Secoviridae: The Amalgamation of the Families Sequiviridae and Comoviridae

Hélène Sanfaçon, Agriculture and Agri‐Food Canada, Summerland, British Columbia, Canada

Published online: September 2009

DOI: 10.1002/9780470015902.a0000764.pub2

Several plant viruses share features with animal and human viruses of the family Picornaviridae, including a conserved structure of both the virus particle and the viral genome, expressing viral proteins by proteolytic cleavage of large polyproteins and encoding replication proteins with conserved sequence motifs. Members of the family Comoviridae were originally described as the only plant picorna-like viruses. Other plant picorna-like viruses were later discovered and classified in the family Sequiviridae. Sequiviridae and Comoviridae are related to each other in phylogenetic studies and share the common property of encoding specialized proteins to enable their movement in the plant. Recently, it was proposed to regroup plant picorna-like viruses into a single family termed ‘secoviridae’. The proposed family amalgamates the families Comoviridae and Sequiviridae, and incorporates other plant picorna-like viruses currently classified in the genera Sadwavirus and Cheravirus, and the proposed genus ‘Torradovirus’.

Key concepts:

  • Many plant viruses are related to the animal and human picornaviridae and to other picorna-like viruses infecting algae and arthropods.
  • A recent update in the taxonomy of plant picorna-like viruses has lead to the creation of the family ‘secoviridae’ which amalgamates the families Comoviridae and Sequiviridae as well as the existing genera Cheravirus, Sequivirus and the proposed genus ‘torradovirus’.
  • Secoviridae share many common characteristics including having both similar virus particle structures and genomic organizations, and requiring a specialized protein to facilitate their movement within the host plant.
  • Secoviridae produce their proteins in the form of large polyproteins that are cleaved at specific sites by a viral proteinase.
  • Replication of the viral RNA occurs in large protein complexes in association with intracellular membranes from the host.
  • Plant cells infected with secoviridae 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 probably involved in the movement of the virus from cell to cell.
  • Secoviridae 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.

Keywords: picornavirales; proteinase; virus taxonomy; plant–virus interactions; cell-to-cell movement; virus replication

Figure 1. Compared architecture of the capsids of members of the proposed 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 (Sequivirus, Waikavirus, Cheravirus and roposed torradovirus), 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., 1999), 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., 1995a; Chandrasekar and Johnson, 1998; Seitsonen et al., 2008).
Figure 2. Genomic organization of Secoviridae compared with that of a poliovirus (PV), 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: 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 Secoviridae 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 Secoviridae are shown in yellow (replication proteins), blue (coat protein(s)) and green (movement protein). Highly conserved motifs are represented by the star (RNA-dependent RNA polymerase motif), the diamond (proteinase motif), the triangle (nucleotide-binding site motif within the putative helicase domain) and the red circle (proteinase 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 movement protein (shown in green) will be released from the smaller polyprotein. Virus abbreviations are as in Table 1.
Figure 3. Electron micrograph depicting purified nepovirus particles. Purified Tomato ringspot virus particles in negative staining. Note the empty particle which is penetrated by the negative stain (arrow). Bar represents 25 nm. Reprinted with permission from Sanfacon H (2008) Nepovirus. In: Mahy BWJ and Van Regenmortel MH (eds), Encyclopedia of Virology, 3rd edn, vol. 3, pp. 405–413. Oxford: Elsevier.
Figure 4. Hierarchical clustering of Secoviridae based on the Pro-Pol amino acid sequence. Amino acid sequences between the conserved CG motif in the proteinase and the conserved GDD motif in the RNA-dependent RNA polymerase were aligned (Le Gall et al., 2007, 2008). Results are presented as an unrooted radial tree including definitive species of the proposed family Secoviridae (virus abbreviations are as in Table 1). The bar represents a p-distance of 0.1. Different genera within the families are shown with the coloured circles.
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 Tomato ringspot virus-infected cells. (b) Tubular structures containing virus-like particles accumulating near the cell wall (CW) in Peach rosette mosaic virus-infected cells. (c) Tubular structure traversing the cell wall in Arabis mosaic virus-infected cells. Bars represent 200 nm. Reprinted with permission from Sanfacon H (2008) Nepovirus. In: Mahy BWJ and Van Regenmortel MH (eds), Encyclopedia of Virology, 3rd edn, vol. 3, pp. 405–413. Oxford: Elsevier.
close
 References
    Allaire M, Chernaia MM, Malcolm BA and James MN (1994) Picornaviral 3C cysteine proteinases have a fold similar to chymotrypsin-like serine proteinases. Nature 369: 72–76.
    Andret-Link P, Schmitt-Keichinger C, Demangeat G, Komar V and Fuchs M (2004) The specific transmission of Grapevine fanleaf virus by its nematode vector Xiphinema index is solely determined by the viral coat protein. Virology 320: 12–22.
    Argos P, Kamer G, Nicklin MJ and Wimmer E (1984) Similarity in gene organization and homology between proteins of animal picornaviruses and a plant comovirus suggest common ancestry of these virus families. Nucleic Acids Research 12: 7251–7267.
    Bazan JF and Fletterick RJ (1988) Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications. Proceedings of the National Academy of Sciences of the USA 85: 7872–7876.
    Bruening G (1990) Replication of satellite RNA of Tobacco ringspot virus. Seminars in Virology 1: 127–134.
    Canizares MC, Taylor KM and Lomonossoff GP (2004) Surface-exposed C-terminal amino acids of the small coat protein of Cowpea mosaic virus are required for suppression of silencing. Journal of General Virology 85: 3431–3435.
    Carette JE, van Lent J, MacFarlane SA, Wellink J and van Kammen A (2002a) Cowpea mosaic virus 32- and 60-kilodalton replication proteins target and change the morphology of endoplasmic reticulum membranes. Journal of Virology 76: 6293–6301.
    Carette JE, Stuiver M, Van Lent J, Wellink J and Van Kammen A (2000) Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. Journal of Virology 74: 6556–6563.
    Carette JE, Verver J, Martens J et al. (2002b) Characterization of plant proteins that interact with cowpea mosaic virus ‘60K’ protein in the yeast two-hybrid system. Journal of General Virology 83: 885–893.
    Carrier K, Xiang Y and Sanfacon H (2001) Genomic organization of RNA2 of Tomato ringspot virus: processing at a third cleavage site in the N-terminal region of the polyprotein in vitro. Journal of General Virology 82: 1785–1790.
    Carvalho CM, Wellink J, Ribeiro SG, Goldbach RW and Van Lent JW (2003) The C-terminal region of the movement protein of Cowpea mosaic virus is involved in binding to the large but not to the small coat protein. Journal of General Virology 84: 2271–2277.
    Chandrasekar V and Johnson JE (1998) The structure of Tobacco ringspot virus: a link in the evolution of icosahedral capsids in the picornavirus superfamily. Structure 6: 157–171.
    Chen ZG, Stauffacher C, Li Y et al. (1989) Protein-RNA interactions in an icosahedral virus at 3.0 A resolution. Science 245: 154–159.
    Chisholm J, Zhang G, Wang A and Sanfacon H (2007) Peripheral association of a polyprotein precursor form of the RNA-dependent RNA polymerase of Tomato ringspot virus with the membrane-bound viral replication complex. Virology 368: 133–144.
    Digiaro M, Elbeaino T and Martelli GP (2007) Development of degenerate and species-specific primers for the differential and simultaneous RT-PCR detection of grapevine-infecting nepoviruses of subgroups A, B and C. Journal of Virological Methods 141: 34–40.
    Dorssers L, Van der Kroll S, Van der Meer J, Van Kammen A and Zabel P (1984) Purification of Cowpea mosaic virus RNA replication complex: identification of a virus-encoded 110 000-dalton polypeptide responsible for RNA chain elongation. Proceedings of the National Academy of Sciences of the USA 81: 1951–1955.
    Everett KR, Milne KS and Forster RL (1994) Nucleotide sequence of the coat protein genes of Strawberry latent ringspot virus: lack of homology to the nepoviruses and comoviruses. Journal of General Virology 75: 1821–1825.
    Firth AE and Atkins JF (2008) Bioinformatic analysis suggests that a conserved ORF in the waikaviruses encodes an overlapping gene. Archives of Virology 153: 1379–1383.
    Franssen H, Leunissen J, Goldbach R, Lomonossoff G and Zimmern D (1984) Homologous sequences in non-structural proteins from Cowpea mosaic virus and picornaviruses. EMBO Journal 3: 855–861.
    Gaire F, Schmitt C, Stussi-Garaud C, Pinck L and Ritzenthaler C (1999) Protein 2A of grapevine fanleaf nepovirus is implicated in RNA2 replication and colocalizes to the replication site. Virology 264: 25–36.
    Gorbalenya AE, Donchenko AP, Blinov VM and Koonin EV (1989) Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases. A distinct protein superfamily with a common structural fold. FEBS Letters 243: 103–114.
    Han S and Sanfacon H (2003) Tomato ringspot virus proteins containing the nucleoside triphosphate binding domain are transmembrane proteins that associate with the endoplasmic reticulum and cofractionate with replication complexes. Journal of Virology 77: 523–534.
    Hemmer O, Oncino C and Fritsch C (1993) Efficient replication of the in vitro transcripts from cloned cDNA of Tomato black ring virus satellite RNA requires the 48K satellite RNA-encoded protein. Virology 194: 800–806.
    Huet H, Mahendra S, Wang J et al. (1999) Near immunity to Rice tungro spherical virus achieved in rice by a replicase-mediated resistance strategy. Phytopathology 89: 1022–1027.
    Isogai M, Watanabe K, Uchidate Y and Yoshikawa N (2006) Protein-protein- and protein-RNA-binding properties of the movement protein and VP25 coat protein of Apple latent spherical virus. Virology 352: 178–187.
    Iwanami T, Kondo Y and Karasev AV (1999) Nucleotide sequences and taxonomy of Satsuma dwarf virus. Journal of General Virology 80: 793–797.
    Jovel J, Walker M and Sanfacon H (2007) Recovery of Nicotiana benthamiana plants from a necrotic response induced by a nepovirus is associated with RNA silencing but not with reduced virus titer. Journal of Virology 81: 12285–12297.
    Karetnikov A and Lehto K (2008) Translation mechanisms involving long-distance base pairing interactions between the 5¢ and 3¢ non-translated regions and internal ribosomal entry are conserved for both genomic RNAs of Blackcurrant reversion nepovirus. Virology 371: 292–308.
    Laporte C, Vetter G, Loudes AM et al. (2003) Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15: 2058–2075.
    Le Gall O, Candresse T and Dunez J (1995a) A multiple alignment of the capsid protein sequences of nepoviruses and comoviruses suggests a common structure. Archives of Virology 140: 2041–2053.
    Le Gall O, Candresse T and Dunez J (1995b) Transfer of the 3¢ non-translated region of Grapevine chrome mosaic virus RNA-1 by recombination to Tomato black ring virus RNA-2 in pseudorecombinant isolates. Journal of General Virology 76: 1285–1289.
    Le Gall O, Christian P, Fauquet CM et al. (2008) Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T=3 virion architecture. Archives of Virology 153: 715–727.
    Le Gall O, Sanfacon H, Ikegami M et al. (2007) Cheravirus and Sadwavirus: two unassigned genera of plant positive-sense single-stranded RNA viruses formerly considered atypical members of the genus Nepovirus (family Comoviridae). Archives of Virology 159: 1767–1774.
    Lin T, Chen Z, Usha R et al. (1999) The refined crystal structure of cowpea mosaic virus at 2.8 A resolution. Virology 265: 20–34.
    Nolke G, Cobanov P, Uhde-Holzem K et al. (2008) Grapevine fanleaf virus (GFLV)-specific antibodies confer GFLV and Arabis mosaic virus (ArMV) resistance in Nicotiana benthamiana. Molecular Plant Pathology 10: 41–49.
    Peters SA, Voorhorst WG, Wery J, Wellink J and van Kammen A (1992) A regulatory role for the 32K protein in proteolytic processing of Cowpea mosaic virus polyproteins. Virology 191: 81–89.
    Pouwels J, Van Der Krogt GN, Van Lent J, Bisseling T and Wellink J (2002) The cytoskeleton and the secretory pathway are not involved in targeting the Cowpea mosaic virus movement protein to the cell periphery. Virology 297: 48–56.
    Ratcliff F, Harrison BD and Baulcombe DC (1997) A similarity between viral defense and gene silencing in plants. Science 276: 1558–1560.
    Reavy B, Mayo MA, Turnbull-Ross AD and Murant AF (1993) Parsnip yellow fleck and rice tungro spherical viruses resemble picornaviruses and represent two genera in a proposed new plant Picornavirus family (Sequiviridae). Archives of Virology 131: 441–446.
    Ritzenthaler C, Laporte C, Gaire F et al. (2002) Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. Journal of Virology 76: 8808–8819.
    Ritzenthaler C, Schmit A-C, Michler P, Stussi-Garaud C and Pinck L (1995) Grapevine fanleaf nepovirus P38 putative movement protein is located on tubules in vivo. Molecular Plant Microbe Interactions 8: 379–387.
    Rott ME, Tremaine JH and Rochon DM (1991) Comparison of the 5¢ and 3¢ termini of Tomato ringspot virus RNA1 and RNA2: evidence for RNA recombination. Virology 185: 468–472.
    Seitsonen JJ, Susi P, Lemmetty A and Butcher SJ (2008) Structure of the mite-transmitted Blackcurrant reversion nepovirus using electron cryo-microscopy. Virology 378: 162–168.
    Turnbull-Ross AD, Reavy B, Mayo MA and Murant AF (1992) The nucleotide sequence of parsnip yellow fleck virus: a plant picorna-like virus. Journal of General Virology 73: 3203–3211.
    Van Bokhoven H, Le Gall O, Kasteel D et al. (1993) Cis- and trans-acting elements in Cowpea mosaic virus RNA replication. Virology 195: 377–386.
    Verbeek M, Dullemans AM, van den Heuvel JF, Maris PC and van der Vlugt RA (2007) Identification and characterisation of Tomato torrado virus, a new plant picorna-like virus from tomato. Archives of Virology 152: 881–890.
    Vigne E, Komar V and Fuchs M (2004) Field safety assessment of recombination in transgenic grapevines expressing the coat protein gene of Grapevine fanleaf virus. Transgenic Research 13: 165–179.
    Voinnet O, Pinto YM and Baulcombe DC (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proceedings of the National Academy of Sciences of the USA 96: 14147–14152.
    Wang A and Sanfacon H (2000) Proteolytic processing at a novel cleavage site in the N-terminal region of the Tomato ringspot nepovirus RNA-1-encoded polyprotein in vitro. Journal of General Virology 81: 2771–2781.
    Wellink J, van Bokhoven H, Le Gall O, Verver J and van Kammen A (1994) Replication and translation of cowpea mosaic virus RNAs are tightly linked. Archives of Virology. Supplementum 9: 381–392.
    Wellink J, van Lent JW, Verver J et al. (1993) The Cowpea mosaic virus M RNA-encoded 48-kilodalton protein is responsible for induction of tubular structures in protoplasts. Journal of Virology 67: 3660–3664.
    Wetzel T, Chisholm J, Bassler A and Sanfacon H (2008) Characterization of proteinase cleavage sites in the N-terminal region of the RNA1-encoded polyprotein from Arabis mosaic virus (subgroup A nepovirus). Virology 375: 159–169.
    Wieczorek A and Sanfacon H (1993) Characterization and subcellular localization of Tomato ringspot nepovirus putative movement protein. Virology 194: 734–742.
    Yaegashi H, Yamatsuta T, Takahashi T et al. (2007) Characterization of virus-induced gene silencing in tobacco plants infected with Apple latent spherical virus. Archives of Virology 152: 1839–1849.
    Zhang G and Sanfacon H (2006) Characterization of membrane-association domains within the Tomato ringspot nepovirus X2 protein, an endoplasmic reticulum-targeted polytopic membrane protein. Journal of Virology 80: 10847–10857.
    Zhang SC, Zhang G, Yang L, Chisholm J and Sanfacon H (2005) Evidence that insertion of Tomato ringspot nepovirus NTB-VPg protein in endoplasmic reticulum membranes is directed by two domains: a C-terminal transmembrane helix and an N-terminal amphipathic helix. Journal of Virology 79: 11752–11765.
 Further Reading
    Büchen-Osmond C (2003) The Universal Virus Database ICTVdB. Computing in Science and Engineering 5(3): 16–25 (database available at the following URL: http://phene.cpmc.columbia.edu/).
    book Fauquet CM, Mayo MA, Maniloff J, Desselberger U and Ball LA (eds) (2005) Virus Taxonomy, Eighth Report of the International Committee on the Taxonomy of Viruses (ICTV). [See in particular chapters on Sequiviridae (pp. 793–798), Sadwavirus (pp. 799–802), Cheravirus (pp. 803–805), Comoviridae (pp. 807–818). The updated Ninth Report of the ICTV is scheduled to be published in 2010. Recent updates to virus taxonomy can be found at the ICTV URL: http://www.ictvonline.org/index.asp?bhcp=1]. London: Elsevier/Academic Press.
    book 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 (2005) Replication of positive-strand RNA viruses in plants: contact points between plant and virus components. Canadian Journal of Botany 83: 1529–1549.
    book 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. III, 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.

Related Sub-Topics:

Viruses Infecting Plants | Plant Disease
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Secoviridae: The Amalgamation of the Families Sequiviridae and Comoviridae
 
How to Cite close
Sanfaçon, Hélène(Sep 2009) Secoviridae: The Amalgamation of the Families Sequiviridae and Comoviridae. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000764.pub2]