mail:
Garrido-Aranda, A., Departamento de Biología Molecular y Bioquímica, Facultad de Ciencias,
­Universidad de Malága, E-29071 Malaga, Spain. E-mail:
Gaziola, S.A., Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, Brazil. E-mail:
Gessler, A., Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zurcherstrasse
111, 8903 Birmensdorf, Switzerland. E-mail:
Gotor, C., Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas
(CSIC) and Universidad de Sevilla, Sevilla, Spain. E-mail:
Handa, A.K., Department of Horticulture and Landscape Architecture, Purdue University, West
Lafayette, IN 47907, USA. E-mail:
He, Z-H., Department of Biology, San Franscisco State University, 1600 Holloway Avenue, San Franscisco,
CA 94132, USA. E-mail:
Hernandez-Ruiz, J., Department of Plant Physiology, Faculty of Biology, University of Murcia,
30100-Murcia, Spain. E-mail:
Hoefgen, R., Max Planck Institute of Molecular Plant Physiology, 14424 Potsdam-Golm, Germany.
E-mail:
Hubberten, H-M., Max Planck Institute of Molecular Plant Physiology, 14424 Potsdam-Golm,
Germany. E-mail:
Hudson, A.O., Thomas H. Gosnell School of Life Sciences, Rochester Institute of Technology, 85
Lomb Memorial Drive, Rochester, NY 14623, USA. E-mail:
Ingle, R.A., Department of Molecular and Cell Biology, University of Cape Town, Private Bag,
­Rondebosch 7701, South Africa. E-mail:
Ishihara, A., Faculty of Agriculture, Tottori University, Koyama, Tottori 680-8553, Japan. E-mail:

Leasure, C.D., Department of Biology, San Franscisco State University, 1600 Holloway Avenue, San
Franscisco, CA 94132, USA. E-mail:
Levesque, C.L., Department of Animal Science, South Dakota State University, Box 2170, Brookings,
SD 57007, USA. E-mail:

Limami, A.M., Research Institute of Horticulture and Seeds, University of Angers, 2 Bd Lavoisier,
F-49045 Angers, France. E-mail:
Madu, W.C., Imo State Polytechnic, Owerri, Nigeria. E-mail:
Majumdar, R., USDA Agricultural Research Service, 308 Sturtevant Hall, Geneva, NY 14456,
USA. E-mail:
Matsukawa, T., Faculty of Biology-Oriented Science and Technology, Kinki University, Kinokawa
649-6493, Japan. E-mail:
Mattoo, A.K., Sustainable Agricultural Systems Laboratory, USDA Agricultural Research Service,
Beltsville Agricultural Research Center, Beltsville, MD 20705-2350, USA. E-mail: autar.mattoo@
ars.usda.gov
Medici, L.O., Departamento de Ciências Fisiológicas, Universidade Federal Rural do Rio de Janeiro,
Seropédica CEP 23890-000, Brazil. E-mail:
Mehrsheikh, A., Regulatory Product Safety Center, Monsanto, 800 North Lindberg Boulevard,
St Louis, MO 63167, USA. E-mail:
Minocha, R., USDA Forest Service, Northern Research Station, Durham, NH 03824, USA. E-mail:





Contributorsxxi

Minocha, S.C., Department of Biological Sciences, University of New Hampshire, Durham, NH
03824, USA. E-mail:
Molina-Rueda, J.J., Departamento de Biología Molecular y Bioquímica, Facultad de Ciencias,
­Universidad de Malága, E-29071 Malaga, Spain. E-mail:
Nazareno, A.C., Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”,
­Universidade de São Paulo, Piracicaba, Brazil. E-mail:
Nomura, T., Biotechnology Research Center, Toyama Prefectural University, 5180 Kurokawa,
­Imizu, Toyama 939-0398, Japan. E-mail:

Oikawa, A., Faculty of Agriculture, Yamagata University, Tsuruoka 997-8555, Japan. E-mail: oikawa@
tds1.tr.yamagata-u.ac.jp
Okazaki, Y., Metabolomics Research Group, RIKEN Center for Sustainable Resource Science,
Yokohama 230-0045, Japan. E-mail:
Okumoto, S., Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, 512
Latham Hall, Blacksburg, VA 24061, USA. E-mail:
O’Leary, B., Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1
3RB, UK. E-mail:
Ortega, J.L., Department of Plant and Environmental Sciences, New Mexico State University, Las
Cruces, New Mexico 88003, USA. E-mail:
Osuji, G.O., College of Agriculture and Human Sciences, Prairie View A&M University, Prairie View,
TX 77446, USA. E-mail:
Palma, J.M., Departamento de Bioqmica, Biología Celular y Molecular de Plantas, Estación
­Experimental del Zaídin, Consejo Superior de Investigaciones Científicas (CSIC), Apartado 419,
E-18080 Granada, Spain. E-mail:
Pfautsch, S., Hawkesbury Institute of the Environment, University of Western Sydney, Locked Bag
1797, Penrith, NSW 2751, Australia. E-mail:
Planchet, E., Research Institute of Horticulture and Seeds, University of Angers, 2 Bd Lavoisier,
F-49045 Angers, France. E-mail:
Plaxton, W.C., Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada.
E-mail:
Price, M.B., Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, 512
Latham Hall, Blacksburg, VA 24061, USA. E-mail:
Raychaudhuri, A., Monsanto, 700 Chesterfield Parkway West, Chesterfield, MO 63011, USA.
E-mail:
Romero, L.C., Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones
Científicas (CSIC) and Universidad de Sevilla, Sevilla, Spain. E-mail:
Rutherfurd, S.M., Riddet Institute, Massey University, Private Bag 11222, Palmerston North, New
Zealand. E-mail:
Saito, K., Metabolomics Research Group, RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Japan. E-mail:

Saltmiras, D.A., Regulatory Product Safety Center, Monsanto, 800 North Lindberg Boulevard,
St Louis, MO 63167, USA. E-mail:
Schmidt, D., Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade
de São Paulo, Piracicaba, Brazil. E-mail:
Sengupta-Gopalan, C., Department of Plant and Environmental Sciences, New Mexico State
­University, Las Cruces, New Mexico 88003, USA. E-mail:
Stotz, H.U., School of Life and Medical Science, University of Hertfordshire, Hatfield, AL10 9AB, UK.
E-mail:
Sue, M., Department of Applied Biology and Chemistry, Tokyo University of Agriculture, Setagaya,
Tokyo 156-8502, Japan. E-mail:
Tebayashi, S., Faculty of Agriculture, Kochi University, Nangoku 783-8502, Japan. E-mail: tebayasi@
kochi-u.ac.jp


xxiiContributors

Tokuhisa, J., Department of Horticulture, Virginia Tech., Blacksburg, VA 24061, USA. E-mail:

Upadhyay, R.K., Sustainable Agricultural Systems Laboratory, USDA Agricultural Research Service,
Beltsville Agricultural Research Center, Beltsville, MD 20705-2350, USA. Present address: Pennsylvania
State University Harrisburg, Middletown, PA 17057, USA. E-mail:
Watanabe, M., Max Planck Institute of Molecular Plant Physiology, 14424 Potsdam-Golm, Germany.
E-mail:


Preface

Rationale
As a long-standing member of the academic community in Edinburgh, I have been immensely
enthused by the very concept of the Higgs boson particle and the profound implications of recent

discoveries highlighted in the media. The ensuing exuberance is still palpable and continues to cause
reverberations throughout the scientific world, even as I compose this Preface. Biochemists, of
course, have their own ‘God Molecules’ in the form of amino acids, the fundamental ‘particles’ of all
living organisms. In ‘Astrobiology: seeds of life?’ Shock (2002) referred to the occurrence of amino
acids in the interstellar medium, and speculation continues to this day as to the primordial processes
preceding the formation of these indispensable molecules. It is salutary to note the extreme conditions
permitting synthesis of amino acids in ongoing research investigations (Neish et al., 2010; Parker
et al., 2011).
The consistent and ubiquitous distribution of precisely the same 20 amino acids in diverse living organisms is widely recognized. The preordained sequence and configurational prerequisites of
amino acids in cellular protein structure and activity are features of profound biological significance.
As a consequence, the term ‘canonical’ amino acids is frequently invoked to exemplify the fundamental requirements for biosynthetic processes in living organisms. Nevertheless, there are efforts
now being directed at expanding the genetic lexicon to circumvent the above-mentioned sequence
and structural constraints in order to facilitate the incorporation of xenobiotic amino acids into proteins (Young and Schultz, 2010).
In addition, specific amino acids have also been selected for special attention. For example, glutamate has been accorded with the title of an amino acid of ‘particular distinction’ in the context of
mammalian metabolism (Young and Ajami, 2000). Equally, the diversity of functions ensures an
important position for glutamate in the biochemistry of higher plants. However, the statement by
Young and Ajami (2000) inevitably invites contradiction as there is much evidence in the literature
to support the contention that other amino acids are similarly endowed with unique functions in
higher plants, as in mammals. In all living organisms, the transport characteristics of amino acids
are determined by structural and chemical orientation. The metabolic significance in human and
livestock nutrition is further enhanced by classification of amino acids into essential (indispensable)
and non-essential (dispensable) nutrients and glucogenic and ketogenic precursors. Thus, there has
long been a rich diversity of interdisciplinary issues which, over the years, I have exploited in the
publication of three titles: Amino Acids in Farm Animal Nutrition (D’Mello, 1994), Amino Acids in Animal
Nutrition (D’Mello, 2003) and Amino Acids in Human Nutrition and Health (D’Mello, 2012).
xxiii


xxivPreface

The publication of Amino Acids in Higher Plants reflects my continuing commitment to the cause
of amino acids both at the fundamental and practical levels, following the model adopted in my previous books (D’Mello, 1994, 2003, 2012). Amino Acids in Higher Plants has been designed specifically
for academic, research and corporate institutions worldwide, particularly in Europe, the USA,
­Canada, Japan, Australia and New Zealand, but generally in all countries where English is a primary
medium for instruction. This book should appeal to final year undergraduate and graduate students
as well as to teaching and research staff. It is anticipated that it will be recommended reading for
courses in the biological sciences, including botany, biochemistry, genetics and agronomy, but the
multidisciplinary approach adopted in this volume should serve to attract a wider readership. Amino
Acids in Higher Plants is also designed with the commercial sector in mind, particularly companies
with progressive R&D agendas.

Overview
The chapters in Amino Acids in Higher Plants are arranged within a thematic structure as outlined
below. The nature of the subjects under consideration and the need for continuity necessarily
involves a certain amount of overlap. This should not be perceived as a detraction, as individual
chapters are self-contained as a result, thereby reducing the need for cross-referencing to other sections
of the book. This approach has also allowed authors increased flexibility in terms of emphasis and
interpretation.

Part I  Enzymes and metabolism
As in my most recent volume (D’Mello, 2012), this section pursues the theme of amino acid metabolism through the driving actions of the principal enzymes, emphasizing recent advances particularly with reference to localization, biophysical characterization and regulation. Indeed, several of
the enzymes and their associated pathways are common to both plants and animals. A key feature
concerns the expression of enzymes and genetic manipulation. Other subdivisions in these chapters
are designed to address issues such as cellular and sub-cellular functions, substrate requirements
and availability, cofactor constraints and enzyme kinetics. A number of enzymes under review in this
section catalyse rate-limiting steps in important metabolic pathways leading to the synthesis of
physiologically active intermediates and end-products, including phytoalexins. In terms of regulation, both transcriptional and translational mechanisms are considered here for several enzymes and
pathways. The changing facets of amino acid biochemistry in plants is another pervading theme
allowing the consideration of comparative issues and integration of nitrogen with carbon
­metabolism. Part I has also been designed with the aim of underpinning issues such as signalling as

well as immunity and environmental responses in plants.

Part II  Dynamics
This section includes two chapters designed to explore transport dynamics at the cellular and wholeplant levels and the relationship to external factors. Transport and fluxes at the whole-organism level
have been reviewed in Amino Acids in Human Nutrition and Health (D’Mello, 2012). The extent to
which comparative issues will emerge in the two chapters in Part II is a cogent theme for current
thinking and future research. Not unexpectedly, therefore, there is a need to consider the uptake of
amino acids, transporter superfamilies and associated proteins as well as exchanges between cellular
compartments. Specifically, metabolic transactions between the xylem and phloem, regulatory
mechanisms in export dynamics and interactions with the rhizosphere will be pertinent components