d

1396 AND CLASSIFICATION - GENERAL

regulated expression systems for cloned DNA Further Reading that can achieve >50% of total cellular in the form of a desired product. These systems Beck PJ, Gonzalez S, Ward CL and Molineux IJ (1989) have been adapted for eucaryotic cells as well for Sequence of T3 DNA from’ 2.5 . The T7 sequence is very rare, through gene 9. J. Mol. Biol., 210: 687. Chung Y-B, Nardone C and Hinkle DC (1990) Bacteriophage even in mammalian cells, and with the appro- T7 DNA packaging. J. Mol. Biol., 216: 939. priate constructs highly selective cloned gene Dunn IJ and Studier FW (1983) Complete nucleotide expression can be attained. Typically, the sequence of bacteriophage T7 DNA and the locations of III gene 10 promoter is employed, with or T7 genetic elements. J. Mol. Biol., 166: 477. without gpl0 translational start sequences, and Molineux I J (1991) -parasite interactions: recent devel- opments in the of abortive phage . The T7 RNA polymerase is supplied from a resident New , 3: 230. or , or by phage . Semer P (1990) In: Adolph KW (ed.) Double-stranded DNA packaged in ; conformation; ener- See also: Bacteriophage recombination; Host-con- getics and packaging pathway. : Eukaryotic, trolled modification and restriction. Prokaryotic, and Viral,vol. 3, p. 203. Boca Raton: CRC Press. Studier FW (1991) Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J. Mol. Biol. 219: 37.

TANAPOX

See Yabapox and

TAXONO MY AND CLASSIFICATIO N - GENERAL Claude M 4auquet The Scrip4 Research Institute La jolla, California, USA

History Classification of viruses is a fairly new exercise considering the first evidence of the existence of a Humans have a tendency to classify and name every- virus was made at the end of the last century. John- thing and viruses are no exception. Classifications son, a virologist, drew attention to the need for are extremely useful for showing similar characteris- virus and classification as early as tics and properties. Thus, appropriately chosen clas- 1927. The first efforts to classify viruses employed sification criteria become extremely informative in a range of ecological and biological properties includ- the case of newly discovered viruses. Unfortunately ing pathogenic properties for human and for virus taxonomy there are no fossils, so evolution- viruses and symptoms for plant viruses. For exam- ary relationships are very speculative. Only a virus ple, viruses that share the pathogenic property of classification would be able to provide indications causing hepatitis (e.g. virus, of the evolution of viruses. In theory, nomenclature virus, virus, virus) and classification are totally independent, but for were grouped together as ‘the hepatitis viruses’. Vir- viruses both issues are often considered at the same ology developed substantially in the 1930s and the time. As a result, virus taxonomic names have first classifications of viruses reflected this develop- always been the subject of passionate discussions. ment. Holmes published in 1939 a classification of

- _. -. . ENCYCLOPEDIA OF Cowright 8 1994 Acalemìc hes~ Ltd ISBN 0-12-226960-5 All rights of reproducìon in ay fonn resewed O 10023336 TAXONOMY AND CLASSIFICATION - GENERAL 1397

plant viruses based on host reactions and differential usefulness of the scheme is being demonstrated by hosts using a binomial-trinomial nomenclature its wide application. It has replaced all competing based on the name of the infected plant, but only classification schemes for all viruses. 89 viruses were classified. In the 1950s, with the At the first meeting of the ICNV in Mexico City development of electron microscopy and biochemi- (1970), two families with a corresponding two gen- cal studies, the first groupings of viruses based on era and 24 floating genera were accepted to begin common virion properties emerged: the Herpes- the grouping of vertebrate, invertebrate and bacter- virus group, the Myxovirus group, and the Poxvirus ial viruses. In addition, 16 groups were group. During this period, there was an explosion of designated. The Fifth ICTV Report describes one newly discovered viruses. In response, several indi- , 40 families, nine subfamilies, 102 genera, viduals and committees independently proposed two floating genera and two subgenera for verte- systems but none was widely brate, invertebrate, bacterial and fungal viruses and used. It became obvious that only an international 32 groups and seven subgroups for plant viruses association of virologists would be able to propose a (Table 1). While most virologists shifted to the comprehensive and universal system of virus classifi- grouping of viruses in families and genera, plant vir- cation. ologists have persisted in clustering plant viruses in At the International Congress for ‘groups’ until very recently. It is only in 1993 that held in Moscow in 1966, the Intemational Commit- the ICTV will propose a uniform system for all tee on Nomenclature of Viruses (ICNV) was estab- viruses with two orders, 50 families, 9 subfamilies, lished by an international group of 43 virologists. 126 genera, 23 floating genera and 4 subgenera An international organization was set up with the encompassing 2644 assigned virus . aim of developing a unique world-wide recognized The descriptions of virus families can provide taxonomy and nomenclature system for all viruses. valuable information for new ‘unknown’ members. [The name of the ICNV was changed in 1974 to a Therefore, the ICTV work is not only a taxonomic j more appropriate one: the International Committee exercise for evolutionists but a valuable source of on Taxonomy of Viruses (ICTV), which is active information for virologists, teachers, medical doc- \today. The ICTV is now considered the official tors and epidemiologists. Since the establishment body for all matters related to taxonomy and nomen- of the ICTV, five virus taxonomic reports have clature of viruses. been published and new reports will appear every Since the founding of the ICTV, all virologists three years. agreed that the hundreds of viruses isolated from dif- ferent should be classified together in a unique system, but separate from other microorgan- isms such as bacteria and mycoplasma. However, How Does the ICTV Operate? there was much controversy on the way to do it. Lwoff, Horne and Tournier argued for the adoption The ICTV is a Committee of the Virology Division of a system for the classifying of viruses into sub- of the International Union of Microbiological phyla, classes, orders, suborders and families. Des- Societies. The ICTV operates through a number of cending hierarchical divisions would have been committees, subcommittees and study groups of based on type (DNA or RNA), strand- more than 372 eminent virologists with expertise in edness (single or double), presence or absence of an human, animal, , protozoal, bacterial, myco- envelope, symmetry and so on. This hierarch- plasmal, fungal, algal and plant viruses. Taxonomic ical system has never been recognized by the ICTV; proposals are initiated and formulated by the study nevertheless, the rest of the proposal became the groups. These proposals are revised and accepted basis of the universal taxonomy system now in place by the subcommittees and presented for Executive and all ICTV reports reflect this scheme. Until 1990, Committee approval. All decisions are finally the scheme did not utilize any hierarchical classifica- &rmed at a plenary session held at each virology tion level higher than the , but the system has congress where all members of ICTV and more recently begun to move in this direction. A first than 50 representatives of national microbiological order, , has been accepted in 1990, societies are represented. Presently, there are 45 and a second one, , has been proposed study groups working in concert with six subcom- for consideration in 1993. In its non-Linnean struc- mittees, namely, the vertebrate, invertebrate, plant, ture, the scheme is quite different from that used for bacteria, and virus data subcommittees. the taxonomy of bacteria and other organisms. The The ICTV is a non-profit association composed of groups Table I. List of orders, families and of viruses"

Nature of the presentation Order Family or group Morphology configuration Genome size Virus host Number of species criteria WP) ~ - Members Tentative Total dsDNA Enveloped Bacilliform I circular supercoiled 90-230 Invertebrate 14 14 Isometric I circular 3 Vertebrate 5 5 Isometric I linear 120-220 Vertebrate 19 4 23' Lipothrim'ridae Rod I linear 16 Bacteria 2 2 Plasmaviridoe Pleomorphic I circular 12 Bacteria 2 5 7 Polydnaviridae Rod, fusiform I circular supercoiled 2-28 Invertebrate 2 2 Pom'ridae Ovioid I linear 130-375 Vertebrate, 61 16 77 invertebrate SSV-I group Lemon-shape I circular supercoiled 15 Bacteria 3 3 dsDNA Nonenveloped Tailed phage I linear 336 Bacteria 83 83 (Caudovirales) Tailed phage I linear 40 Bacteria 51 51 ISiphoviridae Tailed phage I linear 53 Bacteria III III Isometric I linear 32-48 Verte brate III III CaulimoViNs Isometric I circular 8 Plant II 6 17 Commelina yellow Bacilliform I circular 8 Plant 4 II 15 mottle virus group Corticoviridae Isometric I circular supercoiled 10 Bacteria I I 2 160-400 lridoviridae Isometric I linèar Vertebrate, 70 2 72 invertebrate Papovaviridae Isometric I circular 5-8 Vertebrate 28 28 Isom et r i c I linear 250-350 Algae 47 47 Isometric I linear 27 Fungus I I Teaiviridae Isometric I linear 16 Bacteria 8 8 ssDNA Nonenveloped Geminivirus Isometric I or 2 circular 3-6 Plant 35 13 48 lnoviridae Rod I circular 7-20 Bacteria, 32 32 mycoplasmas Isometric I circular 6 Bacteria 28 28. Isometric I -strand 6-8 Vertebrate, 4 II 15 invertebrate dsRNA Enveloped Cystoviridae Isometric 3 segments 17 Bacteria I I dsRNA Nonenveloped Isometric 2 segments 6 Vertebrate, 5 5 invertebrate Cryptovirus Isometric 2 segments 3-5 Plant 20 10 30 Isometric 2 segments 4- IO Fungus 9 5 14 Isometric IO- I2 segments 19-62 Vertebrate, I36 33 I69 invertebrate, plant Isometric I segment . .. 5-7 Fungus 4 8 12 Nature of the presentation Order Family or group Morphology Genome configuration Genome size Virus host Number of species criteria (kb) Members Tentative Total ssRNA Enveloped: ’ Pleomorphic I +segment 28-33 Vertebrate II 3 14 no DNA step; Isometric I +segment 10-22 Vertebrate, . 35 19 54 positive sense genome invertebrate Togaviridoe Isom et r i c I +segment 10-13 Vertebrate, 29 2 31 invertebrate ssRNA Enveloped; no DNA step; Bacilliform I -segment 13 Vertebrate 2 2 negative non- Mononegavirales Helical I -segment 15-16 Vertebrate 32 4 36 segmented genome Bacilliform I -segment IO- I3 Vertebrate, 75 100 I75 invertebrate, plant SRNA Enveloped: Arenaviridoe Spherical 2 - segments II Vertebrate 15 15 no DNA step: Bunyaviridae Spherical 3 - segments 12-23 Vertebrate 253 45 298 invertebrate, plant negative segmented Helical 8 - segments 13- I4 Vertebrate 3 2 5 genome ssRNA Enveloped: Retroviridae Spherical dimer I +segment 7-10 Vertebrate 32 32 DNA step ssRNA Nonenveloped: Isometric I +segment 8 Vertebrate 4 I 5 monopartite genome; cOmOV¡NS Isometric I +segment 4 Plant 8 9 17 Isometric particles Levivirfdae Isometric I +segment 3-4 Bacteria 43 43 Isometric I+segment 6 Plant 14 12 26 Maize chlorotic Isometric I +segment 9 Plant I 2 3 dwarf virus group Isometric +segment 6-7 Plant 3 3 Necrovirus Isometric +segment 4-5 Plant 2 2 4 Parsnip yellow Isometric +segment IO Plant 2 I 3 fleck virus group Picomaviridae Isometric +segment 7-8 Vertebrate, 215 13 228 invertebrate Sobernovirus Isometric +segment 4 Plant IO 6 16 \, Jetraviridae Isometric +segment 5 Invertebrate I 14 15 Isometric +segment 5 Plant 12 12 Isometric +segment 6 Plant 18 I 19 ssRNA Nonenveloped; cClp¡//OV¡NS Rod +segment 7 Plant 2 2 4 monopartite genome: Rod +segment 7-8 Plant 27 29 56 rod-shapedparticles Rod I +segment 7-18 Plant 10 12 22 39 Rod I+segment 6 Plant 18 21 P0t)”iNS Rod I +segment 8- 10 Plant 73 84 I57 Tobomovirus Rod I +segment 6 Plant 12 2 14

Continued Table I. Continued

Nature of the presentation Order Family or group Morphology Genome configuration Genome size Virus host Number of species criteria (kb) Members Tentative Total

SRNA Nonenveloped; Isometric 2+segments 9 Plant 14 14 bipartite genome; Dionthovirus Isometric 2+segments 4 Plant 3 3 isometric particles Isometric 2+segments 10 Plant 3 3 Isometric 2+segments 12 Plant 28 : 8 36 Nodoviridae Isometric 2+segments 5 Invertebrate 6 6 Pea enation mosaic Isometric 2+ segments 9 Plant I I virus group ssRNA Nonenveloped; Rod 2+segments 9-1 I Plant 5 6 II bipartite genome; Rod 2+segments 9-1 I Plant 3 3 rod-shapedparticles ssRNA Nonenveloped; Alfalfa Bacilliform 3+segments 8 Plant I I tripartite genome; group bacilliform particles ssRNA Nonenveloped; Isometric 3+segments 8 Plant 6 6 tripartite genome; Isometric 3 +segments 9 Plant 3 I 4 isometric particles /larvirus Isometric 3+segments 8 Plant 20 20 IO SRNA Nonenveloped; Rod 3+segments Plant 4 4 tripartite genome; rod-shapedparticles SRNA Nonenveloped; Rod 4 - ? segments 19 Plant 3 4 7 tetrapartite genome

Total no. species I970 530 2500

The taxa are listed according the Fifth ICTV Report with the following criteria: nature and strandedness of the nucleic acid, presence or absence of a lipoprotein envelope, the single-stranded (ss)RNA enveloped viruses are arranged on the basis of genome strategy and the SRNA nonenveloped viruses are arranged on the basis of the number of segments of their genome and their particle morphology. For each family or group of viruses, also indicated are the morphology of the virions, , the genome configuration, the genome size in kb, the virus host, the number of species and tentative members in the taxa, and the total number of species listed in 1990. ~ ~ ~ ~~ TAXONOMY AND CLASSIFICATION - GENERAL 1401 prominent virologists representing countries from cation. In the case of viruses, it has been determined throughout the world and names and taxa are that at least 60 characters would be needed for a accepted following a democratic process. ICTV complete virus description. Thus, the limiting fac- does not impose any taxonomic word or taxa but tor for applying the Adansonian system is the lack ensures that the propositions are compatible with of data in many instances. The increasing number ICTV rules for homogeneity and consistency. The of viral nucleic acid sequences allows the compari- ICTV regularly publishes reports that describe all son of viruses to generate different phylogenetic the virus taxa with a list of classified viruses as well trees according to the gene or set of used. To as compilations of virus families and genera. A last date, none of them has satisfactorily provided a report was published in 1991 and the next will be clear classification of all viruses. A multidimen- published in 1994. With the increasing number of sional classification, taking into account all the viruses and virus strains and the explosion of data criteria necessary to describe viruses, would prob- on many descriptive aspects of viruses and viral dis- ably be the most appropriate way of representing eases, ICTV decided to launch an international virus the virus classification but it would not be very database project. This project, termed ICTVdB@,is easy to use. scheduled to be fully operational and accessible to For nearly the last 20 years, ICTV has been clas- the scientific community around the year 2000. sifying viruses essentially at the family and levels using a nonsystematic polythetic approach. This has clustered viruses first in genera and then in families. A subset of characters including physico- System for Virus Classification chemical, structural, genomic and biological criteria has then been used to compare and group viruses. There are two systems for classifying organisms: the This subset of characters may change from one Linnean and the Adansonian systems. The Linnean family to another according to the availability of system is the monothetic hierarchical classification the data and the importance of a particular charac- applied by Linnaeus to and while ter. It is obvious that there is no homogeneity in the Adansonian system is a polythetic hierarchical this respect throughout the virus classification and system proposed by Adanson in 1763. Maurin and that virologists weigh differently the criteria in this collaborators proplosed to apply the Linnean classifi- subjective process. Nevertheless, we can see a rather cation system to viruses in 1984. Although the good stability of the current ICTV classification. system is very convenient to use, there are shortcom- When sequence, genomic organization and replica- ings when it is applied to the classification of viruses. tive cycle data are used for taxonomic purposes First, it is difficult to appreciate the validity of a par- they usually confirm the actual classification. It is ticular criterion. For example, it may not be appro- also obvious that hierarchical classifications above priate to use the number of genomic components the family level will encounter conflicts between as a hierarchical criterion. Second, there are no phenotypic and genotypic criteria and ,that virolo- reasons for privileging a particular criterion from gists will have to consider the entire classification another so it is difficult to rank all the available process to progress in this direction. criteria. For example, is the nature of the genome Currently, and for practical reasons only, virus (DNA/RNA) more important than the presence of classification is structured according to the presenta- an envelope or the shape of the virus particles? tion indicated in Tables 1 and 2. This order of The Adansonian system considers all available presentation of virus families and groups does not criteria at once and makes several classifications con- reflect any hierarchical or phylogenetic classifica- sidering the criteria successively. The criteria lead- tion but only a convenient order of presentation. ing to the same classifications are considered as Since a taxonomic structure above the level of correlated and are therefore not discriminatory. family or group (with the exception of the order Subsequently, a subset of criteria are considered. Mononegavirales and the pending order Caudovir- The process is repeated until all criteria can be ales) has not been developed extensively, any listing ranked to provide the best discrimination of the must be arbitrary. The order of presentation is gen- species. This system was not frequently used due erally the same as in the Fifth ICTV Report. The to its labor-intensive nature, but with present-day order of presentation of virus families and groups computers it can be easily implemented. Further- follows three criteria: (1) the nature of the viral more, qualitative and quantitative data can be simul- nucleic acid, (2) the strandedness of the nucleic taneously considered to generate such a classifi- acid and (3) the presence or absence of a lipoprotein 1402 TAXONOMY AND CLASSIFICATION - GENERAL

Table 2. Order of presentation of virus classification in and human virologists of ICTV for many years, the Fifth ICTV Report but has never been implemented. This suggestion was in fact withdrawn from ICTV nomenclature A.B. DNA/RNA rules in 1990 and consequently such names as Her- Double-stranded/single-stranded pesvirus varicella or Polyomavirus hominis should C. Envelopedlnonenveloped not be used. For several years, plant virologists for the ssRNA enveloped viruses only: have set up a different nomenclature, using the ver- DNA/no DNA step in the replication cycle nacular name of a virus but replacing the word Positive/negative sense genome ‘virus’ by the group (genus) name; for example, Monopartitelmultipartitegenome cucumber mosaic cucumovirus and tobacco mosaic for the ssRNA nonenveloped viruses only: . Though this usage is favored by Mono/bi/tri/tetrapartite genome many scientists and examples of such practice can lsometridbacilliform/rod-shaped particles be found for human, animal and insect viruses (e.g. human , canine calicivirus, Acheta denso- virus), it has not been adopted by the ICTV. envelope. There are no known single-stranded The ICTV has a set of rules for virus nomencla- (ss)DNA viruses with envelopes, so these three ture and orthography of taxonomic names. The criteria give rise to seven clusters comprising the international genus names universally end in ‘-virus’, the international subfamily names end in 73 families and groups of viruses (comprising one floating genus). Within two of these clusters, the ‘-virinae’, the international family names end in ssRNA enveloped and nonenveloped viruses, the ‘-viridae’ and the international order names end in families have been arranged as follows: the ssRNA ‘-virales’. In formal taxonomic usage, the virus enveloped viruses are arranged on the basis of gen- order, family, subfamily and genus names are ome strategy, i.e. DNA/no DNA step in the replica- printed in italics (or underlined) and the first letter tion cycle, positivelnegative sense genome and mono- is capitalized. Species names, which are used in partite/multipartite genome. The ssRNA nonenve- English vernacular form, are not capitalized or loped viruses are arranged on the basis of number of italicized (or underlined). In formal usage, the segments of RNA of their genome, i.e. mono-/bi-/ name of the precedes the name of the taxo- tri-/tetrapartite genome and their virion morphology: nomic unit; for example, ‘the family Picornaviridae’ isometric/bacilliform/rod-shapedparticles. or ‘the genus Rhinovirus’. In informal vernacular usage, virus order, family, subfamily, genus and species names are written in lower case Roman script; they are not capitalized or italicized (or Nomenclature of Virus Taxa underlined). Additionally, in informal usage, the name of the taxon should not include the formal suf- The debate over virus nomenclature has generated fix, and it should follow the term for the taxonomic significant controversy and discussion over the unit; for example, ‘the mononegavirales order’, ‘the years and was the primary reason for virologists to adenovirus family’, ‘the genus’ or establish the ICNV. In the earliest examples of ‘the tobamovirus group’. virus taxonomy, Gibbs proposed to adopt a crypto- To avoid ambiguous identifications, it has been gram to add precision to the vernacular names of recommended to journal editors to follow ICTV the viruses. The cryptograms used a combination guidelines for proper virus identification and nomen- of letters and numbers to describe the structure, clature, and to cite viruses with their full taxonomic the biochemical composition of the genome, the terminology when they are first cited in an article, as host type and the transmission properties of the in the following examples. virus. This system of virus identification was set up in the first ICTV report but was never used and Order Mononegavirales, Family , therefore abandoned. Subfamily Paramyxovirinae, genus Paramyxo- When a family, genus or virus group is approved virus, avian paramyxovirus 1. by ICTV, a or type member is desig- Order Mononegavirales, Family Rhabdoviridae, nated. However, none of these type species has Plant rhabdovirus group, Plant rhabdovirus sub- received an official name and only English vernacu- group A, necrotic yellows virus. lar names are indicated. Use of latinized binomial Family , genus Iridovim, Chilo irides- names for virus names was supported by animal cent virus. TAXONOMY AND CLASSIFICATION - GENERAL 1403

0 Family Podoviridae, genus group, coli- tion of a virus species with the goal of a better usage phage T7. of a virus classification. These include: (1) homo- geneity of the different taxa; (2) diagnostic related matters; (3) virus collections; (4) evolution studies; (5) ; (6) sequence database projects; A Universal Classification System and (7) virus database projects.

The present universal system of virus taxonomy is set arbitrarily at hierarchical levels of order, family Virus families, genera and groulps (in some cases subfamily), genus and species. There is no formal definition for a genus, but it is Lower hierarchical levels, such as , commonly considered as: ‘a population of virus spe- strain, variant, pathotype and isolate, are estab- cies that share common characteristics and are dif- lished by international specialty groups or/and by ferent from other populations of species’. Although culture collections, but not by the ICTV. this definition is somewhat elusive, this level of clas- sification seems stable and useful; some genera have been moved from one family to another but the com- Virus species position and description of these genera have The species taxon is always regarded as the most remained stable over the years. The characteristics important taxonomic level in classification but it defining a genus are different from one family to has proved to be the most difficult to apply for another and there is a tendency to create genera viruses. The ICTV definition of a virus species was with fewer differences between them. Upon exami- long considered to be ‘a concept that will normally nation, there is more and more evidence that the be represented by a cluster of strains from a variety members of a genus have a common evolutionary of sources, or a population of strains from a particu- origin. The use of subgenera is very limited in lar source, which have in common a set or pattern of current virus classification (see Table 1); only one correlating stable properties that separates the subgenus classification exists in the entire family cluster from other clusters of strains’. This was a Bamloviridae and there are three other examples in general definition which was in fact not very precise plant virus groups. However, these may disappear for delineating species in a particular family or in all when plant virus groups are reorganized into famil- families. Furthermore, this definition directly ies and genera (see below). Since the creation of addressed the definition of a virus strain, which the ICTV, plant virologists have always kept the had never been attempted in the history of virus tax- classification of plant viruses in ‘groups’ and onomy. In 1990, Van Regenmortel proposed another strongly refused to place them in genera and famil- species definition which has been accepted by the ies. However, due to obvious similitude, plant reo- ICTV Executive Committee in 1991. This defini- viruses and rhabdoviruses have been integrated tion states: ‘A virus species is a polythetic class of into the families Reoviridae and Rhabdoviridae viruses that constitutes a replicating lineage and (Table 1). This position was mostly due to the occupies a particular ecological niche.’ The major refusal of plant virologists to accept binomial advantage in this definition is that it can accommo- nomenclature. Since this form of nomenclature has date the inherent variability of viruses and it does been withdrawn from the ICTV rules, they have not depend on the existence of a unique characteris- subsequently accepted classification of plant viruses tic. Members of a polythetic class are defined by into genera and families. The current classification more than one property and no single property is still presents plant viruses in groups but the next absolutely essential and necessary. Thus in each report will only have families and genera for all family it might be possible to determine the set of ‘virus kingdoms’. Five plant virus families and 39 properties of the taxonomic level ‘species’ and to genera have been proposed for the next ICTV check if the family members are species of this Report. family or if they belong to a lower taxonomic level. The ICTV is currently conducting this exercise throughout all virus families. This should ulti- Virus orders mately result in an excellent evaluation of a precise As mentioned previously, the upper hierarchical definition of each virus species in the entire classifi- levels of the virus classification are extremely diffi- cation. cult to establish. Despite several general proposi- Several practical matters are related to the defini- tions in the past, none of them have been accepted. 1404 TAXONOMY AND CLASSIFICATION - GENERAL

~

Table 3. List of descriptive characters used in virus taxonomy at the family level

I. Virion properties A. Morphology properties of virions I. Virion size 2, 3, Virion shape Presence or absence of an envelope and peplomers 4. Capsomeric symmetry and structure B. Physical properties of virions I. 2. Molecular mass of virions Buoyant density of virions 3. Sedimentation coefficient 4. pH stability 5. Thermal stability 6. 7. Cation (Mg2+, Mn2+) stability Solvent stability 8. Detergent stability 9. Radiation stability C. Properties of genome I. Type of nucleic acid - DNA or RNA 2. Strandedness - single stranded or double stranded 3. Linear or circular 4. Sense - positive, negative or ambisense 5. Number of segments 6. Size of genome or genome segments 7. Presence or absence and type of 5’-terminal cap 8. Presence or absence of 5’-terminal covalently linked polypeptide 9. Presence or absence of 3’-terminal poly(A) tract (or other specific tract) IO. Nucleotide sequence comparisons D. Properties of proteins I. Number of proteins 2. Size of proteins 3, Functional activities of proteins (especially virion transcriptase, virion , virion hemagglutinin, virion neuraminidase, virion fusion ) E. Lipids I, Presence or absence of lipids 2. Nature of lipids F. Carbohydrates I, Presence or absence of carbohydrates 2. Nature of carbohydrates

II. Genome organization and replication I. Genome organization 2. Strategy of replication of nucleic acid 3I Characteristics of transcription 4. Characteristics of and post-translational processing 5. Site of accumulation of virion proteins, site of assembly, site of maturation and release 6. Cytopathology, inclusion body formation

111. Antigenic properties I. Serological relationships 2. Mapping epitopes TAXONOMY AND CLASSIFICATION - GENERAL 1405

Table 3. Continued

IV. 6iological properties I, Host range, natural and experimental 2. Pathogenicity, association with 3. Tissue tropisms, pathology, histopathology 4. Mode of transmission in nature 5. relationships 6. Geographic distribution

ENVELOPED NON-ENVELOPED

ds DNA dsDNA T

Plasmaviridae 0 prdlle section Corticoviridae Tectiviridae Io Myoviridae, isometric head I SSV’group a zn -Myoviridae, elongated head Sip hoviridae -@ Podoviridae saDNA 0 a Microviridae Inoviridae, 5 Inoviridae, lnovirus

I ds RNA $sRNA

a 2 63 U Cystoviridae0 Leviviridae - 1OOnm

Fig. I Diagrammatic representation of the families of viruses infecting bacteria, grouped according to the nature and strandedness of their genome and the presence or absence of an envelope. Reproduced with permission from Springer- Verlag. R

1406 TAXONOMY AND CLASSIFICATION - GENERAL

ENVELOPED NON-ENVELOPED

dbDNA dsDNA

Phycodnaviridae a 2 C

Rhizidiovirus63

- dsRNA dsRNA

a K2

Totiviridae Partitiviridae

1OOnm

Fig. 2 Diagrammatic representation of the families of viruses infecting algae, fungi and , grouped according to the nature and strandedness of their genome and the presence or absence of an envelope. Reproduced with per- mission from Springer-Verlag.

Nevertheless, it has been stated several times that is under consideration; it is named Caudovirales, the creation of orders could be considered on a case- and it'includes all the families of dsDNA phages by-case basis. The first virus order Mononegavirales having a tail, including Myoviridae, Podoviridae was established in 1990. This order comprises the and . Many members of the ICTV non-segmented ssRNA negative-sense viruses, advocate the creation of many more orders, but it namely the families Filoviridae, Paramyxoviridae has been decided to proceed cautiously to avoid and Rhabdoviridae. This decision has been taken creation of short- orders. The creation of formal because of the great similitude between these taxa higher than orders, for example, kingdoms, families at many points of view including the repli- classes and subclasses, has not been considered by cation strategy of these viruses. A second order ICTV. TAXONOMY AND CLASSIFICATION - GENERAL 1407

ENVELOPEC NON-ENVELOPED

drDNA I

< e= Commollno yollow motllo vlruo Il GOmlnMNSI, II, 111

88RNA drRNA

Reoviridae@ Y.nt rocwilru la

Comovlrus@@ Cyprovlru.@@I, II 0000 Alfolfo moulc vlrur Fabavlrus NO~OV~NS Poo onotlon morolc --J vlrur camovl~us -,n Molzo chlorotlc TonulvlNs 11 dwarl vlrur Hord8lvlrus Mandvlrus Rhabdoviridae N.crOVlNS 00 Plrrtrhbdovln* Tobravlrus Subgroup A Poronlp yollow 63 Subgrq B flock vlrur luf.0~1~~11 Sob.movlNs Fumvlrus t -i Tombusvlrus 7ymovlrus TOb."V/N8

Bun yaviridae TOSpOVlNS

1 OOnm

Fig. 3 Diagrammatic representation of the families of viruses infecting plants, grouped according to the nature and strandedness of their genome and the presence or absence of an envelope. Reproduced with permission from Springer- Vlerlag.

Virus Taxa Descriptions scopy, structural data), biology (serology and virus properties) and physicochemical properties of Virus classification continues to evolve with the viruses (nature and size of genome, number and technologies availiable for describing viruses. The size of viral proteins). Since 1970, the third wave first wave of descriptions, before 1940, mostly took of virus descriptions has included genome and into account the visual symptoms of the replicative information (sequence of genes, caused by viruses and their modes of trans- sequence of proteins), as well as molecular mission. A second wave, between 1940 and 1970, relationships with virus hosts. There has been a cor- brought an enormous amount of information from relative modification of the list of virus descrip- studies of virion morphology (electron micro- tors and Table 3 lists the family and genera I

GENERAL ~~~- 1408 TAXONOMY AND CLASSIFICATION -

ENVELOPED NON-ENVELOPED

I d8DNA i8DNA

Poxviridae, @lridoviridae

U 2 a Baculoviridae, Eubaculovirinae BsDNA

Baculoviridae, Nudibaculovirinae e Parvoviridae

Pol ydna viridae, lchnovirus

Polydnaviridae,

I e Picornaviridac ..... - a Togaviridae Bun yaviridae Kz Reo viridae Tetraviridae

1OOnm Rhabdoviridae Birnaviridae II

Fig. 4 Diagrammatic representation of the families of viruses infecting invertebrates, grouped according to the nat- ure and strandedness of their genome and the presence or absence of an envelope. Reproduced with permission from Springer-Verlag.

descriptors which are used in the ICTV Fifth could quickly be provided. As a result, virology pro- Report. gressed simultaneously for all viruses infecting ani- The impact of descriptions on virus classification mals, , plants and bacteria. Thin sections of has been particularly influenced by electron micro- infected tissues brought a new dimension to virus scopy and the negative staining technique for vir- classification by providing information about virion ions. This technique had an immediate effect on morphogenesis and cytopathogenic effects. These diagnostics and classification of viruses. With nega- techniques in conjunction with the determination tive staining, viruses could be identified from poorly of the nature of the genome provided a major source purified preparations of all types of tissues and infor- of information for the system of virus classification mation about size, shape, structure and symmetry, established in the 1980s (Figs 1-5). TAXONOMY AND CLASSIFICATION - GENERAL 1409 - ENVELOPED NON-ENVELOPED I &DNA t I

Q Adenoviridae 2 C Pmviridae, ChordopoxvirirIae Iridoviridae 63 Papovaviridae e Herpesviridae Hepadnaviridae IrrDNA Parvoviridae I I asRNA I drRNA

Reoviridae Bon yaviridae Param yxoviridae

Birnaviridae

a Tor&& Orthomyxolviridae Arensviridae 2 pe 88RNA

Togaviridae Flaviviridae. @ Picornaviridae

Retroviridae Rhabdoviridae @ Calicivïridae

- Filoviridae 1nnnm

Fig. 5 Diagrammatic representation of the families of viruses infectingvertebrates, grouped according to the nature and strandedness of their genome and the presence or absence of an envelope. Reproduced wtih permission from Springer-Verlag.

In many instances the properties of viruses ously analyzed to warrant the formation of a new belonging to the same genus are correlated. genus. Thus, the classification of a few of them will likely Table 3 lists 45 different categories of proper- be sufficient to allow the classification of a new ties but each category includes many items. Lists virus into an established genus. For example, a of virus descriptors usually comprise between 500 plant virus with filamentous particles of 700 to and 1000 descriptors. The establishment of a uni- 850 nm and transmitted by is likely to be a versal list of virus descriptors is under way and . Establishment of new genera in the should be adopted by ICTV in 1993. It will con- future will require more information. Most of the tain a common set of descriptors for all viruses properties listed in Table 3 will have to be rigor- and discrete subsets for specific viruses in relation r U

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I4I O TENUlVlRUSES

to their specific hosts (human, animal, insect, plant Report of the Intemational Committee on Taxonomy of and bacterial). Viruses. Arch. Virol. suppl. 2 (whole issue). Francki RIB, Milne RG and Hatta T (1985) Atlas of Plant Viruses. Boca Raton, Florida: CRC Press. See also: Bacteriophage taxonomy and classifica- Lwoff A, Home Rand Tournier P (1962) A system of viruses. tion. Cold Spring Harbor Symp. Quant. Biol. Matthews REF (1983) The History of Viral Taxonomy. A Critical Appraisal of Viral Taxonomy, p. 1. Boca Raton, Florida: CRC Press. Murphy FA and Kingsbury DW (1990) Virus taxonomy. In: Fields BN et al. (eds) Virology, 2nd edn, p. 9. New York: Further Reading Raven Press. Van Regenmortel MHV (1990) Virus species, a much over- Francki RIB, Fauquet CM, Knudson DL and Brown F looked but essential concept in virus classification. Intemir- (1991) Classification and Nomenclature of Viruses. Fifth ology 31: 241.

TEN UlVlRUSES Bryce Falk University of California, Davis Davis, California, USA

Taxonomy and Classification and stunting. The similarity of their biological properties and symptomatology led to an early The are a relatively newly recognized artificial grouping of these viruses. Receilt work on group of plant viruses, however, the diseases they the physical, chemical and molecular properties of cause have been known since the early 1900s. There the tenuiviruses has confirmed their relationships to are currently five recognized tenuiviruses including: each other, and shown them to be distinctly different rice stripe virus (RStV); maize stripe virus (MStV); from most other plant viruses. rice hoja blanca virus (RHBV); rice grassy stunt virus (RGSV); and European wheat striate mosaic virus (EWSMV) (see also Table 1). Based upon their similar biological properties these viruses Virus Structure and Composition have been loosely grouped together for several years. However, only since 1981 have some of the The name for the tenuivirus group is derived from the unique and interesting molecular properties of the slender (tenuous), filamentous ribonucleoprotein tenuiviruses become known. particles associated with these viruses. Such particles have been identified in cells of tenuivirus-infected plant and insect hosts. Electron microscopic analysis has shown the particles to be threadlike, very thin in Biological Properties diameter (8-10 nm) and often without defined lengths. These particles have often been referred to All tenuiviruses are transmitted to plants by specific as virions or virus particles. However, recent evidence delphacid planthoppers (Homoptera: Delphacidae, obtained by examining the filamentous particles using see Table 1). They are not mechanically transmissible high-resolution electron microscopy, and by in vitro even experimentally. The plant host ranges of all characterization of the particles suggests that they tenuiviruses are limited to monocotyledonous species are likely to be ribonucleoprotein components of a within the family . The symptoms induced yet to be identified larger, more complex virion. in infected plants are generally similar for the Filamentous ribonucleoprotein particles (RNPs) different tenuiviruses and includes general leaf have been purified from plants infected by MStV, striping, a distinct white coloring of the leaf stripes RStV, RGSV and RHBV. Electron microscopic

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