The current state of plant virus taxonomy (2001)

Virus taxonomy can be defined as the arranging of viruses into related clusters, identification of the extent of relatedness within and among these clusters, and the naming of the clusters (= taxa). The first internationally organized initiative for the naming and classification of animal, plant and microbial viruses was the formation of the International Committee on Nomenclature of Viruses in 1966. This was renamed the International Committee on Taxonomy of Viruses (ICTV) in 1973 and has since produced seven reports reviewing the state of virus taxonomy, the latest of which was published recently (Van Regenmortel et al., 2000). This brief review describes the current classification of plant viruses, outlines the principles used in virus classification and their application, and highlights the taxa created since the previous ICTV Report (Murphy et al., 1995) was published. Most plant viruses are classified in 649 species, most of which are classified among 73 genera. Forty-nine genera are classified among 15 families; the remaining 24 genera have not been assigned to a family. Some species are recognized as members of a family but have not been assigned to a particular genus; 15 other recognized distinct species of uncertain taxonomic status, designated Unassigned Species, have yet to be assigned to a genus or family. The current classification is shown in Table 1, which also shows the classification of viroids (7 genera in 2 families). As in the 7th ICTV Report (van Regenmortel et al., 2000), the families and genera are arranged according to their genome types (ssDNA, dsRNA, etc.), although this grouping has no taxonomic status. A complete listing of plant virus and viroid species then recognized, together with their recommended abbreviations, has been published in Fauquet and Mayo (1999). The main guiding principles in devising a taxonomy for viruses have been discussed in Mayo and Pringle (1998). They are: stability—that is that once decided, names and relationships should remain unaltered for as long as possible, thereby facilitating reference to older literature. Unlike other biological taxonomies, that for viruses has no Rule of Priority. That this system has functioned well is possibly due to the relatively few virus species (currently 1550 of all types) that have been described. utility—that is, the scheme of taxonomic relationships should be found to be useful by the wider virology community. To this end, ICTV decisions are taken in consultation with, and usually at the prompting of, study groups of interested virologists. Utility is usually the result of a prior demand for taxonomic order. It can be assessed by the compliance of working virologists. acceptability—that is, working virologists should be happy to use the names and taxonomic relationships listed. All decisions are susceptible to modification by succeeding taxonomic proposals. Unacceptable names and taxa are eliminated in this way. flexibility—that is that the taxonomy is amenable to revision and reassessment in the light of new discoveries. Newly recognized viruses are constantly being described, as are novel details in the genetic structures of known viruses. A useful taxonomy and nomenclature must therefore adapt to new information. The ICTV is a committee of the Virology Division of the International Union of Microbiological Societies (IUMS), which represents the interests of member microbiological societies. ICTV comprises national members nominated by countries with microbiological societies affiliated to IUMS, life members elected by ICTV, and the elected members of the Executive Committee (EC). Decisions of ICTV are made at plenary sessions of the International Virology Congresses (convened every 3 years) and by postal voting. Statutes define the constitution of ICTV, its mode of operation and how it is constituted. The current version of the Statutes is published in the 7th ICTV Report (Van Regenmortel et al., 2000). The ICTV is advised by its EC, which consists of elected officials among whom are the chairs of subcommittees that represent the major fields of virology. The Plant Virus Subcommittee has at present 21 study groups, each of which is concerned with a particular taxon or group of taxa. The groups make proposals for changes to taxonomy within their fields of interest to accommodate new information as it emerges. Proposals approved by the subcommittees are considered by the EC and, if approved, are presented to the ICTV for ratification. Proposals from outside the ICTV structure are normally referred to the appropriate study group for discussion, or failing this, to the appropriate subcommittee. The Executive Committee of the ICTV has developed an International Code of Nomenclature based on ad hoc rules (Mayo and Horzinek, 1998; Van Regenmortel et al., 2000). These present the modus operandi of the ICTV and are the justification for the decisions of the executive committee and its subcommittees. Many of the rules contained in the code are self-evident. Others, however, have been devised in response to pressures from the virology community for guidance, or even pleas for consistency, in decision-making. Some issues that have provoked comment recently are: The rules state that a new name should be distinctive (Rule 3.14), easy to remember (Rule 3.12), be free of association with any individual’s name (Rule 3.11), and avoid absurdity or offence in any language (Rule 3.19). Also, names should not convey particular meaning such that some members of the taxon would seem not to belong in it (Rule 3.18). Unlike the names of species in all other biological disciplines, those of virus species are not latinized. Thus species names have no gender. The names of genera must end in ‘-virus’ and the names of families must end in ‘-viridae’. Because taxa have been named in the past under less well developed rules, some in the current list have names that are in contravention of current practice. However, in the interests of the stability of nomenclature, few have been altered. All taxon names (including those of species) are written in italic script and have a capital initial letter for the first name. However, in vernacular usage the name is not used formally and italic script is not necessary. Thus, the potyvirus Tobacco etch virus is classified in genus Potyvirus and family Potyviridae. Collective names such as ‘potyviruses’ and ‘nepoviruses’ are never italicised. How the ICTV decides that particular virus isolates belong to one or another species, or are strains within a single species, has been a contentious issue (Van Regenmortel et al., 1997). The basis for decisions is the definition of a virus species that has been accepted by ICTV. It is: ‘A virus species is a polythetic class of viruses that contitutes a replicating lineage and occupies a particular ecological niche’ (Van Regenmortel, 1990). The current ICTV Report (Van Regenmortel et al., 2000) lists the criteria used to differentiate distinct species from virus strains. It is important to emphasize that the criteria used for demarcating species in different families can, and sometimes do, differ. This is both because families can be intrinsically different and because the criteria used are determined by virologists in different study groups. In Table 1, the taxa that were not in the previous ICTV Report (Murphy et al., 1995) are marked in bold text. The most striking novelties are that retrotransposons found in plants are now classified in two genera in two families (Pseudoviridae and Metaviridae) and that viroids have been classified in seven genera distributed among two families. The latest report also contains three new plant virus families (Luteoviridae, Caulimoviridae and Closteroviridae), 26 new genera and three renamed genera in family Geminiviridae (Mastrevirus, Curtovirus and Begomovirus). M.A.M. and A.A.B. are, respectively, Secretary of the ICTV Executive Committee and Chair of the Plant Virus Subcommittee; M.A.M. is supported by funding from the Scottish Executive Rural Affairs Department, and A.A.B. by Horticulture Research International.