Plant Epigenetics (eBook)

​Prof. Dr. Nikolaus Rajewsky,Berlin Inst. for Medical Systems Biology, MaxDelbrückCenter for Molecular Medicine,Berlin-Buch,Germanyrajewsky@mdc-berlin.deProf. Dr. Stefan Jurga, Adam Mickiewicz University, Nanobiomedical Center,Poznań,Polandstjurga@amu.edu.plProf. Dr. Jan Barciszewski, Polish Academy of Sciences,Institute of Bioorganic Chemistry,Poznań,Polandjan.barciszewski@ibch.poznan.pl

Preface 6
Plant Epigenetics: From Genotype to Phenotype 6
Contents 9
Conservation, Divergence, and Abundance of MiRNAs and Their Effect in Plants 12
1 Introduction 13
2 General Aspects of MiRNAs 13
3 Biogenesis and Action of MiRNAs 14
4 Classification, Conservation, Divergence, and Abundance of MiRNAs in Plants 16
5 MiRNA Functions in Plants 18
6 Pleiotropic Effects of MiRNAs 26
7 Conclusions and Future Prospects 27
References 27
The Role of MiRNAs in Auxin Signaling and Regulation During Plant Development 34
1 Introduction 35
1.1 Auxins 35
1.2 MiRNAs 37
2 Biogenesis and Function of MiRNAs in Plants 40
3 Evolution of Plant MicroRNA Genes 42
4 Gene Regulation by MicroRNAs in Plants 44
5 MiRNAs in Auxins Signaling and Homeostasis 45
5.1 Auxin Homeostasis and MiRNAs 47
5.2 Auxin Signaling and MiRNAs 48
6 Role of MiRNA in Plant Growth and Development Mediated by Auxins 49
7 Concluding Remarks 51
References 52
Growing Diversity of Plant MicroRNAs and MIR-Derived Small RNAs 60
1 Introduction 61
2 Micro RNAs in the Plant Small RNA World 61
3 MiRNA-Mediated DNA Methylation 63
3.1 First Evidences for an Indirect Link Between MiRNAs and DNA Methylation 64
3.2 MIR-Derived sRNAs: The Real Players in MiRNA-Mediated DNA Methylation 65
4 Epigenetic Control of MIR Genes 67
4.1 Impact of Histone Modifications of MIR Loci on MiRNA Expression 67
4.2 DNA Methylation of MIR Genes Affects MiRNA Expression 68
4.3 Link Between MIR Gene DNA Methylation and Plant Stress Response 69
5 Computational Tools for Plant MiRNA Analysis from NGS Datasets 70
References 74
An Evolutionary View of the Biogenesis and Function of Rice Small RNAs 79
1 Introduction 80
2 Evolution of Core RNA Interference (RNAi) Pathway Genes in Rice 81
2.1 Dicer-Like 83
2.2 RNA-Dependent RNA Polymerases 84
2.3 Hua Enhancer 1 84
2.4 Argonaute 85
3 Evolution of Rice Small RNAs and Their Targets 86
3.1 Canonical miRNAs 86
3.1.1 Evolution of miRNAs in AA Genome Oryza Species 86
3.1.2 MiRNA Genes Under Positive Selection in Cultivated Rice 87
3.1.3 MiRNA Targets Under Positive Selection in Cultivated Rice 90
3.2 Long miRNAs 90
3.3 Phased siRNAs 91
3.4 Heterochromatic siRNAs 92
4 Conclusions and Future Prospects 93
References 93
Small RNAs: Master Regulators of Epigenetic Silencing in Plants 99
1 Introduction 100
2 Nuclear sRNA-Dependent Gene Silencing 102
3 Small RNA-Directed DNA Methylation in Plants 105
4 Mechanism of Transposon Repression by sRNAs and Silencing of Transposons 109
5 Conclusion and Future Perspectives 110
References 111
Small RNA Biogenesis and Degradation in Plants 117
1 Introduction 118
2 miRNA Biogenesis in Plants 118
3 The Biogenesis of ta-siRNAs and pha-siRNAs 121
4 The Biogenesis of Natural cis-antisense siRNAs (nat-siRNAs) 123
5 The Production of sRNAs Involved in RNA-Direct DNA Methylation (RdDM) 124
5.1 The Biogenesis of Canonical ra-siRNAs 124
5.2 The Biogenesis of Non-canonical sRNAs Involved in RdDM 125
6 Methylation Stabilizes miRNAs and siRNAs 126
7 Uridylation Triggers the Degradation of siRNAs and miRNAs 128
8 Exoribonucleases Degrading sRNAs in Plants 129
9 Perspective 130
References 131
Plant Epigenetics: Non-coding RNAs as Emerging Regulators 138
1 Introduction 139
2 MicroRNAs in Plants 140
3 Small Interfering RNAs (siRNAs) 141
3.1 Secondary SiRNAs 141
3.2 Heterochromatic SiRNAs and RNA-Directed DNA Methylation 143
4 Long Non-Coding RNAs 145
4.1 Plant LncRNAs, Professional Hijackers 147
4.2 LncRNAs Mediate Chromatin Modifications and Remodeling 149
4.3 LncRNAs and Epigenomic Regulation of Flowering 150
4.4 LncRNAs Link Hormone Signaling with Chromatin Modifications and Genome 3D-Conformation 151
5 Concluding Remarks 151
References 152
Genome-Wide Function Analysis of lincRNAs as miRNA Targets or Decoys in Plant 157
1 Introduction 158
2 Materials 159
2.1 Hardware Requirements 159
2.2 Software Requirements 159
2.3 Data Resources 159
3 Methods 161
3.1 Identification of Unique Maize miRNAs 161
3.2 Set up the Relationship Between Unique miRNAs and lincRNAs 162
3.3 Set up the Relationship Between Unique miRNAs and mRNAs 162
3.4 Functional Prediction of lincRNAs Acting as miRNA Targets Based on the lincRNA-mRNA Co-expression Networks 163
3.4.1 Identification of lincRNAs Acting as miRNA Targets 163
3.4.2 Construction of lincRNA-mRNA Co-expression Networks 164
3.4.3 Functional Prediction of lincRNAs as miRNA Targets 165
3.5 Functional Prediction of lincRNAs Acting as miRNA Decoys Based on CeRNA Hypothesis 166
3.5.1 Identification of mRNAs Acting as miRNA Targets 166
3.5.2 Identification of lincRNAs as miRNA Decoys 166
3.5.3 Functional Prediction of lincRNAs as miRNA Decoys Based on CeRNA Hypothesis 168
4 Notes 168
References 169
Plant Non-coding RNAs and the New Paradigms 171
1 Introduction 172
2 LncRNAs 173
2.1 LncRNA Transcriptional Activity 173
2.2 LncRNA Posttranscriptional Activity 175
2.3 LncRNAs: Non-coding Transcripts or Dual RNAs? 177
3 MiRNAs 178
3.1 MiRNAs: Specialized Products of LncRNAs 178
3.2 MiRNA Activity 181
3.3 Function of MiRNA-Guided Translation Inhibition 183
4 Conclusion 185
References 185
Epigenetic Regulation by Noncoding RNAs in Plant Development 191
1 Introduction 192
2 Diverse Noncoding RNAs 192
3 miRNAs and Epigenetics in Plant 193
3.1 MiRNAs and Vegetable Organ Development 193
3.2 miRNAs and Floral Transition 195
3.3 miRNAs and Male Reproductive Development 195
3.4 miRNAs and Female Reproductive Development 197
4 lncRNAs and Epigenetics in Plant 198
4.1 lncRNAs Discoveries in Different Plant Model Species 198
4.2 The Regulation Pathways of lncRNAs Related to Plant Development 199
4.3 lncRNAs in Reproductive Development 200
4.4 Stress-Responsive lncRNAs in Plants 201
5 Conclusion and Prospects 202
References 203
RNAi Suppressors: Biology and Mechanisms 207
1 Introduction 209
2 RNAi and the Suppressors 209
3 Antiviral RNAi 210
3.1 Viral SiRNA Generation 210
3.2 Transcriptional Control of Viral Genes 212
3.3 Post-transcriptional Control of Viral Proteins 213
3.3.1 Post-transcriptional Gene Silencing 213
3.3.2 Host MiRNA Control of Viral Genes 214
4 Viral Counterstrategy 217
4.1 Earlier Experiments to Confirm RNA Silencing Suppression 217
4.2 Assays to Detect RNA Silencing Suppressors 218
4.2.1 Agrobacterium-Mediated Transient Assay 218
4.2.2 Reversal of Transgene Induced Silencing 219
4.2.3 Crossing Assay 219
4.2.4 Grafting Assay 219
4.2.5 Specific Biochemical Assays 220
5 Functional Mechanism of Viral Suppressors of RNAi 220
5.1 Interaction Between DsRNA-VSRs 220
5.2 Viral Suppressors Target RNAi Effectors 221
5.3 Suppression of Systemic RNAi by VSRs 221
5.4 Epigenetic Modifications 221
6 Few Representative VSRs 222
6.1 HC-Pro of Potyviruses 222
6.2 Cucumoviruses 2b (CMV-2b) 223
6.3 Tombusviruses P19 224
6.4 Geminivirus AC2 225
6.5 Polerovirus P0 227
7 Disease or Pathogenicity: Host MicroRNA Dysregulation and Affected Functions 227
8 VSR-Targeted Antiviral Strategy 228
8.1 Artificial MiRNA Strategy 228
8.2 Artificial TasiRNA Strategy 229
9 Future Perspectives 229
References 231
Analysis of Nucleic Acids Methylation in Plants 239
1 General Functions of DNA and RNA Methylation in Plants 240
1.1 DNA Cytosine Methylation in Plants 240
1.2 RNA Cytosine Methylation in Plants 240
1.3 RNA Adenine Methylation in Plants 241
2 Global Detection of DNA and RNA Methylation in Plants 241
2.1 Liquid Chromatography 241
2.2 Liquid Chromatography-Mass Spectrometry 243
2.3 Capillary Electrophoresis 244
2.4 Thin Layer Chromatography 244
2.5 Immuno-Based Detection 245
3 Location Analysis of DNA and RNA Methylation in Plants 245
3.1 Affinity Enrichment-Sequencing Analysis 246
3.2 Bisulfite Conversion-Sequencing Analysis 247
3.3 Single-Molecule Detection 249
4 Conclusions and Perspectives 249
References 250
DNA Methylation in Plants by microRNAs 254
1 Introduction 255
2 DNA Methylation by 20-22 nt Canonical miRNAs 257
2.1 In Arabidopsis 257
2.2 In Moss 257
3 DNA Methylation by siRNAs Produced from miRNA Loci 258
4 DNA Methylation by lmiRNAs 260
5 DNA Methylation by siRNAs or lmiRNAs Originating from miRNA Genes Located in the Introns 261
6 DNA Methylation by miRNA-Triggered TAS/PHAS Loci-Derived siRNAs 261
7 miRNA-Triggered easiRNA Biogenesis to Prevent RDR2-Dependent RdDM 263
8 miRNAs Directly Regulating Players of Methylation 264
9 Conclusions and Perspectives 264
References 267
DNA Methylation in Plants and Its Implications in Development, Hybrid Vigour, and Evolution 270
1 Introduction 271
1.1 The Machinery of DNA Methylation and Demethylation 271
1.2 Features and Distribution of DNA Methylation in Plants 272
1.3 General Aspects of the Possible Roles of DNA Methylation in Plants 274
2 Patterns of DNA Methylation Are Proposed to Change in Response to Environmental Stresses 275
2.1 Some Examples of Responses to Biotic and Abiotic Stresses 276
3 DNA Methylation During Plant Development 277
3.1 Does DNA Methylation Change During Development and Among Plant Tissues? 278
4 DNA Methylation and Its Suggested Role for Evolution in Plants 279
5 Proposed Function and Evidences for the Influence of the Epigenetic State in Heterosis 280
6 Conclusions and Perspectives 281
References 282
Dynamic DNA Methylation Patterns in Stress Response 288
1 Introduction 289
2 DNA Methylation in Plants 290
3 Genome-Wide DNA Methylation Under Stress 291
3.1 Correlation of DNA Methylation Patterns with Stress Tolerance of Different Genotypes 293
3.2 Inheritable Changes in DNA Methylation Patterns in Plants Subjected to Stress 294
4 Involvement of DNA Methylation Changes in the Control of Stress-Responsive Genes 296
4.1 Changes in DNA Methylation of Specific Stress-Responsive Genes 296
4.2 Hierarchic Control of DNA Methylation in the Induction of Stress-Related Genes 299
5 Regulation of Dynamics of DNA Methylation Under Stress 301
6 Conclusions 303
References 304
Locus-Specific DNA Methylation Analysis and Applications to Plants 310
1 Introduction 311
2 DNA Methylation in Plants 312
2.1 Generalities 312
2.2 Distribution of DNA Methylation in Plants 313
2.3 Differences Between Plant Genomes 314
3 Locus-Specific DNA Methylation Analysis Methods 315
3.1 Methods Not Involving Sodium Bisulfite Conversion 315
3.1.1 Methods Involving Methylation-Sensitive Restriction Enzyme and PCR 315
3.1.2 Methods Involving Anti-meCytosine Antibody and PCR 318
3.2 Methods Involving Sodium Bisulfite Conversion 319
3.2.1 Bisulfite Conversion 320
3.2.2 Primer Design 321
3.2.3 Methods Without Sequencing 322
High Resolution Melting Analysis 323
Other Methods 323
3.2.4 Methods Including Sequencing Experiments 324
Cloning Combined to Sanger Sequencing 324
Pyrosequencing 326
4 Conclusion: Perspectives 328
References 329
Epigenetics in Plant Reproductive Development: An Overview from Flowers to Seeds 335
1 Introduction 336
2 Flowering and Pollen Development 338
3 Flower and Fruit Development 339
3.1 Histone Acetylation Mediated Regulation 339
3.2 DNA Methylation-Mediated Regulation 341
3.3 MiRNA Mediated Regulation 342
4 Fruit Ripening 344
4.1 DNA Methylation-Mediated Regulation 346
4.2 MiRNA Mediated Regulation 347
4.3 LncRNA Mediated Regulation 348
5 Seed Development 349
5.1 Seed Dormancy 350
5.2 Embryo-Endosperm Interaction 353
5.3 Genomic Imprinting 355
6 Conclusions and Future Prospects 356
References 357
Epigenetic Regulation of Phase Transitions in Arabidopsis thaliana 364
1 Introduction 365
2 Epigenetic Regulation of the Embryo-to-Seedling Transition 368
3 Epigenetic Regulation of the Juvenile-to-Adult and Vegetative-to-Reproductive Transitions 372
4 Epigenetic Reprogramming 377
5 Conclusions and Future Prospects 379
References 382
Epigenetics in Plant-Pathogen Interactions 389
1 Introduction 390
2 Epigenetic Modification Marks in Plants 391
2.1 DNA Methylation 391
2.2 Histone Modifications 393
3 Overview of Gene/Genomic Regulation in Plants Based on Epigenetics 394
3.1 Control of Developmental Switches: Vegetative to Reproductive Transition 394
3.2 Silencing of Transposable Elements 395
3.3 The RNA Silencing Pathways Involved in TE Silencing: 24nt-Long and 22nt-Long siRNAs in RNA-Directed DNA Methylation 395
3.4 Parental Imprinting 396
3.5 Paramutation 397
3.6 Virus-Induced Gene Silencing 397
3.6.1 RdRM-Induced by Viral and Subviral Infectious Entities 399
3.6.2 Influence of Viral Silencing Suppressor on Virus-Induced RdRM 400
4 Epigenetic Modifications and Systemic Acquired Resistance 401
5 Conclusions and Perspectives 404
References 405
Epigenetic Reprogramming During Plant Reproduction 409
1 Introduction 410
2 Epigenetic Mechanisms Mediated by DNA Methylation 411
2.1 DNA Methylation by DNA Methyltransferases 411
2.2 DNA Demethylation by DEMETER Family Glycosylases 412
3 Epigenetic Mechanisms Mediated by Histone Modifications 412
3.1 Histone Modification by the PRC2 412
3.1.1 Endosperm Development 413
3.1.2 Seed to Seedling Phase Transition 413
3.1.3 Vegetative to Reproductive Phase Transition 414
3.1.4 Vernalization 414
4 Epigenetic Reprogramming During Arabidopsis Male Gametogenesis (Fig. 1) 414
4.1 Microgametogenesis in Arabidopsis 414
4.2 Chromatin Reorganization During Pollen Mother Cell Differentiation 416
4.3 Chromatin Remodeling During Male Gametogenesis 416
4.4 Dynamic Changes of DNA Methylation During Male Gametogenesis 417
5 Epigenetic Reprogramming During Arabidopsis Female Gametogenesis (Fig. 2) 419
5.1 Megagametogenesis in Arabidopsis 419
5.2 Mobile siRNAs During Megaspore Mother Cell Differentiation and Meiosis 420
5.3 Chromatin Reorganization During Megasporogenesis and Megagametogenesis 421
5.4 Active DNA Demethylation by the DEMETER Glycosylase in the Gametophytes 421
6 Conclusions and Future Perspectives 423
References 424
Rice Epigenomics: How Does Epigenetic Manipulation of Crops Contribute to Agriculture? 430
1 Introduction 431
2 Epigenome Regulation in Arabidopsis and Rice 432
3 Epigenome Regulation in Response to Abiotic Stresses 436
4 Stable Maintenance of Altered Epigenomic State for Agricultural Applications 438
5 Perspectives 439
References 440
Epigenetic Characterization of Satellite DNA in Sugar Beet (Beta vulgaris) 447
1 Introduction: Sugar Beet (Beta vulgaris) and Its Wild Relatives 448
2 Genomes, Chromosomes and Satellite DNAs 449
3 Satellite DNAs Are a Major Repeat Class in Sugar Beet Heterochromatin and Centromeric Chromatin 450
4 Epigenetic Characterization of Satellite DNA Suggests Their Potential Function in the Establishment and Maintenance of Heter... 454
5 Satellite DNA-Directed Heterochromatization 459
6 Conclusion 461
References 462
Universal and Lineage-Specific Properties of Linker Histones and SWI/SNF-Chromatin Remodeling Complexes in Plants 465
1 Introduction: Chromatin in Plants and Animals: Commonalities and Differences After Over One Billion Years of Separate Evolut... 466
2 Linker Histones and SWI/SNF Remodeling Complexes in Chromatin Organization and Regulatory Mechanisms: Conclusions from Studi... 467
2.1 Linker Histones 467
2.2 SWI/SNF Chromatin Remodeling Complexes 470
2.2.1 Mechanisms of Chromatin Remodeling 471
2.2.2 Biological Roles of SWI/SNF Remodelers 473
2.2.3 Targeting of SWI/SNF Complexes to Specific Sites in the Genome 474
3 Linker Histones in Plants 475
3.1 Structural Features and Phylogenetic Relationships Distinguishing Plant H1s 475
3.2 Universally Conserved and Lineage-Specific Functions of Plant H1s 478
4 SWI/SNF Complexes in Plants 480
4.1 Composition of Plant SWI/SNF Complexes 480
4.2 Biological Roles of Plant SWI/SNF Complexes 482
4.3 Mechanisms Underlying the Functions and Targeting of Plant SWI/SNF Complexes 483
5 Are Linker Histones and Chromatin Remodeling Structurally and Functionally Coupled? 486
6 Concluding Remarks 488
References 488
Abiotic Stress Induced Epigenetic Modifications in Plants: How Much Do We Know? 495
1 Introduction 497
2 The Pillars of Epigenetics 498
2.1 DNA Methylation 498
2.2 Histone Modifications 500
2.3 Small RNAs 500
3 RNA-Directed DNA Methylation Pathway 501
4 Chromatin Modifications 502
5 Abiotic Stress Directed Epigenetic Changes 502
5.1 Stress Memory 503
6 Abiotic Stressors 504
6.1 Salt Stress 504
6.2 Drought Stress 505
6.3 Heat Stress 506
6.4 Submergence Stress 507
6.5 Cold Stress 508
6.6 Heavy Metal Stress 509
7 Conclusion and Future Prospectus 509
References 510
Apple Latent Spherical Virus (ALSV) Vector as a Tool for Reverse Genetic Studies and Non-transgenic Breeding of a Variety of C... 515
1 Introduction: Significance of ALSV Vector in Plant Reverse Genetics and Epigenetic Breeding Technology 516
2 Characteristics of the ALSV Vector 517
3 Practical Protocol for Preparation and Infection of ALSV Vector 523
3.1 Vector Preparation 523
3.2 Agroinoculation of N. benthamiana 523
3.2.1 Preparation of Agrobacterium Cultures 523
3.2.2 Pre-treatment of Agrobacterium 524
3.2.3 Agroinoculation 524
3.3 RT-PCR Analysis for Detection of ALSV Infection 524
3.3.1 Sampling of Leaves 524
3.3.2 RNA Extraction 526
3.3.3 RT-PCR Analysis 526
3.4 Rub-inoculation of Leaf Sap onto C. quinoa 527
3.4.1 Sampling of N. benthamiana Leaves 527
3.4.2 Rub-inoculation 528
3.5 Bentonite Solution 528
3.5.1 Preparation of Phosphate Buffers 528
3.5.2 Preparation of Bentonite Solution 528
3.6 Virus Extraction 529
3.6.1 Crushing Infected Leaves in Blender 529
3.6.2 Rough Purification by Using Bentonite Solution 529
3.6.3 Preparation of Virus Particle 530
3.6.4 Extraction of Viral RNA 530
3.7 Preparation of Gold Particle 530
3.7.1 Mixing Viral RNA with Gold Particle 531
3.7.2 Preparation of RNA-coated Gold Particle 531
3.8 Particle Bombardment with NepaGene System 531
3.8.1 Setting up the Gene Gun 531
3.8.2 Shooting Gold Particle 532
3.8.3 RT-PCR Analysis 533
4 Application of ALSV Vector for Gene Expression and Gene Silencing 533
5 Application of ALSV Vector for Transcriptional Gene Silencing 534
References 537
Erratum to: Growing Diversity of Plant MicroRNAs and MIR-Derived Small RNAs 539