Arch Virol (2009) 154:899–907 DOI 10.1007/s00705-009-0367-z VIROLOGY DIVISION NEWS Secoviridae: a proposed family of plant viruses within the order Picornavirales that combines the families Sequiviridae and Comoviridae, the unassigned genera Cheravirus and Sadwavirus, and the proposed genus Torradovirus He´le`ne Sanfac¸on Æ Joan Wellink Æ Olivier Le Gall Æ Alexander Karasev Æ Rene´ van der Vlugt Æ Thierry Wetzel Received: 21 November 2008 / Accepted: 16 March 2009 / Published online: 7 April 2009 Ó Her Majesty the Queen in Right of Canada 2009 Abstract The order Picornavirales includes several plant specialized proteins or protein domains to move through viruses that are currently classified into the families Com- their host. In phylogenetic analysis based on their repli- oviridae (genera Comovirus, Fabavirus and Nepovirus) and cation proteins, these viruses form a separate distinct Sequiviridae (genera Sequivirus and Waikavirus) and into lineage within the picornavirales branch. To recognize the unassigned genera Cheravirus and Sadwavirus. These these common properties at the taxonomic level, we pro- viruses share properties in common with other picornavi- pose to create a new family termed ‘‘Secoviridae’’ to rales (particle structure, positive-strand RNA genome with include the genera Comovirus, Fabavirus, Nepovirus, a polyprotein expression strategy, a common replication Cheravirus, Sadwavirus, Sequivirus and Waikavirus. Two block including type III helicase, a 3C-like cysteine pro- newly discovered plant viruses share common properties teinase and type I RNA-dependent RNA polymerase). with members of the proposed family Secoviridae but have However, they also share unique properties that distinguish distinct specific genomic organizations. In phylogenetic them from other picornavirales. They infect plants and use reconstructions, they form a separate sub-branch within the Secoviridae lineage. We propose to create a new genus termed Torradovirus (type species, Tomato torrado virus) Electronic supplementary material The online version of this and to assign this genus to the proposed family article (doi:10.1007/s00705-009-0367-z) contains supplementary Secoviridae. material, which is available to authorized users. H. Sanfac¸on (&) Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, P. O. Box 5000, Introduction 4200 Highway 97, Summerland, BC V0H-1Z0, Canada e-mail: [email protected] The creation of the order Picornavirales has given a useful J. Wellink framework for the taxonomy of a large group of viruses, Wageningen University, Wageningen, The Netherlands previously referred to as ‘picorna-like viruses’ or ‘members of the picornavirus-like superfamily or supergroup’ [23]. O. Le Gall INRA Bordeaux-Aquitaine and Universite´ Victor Segalen, Members of the order Picornavirales share many common Villenave d’Ornon, France properties. They all have small icosahedral particles (25– 30 nm) with a pseudo-T = 3 symmetry. The coat pro- A. Karasev tein(s) structure is similar among picornavirales. It is made Department of PSES, University of Idaho, Moscow, ID, USA up of jelly rolls that can all be present in one large CP, or R. van der Vlugt divided among two or three smaller CPs [8, 23 and refer- Plant Research International, Wageningen, The Netherlands ences therein]. All picornavirales have a positive-strand RNA genome that may be monopartite or bipartite. Each T. Wetzel RLP Agroscience, AlPlanta, Neustadt an der Weinstrasse, genome segment encodes a large polyprotein. This poly- Germany protein is cleaved by cysteine proteinases (such as the 123 900 H. Sanfac¸on et al. picornavirus 3C proteinase) that are structurally related to Table 1 Proposed structure of the family Secoviridae chymotrypsin [1, 9, 13]. The genome organization is con- Subfamily Genus Type species served among picornavirales. The genome contains a typical ‘replication block’ that includes a type III helicase, Comovirinae Comovirus Cowpea mosaic virus (CPMV) the 3C-like proteinase and a type I RNA-dependent RNA- Comovirinae Fabavirus Broad bean wilt virus 2 (BBWV2) polymerase (Hel–Pro–Pol) [23]. The order Picornavirales Comovirinae Nepovirus Tobacco ringspot virus (TRSV) includes viruses that infect vertebrates, insects, arthropods, N/A Sequivirus Parsnip yellow fleck virus (PYFV) higher plants, fungi and algae. N/A Waikavirus Rice tungro spherical virus (RTSV) The family Comoviridae was for a long time the only N/A Sadwavirus Satsuma dwarf virus (SDV) known group of plant ‘‘picorna-like viruses’’ [12, 18]. N/A Cheravirus Cherry rasp leaf virus (CRLV) Members of the family Comoviridae have bipartite gen- N/A Torradovirus Tomato torrado virus (ToTV) omes and contain either a single coat protein (genus N/A not applicable Nepovirus) or two coat proteins (genera: Comovirus and Fabavirus that are mainly distinguished on the basis of their mode of transmission and hierarchical clustering of clusters with cheraviruses in phylogenetic analysis using amino acid sequences). The discovery of plant ‘‘picorna- the amino acid sequence of replication proteins and has like viruses’’ with a monopartite genome and three CP other characteristics typical of cheraviruses [22]. Recently, subunits resulted in the creation of a distinct family, the elucidation of the complete genomic sequence of Sequiviridae, which currently includes two genera tomato torrado virus (ToTV) and tomato marchitez virus (Sequivirus and Waikavirus, distinguished by their specific (ToMarV), two plant ‘‘picorna-like viruses’’ of a new type, genomic organization and mode of transmission) [19]. The also suggests that they do not belong to any of the existing molecular characterization of a number of new viruses as genera and that a new genus should be created within the well as viruses previously considered to be members of the order Picornavirales [44, 45]. The ‘‘plant picornavirales’’ genus Nepovirus revealed that they differ significantly ICTV study group reevaluated the taxonomy of this group from nepoviruses, comoviruses and fabaviruses [22]. These of viruses and proposed to create a new family that would new viruses have a bipartite genome and encode either two encompass all plant viruses that currently belong to the or three CP subunits, which distinguishes them from the order Picornavirales (these viruses will be referred to as nepoviruses. In phylogenetic studies based on their repli- plant picornavirales in the remainder of this paper). cation proteins, they were found to be related to members Because the proposed family is mainly an amalgamation of of the families Comoviridae or Sequiviridae, but branched the families Sequiviridae and Comoviridae (as well as the in separate clades. Two new genera were created [22]. The unassigned genera Cheravirus and Sadwavirus), the name genus Cheravirus includes viruses that have three CPs [20], ‘‘Secoviridae’’ was selected for the new family. The family and the genus Sadwavirus includes viruses that have two is proposed to include the genera Comovirus, Fabavirus, CPs [21]. Originally, various studies proposed that the new Nepovirus, Sequivirus, Waikavirus, Cheravirus and Sad- genera should be included in the families Comoviridae or wavirus (Table 1). In addition, the study group proposed to Sequiviridae or that a new family should be created [10, 14, create a new genus termed Torradovirus and to assign this 16, 17, 24, 40]. However, at the time of creation of these new genus to the proposed family Secoviridae. The ICTV genera, the executive committee from the International executive committee approved the proposals in 2008 and Committee for the Taxonomy of Viruses (ICTV) felt that a posted them for ratification by the ICTV membership. This reevaluation of the taxonomy of plant picorna-like viruses paper discusses the rationale for the creation of the family was necessary before the two new genera could be assigned Secoviridae and genus Torradovirus and outlines the to either existing families or to a new family. Thus, for the common characteristics of members of the new family as time being, the genera Cheravirus and Sadwavirus are well as criteria distinguishing genera within the family. included in the order Picornavirales but are not assigned to any family [20–23]. The current classification has limitations in that prop- Rationale for the creation of the proposed family erties shared by cheraviruses, sadwaviruses and other plant Secoviridae viruses classified in the order Picornavirales are not rec- ognized. In addition, some viruses are still difficult to Although the diversity in the genomic organization of plant assign to existing genera/families. For example, strawberry picornavirales is apparent (Fig. 1), these viruses share latent ringspot virus (SLRSV), a founder member of the many common features. In addition to having characteris- nepovirus ‘‘group’’ is currently considered a tentative tics in common with other picornavirales as discussed sadwavirus because it encodes two CP subunits, but it above (general capsid structure, polyprotein strategy for 123 The proposed plant virus family Secoviridae 901 RNA2 RNA1 COMOVIRINAE (proposed sub-family) AUG HelPro Pol An Comovirus (CPMV) MP An CPL CPS HelPro Pol An Fabavirus (BBWV2) MP An CPL CPS Nepovirus A Subgroup A (ArMV) MP CP n HelPro Pol An Subgroup B (TBRV) MP CP An HelPro Pol An Subgroup C (ToRSV) MP CP An HelPro Pol An ADDITIONAL GENERA Sadwavirus MP An HelPro Pol An (Type species: SDV) CPL CPS Tentative species MP? CP ? An HelPro Pol A SMoV and BRNV n Tentative species A MP n HelPro Pol An SLRSV CPL CPS CP2 Cheravirus (CRLV and ALSV) A MP n HelPro Pol An CP1 CP3 CP2 Proposed Torradovirus (ToTV) A MP? n HelPro Pol An CP1 CP3 CP2 Sequivirus (PYFV) Hel Pro Pol CP1 CP3 CP2 Waikavirus (RTSV) Hel Pro Pol An CP1 CP3 Fig. 1 Genome organization of plant picornavirales. Hel Helicase, polyproteins differing by their translation initiation site as indicated Pro 3C-like Proteinase, Pol RNA-dependent RNA polymerase, CP by the second AUG above the CPMV polyprotein. Dashed lines capsid protein, MP movement protein, An poly(A). Question marks below the 30 or 50 UTR represent areas of sequence identity (?) after MP or CP indicate that the position and/or function of the between RNA1 and RNA2.