Annual Plant Reviews, The Plant Hormone Ethylene, Volume 44 The Plant Hormone Ethylene Annual Plant Reviews Series

The plant hormone ethylene is one of the most important, being one of the first chemicals to be determined as a naturally-occurring growth regulator and influencer of plant development. It was also the first hormone for which significant evidence was found for the presence of receptors.

This important new volume in Annual Plant Reviews is broadly divided into three parts. The first part covers the biosynthesis of ethylene and includes chapters on S-adenosylmethionine and the formation and fate of ACC in plant cells. The second part of the volume covers ethylene signaling, including the perception of ethylene by plant cells, CTR proteins, MAP kinases and EIN2 / EIN3. The final part covers the control by ethylene of cell function and development, including seed development, germination, plant growth, cell separation, fruit ripening, senescent processes, and plant-pathogen interactions.

The Plant Hormone Ethylene is an extremely valuable addition to Wiley-Blackwell's Annual Plant Reviews. With contributions from many of the world's leading researchers in ethylene, and edited by Professor Michael McManus of Massey University, this volume will be of great use and interest to a wide range of plant scientists, biochemists and chemists. All universities and research establishments where plant sciences, biochemistry, chemistry, life sciences and agriculture are studied and taught should have access to this important volume.

List of Contributors xv

Preface xxiii

1 100 Years of Ethylene – A Personal View 1
Don Grierson

1.1 Introduction 1

1.2 Ethylene biosynthesis 2

1.3 Ethylene perception and signalling 7

1.4 Differential responses to ethylene 9

1.5 Ethylene and development 10

1.6 Looking ahead 13

Acknowledgements 14

References 14

2 Early Events in the Ethylene Biosynthetic Pathway – Regulation of the Pools of Methionine andS-Adenosylmethionine 19
Katharina B¨ urstenbinder and Margret Sauter

2.1 Introduction 20

2.2 The metabolism of Met and SAM 22

2.3 Regulation of de novo Met synthesis 25

2.4 Regulation of the SAM pool 27

2.4.1 Regulation of SAMS genes by ethylene and of SAMS enzyme activity by protein-S-nitrosylation 29

2.5 The activated methyl cycle 30

2.6 The S-methylmethionine cycle 32

2.7 The methionine or Yang cycle 35

2.7.1 The Yang cycle in relation to polyamine and nicotianamine biosynthesis 39

2.7.2 Regulation of the Yang cycle in relation to ethylene synthesis 40

2.8 Conclusions 42

Acknowledgement 43

References 44

3 The Formation of ACC and Competition Between Polyamines and Ethylene for SAM 53
Smadar Harpaz-Saad, Gyeong Mee Yoon, Autar K. Mattoo, and Joseph J. Kieber

3.1 Introduction 53

3.2 Identification and characterization of ACC synthase activity in plants 54

3.2.1 Historical overview 54

3.2.2 Purification and properties of the ACC synthase protein 56

3.3 Analysis of ACC synthase at the transcriptional level 58

3.3.1 Molecular cloning of ACC synthase genes 58

3.3.2 Transcriptional regulation of the ACC synthase gene family 59

3.4 Post-transcriptional regulation of ACS 62

3.4.1 Identification and characterization of interactions with ETO1 62

3.4.2 Regulation of ACS degradation 64

3.5 Does ACC act as a signal? 65

3.6 Biosynthesis and physiology of polyamines 67

3.6.1 SAM is a substrate for polyamines 67

3.6.2 Physiology of polyamine effects in vitro and in vivo 67

3.6.3 Concurrent biosynthesis of ethylene and polyamines 70

3.6.4 Do plant cells invoke a homeostatic regulation of SAM levels? 72

Acknowledgements 72

References 72

4 The Fate of ACC in Higher Plants 83
Sarah J. Dorling and Michael T. McManus

4.1 Introduction 83

4.2 History of the discovery of ACC oxidase as the ethylene-forming enzyme 84

4.2.1 Early characterization of ACC oxidase 84

4.2.2 Cloning of the ethylene-forming enzyme as an indicator of enzyme activity 85

4.2.3 Initial biochemical demonstration of ethylene-forming enzyme activity in vitro 86

4.3 Mechanism of the ACC oxidase-catalyzed reaction 86

4.3.1 Investigation of the ACO reaction mechanism 87

4.3.2 Metabolism of HCN 89

4.3.3 Evidence of the conjugation of ACC 91

4.4 Transcriptional regulation of ACC oxidase 92

4.4.1 ACO multi-gene families 92

4.4.2 Differential expression of members of ACO multi-gene families in response to developmental and environmental stimuli 94

4.4.3 Transcriptional regulation of ACO gene expression 96

4.4.4 Crosstalk between ethylene signalling elements and ACO gene expression 97

4.5 Translational regulation of ACC oxidase 97

4.6 Evidence that ACC oxidase acts as a control point in ethylene biosynthesis 100

4.6.1 Cell-specific expression of ACC oxidase 102

4.6.2 Differential expression of ACS and ACO genes 103

4.7 Evolutionary aspects of ACC oxidase 104

Acknowledgements 105

References 105

5 Perception of Ethylene by Plants – Ethylene Receptors 117
Brad M. Binder, Caren Chang and G. Eric Schaller

5.1 Historical overview 118

5.2 Subfamilies of ethylene receptors and their evolutionary history 120

5.3 Ethylene binding 123

5.3.1 Requirements for a metal cofactor 123

5.3.2 Characterization of the ethylene-binding pocket and signal transduction 124

5.4 Signal output from the receptors 126

5.5 Overlapping and non-overlapping roles for the receptor isoforms in controlling various phenotypes 128

5.6 Post-translational regulation of the receptors 131

5.6.1 Clustering of receptors 131

5.6.2 Ethylene-mediated degradation of receptors 132

5.6.3 Regulatory role of REVERSION-TO-ETHYLENE SENSITIVITY1 (RTE1)/GREEN-RIPE (GR) 133

5.6.4 Other proteins that interact with the ethylene receptors 134

5.7 Conclusions and model 135

Acknowledgements 137

References 138

6 Ethylene Signalling: the CTR1 Protein Kinase 147
Silin Zhong and Caren Chang

6.1 Introduction 148

6.2 Discovery of CTR1, a negative regulator of ethylene signal transduction 148

6.2.1 Isolation of the Arabidopsis CTR1 mutant 148

6.2.2 CTR1 mutant phenotypes in Arabidopsis 149

6.2.3 Placement of CTR1 in the ethylene-response pathway 150

6.3 CTR1 Encodes a serine/threonine protein kinase 151

6.3.1 Molecular cloning and sequence analysis of the Arabidopsis CTR1 gene 151

6.3.2 CTR1 biochemical activity 152

6.4 The CTR1 gene family 153

6.4.1 The CTR multi-gene family in tomato 153

6.4.2 Functional roles of tomato CTR genes 153

6.4.3 Transcriptional regulation of CTR-like genes 155

6.5 Regulation of CTR1 activity 156

6.5.1 Physical association of CTR1 with ethylene receptors 158

6.5.2 Membrane localization of CTR1 159

6.5.3 An inhibitory role for the CTR1 N-terminus? 159

6.5.4 Other factors that potentially interact with and regulate CTR1 activity 160

6.6 Elusive targets of CTR1 signalling 161

6.7 CTR1 crosstalk and interactions with other signals 162

6.8 Conclusions 163

Acknowledgements 164

References 164

7 EIN2 and EIN3 in Ethylene Signalling 169
Young-Hee Cho, Sangho Lee and Sang-Dong Yoo

7.1 Introduction 169

7.2 Overview of ethylene signalling and EIN2 and EIN3 172

7.3 Genetic identification and biochemical regulation of EIN2 173

7.4 EIN3 regulation in ethylene signalling 174

7.4.1 Genetic identification and biochemical regulation of EIN3 174

7.4.2 Structural and functional analysis of ein3 function 178

7.4.3 Function of EIN3 as transcription activator 180

7.5 Functions of ERF1 and other ERFs in ethylene signalling 181

7.6 Future directions 183

Acknowledgements 184

References 184

8 Ethylene in Seed Development, Dormancy and Germination 189
Renata Bogatek and Agnieszka Gniazdowska

8.1 Introduction 189

8.2 Ethylene in seed embryogenesis 192

8.2.1 Ethylene biosynthesis during zygotic embryogenesis 192

8.2.2 Ethylene involvement in the regulation of seed morphology 194

8.3 Ethylene in seed dormancy and germination 194

8.3.1 Ethylene biosynthesis during dormancy release and germination 194

8.3.2 The role of ethylene in seed heterogeneity 199

8.4 Ethylene interactions with other plant hormones in the regulation of seed dormancy and germination 199

8.5 Ethylene interactions with ROS in the regulation of seed dormancy and germination 202

8.6 Ethylene interactions with other small gaseous signalling molecules (NO, HCN) in the regulation of seed dormancy and germination 204

8.7 Concluding remarks 207

Acknowledgements 209

References 209

9 The Role of Ethylene in Plant Growth and Development 219
Filip Vandenbussche and Dominique Van Der Straeten

9.1 Introduction 219

9.2 Design of root architecture 220

9.3 Regulation of hypocotyl growth 225

9.4 Shoot architecture and orientation: post-seedling growth 229

9.4.1 Inhibition of growth by ethylene 229

9.4.2 Stimulation of growth by ethylene 229

9.4.3 Shoot gravitropism 231

9.4.4 Control of stomatal density and aperture 231

9.4.5 Activity of the shoot apical meristem 231

9.5 Floral transition 232

9.6 Determination of sexual forms of flowers 232

9.7 Ethylene effects on growth controlling mechanisms 233

9.8 Conclusions 234

Acknowledgements 234

References 234

10 Ethylene and Cell Separation Processes 243
Zinnia H. Gonzalez-Carranza and Jeremy A. Roberts

10.1 Introduction 243

10.2 Overview of the cell separation process 244

10.2.1 Abscission 245

10.2.2 Dehiscence 249

10.2.3 Aerenchyma formation 251

10.2.4 Stomata development and hydathode formation 252

10.2.5 Root cap cell sloughing and lateral root emergence 254

10.2.6 Xylem differentiation 257

10.3 Transcription analyses during cell separation 258

10.4 Relationship between ethylene and other hormones in the regulation of cell separation 259

10.4.1 Ethyene and IAA 259

10.4.2 Ethylene and jasmonic acid 260

10.4.3 Ethylene and abscisic acid 261

10.5 Ethylene and signalling systems during cell separation 261

10.5.1 Role of IDA, IDA-like, HAESA and HAESA-like genes 261

10.5.2 MAP kinases 262

10.5.3 Nevershed 262

10.6 Application of knowledge of abscission to crops of horticultural and agricultural importance 262

10.7 Conclusions and future perspectives 263

References 265

11 Ethylene and Fruit Ripening 275
Jean-Claude Pech, Eduardo Purgatto, Mondher Bouzayen and Alain Latch´e

11.1 Introduction 276

11.2 Regulation of ethylene production during ripening of climacteric fruit 276

11.2.1 Regulation of ethylene biosynthesis genes during the System 1 to System 2 transition 277

11.2.2 ACS gene alleles are major determinants of ethylene biosynthesis and shelf-life of climacteric fruit 280

11.2.3 Genetic determinism of the climacteric character 281

11.3 Transcriptional control of ethylene biosynthesis genes 282

11.4 Role of ethylene in ripening of non-climacteric fruit 283

11.5 Manipulation of ethylene biosynthesis and ripening 284

11.6 Ethylene-dependent and -independent aspects of climacteric ripening 286

11.7 Ethylene perception and transduction effects in fruit ripening 288

11.7.1 Ethylene perception 288

11.7.2 Chemical control of the post-harvest ethylene response in fruit ripening 289

11.7.3 Ethylene signal transduction 290

11.7.4 The transcriptional cascade leading to the regulation of ethylene-responsive and ripening-related genes 291

11.8 Hormonal crosstalk in fruit ripening 292

11.8.1 Ethylene and abscisic acid 293

11.8.2 Ethylene and jasmonate 293

11.8.3 Ethylene and auxin 294

11.8.4 Ethylene and the gibberellins 295

11.9 Conclusions and future directions 295

Acknowledgements 296

References 296

12 Ethylene and Senescence Processes 305
Laura E. Graham, Jos H.M. Schippers, Paul P. Dijkwel and Carol Wagstaff

12.1 Introduction 306

12.2 Overview of ethylene-mediated senescence in different plant organs 306

12.2.1 Leaf senescence 306

12.2.2 Pod senescence 310

12.2.3 Petal senescence 312

12.3 Transcriptional regulation of ethylene-mediated senescence processes 314

12.3.1 Global regulation 314

12.3.2 Transcription factors and signalling pathways 315

12.4 Interaction of ethylene with other hormones in relation to senescence 323

12.5 The importance of ethylene-mediated senescence in post-harvest biology 325

12.5.1 Post-harvest factors affected by ethylene 325

12.5.2 Ways of controlling ethylene-related post-harvest losses 327

12.5.2.1 Packaging 327

12.5.2.2 1-Methylcyclopropene 328

12.6 Conclusions and future perspectives 329

References 329

13 Ethylene: Multi-Tasker in Plant–Attacker Interactions 343
Sjoerd Van der Ent and Corn´e M.J. Pieterse

13.1 Introduction 344

13.2 Hormones in plant defence signalling 346

13.2.1 Hormones as defence regulators 346

13.2.2 Salicylic acid 347

13.2.3 Jasmonic acid 347

13.2.4 Ethylene 348

13.3 Implications of ethylene in basal defence and disease susceptibility 348

13.3.1 Studies with Arabidopsis thaliana 348

13.3.2 Studies with tobacco 350

13.3.3 Studies with tomato 351

13.3.4 Studies with soybean 352

13.3.5 Other plant species 352

13.4 Implications of ethylene in systemic immune responses 353

13.4.1 Systemic induced immunity 353

13.4.2 Rhizobacteria-mediated ISR 354

13.4.3 Genetic dissection of the ISR pathway in Arabidopsis 356

13.4.4 Priming for enhanced JA/ethylene-dependent defences 358

13.4.5 Molecular mechanisms of priming for enhanced defence 360

13.4.6 Costs and benefits of priming for enhanced defence 362

13.5 Ethylene modulates crosstalk among defence-signalling pathways 362

13.5.1 Crosstalk in defence signalling 362

13.5.2 Interplay among SA, JA and ethylene signalling 363

13.5.3 Ethylene: an important modulator of defence-signalling pathways 365

13.6 Concluding remarks 365

Acknowledgements 366

References 367

Index 379

First 8-page color plate section (between pages 168 and 169)

Second 8-page color plate section (between pages 360 and 361)

Michael McManus is Professor at the Institute of Molecular Biosciences at Massey University, New Zealand. He is also an Editorial Board Member of Annual Plant Reviews.