Matthews' Plant Virology
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1 Matthews' Plant Virology Fourth Edition Roger Hull i Emeritus Research Fellow John lnnes Center Norwich Research Park Colney, Norwich Technische Universitat Darmstadt FACHBEREICH 10 BIOLOGIE Bibtiothek SchhittspahnstraBe Darmstadt Inv.-Nr. ACADEMIC PRESS A Harcourt Science and Technology Company San Diego San Francisco New York Boston hondon Sydney Tokyo
2 Contents About the Author v Preface xix Chapter 1 Introduction f_ 1 I. Historical Background 1 II. Definition of a Virus 9 III. About this Edition 11 Chapter 2 Nomenclature and Classification of Plant Viruses 13 I. Nomenclature 13 A. Historical aspects 13 B. Systems for classification 14 C. Families, genera, species and groups 15 D. Plant virus families, genera and orders 19 E. Use of virus names 19 II. Criteria Used for Classifying Viruses 21 A. Structure of the virus particle 21 B. Physicochemical properties of virus particles 21 C. Properties of viral nucleic acids 21 D. Viral proteins 22 E. Serological relationships 24 F. Activities in the plant 25 G. Methods of transmission 26 III. Families and Genera of Plant Viruses 27 A. Family Caulimoviridae 27 B. Family Geminiviridae 28 C. Family Circoviridae 28 D. Family Reoviridae 29 E. Family Partitiviridae 29 F. No family 30 G. Family Rhabdoviridae 30 H. Family Bunyaviridae 30 I. No family 31 J. Family Bromoviridae 31 K. Family Comoviridae 32 L. Family Potyviridae 33 M. Family Tombusviridae 33 vii
3 Vlll CONTENTS N. Family Sequiviridae 35 O. Family Closteroviridae 35 P. Family Luteoviridae 36 Q. Floating genera 37 _ - IV. Retroelements 40 A. Family Pseudoviridae. 41 B. Family Metaviridae ^ 41 VI. Viruses of Lower Plants 42 A. Viruses of algae 42 B. Viruses of fungi 43 C. Viruses of ferns 44 D. Viruses of gymnosperms, 44 E. Summary ' 44 VI. Discussion 44 Chapter 3 Disease Symptoms and Host Range I. Economic Losses due to Plant Viruses 47 II. Macroscopic Symptoms 48 A. Local symptoms 48 B. Systemic symptoms 49 C. Agents inducing* virus-like symptoms 53 D. The cryptoviruses 56 III. Histological Changes 56 A. Necrosis 56 B. Hypoplasia 56 C. Hyperplasia 57 IV. Cytological Effects 58 A. Methods 58 B. Effects on cell structures 59 C. Virus-induced structures in the cytoplasm 62 D. Cytological structures resembling those induced by viruses 66 E. Discussion 67 V. The Host Range of Viruses 67 A. Limitations in host range studies 68 B. Patterns of host range 69 C. The determinants of host range 69 VI. Discussion and Summary 73 Chapter 4 Purification and Composition of Plant Viruses 75 I. Introduction 75 II. Isolation 75 A. Choice of plant material 76 III. Components 86 A. Nucleic acids 87 B. Proteins; 100 C. Other components in viruses 104 D. Discussion and summary 106 Chapter 5 Architecture and Assembly of Virus Particles 109 I. Introduction 109 II. Methods- ; " ; A. Chemical and biochemical studies 109 B. Methods for studying size of viruses 110
4 CONTENTS IX C. Fine structure determination: electron microscopy 111 D. X-ray crystallographic analysis 113 E. Neutron small-angle scattering 114 F. Mass spectrometry 114 ^, G. Serological methods 114? H. Methods for studying stabilizing bonds 116 III. Architecture of Rod-Shaped Viruses 117 A. Introduction 117 B. Tobamovirus genus 118 C. Tobravirus genus 123 D. Other helical viruses 124 ^ IV. Assembly of Rod-Shaped^Viruses 126 A. TMV 126 B. Other rod-shaped viruses 134 V. Architecture of Isometric Viruses 134 A. Introduction 134 B. Quasi-equivalence 135 C. Possible icosahedra 136 x D. Clustering of subunits ^ 137 E. 'True' and 'quasi' symmetries 138 F. Bacilliform particles 138 VI. Small Icosahedral Viruses 138 A. Subunit structure 138 B. Virion structure C. The arrangement of nucleic acid within icosahedral viruses 157 VII. More Complex Isometric Viruses 159 VIII. Enveloped Viruses 160 A. Rhabdoviridae 160 B. Tospoviruses J 162 IX. Assembly of Icosahedral Viruses ^ 163 A. Bromoviruses ( 163 B. Alfalfa mosaic virus 165 C. Other viruses 165 D. RNA selection during assembly of plant reoviruses 167 X. Discussion and Summary 168 Chapter 6 Genome Organization 171 I. Introduction ^ 171 II. General Properties of Plant Viral Genomes 171 A. Information content 171 B. Economy in the use of genomic nucleic acids 172 C. The functions of viral gene products 172 D. Non-coding regions. 174 III. Plant Viral Genome Organization 174 IV. Double-Stranded DNA Viruses 174 A. Family Caulimoviridae C 174 V. Single-Stranded DNA Viruses 180 A. Family Geminiviridae 180 B. Family Circoviridae 183 VI. Double-Stranded RNA Viruses 183 A. Family Reoviridae 183
5 X CONTENTS - - B. Family Partitiviridae. 187 C. Genus Varicosavirus 187 VII. Negative-Sense Single-Stranded RNA Genomes 187 A. Family Rhabdoviridae 187 B. Family Bunyaviridae 188 VIII. Positive-Sense Single-Stranded RNA Genomes 189 A. Family Bromoviridae 189 B. Family Comoviridae 194 ] C. Family Potyviridae 196 ^ D. Family Tombusviridae 198 E. Family Sequiviridae 202 F. Family Closteroviridae *" 203 G. Family Luteoviridae 205 H. Floating genera 207 IX. Summary and Discussion 221 Chapter 7 Expression of Viral Genomes 225 I. Introduction ^c, 225 II. Virus Entry and Uncoating 226 A. Virus entry 226 B. Uncoating of TMV 226 C. Uncoating of bromoviruses 229 D. Uncoating of SBMV 230 E. Uncoating of TYMV 230 F. Discussion 231 III. Viral Genome Expression 232 A. Structure of the genome 233 B. Defining functional ORFs V 235 C. Recognizing activities of viral genes 238 D. Matching gene activities with functional ORFs 240 IV. Synthesis of mrnas 244 A. Negative-sense single-stranded RNA viruses 244 B. Double-stranded RNA viruses. 245 C. DNA viruses 246 V. Plant Viral Genome Strategies 253 A. The eukaryotic protein-synthesizing system 253 B. Virus strategies to overcome eukaryotic translation constraints 254 C. Control of translation 272 D. Discussion 276 E. Positive-sense ssrna viruses that have more than one strategy 276 F. Negative-sense single-stranded RNA viruses 289 G. Double-stranded RNA viruses H. DNA viruses 289 VI. Discussion 290 Chapter 8 Virus Replication 293 I. Introduction 293 II. Host Functions Used by Plant Viruses 293 A. Components for virus synthesis 293 B. Energy 293 C. Protein synthesis 293 D. Nucleic acid synthesis 294
6 CONTENTS XI Chapter 9 - E. Structural components of the cell 294 III. Methods for Studying Viral Replication 294 A. In vivo systems 294 B. In vitro systems 302 IV. Replication of Positive-Sense Single-Stranded RNA Viruses 304 A. Viral templates, 305 B. Replicase 306 C. Sites of replication 310 D. Mechanism of replication 310 E. Replication of brome mosaic virus 310 ''" F. Replication of cucumber mosaic virus 315 G. Replication of alfalfa mosaic virus 316 H. Replication of tobacco mosaic virus 319 I. Replication of potyviruses 322 J. Replication of Comoviridae ^ 324 K. Replication of turnip yellow mosaic virus 326 L. Replication of other (+)-strand RNA viruses 330 M. Discussion 333 V. Replication of Negative-Sense Single-Stranded RNA Viruses 333 A. Plant Rhabdoviridae 333 B. Tospoviruses 335 VI. Replication of Double-Stranded RNA Viruses 336 A. Plant Reoviridae 336 VII. Replication of Reverse Transcribing Viruses 339 A. Reverse transcriptase 339 B. Replication of 'caulimoviruses' ^ 340 C. Replication of (badnaviruses' 344 VIII. Replication of Single-Stranded DNA Viruses 345 A. Methods for studying geminivirus replication 345 B. In vivo observations on geminiviruses 345 C. Rolling-circle replication 345 D. Geminivirus replication 346 E. Nanovirus replication ' 351 IX. Mutation and Recombination 352 A. Mutation 352 B. Recombination 353 C. Defective and defective interfering nucleic acids and particles 363 X. Mixed Virus Assembly 368 XL Discussion 371 Induction of Disease 1: Virus Movement through the Plant and Effects on Plant Metabolism 373 I. Introduction 373 II. Movement and Final Distribution 373 A. Routes by which viruses move through plants 374 B. Methods for studying virus movement 374 C. Transport across nuclear membranes 376 D. Cell-to-cell movement 377 E. Time of movement from first infected cells 396 F. Rate of cell-to-cell movement 396 G. Long-distance movement 397
7 XU CONTENTS H. Rate of systemic movement 401 I. Movement in the xylem 403 J. Final distribution in the plant 403 K. Host factors 408 ^ L. Discussion. 410 III. Effects on Plant Metabolism 411 A. Experimental variables 411 B. Nucleic acids and proteins 413 _ C. Lipids 415 D. Carbohydrates 415 E. Cell wall compounds 417 F. Respiration 418 G. Photosynthesis 418 H. Transpiration 423 I. Activities of specific enzymes 423 J. Hormones 424 K. Low-molecular-weight compounds 424 L. Summary 426 IV. Processes Involved in Symptom Induction. 426 A. Sequestration of raw materials 426 B. Effects on growth 428 C. Effects on chloroplasts ^ 431 D. Mosaic symptoms 432 E. The role of-membranes 434 V. Discussion 435 Chapter 10 Induction of Disease 2: Virus-Plant Interactions I. Introduction 437 II. Definitions and Terminology of Host Responses to Inoculation 437 A. R genes 438 III. Steps in the Induction of Disease 439 A. Ability of virus to replicate in initial cell 440 B. Ability of virus to move out of first cell 442 C. Hypersensitive local response 442 D. HR induced by TMV in N-gene tobacco 443 E. Other viral-host hypersensitive responses 445 F. Host protein changes in the hypersensitive response 448 G. Other biochemical changes during the hypersensitive response 449 H. Systemic necrosis 450 I. Programed cell death and plant viruses 450 J. Local acquired resistance 450 K. Systemic acquired resistance 451 L. Wound healing responses 454 M. Antiviral factors 455 N. Ability of virus to spread through various barriers 455 O. Systemic host response 455 P. Development of mosaic disease 460 Q. Symptom severity 461 R. Recovery 462 IV. Inherent Host Response 463 A. Gene silencing 463
8 CONTENTS XU1 B. Transcriptional and post-transcriptional gene silencing 464 C. Genes involved in post-transcriptional gene silencing 466 D. Mechanism of post-transcriptional gene silencing 467 E. PTGS systemic signaling, 469 F. Induction and maintenance 469 G. PTGS in virus-infected plants 470 h H. Suppression of gene silencing 471 /-I. Other mechanisms of avoiding PTGS 474 J. Discussion 475 V. Influence of Other Agents 475 A. Viroids and satellite RNAs " 475 B. Defective interfering nucleic acids 475 C. Other associated nucleic acids 476 D. Gross-protection 477 E. Concurrent protection 478 F. Interactions between unrelated viruses 478 G. Interactions between viruses and fungi 480 VI. Discussion and Summary 481 Chapter 11 Transmission 1: By Invertebrates, Nematodes and Fungi. 485 I. Introduction 485 II. Transmission by Invertebrates 485 A. Arthropbda 485 B. Nematoda 486 C. Relationships between plant viruses and invertebrates 486 III. Aphids-(Aphididae) 487 A. Aphid life cycle)and feeding habits 487 B. The vector groups of aphids 491 C. Aphid transmission by cell injury 491 D. Types of aphid-virus relationship 491 E. Non-persistent transmission 493 F. Semi-persistent transmission 499 G. Bimodal transmission 500 H. Persistent transmission " 501 IV. Leafhoppers and Planthoppers (Auchenorrhyncha) 506 A. Structure and life cycle 506 B. Kinds of virus-vector relationship 507 C. Semi-persistent transmission 508 D. Persistent transmission, 508 V. Whiteflies (Aleyrodidae) 513 A. Whiteflies 513 B. Begomoviruses 514 C. Closteroviruses and criniviruses 514 VI. Thrips (Thysanoptera) 515 A. Thrip anatomy 515 B. Tospovirus transmission 516 C. Virus-vector relationship 516 D. Route through the thrips 517 VII. Other Sucking and Piercing Vector Groups 518 A. Mealybugs (Coccoidea and Pseudococcoidea) 518 B. Bugs (Miridae and Piesmatidae) 518
9 XIV CONTENTS VIII. Insects with Biting Mouthparts 518 A. Vector groups and feeding habits 518 ' B. Viruses transmitted by beetles 519 C. Beetle-virus relationships 519 IX. Mites (Arachnida), 520 A. Eriophyidae " 520 B. "Tetranychidae 522 X. Pollinating Insects 522 XI. Nematodes (Nematoda) 522 A. Criteria for demonstrating nematode transmission 523 B. Nematode feeding. 523 C. Virus-nematode relationships. 524 D. Virus-vector molecular interactions < 525 XII. Fungi, 526 A. In vitro fungal transmission 526 B. In vivo fungal transmission 527 XIII. Discussion and Summary 527 Chapter 12 Transmission 2: Mechanical, Seed, Pollen and Epidemiology 533 I. Mechanical Transmission 533 A. Source and preparation of inoculum 533 B. Applying the inoculum 534 II. Factors Influencing the Course of Infection and Disease 535 A. The plantbeing inoculated.,,, 536 B. Development of disease ; ' v 538 C. Viral nucleic acid as inoculum 541 D: Nature and number of infectible sites 542 E. Number of particles required to give an infection 544 F. Mechanical transmission in the field 545 v G. Abiotic transmission in soil 546 H. Summary and discussion 546 III. Direct Passage in Living Higher Plant Material 546 A. Through the seed 546 B. By vegetative propagation ; 554 C. By grafting! 554 D. By dodder ''-',/. 555 E. Summary and discussion " 555 IV. Ecology and Epidemiology.-- -.'.,- 555 A. Biological factors 556 B. Physical factors 572 C. Survival through the seasonal cycle 576 D. Disease forecasting 577 E. Conclusions 578 Chapter 13 New Understanding of the Functions of Plant Viruses 583 I. Introduction. 583 II. Early Events 584 III. Mid-stage Events 585 A. Host and virus translation 585 B. Host and virus replication 585 C. Spatial factors in virus expression and replication 586 D. Plant viruses and cytoskeletal elements 588
10 CONTENTS XV IV, Late Events 590 V. Systemic Interactions with Plants 590 VI. Discussion 591 Chapter 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 596 D. Replication of viroids 598 E. Molecular basis for biological activity 606 F. Diagnostic procedures for viroids 607 II. Satellite Viruses and Satellite RNAs 608 A. Satellite plant viruses ^. 609 *" B. Satellite RNAs (satrnas) 614 C. Satellite DNAs 625 D. Complex-dependent viruses 626 E. Discussion 626 Chapter 15 Methods for Assay, Detection and Diagnosis 627 I. Introduction 627 II. Methods Involving Biological Activities of the Virus 628 A. Infectivity assays 628 B. Indicator hosts for diagnosis 632 C. Host range in diagnosis 633, D. Symptom-related methods 634 E. Methods of transmission in diagnosis 634 F. Cytological effects for diagnosis 634 G. Mixed infections 635 H. Preservation of virus inoculum 635 III. Methods Depending on Physical Properties of the Virus Particle 636 A. Stability and physicochemical properties 636 B. Ultracentrifugation 637 C. Electron microscopy 638 D. Chemical assays for purified viruses 640 E. Assay using radioisotopes 640 IV. Methods Depending on Properties of Viral Proteins 641 A. Serological procedures 641 B. Methods for detecting antibody-virus combination 647 C. Collection, preparation and storage of samples 655 D. Monoclonal antibodies 656 E. Phage-displayed single-chain antibodies 657 F. Serologically specific electron microscopy 657 G. Fluorescent antibody 659 H. Neutralization of infectivity 660 I. Electrophoretic procedures V. Methods Involving Properties of the Viral Nucleic Acid 661 A. Type and size of nucleic acid 661 B. Cleavage patterns of DNA 662 C. Hybridization procedures 663 D. Polymerase chain reaction 671 VI. Discussion and Summary 673
11 XVI CONTENTS Chapter 16 Control and Uses of Plant Viruses 675 I. Introduction 675 II. Removal or Avoidance of Sources of Infection 676 A. 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 685 E. Modified planting and harvesting procedures 686 III. Control or Avoidance of Vectors ' 690 A. Air-borne vectors 691 B. Soil-borne vectors 696 IV. Protecting the Plant from Systemic Disease A. Mild strain protection (cross-protection) 699 B. Satellite-mediated protection 700 C. Antiviral chemicals 701 V. Conventional Resistance to Plant Viruses 702 A. Kinds of host response 702 B. Genetics of resistance to viruses 704 C. Tolerance 707 D. Use of conventional resistance for control 707 VI. Transgenic Protection Against Plant Viruses 712 A. Introduction 712 B- Natural resistance genes 712 VII. Pathogen-Derived Resistance 713 A. Protein-based protection 714 B. Nucleic acid-based protection 718 C. Other forms of transgenic protection 724 D. Field releases of transgenic plants 727 E. Potential risks associated with field release of virus transgenic plants 728 VIII. Discussion and Conclusions 730 IX. Possible Uses of Viruses for Gene Technology 731 A. Viruses as gene vectors 731 B. Viruses as sources of control elements for transgenic plants 735 C. Viruses for presenting heterologous peptides 736 D. Viruses in functional genomics of plants 739 E. Summary and discussion 740 Chapter 17 Variation, Evolution and Origins of Plant Viruses 743 I. Strains of Viruses 743 A. Quasi-species 743 B. Virus strains 744 II. Criteria for the Recognition of Strains 744 A. Structural criteria 744 B. Serological criteria 750 C. Biological criteria 757 D. Discussion 761 III. Isolation of Strains 762 A. Strains occurring naturally in particular hosts 762 B. Isolation from systemically infected plants 762 C. Selection by particular hosts or conditions of growth 762 D. Isolation by means of vectors 763
12 CONTENTS XVU E. Isolation of artificially induced mutants 763 F. Isolation of strains by molecular cloning 764 IV. The Molecular Basis of Variation 764 A. Mutation (nucleotide changes), 764 B. Recombination 765 C. Deletions and additions. 766 D. Nucleotide sequence re-arrangement 766 E. Re-assortment of multi-particle genomes 766 F. - The origin of strains in nature 767 V. Constraints on Variation 767 A. Muller's ratchet 767 B. Does Muller's ratchet operate with plant viruses? 768 VI. Virus Strains in the Plant 768 A. Cross-protection 768 B. Selective survival in specific hosts 768 C. Loss of infectivity for one host following passage through another 769 D. Double infections in vivo 770 E. Selective multiplication under different environmental conditions 770 VII. Correlations Between Criteria for Characterizing Viruses and Virus Strains 770 A. Criteria for identity 770 B. Strains and viruses 771 C. Correlations for various criteria 771 VIII. Discussion and Summary 774 IX. Speculations on Origins and Evolution 775 X. Types of Evolution A. Microevolution and macroevolution 776 B. Sequence divergence or convergence 776 C. Modular evolution 777 D. Evidence for virus evolution 777 XL Sources of Viral Genes 791 A. Replicases 792 B. Proteinases 793 C. Coat proteins 793 D. Cell-to-cell movement proteins 793 E. Suppressors of gene silencing 794 XII. Origins of Viruses, Viroids and Satellites 794 A. Origins of viruses 794 B. Origin of viroids 796 C. Origin of satellite viruses and nucleic acids 798 XIII. Selection Pressures for Evolution 799 A. Maximizing the variation 799 B. Controlling the variation 799 C. Adaptation to niches, 802 D. Rates of evolution 802 XIV. Co-evolution of Viruses with their Hosts and Vectors 804 A. Co-evolution of viruses, host plants and invertebrate vectors 804 B. Evolution of angiosperms and insects 804 C. Horizontal transmission through plants of viruses infecting only insects 804
13 XV111 CONTENTS D. Affinities of viruses that replicate in both insects and plants 805 E. Adaptation of plant viruses to their present invertebrate vectors 806 XV. Discussion and Summary 807 Appendix 1A Appendix IB 838 Appendix 2A ' 850 Appendix 2B 852 Appendix 3 ' 854 References 857 Index 983 Plate section appears between pages 74 and 75.
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