List of Contributors xv

Preface xxi

Section 1 Biochemistry of Insect-Plant Interactions

1 Plants Recognize Herbivorous Insects by Complex Signalling Networks 1
Gustavo Bonaventure

1.1 Introduction 1

1.1.1 The feeding behaviour of insects is an important determinant of the plant’s defence response 1

1.1.2 Insect-associated elicitors are specific elicitors of plant responses to insect feeding or egg deposition 2

1.2 Resistance (R) genes in the perception of piercing-sucking insects 6

1.3 Modification of elicitors by plant enzymes 8

1.4 Changes in Vm, Ca2+influx and reactive oxygen intermediate generation are early cellular events induced in plants by insect feeding 9

1.5 Shared signal transduction components in microbe and insect elicitor perception 12

1.6 Regulation of phytohormone accumulation and signaling during insect feeding 14

1.6.1 Jasmonic acid 17

1.6.2 Ethylene 20

1.6.3 Salicylic acid 21

1.7 Interconnection of the phytohormone system in plants 22

1.8 Conclusions and perspectives 23

Acknowledgements 24

References 24

2 Herbivore Oral Secretions are the First Line of Protection Against Plant-Induced Defences 37
Gary W. Felton, Seung Ho Chung, Maria Gloria Estrada Hernandez, Joe Louis, Michelle Peiffer and Donglan Tian

2.1 Introduction 38

2.2 Origin of herbivore secretions and initiation of contact with the host plant 40

2.2.1 Piercing-sucking herbivores 41

2.2.2 Chewing herbivores 42

2.3 How do herbivores deliver effectors to the host plant? 45

2.4 Examples of HAMPs and effectors 46

2.4.1 Piercing-sucking herbivores 46

2.4.2 Chewing herbivores 49

2.5 Effectors and host targets 54

2.6 Effectors and the host plant diet 56

2.7 Metagenomes: The interkingdom crossroads of the host plant, herbivore, and microbiome 56

Acknowledgements 62

References 62

3 Insect Detoxification and Sequestration Strategies 77
David G. Heckel

3.1 Introduction 77

3.2 Diverse roles of insect cytochromes P450 78

3.2.1 Furanocoumarin detoxification by Papilio spp. and others 79

3.2.2 Monoterpene detoxification and pheromone biosynthesis in pine bark beetles 84

3.2.3 Gossypol and CYP6AE14 in Helicoverpa armigera 85

3.2.4 Cactophilic Drosophila and alkaloid detoxification 85

3.3 Cyanogenic glucosides 86

3.4 Glucosinolates 89

3.5 Oglucosides and leaf beetles 93

3.6 Pyrrolizidine alkaloids 97

3.7 Glycosylation of host plant compounds 99

3.8 Non-protein amino acids 101

3.9 Iridoid glucosides 102

3.10 Cardenolides 103

3.11 Conclusions 106

Acknowledgements 107

References 107

4 Plant Semiochemicals – Perception and Behavioural Responses by Insects 115
Andreas Reinecke and Monika Hilker

4.1 Introduction 115

4.2 A semiochemical’s route to the neuron 118

4.2.1 Surfing the surface – A matter of chemo-physical interaction 120

4.2.2 Odorant binding proteins, chemosensory proteins 122

4.2.3 Eliciting signals – Odorant receptors and sensory neuron responses to odorants 123

4.2.4 The clean-up company – Odorant-degrading enzymes 128

4.2.5 Odour perception – Summary 128

4.3 Behavioural responses of insects to plant volatiles 129

4.3.1 Biotic habitat factors influencing plant odour dispersal and insect orientation 130

4.3.2 Biotic factors affecting plant odour emission 131

4.3.3 ‘Wise’ responses to plant odours? The impact of odour experience on insect behaviour 132

4.3.4 Sick insects and their responses to plant odour 134

4.3.5 Age-dependency of insect responses to plant odour 134

4.3.6 Adjusting the responses to plant odour according to the needs 135

4.4 Conclusions 136

References 137

Section 2 Genetics and Genomics of Insect-Plant Interactions

5 Plant Transcriptomic Responses to Herbivory 155
Hanna M. Heidel-Fischer, Richard O. Musser and Heiko Vogel

5.1 Introduction 155

5.2 Mechanical wounding, feeding mode and HAMPs 157

5.3 Wounding rates and salivary gland applications 158

5.4 Responses to insects from different feeding guilds 165

5.4.1 Chewing herbivores 167

5.4.2 Piercing-sucking herbivores 168

5.4.3 The pitfalls of the generalist-specialist paradigm 171

5.5 A meta-analysis of microarray studies on transcriptomic responses to herbivory 172

5.6 Simultaneous attack or multiple feeding 176

5.7 Transcriptomics responses to herbivory – An outlook 179

5.7.1 Open questions 179

5.7.2 New tools and approaches 181

Acknowledgements 182

References 182

6 Transcriptome Responses in Herbivorous Insects Towards Host Plant and Toxin Feeding 197
Heiko Vogel, Richard O. Musser and Maria de la Paz Celorio-Mancera

6.1 Introduction 198

6.2 Challenges for insect herbivores and inducible responses 200

6.2.1 Phytohormones 202

6.2.2 Plant defensive chemicals – Toxins and deterrents 205

6.2.3 Proteinaceous effectors 210

6.2.4 Plant nutrients 212

6.2.5 Whole plant, tissue and organ feeding 214

6.2.6 Common expression signatures and specific differences 215

6.3 Genomic responses to plant and toxin feeding – An outlook 218

6.3.1 Open questions 218

6.3.2 New tools and approaches 221

Acknowledgements 223

References 223

7 Quantitative Genetics and Genomics of Plant Resistance to Insects 235
Daniel J. Kliebenstein

7.1 Introduction 235

7.2 Metabolites 238

7.2.1 Glucosinolates 238

7.2.2 Maysin 245

7.2.3 Tomato trichome chemistry 245

7.2.4 Saponins 246

7.3 Physical defences 246

7.4 Signal transduction variation 248

7.5 Physiology 249

7.6 Why have genetic variation in defence? 249

7.7 Summary 250

References 252

Section 3 Ecology and Evolution of Insect-Plant Interactions

8 Costs of Resistance in Plants: From Theory to Evidence 263
Don Cipollini, Dale Walters and Claudia Voelckel

8.1 The cost-benefit paradigm 263

8.1.1 Hypotheses of plant defence 265

8.1.2 Why do plants have induced defences? 272

8.2 Measuring fitness costs and benefits of plant defence traits 276

8.2.1 Generating trait variation 276

8.2.2 The empirical evidence for costs of resistance 284

8.3 Ecologically relevant settings 289

8.3.1 Competition 290

8.3.2 Nutrient availability 293

8.3.3 Multiple enemies 294

8.3.4 Enemies vs. mutualists 295

8.4 Conclusions 297

References 297

9 Plant-mediated Interactions Among Insects within a Community Ecological Perspective 309
Erik H. Poelman and Marcel Dicke

9.1 Introduction to plant-mediated species interactions 309

9.1.1 Plant-based insect community structure 309

9.1.2 Plant-mediated species interactions 311

9.2 Plant-mediated species interactions among herbivores 313

9.2.1 Specificity of plant responses to herbivores 313

9.2.2 Asymmetric plant-mediated effects on herbivore performance 314

9.2.3 Plant-mediated effects on herbivore oviposition 315

9.3 Three trophic level interactions 316

9.3.1 Attraction of natural enemies 316

9.3.2 Herbivore diversity affects plant-mediated interactions with natural enemies 318

9.4 Aboveground-belowground interactions 319

9.5 Herbivore-pollinator interactions 320

9.6 Plant-mediated species interactions in a community 322

9.6.1 Plant-mediated interactions involving multiple herbivores 322

9.6.2 Carnivores affecting plant-mediated interactions in communities 325

9.6.3 Plant-mediated interactions beyond individual plants 326

9.7 Synthesis in the context of plant fitness and future directions 327

References 329

10 The Altitudinal Niche-Breadth Hypothesis in Insect-Plant Interactions 339
Sergio Rasmann, Nadir Alvarez and Löıc Pellissier

10.1 Introduction – Variation of niche-breadth along ecological gradients 340

10.2 Herbivorous insects, from specialists to generalists 343

10.3 Evidence for an altitudinal gradient in niche-breadth and climatic variability 344

10.3.1 Does environmental variability increase with increasing altitude? 345

10.3.2 Does variability in host-plant population size increase with increasing altitude? 346

10.4 The altitudinal niche-breadth paradigm 348

10.4.1 Pollinators 348

10.4.2 Herbivores, plant quality and plant defences 349

10.4.3 Predator effects on herbivores 350

10.5 Outlook – Other factors influencing altitudinal niche breadth evolution studies 351

10.5.1 Phylogenetic constraints and correlated life-history traits 351

10.5.2 Phylogeography 352

10.5.3 Phytophagous insect abundance 352

10.5.4 Range size 353

10.5.5 Non-linear relationship along the altitudinal clines 353

10.6 Conclusion 354

Acknowledgements 354

References 354

11 Revisiting Plant-Herbivore Co-Evolution in the Molecular Biology Era 361

Georg Jander

11.1 Introduction 361

11.2 Glucosinolates in the Brassicaceae 363

11.3 Benzoxazinoids in the Poaceae 365

11.4 Evolution from primary metabolism 367

11.5 Convergent evolution of defence pathways 368

11.6 Rapid adaptation through modular biosynthetic pathways 370

11.7 Specialist herbivores have evolved to detoxify secondary metabolites 371

11.8 Costs of plant resistance 372

11.9 Molecular phylogenetic evidence for co-evolution 374

11.10 The benefits of metabolic pathway co-regulation 374

11.11 Modification of secondary metabolites as a form of defensive priming 375

11.12 Use of secondary metabolites as defensive signals 377

11.13 Conclusion and future prospects 378

References 379

Index 385

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