Wheat streak mosaic virus: a century old virus with rising importance worldwide

Abstract

Wheat streak mosaic virus (WSMV) causes wheat streak mosaic, a disease of cereals and grasses that threatens wheat production worldwide. It is a monopartite, positive-sense, single-stranded RNA virus and the type member of the genus Tritimovirus in the family Potyviridae. The only known vector is the wheat curl mite (WCM, Aceria tosichella), recently identified as a species complex of biotypes differing in virus transmission. Low rates of seed transmission have been reported. Infected plants are stunted and have a yellow mosaic of parallel discontinuous streaks on the leaves. In the autumn, WCMs move from WSMV-infected volunteer wheat and other grass hosts to newly emerged wheat and transmit the virus which survives the winter within the plant, and the mites survive as eggs, larvae, nymphs or adults in the crown and leaf sheaths. In the spring/summer, the mites move from the maturing wheat crop to volunteer wheat and other grass hosts and transmit WSMV, and onto newly emerged wheat in the fall to which they transmit the virus, completing the disease cycle. WSMV detection is by enzyme-linked immunosorbent assay (ELISA), reverse transcription-polymerase chain reaction (RT-PCR) or quantitative RT-PCR (RT-qPCR). Three types of WSMV are recognized: A (Mexico), B (Europe, Russia, Asia) and D (USA, Argentina, Brazil, Australia, Turkey, Canada). Resistance genes Wsm1, Wsm2 and Wsm3 have been identified. The most effective, Wsm2, has been introduced into several wheat cultivars. Mitigation of losses caused by WSMV will require enhanced knowledge of the biology of WCM biotypes and WSMV, new or improved virus detection techniques, the development of resistance through traditional and molecular breeding, and the adaptation of cultural management tactics to account for climate change.

Keywords: Aceria tosichella; Tritimovirus; WSMV; cereal crops; wheat curl mite.

Figure 1

Genome architecture of Wheat streak mosaic virus (WSMV). The genome size of WSMV is 9.3–9.4 kb and has a single open reading frame, which is transcribed into a large polyprotein. This polyprotein is composed of 10 proteins: P1 (P1 protein: 40 kDa); HC‐Pro (helper component protease: 44 kDa); P3 (P3 protein: 32 kDa); 6K1 and 6K2 (6 kDa protein); CI (cytoplasmic inclusion protein: 73 kDa); VPg (viral protein genome‐linked proteinase: 23 kDa); NIa (nuclear Inclusion putative protease: 26 kDa); NIb (Nuclear Inclusion putative polymerase: 57 kDa) CP (coat protein: 37 kDa). nt, nucleotides; UTR, untranslated region.

Figure 2

Scanning electron microscopy (SEM) image of wheat curl mite (Aceria tosichella) specimens on a wheat leaf.

Figure 3

Wheat streak mosaic virus (WSMV) disease symptoms on hosts. (A) WSMV‐infected wheat cv. Cubus showing advanced symptoms with linear streaks coalescing into almost solid yellow areas. (B) WSMV‐infected wheat cv. Vlada mechanically inoculated with WSMV isolate (CZlab, accession no. FJ216408). (C) A section of a wheat field affected by a severe epidemic of wheat streak mosaic in western Nebraska, USA in May 2017. Note the intense yellowing and stunting of the wheat crop.

Figure 4

The life cycle of Wheat streak mosaic virus (WSMV).

Figure 5

Genetic diversity of various types of Wheat streak mosaic virus (WSMV). (A) Based on the whole genome of WSMV. (B) Based on the coat protein gene sequence of WSMV. An isolate from Mexico (El‐Batán) represents clade A; isolates from Europe represent clade B and include an Asian isolate from Iran (Saadat‐shahr); WSMV grass isolates from the Czech Republic are classified into type B1; an isolate from Iran (AF454458) represents clade C; isolates from the USA, Argentina, Turkey and Australia represent clade D. Oat necrotic mottle virus (ONMV) (AY377938_ONMV) was used as an outgroup. For the generation of the tree, nucleotide sequences were aligned using ClustalX2 (Larkin et al., 2007) and the tree was constructed using MEGA 7 (Kumar et al., 2016) as described previously (Singh et al., 2018). The tree was viewed using ITOL (https://itol.embl.de/). The neighbour‐joining method was used for the construction of the tree and the reliability of the branches was inferred from a bootstrap analysis of 1000 replicates. The dataset supporting the results for the study has been submitted to the TreeBASE repository (http://treebase.org/treebase-web/home.html) and is publicly accessible at http://purl.org/phylo/treebase/phylows/study/TB2:S22140. (C, D) Recombinant analysis of WSMV based on the full genome and coat protein nucleotide sequences. Analyses were performed using various algorithms included in the RDP software package (Martin et al., 2015) as described previously (Singh and Kundu, 2017). The type strain AF285169_PV57 (USA) was used as a reference. The order of the designation of the recombination events is as follows: accession number, algorithm used (R, RDP; G, GENECONV; C, Chimaera; MaxChi; B, Bootscan; SS, SiScan; 3seq; LARD), P‐value and nucleotide position. Only recombination events with P < 0.05 detected by at least three different algorithms are shown. Numbers of events with P > 0.05 are given in parentheses. Recombination events were observed in five algorithms: RDP, GENECONV, Bootscan, Chimaera and SiScan. Algorithms MaxChi, 3seq and LARD did not detect significant recombination events.