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Massimo Turina, Brad I Hillman, Keramat Izadpanah, Mina Rastgou and Cristina Rosa
A summary of this ICTV Report chapter has been published as an ICTV Virus Taxonomy Profile article in the Journal of General Virology, and should be cited when referencing this online chapter as follows:
Turina, M., Hillman, B.I., Izadpanah, K., Rastgou, M., Rosa, C. and ICTV Report Consortium. 2017, ICTV Virus Taxonomy Profile: Ourmiavirus, Journal of General Virology, 98:129–130.
Members of the genus Ourmiavirus are plant viruses with non-enveloped bacilliform virions composed of a single coat protein. The genome consists of three positive sense ssRNAs, each encoding a single protein. The virions possess a unique structure with a series of discrete lengths from 30 to 62 nm. The RNA dependent RNA polymerase (RdRp) has closest similarity to that of recently discovered invertebrate viruses related to viruses of the family Narnaviridae; the movement protein (MP) is similar to the MPs of tombusviruses; the coat protein (CP) shows limited similarity to the CPs of several plant and animal viruses. This combination of characters is not found in any other virus taxon.
Table 1.Ourmiavirus. Characteristics of Ourmiavirus
Ourmia melon virus VE9 (RNA1: EU770623; RNA2:EU770624; RNA3: EU770625), species Ourmia melon virus, genus Ourmiavirus
Bacilliform (18 nm×30–62 nm); A single coat protein of 23.8 kDa
Tri-segmented positive-strand RNA virus (2.8; 1.1; 0.97 kb respectively)
Cytoplasmic; possible nucleolar localization of the coat protein; virion assembly coupled to active replication
From genomic uncapped RNA; each genomic segment is monocistronic.
Unassigned genus; RdRp has similarities to recently discovered, unclassified invertebrate viruses related to members of the Narnaviridae
The bacilliform virions of Ourmiaviruses constitute a series of particles with conical ends (apparently hemi-icosahedra) and cylindrical bodies 18 nm in diameter. The bodies of the particles are composed of a series of double disks, the most common particle having two disks (particle length 30 nm), a second common particle having three disks (particle length 37 nm) with rarer particles having four disks (particle length 45.5 nm) and six disks (particle length 62 nm). There is no envelope. (Figure 1.Ourmiavirus and Figure 2.Ourmiavirus).
Figure 1.Ourmiavirus. Diagram of virion surface of a member of the genus Ourmiavirus, showing arrangement of double disks and conical ends in particles of different length. Each row of five triangles represents a double disk.
Figure 2.Ourmiavirus. Virion morphology: (A, B, C) Negative contrast electron micrographs (uranyl acetate) of purified particles of Ourmia melon virus. The bar represents 100 nm. (D, E) Features of the two commonest particle types, enhanced by photographic superimposition.
The Mr of virions and their sedimentation coefficients are not known. The buoyant density in CsCl of all particle sizes is 1.375 g cm−3. The particles are stable at pH 7. Thermally, Ourmiaviruses are relatively stable; infectivity is retained in crude sap after heating for 10 min at 70 °C but not 80 °C, and is retained after at least one freeze–thaw cycle. The particles are stable after CsCl density gradient centrifugation, treatment with Triton X-100, and treatment with chloroform but not n-butanol.
The genome is comprised of three positive sense ssRNAs. In Ourmia melon virus (OuMV), the three RNAs are 2814, 1064 and 974 nt in length. The genomic segments of the other members of the genus are similar in size (Rastgou et al., 2009).
The single structural protein (CP) of Ourmia melon virus is 23.8 kDa and is encoded by RNA3; the two non-structural proteins are the RdRp (97.5 kDa, encoded by RNA1) and the MP (31.6 kDa, encoded by RNA2). The sizes of the predicted proteins are similar for members of the other two species (Rastgou et al., 2009), Epirus cherry virus and Cassava virus C.
Each genomic RNA has one ORF (Figure 3.Ourmiavirus). RNA1 encodes a protein carrying the GDD motif typical of RdRps. There is evidence that RNA2 encodes the cell-to-cell movement protein (Crivelli et al., 2011). The product of RNA3 is the CP. A protein fusion of the CP to GFP localizes specifically to the nucleolus (Rossi et al., 2014) but there is no direct evidence of the CP in the nucleus during infection (Rossi et al., 2015). Synthesis of CP from actively replicating RNA3 is necessary for both virion assembly and systemic infection of the host (Crivelli et al., 2011). There is no evidence for the presence of subgenomic RNAs or the production of additional proteins by ribosomal read through or frameshifting. The MP may undergo post-translational modification. Alanine scanning mutagenesis of conserved residues in the MP showed their importance in determining symptoms, movement, and formation of tubular structures that may play a role in cell-to-cell movement (Margaria et al., 2016). Details of replication are not known except that CP interferes with the plant silencing defense only in the context of virus infection (Rossi et al., 2015).
Figure 3.Ourmiavirus. Diagram of the genome organization of Ourmia melon virus isolate VE9 showing the size of each RNA and the positions and sizes of the ORFs. CP, coat protein; MP, movement protein; RdRp, RNA-dependent RNA polymerase.
The virions of Ourmia melon virus (i.e. the assembled coat protein) are good immunogens, as are the tubular structures associated with the MP. Antisera to these proteins do not react in Western blots to proteins in extracts of plants infected with members of either of the other two virus species in the genus.
Ourmia melon virus can easily be mechanically transmitted to a wide range of dicot plants (about 40 species in 15 families have been reported), usually inducing systemic ringspots, mosaic and necrosis, with local lesions on some hosts. Tissue tropism is controlled by the KR-rich region at the amino terminus of the CP (Rossi et al., 2015). No vector has been identified but several species of weeds around infected fields are commonly infected, suggesting horizontal transmission of the virus. However, no experimental transmission has been obtained with several aphid species, the whiteflies Trialeurodes vaporariorum and Bemisia tabaci or the mite Tetranychus urticae. Attempts at transmission through soil or irrigation water were unsuccessful. Experimental seed-transmission rates are 1–2% in Nicotiana benthamiana and N. megalosiphon. Members of different species in the genus occur in geographically diverse areas and on widely different hosts, though there are experimental hosts in common.
Ourmia: from Ourmia (Urmia, Orumieh) in north-western Iran where the Ourmia melon virus was first found. (Lisa et al., 1988)
Epirus: from Epirus, Greece, where Epirus cherry virus was isolated. (Avgelis et al., 1989)
Cassava: cassava virus C has been isolated from cassava in various parts of Africa. (Aiton et al., 1988)
Viruses of the genus Ourmiavirus are exceptional, having particles of unique morphology and a unique combination of phylogenetic affinities for the three different genomic RNAs. A recent study that characterized the virome of 220 species of invertebrates has unveiled a relationship of the RdRp of Ourmiaviruses with a new clade of Ourmia-like viruses found in samples from subphylum Chelicerata and Crustacea and superphylum Lophotrochozoa (Figure 4.Ourmiavirus) (Shi et al., 2016). Fungal Ourmia-like viruses are present in a separate clade (Figure 4.Ourmiavirus). Thus, the RdRp encoded by RNA1 has affinity with the RdRp of a number of viruses from the Narnaviridae family, but is distinct from yeast viruses in the genus Narnavirus (Figure 4.Ourmiavirus). The occurrence of such a well-defined clade related to Narnaviridae could be the basis for future establishment of a new virus family, the “Ourmiaviridae”: the family would comprise a genus for Ourmia-like viruses isolated from invertebrates, a genus for Ourmia-like mycoviruses, and plant viruses from the genus Ourmiavirus (Figure 4.Ourmiavirus). The MP encoded by RNA2 has clear similarities with the MPs of viruses in the family Tombusviridae (Rastgou et al., 2009). The CP shows distant affinities with the CPs of sobemo-, tombus- and luteoviruses (plant viruses) and nodaviruses (animal viruses) (Rastgou et al., 2009).
Figure 4.Ourmiavirus. Phylogenetic analysis of RdRp of Ourmiaviruses and related viruses. Amino acid sequences were aligned with Clustal and used to produce a phylogenetic tree using the Maximum Likelihood method and the LG (G+I) protein substitution model. Bootstrap values are indicated on branches supported in >70% of replicates. The tree is midpoint rooted. The tree topology shows a new clade of Ourmia-like viruses found in samples from subphylum Chelicerata and Crustacea and superphylum Lophotrochozoa. This phylogenetic tree and corresponding sequence alignment are available to download from the Resources page.
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