Pathogenetic roles of beet necrotic yellow vein virus RNA5 in the exacerbation of symptoms and yield reduction, development of scab‐like symptoms, and Rz1‐resistance breaking in sugar beet

Abstract

Beet necrotic yellow vein virus (BNYVV) generally has a four-segmented positivesense RNA genome (RNAs 1-4), but some European and most Asian strains have an additional segment, RNA5. This study examined the effect of RNA5 and RNA3 on different sugar beet cultivars using a Polymyxa-mediated inoculation system under field and laboratory conditions. In field tests, the degree of sugar yield served as an index for assessing the virulence of BNYVV strains. Japanese A-II type isolates without RNA5 caused mostly 15%-90% sugar yield reductions, depending on the susceptibility of sugar beet cultivars, whereas the isolates with RNA5 induced more than 90% yield losses in the seven susceptible cultivars, but small yield losses in one Rz1-resistant and Rizor cultivars. However, a laboratory-produced isolate containing RNA5 but lacking RNA3 caused higher yield losses in Rizor than in susceptible plants, and induced scab-like symptoms on the root surface of both susceptible and resistant plants. In laboratory tests, A-II type isolates without RNA5 had low viral RNA accumulation levels in roots of Rizor and Rz1-resistant plants at early stages of infection, but in the presence of RNA5, viral RNA3 accumulation levels increased remarkably. This increased RNA3 accumulation was not observed in roots of the WB42 accession with the Rz2 gene. In contrast, the presence of RNA3 did not affect RNA5 accumulation levels. Collectively, this study demonstrated that RNA5 is involved in the development of scab-like symptoms and the enhancement of RNA3 accumulation, and suggests these characteristics of RNA5 are associated with Rz1-resistance breaking.

Epidemic progress of beet necrotic yellow vein virus: Evidence from an investigation in Japan spanning half a century

“…It seems unlikely that original D, O, and T strains of BNYVV were directly involved in RB (such as seen in Europe and the United States) because they were already present before cultivating resistant cultivars. However, differences in virulence to Rz1-resistant sugar beet cultivars were previously shown among three strains (Chiba et al, 2011;Tamada et al, 2021). For example, in field tests, a T-type iso- variants were most commonly present, followed by P-type variants (p25, SYHG tetrad); mixed infections of these types were also found.…”

“…Taken together, it is clear that the BNYVV isolates with T-type p25 are more aggressive to resistant plants and susceptible plants than virus isolates with O-or D-subgroup p25, although the involvement of other genes such as those related to replication, movement, or cysteinerich protein in the virulence of the T-type strain cannot be ruled out.An additional important factor affecting the BNYVV epidemics and pathogenicity is the presence of the RNA5 segment. A previous study(Tamada et al, 2021) revealed that the presence of RNA5 remarkably increased viral RNA3 accumulation levels in rootlets of the Rz1-resistant plants, suggesting that RNA5-containing virus can overcome Rz1 resistance. Similarly, the French P-type virus (with RNA5), which contains P-subgroup p25(Chiba et al, 2011), can overcome Rz1 resistance in greenhouse conditions(Bornemann & Varrelmann, 2011;Chiba et al, 2011;Pferdmenges et al, 2009).Galein et al (2018) examined the variability and virulence of BNYVV in sugar beet plant fields in the Pithiviers area, France, with different resistant genotypes over a 4-year period, where P-type p25, A-type p25 (Italy subgroup) and B-type p25 (Germany subgroup) strains were present.…”

“…RB variants are thought to be generated by single or multiple amino acid changes in the p25 protein of BNYVV, encoded by p25 on RNA3 (Acosta-Leal et al, 2008;Chiba et al, 2008Chiba et al, , 2011Schirmer et al, 2005); for example, a single amino acid change from alanine to valine at position 67 in the p25 protein was shown to be sufficient to produce a strain of BNYVV capable of defeating the Rz1 resistance gene (Chiba et al, 2011;Koenig et al, 2009). Furthermore, it has been proven that some RNA5 (carrying the p26 gene)-containing BNYVV isolates can also overcome Rz1 resistance in sugar beet plants (Chiba et al, 2011;Galein et al, 2018;Pferdmenges et al, 2009;Tamada et al, 2021).…”

“…late (H45) caused more severe yield losses in the Rizor-resistant plants as well as susceptible plants compared with D-or O-type isolates (K80 or M87)(Tamada et al, 2021). In laboratory tests, Ttype isolate (T41) showed higher levels of viral RNA3 accumulation in Rz1-resistant plants than O-or D-type isolates (O11 or D104)(Chiba et al, 2008;Tamada et al, 2021). Moreover, the results of competition experiments using P. betae cultures carrying mixtures of three strain isolates showed that T-subgroup p25 (90%) dominated over O-subgroup p25 (5%) and D-subgroup p25 (5%) in Rz1-resistant plants (n = 20) (table 4 inChiba et al, 2011).…”

Pest categorisation of beet necrotic yellow vein virus

“…Early infections result in more severe losses, while late‐season infections may not result in visible root symptoms but still cause significant reductions in sucrose content (Neher and Gallian, 2014). In addition, RNA‐5‐containing isolates may cause more severe symptoms (scab‐like symptoms on the surface of taproots) leading to more than 90% sugar yield reduction in susceptible cultivars and about 17%–59% reduction in resistant cultivars (Tamada et al., 2020). In red table beet ( B. vulgaris subsp.…”