Matthews' Plant Virology

Fourth Edition

Roger Hulli

Emeritus Research FellowJohn lnnes Center

Norwich Research ParkColney, Norwich

Technische Universitat DarmstadtFACHBEREICH 10 — BIOLOGIE

— B i b t i o t h e k —SchhittspahnstraBe 10

0-64287 D a r m s t a d t

Inv.-Nr.

ACADEMIC PRESSA Harcourt Science and Technology Company

San Diego San Francisco New York Boston hondon Sydney Tokyo

Contents

About the Author vPreface xix

Chapter 1 Introduction f_ 1I. Historical Background 1

II. Definition of a Virus 9III. About this Edition 11

Chapter 2 Nomenclature and Classification of Plant Viruses 13I. Nomenclature 13

A. Historical aspects 13B. Systems for classification 14C. Families, genera, species and groups 15D. Plant virus families, genera and orders 19E. Use of virus names 19

II. Criteria Used for Classifying Viruses 21A. Structure of the virus particle 21B. Physicochemical properties of virus particles 21C. Properties of viral nucleic acids 21D. Viral proteins 22E. Serological relationships 24F. Activities in the plant 25G. Methods of transmission 26

III. Families and Genera of Plant Viruses 27A. Family Caulimoviridae 27B. Family Geminiviridae 28C. Family Circoviridae 28D. Family Reoviridae 29E. Family Partitiviridae 29F. No family 30G. Family Rhabdoviridae 30H. Family Bunyaviridae 30I. No family 31J. Family Bromoviridae 31K. Family Comoviridae 32L. Family Potyviridae 33M. Family Tombusviridae 33

vii

Vlll CONTENTS

N. Family Sequiviridae 35O. Family Closteroviridae 35P. Family Luteoviridae 36Q. Floating genera 37

_ - IV. Retroelements 40A. Family Pseudoviridae . 41B. Family Metaviridae ^ 41

VI. Viruses of Lower Plants 42A. Viruses of algae 42B. Viruses of fungi 43C. Viruses of ferns 44D. Viruses of gymnosperms , 44E. Summary ' 44

VI. Discussion 44Chapter 3 Disease Symptoms and Host Range -- 47

I. Economic Losses due to Plant Viruses 47II. Macroscopic Symptoms 48

A. Local symptoms 48B. Systemic symptoms 49C. Agents inducing* virus-like symptoms 53D. The cryptoviruses 56

III. Histological Changes 56A. Necrosis 56B. Hypoplasia 56C. Hyperplasia 57

IV. Cytological Effects 58A. Methods 58B. Effects on cell structures 59C. Virus-induced structures in the cytoplasm 62D. Cytological structures resembling those induced by viruses 66E. Discussion 67

V. The Host Range of Viruses 67A. Limitations in host range studies 68B. Patterns of host range 69C. The determinants of host range 69

VI. Discussion and Summary 73Chapter 4 Purification and Composition of Plant Viruses 75

I. Introduction 75II. Isolation 75

A. Choice of plant material 76III. Components 86

A. Nucleic acids 87B. Proteins; 100C. Other components in viruses 104D. Discussion and summary 106

Chapter 5 Architecture and Assembly of Virus Particles 109I. Introduction 109

II. M e t h o d s - ; ••" •• ;- 109

A. Chemical and biochemical studies 109B. Methods for studying size of viruses 110

CONTENTS IX

C. Fine structure determination: electron microscopy 111D. X-ray crystallographic analysis 113E. Neutron small-angle scattering 114F. Mass spectrometry 114

^ , G. Serological methods 114? H. Methods for studying stabilizing bonds 116

III. Architecture of Rod-Shaped Viruses 117A. Introduction • 117B. Tobamovirus genus 118C. Tobravirus genus 123D. Other helical viruses 124

^ IV. Assembly of Rod-Shaped^Viruses 126A. TMV 126B. Other rod-shaped viruses 134

V. Architecture of Isometric Viruses 134A. Introduction 134B. Quasi-equivalence 135C. Possible icosahedra 136

x D. Clustering of subunits ^ 137E. 'True' and 'quasi' symmetries 138F. Bacilliform particles 138

VI. Small Icosahedral Viruses 138A. Subunit structure 138B. Virion structure - 139C. The arrangement of nucleic acid within icosahedral viruses 157

VII. More Complex Isometric Viruses 159VIII. Enveloped Viruses 160

A. Rhabdoviridae 160B. Tospoviruses J 162

IX. Assembly of Icosahedral Viruses ^ 163A. Bromoviruses ( 163B. Alfalfa mosaic virus 165C. Other viruses 165D. RNA selection during assembly of plant reoviruses 167

X. Discussion and Summary 168Chapter 6 Genome Organization 171

I. Introduction ^ 171II. General Properties of Plant Viral Genomes 171

A. Information content 171B. Economy in the use of genomic nucleic acids 172C. The functions of viral gene products 172D. Non-coding regions. 174

III. Plant Viral Genome Organization 174IV. Double-Stranded DNA Viruses 174

A. Family Caulimoviridae C 174V. Single-Stranded DNA Viruses 180

A. Family Geminiviridae 180B. Family Circoviridae 183

VI. Double-Stranded RNA Viruses 183A. Family Reoviridae 183

X CONTENTS

- - B. Family Partitiviridae . 187C. Genus Varicosavirus 187

VII. Negative-Sense Single-Stranded RNA Genomes 187A. Family Rhabdoviridae 187

__ B. Family Bunyaviridae 188VIII. Positive-Sense Single-Stranded RNA Genomes 189

A. Family Bromoviridae 189B. Family Comoviridae 194

] C. Family Potyviridae 196^ D. Family Tombusviridae 198

E. Family Sequiviridae 202F. Family Closteroviridae *" 203G. Family Luteoviridae 205H. Floating genera 207

IX. Summary and Discussion 221Chapter 7 Expression of Viral Genomes 225

I. Introduction ^c, 225II. Virus Entry and Uncoating 226

A. Virus entry 226B. Uncoating of TMV 226C. Uncoating of bromoviruses 229D. Uncoating of SBMV 230E. Uncoating of TYMV 230F. Discussion 231

III. Viral Genome Expression 232A. Structure of the genome 233B. Defining functional ORFs V 235C. Recognizing activities of viral genes 238D. Matching gene activities with functional ORFs 240

IV. Synthesis of mRNAs 244A. Negative-sense single-stranded RNA viruses 244B. Double-stranded RNA viruses . 245C. DNA viruses 246

V. Plant Viral Genome Strategies 253A. The eukaryotic protein-synthesizing system 253B. Virus strategies to overcome eukaryotic translation constraints 254C. Control of translation 272D. Discussion 276E. Positive-sense ssRNA viruses that have more than one strategy 276F. Negative-sense single-stranded RNA viruses 289G. Double-stranded RNA viruses . 289

- H. DNA viruses 289VI. Discussion 290

Chapter 8 Virus Replication 293I. Introduction 293

II. Host Functions Used by Plant Viruses 293A. Components for virus synthesis 293B. Energy 293C. Protein synthesis 293D. Nucleic acid synthesis 294

CONTENTS XI

- E. Structural components of the cell 294III. Methods for Studying Viral Replication 294

A. In vivo systems 294B. In vitro systems 302

IV. Replication of Positive-Sense Single-Stranded RNA Viruses 304A. Viral templates , 305B. Replicase 306C. Sites of replication 310D. Mechanism of replication 310E. Replication of brome mosaic virus 310

''" F. Replication of cucumber mosaic virus 315G. Replication of alfalfa mosaic virus 316H. Replication of tobacco mosaic virus 319I. Replication of potyviruses 322J. Replication of Comoviridae ^ 324K. Replication of turnip yellow mosaic virus 326L. Replication of other (+)-strand RNA viruses 330M. Discussion 333

V. Replication of Negative-Sense Single-Stranded RNA Viruses 333A. Plant Rhabdoviridae 333B. Tospoviruses 335

VI. Replication of Double-Stranded RNA Viruses 336A. Plant Reoviridae 336

VII. Replication of Reverse Transcribing Viruses 339A. Reverse transcriptase 339B. Replication of 'caulimoviruses' ^ 340C. Replication of (badnaviruses' 344

VIII. Replication of Single-Stranded DNA Viruses 345A. Methods for studying geminivirus replication 345B. In vivo observations on geminiviruses 345C. Rolling-circle replication 345D. Geminivirus replication 346E. Nanovirus replication ' 351

IX. Mutation and Recombination 352A. Mutation 352B. Recombination 353C. Defective and defective interfering nucleic acids and particles 363

X. Mixed Virus Assembly 368XL Discussion 371

Chapter 9 Induction of Disease 1: Virus Movement through the Plant and Effects onPlant Metabolism 373

I. Introduction 373II. Movement and Final Distribution 373

A. Routes by which viruses move through plants 374B. Methods for studying virus movement 374C. Transport across nuclear membranes 376D. Cell-to-cell movement 377E. Time of movement from first infected cells 396F. Rate of cell-to-cell movement 396G. Long-distance movement 397

XU CONTENTS

H. Rate of systemic movement 401I. Movement in the xylem 403J. Final distribution in the plant 403K. Host factors 408

^ L. Discussion . 410III. Effects on Plant Metabolism 411

A. Experimental variables 411B. Nucleic acids and proteins 413

_ C. Lipids 415D. Carbohydrates 415E. Cell wall compounds 417F. Respiration 418G. Photosynthesis 418H. Transpiration 423I. Activities of specific enzymes 423J. Hormones 424K. Low-molecular-weight compounds 424L. Summary 426

IV. Processes Involved in Symptom Induction . 426A. Sequestration of raw materials 426B. Effects on growth 428C. Effects on chloroplasts ^ 431D. Mosaic symptoms 432E. The role of-membranes 434

V. Discussion 435Chapter 10 Induction of Disease 2: Virus-Plant Interactions -1 437

I. Introduction 437II. Definitions and Terminology of Host Responses to Inoculation 437

A. R genes 438III. Steps in the Induction of Disease 439

A. Ability of virus to replicate in initial cell 440B. Ability of virus to move out of first cell 442C. Hypersensitive local response 442D. HR induced by TMV in N-gene tobacco 443E. Other viral-host hypersensitive responses 445F. Host protein changes in the hypersensitive response 448G. Other biochemical changes during the hypersensitive response 449H. Systemic necrosis 450I. Programed cell death and plant viruses 450J. Local acquired resistance 450K. Systemic acquired resistance 451L. Wound healing responses 454M. Antiviral factors 455N. Ability of virus to spread through various barriers 455O. Systemic host response 455P. Development of mosaic disease 460Q. Symptom severity 461R. Recovery 462

IV. Inherent Host Response 463A. Gene silencing 463

CONTENTS XU1

B. Transcriptional and post-transcriptional gene silencing 464C. Genes involved in post-transcriptional gene silencing 466D. Mechanism of post-transcriptional gene silencing 467E. PTGS systemic signaling , 469F. Induction and maintenance 469G. PTGS in virus-infected plants 470

h H. Suppression of gene silencing 471/-I. Other mechanisms of avoiding PTGS 474

J. Discussion 475V. Influence of Other Agents 475

A. Viroids and satellite RNAs " 475B. Defective interfering nucleic acids 475C. Other associated nucleic acids 476D. Gross-protection 477E. Concurrent protection 478F. Interactions between unrelated viruses 478G. Interactions between viruses and fungi 480

VI. Discussion and Summary 481Chapter 11 Transmission 1: By Invertebrates, Nematodes and Fungi. 485

I. Introduction 485II. Transmission by Invertebrates 485

A. Arthropbda 485B. Nematoda 486C. Relationships between plant viruses and invertebrates 486

III. Aphids-(Aphididae) 487A. Aphid life cycle)and feeding habits 487B. The vector groups of aphids 491C. Aphid transmission by cell injury 491D. Types of aphid-virus relationship 491E. Non-persistent transmission 493F. Semi-persistent transmission 499G. Bimodal transmission 500H. Persistent transmission " 501

IV. Leafhoppers and Planthoppers (Auchenorrhyncha) 506A. Structure and life cycle 506B. Kinds of virus-vector relationship 507C. Semi-persistent transmission 508D. Persistent transmission , 508

V. Whiteflies (Aleyrodidae) 513A. Whiteflies 513B. Begomoviruses 514C. Closteroviruses and criniviruses 514

VI. Thrips (Thysanoptera) 515A. Thrip anatomy 515B. Tospovirus transmission 516C. Virus-vector relationship 516D. Route through the thrips 517

VII. Other Sucking and Piercing Vector Groups 518A. Mealybugs (Coccoidea and Pseudococcoidea) 518B. Bugs (Miridae and Piesmatidae) 518

XIV CONTENTS

VIII. Insects with Biting Mouthparts 518A. Vector groups and feeding habits 518

' B. Viruses transmitted by beetles 519C. Beetle-virus relationships 519

IX. Mites (Arachnida) , 520A. Eriophyidae " 520B. "Tetranychidae 522

X. Pollinating Insects 522XI. Nematodes (Nematoda) 522

A. Criteria for demonstrating nematode transmission 523B. Nematode feeding . 523C. Virus-nematode relationships . 524D. Virus-vector molecular interactions < 525

XII. Fungi , 526A. In vitro fungal transmission 526B. In vivo fungal transmission 527

XIII. Discussion and Summary 527Chapter 12 Transmission 2: Mechanical, Seed, Pollen and Epidemiology 533

I. Mechanical Transmission 533A. Source and preparation of inoculum 533B. Applying the inoculum • 534

II. Factors Influencing the Course of Infection and Disease 535A. The plantbeing inoculated .,,, 536B. Development of disease • ; ' v 538C. Viral nucleic acid as inoculum 541D: Nature and number of infectible sites 542E. Number of particles required to give an infection 544F. Mechanical transmission in the field 545

v G. Abiotic transmission in soil 546H. Summary and discussion 546

III. Direct Passage in Living Higher Plant Material 546A. Through the seed 546B. By vegetative propagation ; 554C. By grafting ! 554D. By dodder ' ' - ' , / • . 555E. Summary and discussion " 555

IV. Ecology and Epidemiology .--•- .'.,- 555A. Biological factors 556B. Physical factors 572C. Survival through the seasonal cycle 576D. Disease forecasting 577E. Conclusions 578

Chapter 13 New Understanding of the Functions of Plant Viruses 583I. Introduction . 583

II. Early Events 584III. Mid-stage Events 585

A. Host and virus translation 585B. Host and virus replication 585C. Spatial factors in virus expression and replication 586D. Plant viruses and cytoskeletal elements 588

CONTENTS XV

IV, Late Events 590V. Systemic Interactions with Plants 590

VI. Discussion 591Chapter 14 Viroids, Satellite Viruses and Satellite RNAs , 593

I. Viroids 593* ' A. Classification of viroids 593"" B. Pathology of viroids . , 593

C. Structure of viroids 596D. Replication of viroids 598E. Molecular basis for biological activity 606F. Diagnostic procedures for viroids 607

II. Satellite Viruses and Satellite RNAs 608A. Satellite plant viruses ^ . 609

*" B. Satellite RNAs (satRNAs) 614C. Satellite DNAs 625D. Complex-dependent viruses 626E. Discussion 626

Chapter 15 Methods for Assay, Detection and Diagnosis 627I. Introduction 627

II. Methods Involving Biological Activities of the Virus 628A. Infectivity assays 628B. Indicator hosts for diagnosis 632C. Host range in diagnosis 633

, D. Symptom-related methods 634E. Methods of transmission in diagnosis 634F. Cytological effects for diagnosis 634G. Mixed infections 635H. Preservation of virus inoculum 635

III. Methods Depending on Physical Properties of the Virus Particle 636A. Stability and physicochemical properties 636B. Ultracentrifugation 637C. Electron microscopy 638D. Chemical assays for purified viruses 640E. Assay using radioisotopes 640

IV. Methods Depending on Properties of Viral Proteins 641A. Serological procedures 641B. Methods for detecting antibody-virus combination 647C. Collection, preparation and storage of samples 655D. Monoclonal antibodies 656E. Phage-displayed single-chain antibodies • 657F. Serologically specific electron microscopy 657G. Fluorescent antibody 659H. Neutralization of infectivity 660I. Electrophoretic procedures - 660

V. Methods Involving Properties of the Viral Nucleic Acid 661A. Type and size of nucleic acid 661B. Cleavage patterns of DNA 662C. Hybridization procedures 663D. Polymerase chain reaction 671

VI. Discussion and Summary 673

XVI CONTENTS

Chapter 16 Control and Uses of Plant Viruses 675• I. Introduction 675

• II. Removal or Avoidance of Sources of Infection 676A. Removal of sources of infection in or near the crop , 676

v B. Virus-free seed 679•v C. Virus-free vegetative stocks ° 680

D. Propagation and maintenance of virus-free stocks 685E. Modified planting and harvesting procedures 686

III. Control or Avoidance of Vectors ' 690A. Air-borne vectors 691B. Soil-borne vectors 696

IV. Protecting the Plant from Systemic Disease 6981 - A. Mild strain protection (cross-protection) 699

B. Satellite-mediated protection 700C. Antiviral chemicals 701

V. Conventional Resistance to Plant Viruses 702A. Kinds of host response 702B. Genetics of resistance to viruses 704C. Tolerance 707D. Use of conventional resistance for control 707

VI. Transgenic Protection Against Plant Viruses 712A. Introduction 712B- Natural resistance genes 712

VII. Pathogen-Derived Resistance 713A. Protein-based protection 714B. Nucleic acid-based protection 718C. Other forms of transgenic protection 724D. Field releases of transgenic plants 727E. Potential risks associated with field release of virus transgenic plants 728

VIII. Discussion and Conclusions 730IX. Possible Uses of Viruses for Gene Technology 731

A. Viruses as gene vectors 731B. Viruses as sources of control elements for transgenic plants 735C. Viruses for presenting heterologous peptides 736D. Viruses in functional genomics of plants 739E. Summary and discussion 740

Chapter 17 Variation, Evolution and Origins of Plant Viruses 743I. Strains of Viruses 743

A. Quasi-species 743B. Virus strains 744

II. Criteria for the Recognition of Strains 744A. Structural criteria 744B. Serological criteria 750C. Biological criteria 757D. Discussion 761

III. Isolation of Strains 762A. Strains occurring naturally in particular hosts 762B. Isolation from systemically infected plants 762C. Selection by particular hosts or conditions of growth 762D. Isolation by means of vectors 763

CONTENTS XVU

E. Isolation of artificially induced mutants 763F. Isolation of strains by molecular cloning 764

IV. The Molecular Basis of Variation 764A. Mutation (nucleotide changes) , 764B. Recombination 765C. Deletions and additions . 766D. Nucleotide sequence re-arrangement 766E. Re-assortment of multi-particle genomes 766F. - The origin of strains in nature 767

V. Constraints on Variation 767A. Muller's ratchet 767B. Does Muller's ratchet operate with plant viruses? 768

VI. Virus Strains in the Plant 768A. Cross-protection 768B. Selective survival in specific hosts 768C. Loss of infectivity for one host following passage through another 769D. Double infections in vivo 770E. Selective multiplication under different environmental conditions 770

VII. Correlations Between Criteria for Characterizing Viruses andVirus Strains 770A. Criteria for identity 770B. Strains and viruses 771C. Correlations for various criteria 771

VIII. Discussion and Summary 774IX. Speculations on Origins and Evolution 775X. Types of Evolution - 776

A. Microevolution and macroevolution 776B. Sequence divergence or convergence 776C. Modular evolution 777D. Evidence for virus evolution 777

XL Sources of Viral Genes 791A. Replicases 792B. Proteinases 793C. Coat proteins 793D. Cell-to-cell movement proteins 793E. Suppressors of gene silencing 794

XII. Origins of Viruses, Viroids and Satellites 794A. Origins of viruses 794B. Origin of viroids 796C. Origin of satellite viruses and nucleic acids 798

XIII. Selection Pressures for Evolution 799A. Maximizing the variation 799B. Controlling the variation 799C. Adaptation to niches , 802D. Rates of evolution 802

XIV. Co-evolution of Viruses with their Hosts and Vectors 804A. Co-evolution of viruses, host plants and invertebrate vectors 804B. Evolution of angiosperms and insects 804C. Horizontal transmission through plants of viruses infecting

only insects 804

XV111 CONTENTS

D. Affinities of viruses that replicate in both insects and plants 805E. Adaptation of plant viruses to their present invertebrate vectors 806

XV. Discussion and Summary 807Appendix 1A . 813

-Appendix IB 838Appendix 2A ' 850Appendix 2B 852Appendix 3 ' 854References 857Index 983

Plate section appears between pages 74 and 75.