Solemoviridae

Solemoviridae

Merike Sõmera, Denis Fargette, Eugénie Hébrard and Cecilia Sarmiento

The citation for this ICTV Report chapter is the summary shortly to be published as Sõmera et al,. 2021
ICTV Virus Taxonomy Profile: Solemoviridae, Journal of General Virology 

Corresponding author: Merike Sõmera (merike.somera@taltech.ee)
Edited by: F. Murilo Zerbini and Sead Sabanadzovic
Posted: January 2021

Summary

Plant viruses in the family Solemoviridae have stable icosahedral particles (26–34 nm in diameter) assembled on T=3 symmetry and a relatively small (4–4.6 kb) positive-sense, single-stranded, monopartite RNA genome with 4–5 open reading frames (ORFs). These ORFs express a viral suppressor of RNA silencing, a polyprotein and a capsid protein. The polyprotein contains domains of the membrane anchor, a serine protease, a genome-linked viral protein (VPg) and C-terminal protein(s) or an RNA-directed RNA polymerase (RdRP), expressed by means of ribosomal frameshifting. These two variants of the polyprotein are translated via a ribosomal leaky scanning mechanism from genomic RNA and they undergo proteolytic processing at conserved cleavage sites between the domains. The capsid protein (CP) is translated from a subgenomic RNA. Genomic or subgenomic RNAs have a VPg covalently attached to the 5′-terminus and no poly(A) tract at the 3′-terminus. Replication is presumably cytoplasmic. Several sobemoviruses support replication and encapsidation of small circular satellite RNAs. The natural host range is relatively narrow for each virus. Transmission occurs via mechanical wounding, by vegetative propagation or abiotically through soil. Insects (beetles, aphids, thrips, hoppers, mirid bugs, moths) can also be vectors. Viruses infecting legumes or plants from the family Chenopodiaceae may be seed-transmissible. Members of the family are classified into two genera: Sobemovirus and Polemovirus.

Table 1.Solemoviridae. Characteristics of members of the family Solemoviridae

Characteristic

Description

Typical member

southern bean mosaic virus (DQ875594), species Southern bean mosaic virus, genus Sobemovirus

Virion

Non-enveloped icosahedral particles with T=3 icosahedral symmetry, 26–34 nm in diameter, comprised of 180 molecules of capsid protein

Genome

4–4.6 kb positive–sense, non-segmented RNA, with 5′-terminal VPg, no poly(A) tail

Replication

Cytoplasmic

Translation

Directly from genomic RNA by leaky scanning, −1 ribosomal frameshifting, polyprotein proteolytic processing; capsid protein translated from subgenomic RNA

Host range

Different botanical groups of flowering plants; host range of each virus is relatively narrow. Transmitted mechanically and/or by various insect vectors; a few solemoviruses are transmitted via seeds or soil

Taxonomy

Realm Riboviria, kingdom Orthornavirae, phylum Pisuviricota, class Pisoniviricetes, order Sobelivirales; two genera including ca. 20 species

Virion

Morphology

Icosahedral virions are 26–34 nm in diameter assembled on a T=3 lattice symmetry, without a lipid envelope. Detailed virion structures have been determined for several sobemoviruses but not for poinsettia latent virus (PnLV), the only known polemovirus. The PnLV virion with 34 nm in diameter is slightly larger than that of sobemoviruses, whose virions are about 26–32 nm in diameter. The overall structure and particle stabilization of PnLV is expected to be similar (Aus dem Siepen et al., 2005). The primary amino acid sequence of PnLV has 17–30% identity with sobemovirus CPs, equivalent to the identities between sobemovirus CPs. Sobemovirus icosahedral virions are comprised of 180 monomers of viral CP on a T=3 lattice symmetry. The 3D structures of different sobemovirus virions are nearly identical - their superimposed backbone C-α atoms show root mean square deviations of 1.4–1.9 Å (Plevka et al., 2007). CP monomers are chemically identical but can adopt three conformations designated as A, B and C subunits. The A subunits form 12 pentamers at 5-fold axes, whereas three of each B and C subunits assemble into 20 hexamers at 3-fold axes (Figure 1.Solemoviridae) (Opalka et al., 2000). The assembly of the T=3 capsid of sobemoviruses is controlled by the N-termini (known as random domain) of C subunits, which are partly ordered and inserted between the interacting sides of the subunits. The N-terminal arms of A and B subunits are completely disordered. The C-terminal shell domain forms a canonical single jellyroll β-sandwich fold (Rossmann et al., 1983). Upon infection, a co-translational genome release happens by opening of the capsid at the tips of pentamers, whereas translation does not need complete disassembly of virions (Shields et al., 1989, Zink and Grubmüller 2010).

Figure 1.Solemoviridae. Three-dimensional cryo-electron reconstruction of the particle of rice yellow mottle virus at 2.8 Å resolution. The capsid comprises 180 copies of a single capsid protein arranged in T=3 quasi-equivalent symmetry. The icosahedral asymmetric unit contains three subunits: A (in green), B (in brown), and C (in blue). Image from the RCSB PDB (rcsb.org) of PDB ID 1F2N (Opalka et al., 2000).

Nucleic acid

The genome comprises a polycistronic, positive-sense, single-stranded RNA molecule of 4–4.6 kb. The 3′-terminus is non-polyadenylated but has a stable stem-loop or tRNA-like structure (Aus dem Siepen et al., 2005, Sõmera et al., 2015). Several sobemoviruses encapsidate a small circular viroid-like satellite RNA (220–390 nt) (Sehgal et al., 1993).

Proteins

The capsid is comprised of 180 monomers of a single jellyroll capsid protein (CP) of about 26–33 kDa (Aus dem Siepen et al., 2005, Opalka et al., 2000). Identity between primary sequences of CPs reaches up to 80% for very closely related viruses whereas the other solemovirus CPs show identity from 12 to 30%. Virus particle formation is important for vector transmission (Musser et al., 2002), xylem transportation (Opalka et al., 1998) and stability in the environment (Rossmann et al., 1983).

VPg is covalently attached to the 5′-terminus of viral RNA and interacts with the translation initiation complex (Hébrard et al., 2010, Olspert et al., 2011a, Olspert et al., 2011b). In addition, sobemovirus VPg interacts with viral suppressor of RNA silencing and it regulates the activity of viral protease and viral RdRP (Roy Chowdhury and Savithri 2011, Nair et al., 2008, Govind et al., 2012). Multiple functions are supported by its intrinsically disordered nature with the propensity to form more rigid structures upon stabilization (Satheshkumar et al., 2005, Hébrard et al., 2009).

Lipids

None reported.

Carbohydrates

None reported.

Genome organization and replication

The genome organization is conserved, with 4–5 ORFs (Figure 2.Solemoviridae). An additional small non–conserved ORFx has been predicted in several sobemovirus genomes (Ling et al., 2013). Sequence homology searching indicates that the genome of polemovirus PnLV originated from a recombination event between a polerovirus (family Luteoviridae) and a sobemovirus. The PnLV genome shares a close genetic relationship with poleroviruses within the first three-quarters of its genome but to sobemoviruses in the last quarter (Aus dem Siepen et al., 2005). Despite their different evolutionary origins, sobemoviruses and polemoviruses have many genetic features in common. For both groups of viruses the capsid protein is translated from a subgenomic RNA (Sõmera et al., 2015), and a ribosomal leaky scanning strategy is used to express proteins from genomic RNA, these being a putative RNA silencing suppressor from the 5′-proximal ORF and two polyproteins from the next ORFs. These polyproteins contain a common N-terminal part with the motifs characteristic of a membrane-anchoring domain, a serine protease and a VPg. The non-conserved proteins P10 and P8 are translated as the C-terminal domain of the shorter polyprotein. The longer polyprotein whose C-terminal part consists of an RNA-directed RNA polymerase (RdRP) is translated via −1 programmed ribosomal frameshift (−1PRF) following the VPg domain (Sõmera et al., 2015). The −1 PRF signal of sobemoviruses consists of a slippery sequence 5′-UUUAAAC-3′ followed by a stem–loop structure, whereas the polemovirus frameshifting signal consists of the slippery sequence 5′-GGGAAAC-3′ followed by a putative small pseudoknot (Aus dem Siepen et al., 2005, Tamm et al., 2009). Both versions of sobemoviral polyproteins are cleaved to different functional intermediates or definite subunits by the viral protease at E/S, E/T or E/N sites, there being up to four cleavage sites in the shorter polyprotein and up to three cleavage sites in the longer polyprotein (Mäkinen et al., 2000, Nair and Savithri 2010). The processing mechanism of PnLV polyprotein remains to be elucidated, but is possibly cleaved at the sites residing in the domain of viral serine protease as shown for poleroviruses (Rodamilans et al., 2018).

Figure 2.Solemoviridae. Genome organization of southern bean mosaic virus and poinsettia latent virus, representative members of the genera Sobemovirus and Polemovirus, respectively. Red bullets indicate the genome linked viral protein (VPg). Numbers indicate nucleotide positions of encoding ORFs. Solemoviruses express an RNA silencing suppressor and two versions of a polyprotein having different C-termini (from genomic RNA); a capsid protein is expressed from subgenomic RNA. The polyproteins undergo autoproteolytic processing to functional intermediates or subunits. Synthesis of RNA-directed RNA polymerase relies on −1 ribosomal frameshifting (indicated by dashed lines). An additional ORF encoding unknown protein x has been predicted in several sobemovirus genomes.

Replication occurs after synthesis of RdRP. A conserved 5′-end sequence 5′-ACAA(AA)-3′ and the 3′-end stem-loop or tRNA-like structure are considered to be essential for template recognition (Aus dem Siepen et al., 2005, Sõmera et al., 2015). Primer-independent replication has been demonstrated for Sesbania mosaic virus (Govind and Savithri 2010). Several sobemoviruses support replication and encapsidation of small circular satellite RNAs (Symons and Randles 1999).

Biology

Solemoviruses infect flowering plants from different botanical families, including both dicots and monocots. However, the natural host range of each solemovirus is narrow except that sowbane mosaic virus can infect plants from several different orders (Sõmera et al., 2015).

Sobemoviruses are readily transmitted mechanically and many are also transmitted by insects such as beetles, aphids, hoppers and mirid bugs, probably, this representing non–specific mechanical transmission by their mouthparts, although abiotic transmission has also been demonstrated (Sõmera et al., 2015). The polemovirus PnLV is transmitted via grafting and vegetative propagation, although virus infections in virus-free plants grown under quarantine conditions suggests that soil and water transmission may also occur (Aus dem Siepen et al., 2005). Abiotic transmission through soil or water is also highly likely for several sobemoviruses. Viruses that infect plants belonging to the families Fabaceae or Chenopodiaceae can be seed-transmissible (Sõmera et al., 2015). Solemovirus infections range from symptomless to severe diseases (Aus dem Siepen et al., 2005, Sõmera et al., 2015, Trovão et al., 2015, Nascimento et al., 2010). Infection symptoms are described as mosaic and mottling in infected leaves, necrotic lesions, vein clearing, stunting and sometimes sterility. Sobemoviruses colonize leaf parenchymal tissues as well as the vascular tissues of leaves, stems and roots. Their particles have different preferences for vascular movement pathways: several of them move using the xylem whereas others spread through the phloem (Opalka et al., 1998, Otsus et al., 2012). In infected cells, virions are found in both cytoplasm and nuclei. Progression of infection leads to appearance of large crystalline aggregates and inclusions in the cytoplasm and the vacuoles. Changes in chloroplast structure have been reported for several solemovirus infections. 

Antigenicity

Virions and purified CPs are strongly immunogenic. Distant serological relationships exist between the CPs of some viruses belonging to the genus Sobemovirus. Serotypes with different geographical origin have been identified for some viruses. 

Derivation of names

Polemovirus: from genera Polerovirus and Sobemovirus to indicate the chimeric nature of the virus genome.

Sobemovirus: from the type species Southern bean mosaic virus.

Solemoviridae: from genera Sobemovirus and Polemovirus to indicate their close phylogenetic nature.

Genus demarcation criteria

The genera in the family Solemoviridae are differentiated by phylogenies of individual ORFs or proteins. Structural comparisons of encoded proteins or virions may help to resolve phylogenetic relationships.

Relationships within the family

Phylogenetic analysis of CP sequences reveals that solemoviruses cluster (Figure 3B.Solemoviridae). However, analysis of RdRP sequences (Figure 3A.Solemoviridae) reveals that PnLV clusters with potato leafroll virus, a polerovirus belonging to the family Luteoviridae.

Figure 3A.Solemoviridae. Maximum likelihood phylogenetic tree constructed using the amino acid sequences of RNA-directed RNA polymerase domains (starting at a −1 ribosomal frameshifting site). Phylogenetic analysis based on a MUSCLE multiple sequence alignment was performed using the LG amino acid substitution model using Seaview 5.0.4 (http://doua.prabi.fr/software/seaview). Sequences were translated from the complete genomes of the same isolate. The proportion of branches found in bootstrap replicates is indicated where this was > 70%. Coloured dots group members of a genus, with an unclassified virus marked with an open circle. Potato leafroll virus (genus Polerovirus, family Luteoviridae) was used as an outgroup. This phylogenetic tree and the corresponding sequence alignment are available for download from the Resources page

Figure 3B.Solemoviridae. Maximum likelihood phylogenetic tree constructed using the amino acid sequences of capsid proteins. Phylogenetic analysis based on a MUSCLE multiple sequence alignment was performed using the WAG amino acid substitution model using Seaview 5.0.4 (http://doua.prabi.fr/software/seaview). Sequences were translated from the complete genomes of the same isolate. The proportion of branches found in bootstrap replicates is indicated where this was > 70%. Coloured dots group members of a genus, with an unclassified virus marked with an open circle. Potato leafroll virus (genus Polerovirus, family Luteoviridae) was used as an outgroup. The phylogenetic tree and the corresponding sequence alignment are available for download from the Resources page

Relationships with other taxa

The modules in the genome of solemoviruses encoding Pro–VPg–RdRP or CP share sequence homology with the gene modules belonging to viruses of different taxa.

The RdRPs of viruses from family Solemoviridae share the closest phylogenetic relationships with the RdRPs of viruses belonging to the families Alvernaviridae and Barnaviridae in the order Sobelivirales but also with the RdRPs of poleroviruses and enamoviruses from the family Luteoviridae in the order Tolivirales (Wolf et al., 2018). All these viruses are assumed to encode their picornavirus-like RdRP as part of a long polyprotein produced via −1 programmed frameshift mechanism downstream of serine protease and VPg domains (except Heterocapsa circularisquama RNA virus 01 belonging to the family Alvernaviridae for which the polyprotein is a product of translation from a single frame). Although less conserved, the serine protease sequences of these viruses are phylogenetically related to each other. Their VPg sequences are not well conserved but the position of VPg between viral protease and RdRP domains is unique among the phylogenetically related sobemoviruses, polemoviruses, poleroviruses, enamoviruses and barnaviruses (Sõmera et al., 2015). Within the family Solemoviridae, the polyprotein Pro–VPg–RdRP of the polemovirus PnLV shows higher sequence identity with that of poleroviruses than to sobemovirus polyproteins. Also, the product of PnLV 5′-proximal ORF, a putative RNA silencing suppressor, shares homology with the respective proteins of poleroviruses (Aus dem Siepen et al., 2005). The RNA silencing suppressors encoded by the 5′-proximal ORF of sobemoviruses are not conserved and share no significant homology with any other known proteins although they all present two couples of short zinc-finger motifs (Sõmera et al., 2015).

As the CP of the polemovirus PnLV is most closely related with sobemovirus CPs, PnLV is considered as a natural polerovirus–sobemovirus recombinant (Aus dem Siepen et al., 2005). The CPs of solemoviruses are most closely related to the CPs of necroviruses belonging to the family Tombusviridae in the order Tolivirales (Plevka et al., 2007).

Related, unclassified viruses 

Virus name

Accession number

Virus abbreviation

Hubei sclerotinia RNA virus 1

MK889164

HuSRV1

 Member taxa