Soybean mosaic virus: a successful potyvirus with a wide distribution but restricted natural host range

Abstract

Taxonomy: Soybean mosaic virus (SMV) is a species within the genus Potyvirus, family Potyviridae, which includes almost one-quarter of all known plant RNA viruses affecting agriculturally important plants. The Potyvirus genus is the largest of all genera of plant RNA viruses with 160 species.

Particle: The filamentous particles of SMV, typical of potyviruses, are about 7500 Å long and 120 Å in diameter with a central hole of about 15 Å in diameter. Coat protein residues are arranged in helices of about 34 Å pitch having slightly less than nine subunits per turn.

Genome: The SMV genome consists of a single-stranded, positive-sense, polyadenylated RNA of approximately 9.6 kb with a virus-encoded protein (VPg) linked at the 5' terminus. The genomic RNA contains a single large open reading frame (ORF). The polypeptide produced from the large ORF is processed proteolytically by three viral-encoded proteinases to yield about 10 functional proteins. A small ORF, partially overlapping the P3 cistron, pipo, is encoded as a fusion protein in the N-terminus of P3 (P3N + PIPO).

Biological properties: SMV's host range is restricted mostly to two plant species of a single genus: Glycine max (cultivated soybean) and G. soja (wild soybean). SMV is transmitted by aphids non-persistently and by seeds. The variability of SMV is recognized by reactions on cultivars with dominant resistance (R) genes. Recessive resistance genes are not known.

Geographical distribution and economic importance: As a consequence of its seed transmissibility, SMV is present in all soybean-growing areas of the world. SMV infections can reduce significantly seed quantity and quality (e.g. mottled seed coats, reduced seed size and viability, and altered chemical composition).

Control: The most effective means of managing losses from SMV are the planting of virus-free seeds and cultivars containing single or multiple R genes.

Key attractions: The interactions of SMV with soybean genotypes containing different dominant R genes and an understanding of the functional role(s) of SMV-encoded proteins in virulence, transmission and pathogenicity have been investigated intensively. The SMV-soybean pathosystem has become an excellent model for the examination of the genetics and genomics of a uniquely complex gene-for-gene resistance model in a crop of worldwide importance.

Keywords: Potyviridae; R genes; RNA viruses; avirulence/virulence proteins; host responses; signalling; virus-host interactions.

Figure 1

Properties of the Soybean mosaic virus (SMV)–soybean pathosystem. (A) Typical symptoms induced by SMV in a susceptible soybean. (B) Negatively stained filamentous SMV particles of about 750 nm in length. (C) Alate Rhopalosiphum padi which transmits SMV non‐persistently. Rhopalosiphum padi is one of the most important aphid vectors of SMV in the Midwest of the USA. (D) Seed coat mottling of soybean seeds induced by SMV.

Figure 2

Genome organization of Soybean mosaic virus (SMV) illustrating the proteases responsible for cleaving (arrows) the polyprotein precursor to produce mature proteins shown as rectangular boxes. The functions attributed to the SMV encoded proteins are indicated for each cistron. Single amino acid changes in helper‐component proteinase (HC‐Pro) and coat protein (CP) associated with seed and aphid transmission of SMV are indicated parenthetically. CI, cytoplasmic inclusion; NIa, nuclear inclusion a; NIb, nuclear inclusion b; P1, P3, proteins 1 and 3; VPg, virus genome‐linked protein.

Figure 3

Phenotypes of Soybean mosaic virus (SMV) resistance in soybean isolines expressing resistant and susceptible alleles for each of the Rsv genes to inoculation with cDNA clones of avirulent SMV strains modified to express the uidA gene encoding the β‐glucuronidase reporter enzyme. Unifoliate leaves were biolistically inoculated and stained for β‐glucuronidase activity at 14 days post‐inoculation. Note the expression of extreme resistance by (A) the Rsv1 allele in L78–379 against SMV‐G2, (B) the Rsv3 allele in L29 against SMV‐G7, and (C) restriction in movement by the Rsv4 allele in V94–5152 against SMV‐G2.

Figure 4

Avirulence/virulence determinants of SMV shown on a schematic representation of the SMV genome on soybean genotypes containing (A, B) the entire Rsv1‐locus from PI96983, (C) two soybean recombinant inbred lines (RILs) that contained a recombination event within the Rsv1‐locus from PI96983 (Hayes et al., 2004), (D) the Rsv3‐locus in L29, and (E) the Rsv4‐locus in V94‐5152. The location of the mutation and the amino acid residues for each determinant is shown below the viral protein. Data are summarized from (A) (Eggenberger et al., 2008); (B) (Hajimorad et al., 2008, 2011; Wen et al., 2013); (C) (Hayes et al., 2004; Hajimorad et al., 2011; Wen et al., 2011, 2013); (D) (Seo et al., 2009a; Zhang et al., 2009); (E) (Ahangaran et al., 2013; Chowda‐Reddy et al., 2011a; Khatabi et al., 2012; Wang et al., 2015).

Figure 5

Proposed Rsv1 signalling pathway. (A) Example of Rsv1 loss of extreme resistance (ER) screening strategy via virus‐induced gene silencing (VIGS). Inoculation of soybean plants previously infected with a Bean pod mottle virus‐derived VIGS vector containing a fragment of the soybean homologue of PHYTOALEXIN DEFICIENT 4 (PAD4) (Glyma08g00420) suppressed ER and allowed the movement of SMV‐G2 expressing the uida gene out of the inoculation sites (detected by staining for the β‐glucuronidase reporter enzyme). (B) A proposed signalling pathway incorporating gene silencing results from Fu et al. (2009) and Zhang et al. (2012). VIGS suggests that the signalling proteins listed are necessary for Rsv1 resistance. The hierarchy of the signalling pathway is inferred from genetic studies of defence signalling genes in other plant species. EDR1, enhanced disease resistance 1; EDS1, enhanced disease susceptibility 1; HSP90, heat shock protein 90; JAR1, jasmonate resistant 1; NB‐LRR, nucleotide‐binding site leucine‐rich repeat; RAR1, required for Mla12 resistance 1; SGT1, suppressor of the G2 allele of skp1; SMV, Soybean mosaic virus; WRKY, WRKY transcription factor family member.