Secoviridae: A Family of Plant Picorna‐Like Viruses with Monopartite or Bipartite Genomes

Abstract

Members of the family Secoviridae, referred to as secovirids, are plant viruses that share features with animal and human viruses of the family Picornaviridae and other insect or marine viruses of the order Picornavirales. These common features include a conserved structure of the icosahedral virus particles, the expression of viral proteins by proteolytic cleavage of large polyproteins and viral replication proteins with conserved sequence motifs, including the viral RNA‐dependent RNA polymerase and protease. Secovirids also share the distinguishing feature of encoding specialised proteins that enable their movement in plant and counteract plant defence mechanisms, such as RNA silencing. The family Secoviridae includes eight genera. Members of the genera Comovirus, Fabavirus, Nepovirus, Cheravirus, Sadwavirus and Torradovirus have a bipartite positive‐strand RNA genome, whereas members of the genera Sequivirus and Waikavirus have a monopartite genome.

Key Concepts

  • Many plant viruses are related to animal and human viruses of the family Picornaviridae and to other picorna‐like viruses infecting algae and arthropods.
  • A recent update in the taxonomy of plant picorna‐like viruses has led to the creation of the family Secoviridae which amalgamates the previous families Comoviridae and Sequiviridae as well as the genera Cheravirus, Sequivirus and Torradovirus.
  • Secovirids share common characteristics including having both similar virus particle structures and genomic organizations and requiring specialised proteins to facilitate their movement within the host plant or counteract plant defence mechanism.
  • Secovirids produce their proteins in the form of large polyproteins that are cleaved at specific sites by a viral protease.
  • Replication of the viral RNA occurs in large protein complexes in association with intracellular membranes from the host.
  • Plant cells infected with secovirids generally display tubular structures that are composed of the viral movement protein, contain virus‐like particles and traverse the cell wall. These tubular structures are involved in the movement of the virus from cell to cell.
  • Secovirids can be transmitted through seeds and pollen or with the help of nematode or arthropod vectors and their spread in the field is largely dependent on their mode of transmission.
  • Some secovirids have been successfully exploited as plant vectors, allowing epitope presentation for vaccine production, expression of proteins in plants and silencing of endogenous plant genes.

Keywords: picornavirales; protease; virus taxonomy; plant–virus interactions; cell‐to‐cell movement; virus replication

Figure 1. Compared architecture of the capsids of members of the family Secoviridae. In all members of the order Picornavirales, the capsid is formed from 60 subunits (shown at the right of the figure). In the case of human and animal viruses belonging to the family Picornaviridae and of some plant picorna‐like viruses (sequiviruses, waikaviruses, cheraviruses and torradoviruses), each subunit is made up of three proteins, VP1–VP3, and each protein is folded as a single barrel (top of the figure). In comoviruses, fabaviruses and sadwaviruses (middle), the domains corresponding to VP2 and VP3 are fused into a single protein (large coat protein, L) folded in two barrels (Lin et al., ), whereas the VP1 domain is contained in a separate protein folded in a single barrel (small coat protein, S). In nepoviruses (bottom), the three domains are fused into a single coat protein (CP) folded in three barrels (Le Gall et al., ; Chandrasekar and Johnson, ; Seitsonen et al., ).
Figure 2. Genomic organization of members of the family Secoviridae compared with that of Human enterovirus‐C (HEV‐C), a typical member of the family Picornaviridae. The RNA genome is depicted with a horizontal line. The circle at the 5′ end of the genome represents the VPg protein bound to the 5′ end of the RNA (open circle: the presence of a VPg is probable but has not been confirmed experimentally). The polyadenylated tail is also shown at the 3′ end of the RNA (An). The single large polyprotein encoded by a large open reading frame in the RNA of most secovirids is shown with boxes. Vertical lines within the polyproteins represent cleavage sites that have been identified experimentally (solid lines) or that are deduced based on sequence comparisons (dotted lines). Regions of the polyproteins that are conserved among secovirids are shown in yellow (replication proteins), blue (CPs) and green (MP). Highly conserved motifs are represented by the star (RNA‐dependent RNA polymerase motif), the diamond (protease motif), the triangle (nucleotide‐binding site motif within the putative helicase domain) and the red circle (protease cofactor motif). Hatched areas within the open reading frame or broken lines below the untranslated regions indicate areas that are identical between RNA1 and RNA2. In torradoviruses and waikaviruses, additional open reading frames are shown by the smaller boxes above the larger open reading frame. In the case of comoviruses, the two narrow boxes in RNA2 represent alternative translation initiation at two different AUGs to produce two overlapping polyproteins. After proteolytic cleavage of these polyproteins, the 58‐kDa protein (shown in white) will be released from the larger polyprotein and the MP (shown in green) will be released from the smaller polyprotein. Virus abbreviations are as in Table.
Figure 3. Electron micrograph depicting purified nepovirus particles. Purified particles from a Tomato ringspot virus isolate in negative staining. Note the empty particle, which is penetrated by the negative stain (arrow). Bar represents 25 nm. Reprinted from Sanfacon H (2008) © Elsevier.
Figure 4. Hierarchical clustering of members of the family Secoviridae and selected members of the order Picornavirales based on the Pro‐Pol amino acid sequence. The families and genera are delineated on the right. Amino acid sequences between the conserved CG motif in the protease and the conserved GDD motif in the RNA‐dependent RNA polymerase were aligned (Le Gall et al., ; Sanfacon et al., ). Results are presented as a phylogram with Potato virus Y (PVY, a member of the family Potyviridae), used as an outgroup. Black circles indicate nodes supported by bootstrap values above 85%. Virus acronyms are as defined in Tables and . Additional acronyms are as follows: HaRNAV (Heterosigma akashiwo RNA virus), CrPV (Cricket paralysis virus), IFV (Infectious flacherie virus), HAV (Hepatitis A virus), FMDV (Foot‐and‐mouth disease virus), EMCV (Encephalomyocarditis virus) and ERBV (Equine rhinitis B virus).
Figure 5. Electron micrograph depicting cytopathological structures typical of nepovirus‐infected cells. (a) Proliferation of membrane vesicles observed in the vicinity of the nucleus (Nc) in cells infected with a Tomato ringspot virus isolate. (b) Tubular structures containing virus‐like particles accumulating near the cell wall (CW) in cells infected with a Peach rosette mosaic virus isolate. (c) Tubular structure traversing the cell wall in cells infected with an Arabis mosaic virus isolate. Bars represent 200 nm. Reprinted from Sanfacon H (2008) © Elsevier.
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Further Reading

King AMQ, Adams MJ, Carstens EB Lefkowitz EJ (2012) Virus Taxonomy, Ninth Report of the International Committee on the Taxonomy of Viruses (ICTV). [See in particular chapters on Picornavirales (pp. 835–839) and Secoviridae (pp. 881–899)]. London: Elsevier/Academic Press. For updates to virus taxonomy that occurred after publication of the Ninth Report, please refer to the following ICTV URL: http://www.ictvonline.org/index.asp?bhcp=1].

Mahy BWJ and Van Regenmortel MH (eds) (2008) Encyclopedia of Virology, 3rd edn. Vol. 3, pp. 405–413. [See in particular chapters on Cowpea mosaic virus (pp. 569–574), Nepovirus (pp. 405–413) and Sadwavirus (pp. 523–526).] Oxford: Elsevier.

Pouwels J, Carette JE, Van Lent J and Wellink J (2002) Cowpea mosaic virus: effects on host cell processes. Molecular Plant Pathology 3: 411–418.

Sanfacon H, Zhang G, Chisholm J, Jafarpour B and Jovel J (2006) Molecular biology of Tomato ringspot nepovirus, a pathogen of ornamentals, small fruits and fruit trees. In: Teixeira da Silva J, (ed). Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues, 1st edn. Vol. 3, pp. 540–546. London, UK: Global Science Books.

Susi P (2004) Black currant reversion virus, a mite‐transmitted nepovirus. Molecular Plant Pathology 5: 167–173.

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Sanfaçon, Hélène(Apr 2015) Secoviridae: A Family of Plant Picorna‐Like Viruses with Monopartite or Bipartite Genomes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000764.pub3]