1887

Abstract

The A-type of beet necrotic yellow vein virus (BNYVV) is widely distributed in Europe and is one of the major virus types causing rhizomania disease in sugar beet. The closely related P-type is mainly limited to a small region in France (Pithiviers). Both virus types possess four RNAs (RNA1–4), but the P-type harbours an additional fifth RNA species (RNA5). The P-type is associated with stronger disease symptoms and resistance-breaking of , one of the two resistance genes which are used to control BNYVV infection. These characteristics are presumably due to the presence of RNA5, but experimental evidence for this is lacking. We generated the first infectious cDNA clone of BNYVV P-type to study its pathogenicity in sugar beet in comparison to a previously developed A-type clone. Using this tool, we confirmed the pathogenicity of the P-type clone in the experimental host and two species, and . Independent of RNA5 both the A- and the P-type accumulated in lateral roots and reduced the taproot weight of a susceptible sugar beet genotype to a similar extent. In contrast, only the P-type clone was able to accumulate a virus titre in an -resistant variety whereas the A-type clone failed to infect this variety. The efficiency of the P-type to overcome resistance was strongly associated with the presence of RNA5. Only a double resistant variety, harbouring and prevented an infection with the P-type. Reassortment experiments between the P- and A-type clones demonstrated that both virus types can exchange whole RNA components without losing the ability to replicate and to move systemically in sugar beet. Although our study highlights the close evolutionary relationship between the two virus types, we were able to demonstrate distinct pathogenicity properties that are attributed to the presence of RNA5 in the P-type.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001777
2022-08-10
2024-05-12
Loading full text...

Full text loading...

References

  1. Tamada T, Abe H. Evidence that beet necrotic yellow vein virus RNA-4 is essential for efficient transmission by the fungus polymyxa betae. J Gen Virol 1989; 70:3391–3398 [View Article]
    [Google Scholar]
  2. Tamada T, Shirako Y, Abe H, Saito M, Kiguchi T et al. Production and pathogenicity of isolates of beet necrotic yellow vein virus with different numbers of RNA components. J Gen Virol 1989; 70:3399–3409 [View Article]
    [Google Scholar]
  3. Gilmer D, Ratti C, Ictv RC. ICTV Virus Taxonomy Profile: Benyviridae. J Gen Virol 2017; 98:1571–1572 [View Article]
    [Google Scholar]
  4. Tamada T, Kondo H. Biological and genetic diversity of plasmodiophorid-transmitted viruses and their vectors. J Gen Plant Pathol 2013; 79:307–320 [View Article]
    [Google Scholar]
  5. Bouzoubaa S, Quillet L, Guilley H, Jonard G, Richards K. Nucleotide sequence of beet necrotic yellow vein virus RNA-1. J Gen Virol 1987; 68:615–626 [View Article]
    [Google Scholar]
  6. Richards KE, Tamada T. Mapping functions on the multipartite genome of beet necrotic yellow vein virus. Annu Rev Phytopathol 1992; 30:291–313 [View Article]
    [Google Scholar]
  7. Tamada T, Kusume T. Evidence that the 75K readthrough protein of beet necrotic yellow vein virus RNA-2 is essential for transmission by the fungus Polymyxa betae. J Gen Virol 1991; 72:1497–1504 [View Article] [PubMed]
    [Google Scholar]
  8. Chiba S, Hleibieh K, Delbianco A, Klein E, Ratti C et al. The benyvirus RNA silencing suppressor is essential for long-distance movement, requires both zinc-finger and NoLS basic residues but not a nucleolar localization for its silencing-suppression activity. Mol Plant Microbe Interact 2013; 26:168–181 [View Article] [PubMed]
    [Google Scholar]
  9. Lauber E, Guilley H, Tamada T, Richards KE, Jonard G. Vascular movement of beet necrotic yellow vein virus in Beta macrocarpa is probably dependent on an RNA 3 sequence domain rather than a gene product. J Gen Virol 1998; 79:385–393 [View Article] [PubMed]
    [Google Scholar]
  10. Koenig R, Jarausch W, Li Y, Commandeur U, Burgermeister W et al. Effect of recombinant beet necrotic yellow vein virus with different RNA compositions on mechanically inoculated sugarbeets. J Gen Virol 1991; 72:2243–2246 [View Article] [PubMed]
    [Google Scholar]
  11. Flobinus A, Chevigny N, Charley PA, Seissler T, Klein E et al. Beet necrotic yellow vein virus noncoding RNA production depends on a 5’→3’ Xrn exoribonuclease activity. Viruses 2018; 10:E137 [View Article] [PubMed]
    [Google Scholar]
  12. Wu W-Q, Fan H-Y, Jiang N, Wang Y, Zhang Z-Y et al. Infection of Beet necrotic yellow vein virus with RNA4-encoded P31 specifically up-regulates pathogenesis-related protein 10 in Nicotiana benthamiana. Virol J 2014; 11:118 [View Article] [PubMed]
    [Google Scholar]
  13. Rahim MD, Andika IB, Han C, Kondo H, Tamada T. RNA4-encoded p31 of beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. J Gen Virol 2007; 88:1611–1619 [View Article] [PubMed]
    [Google Scholar]
  14. Koenig R, Haeberlé AM, Commandeur U. Detection and characterization of a distinct type of beet necrotic yellow vein virus RNA 5 in a sugarbeet growing area in Europe. Arch Virol 1997; 142:1499–1504 [View Article] [PubMed]
    [Google Scholar]
  15. Lewellen RT, Skoyen IO, Erichsen AW. Breeding sugar beet for resistance to rhizomania: evaluation of host-plant reactions and selection for and inheritance of resistance. Brussels 1987Belgium
    [Google Scholar]
  16. Scholten OE, Jansen RC, Paul Keizer LC, De Bock TSM, Lange W. Major genes for resistance to beet necrotic yellow vein virus (BNYVV) in Beta vulgaris. Euphytica 1996; 91:331–339 [View Article]
    [Google Scholar]
  17. Scholten OE, De Bock TS, Klein-Lankhorst RM, Lange W. Inheritance of resistance to beet necrotic yellow vein virus in Beta vulgaris conferred by a second gene for resistance. Theor Appl Genet 1999; 99:740–746 [View Article] [PubMed]
    [Google Scholar]
  18. Scholten OE, Paul H, Peters D, Van Lent JW, Goldbach RW. In situ localisation of beet necrotic yellow vein virus (BNYVV) in rootlets of susceptible and resistant beet plants. Arch Virol 1994; 136:349–361 [View Article] [PubMed]
    [Google Scholar]
  19. Liu H-Y, Sears JL, Lewellen RT. Occurrence of resistance-breaking beet necrotic yellow vein virus of sugar beet. Plant Dis 2005; 89:464–468 [View Article] [PubMed]
    [Google Scholar]
  20. Bornemann K, Hanse B, Varrelmann M, Stevens M. Occurrence of resistance-breaking strains of Beet necrotic yellow vein virus in sugar beet in northwestern Europe and identification of a new variant of the viral pathogenicity factor P25. Plant Pathol 2015; 64:25–34 [View Article]
    [Google Scholar]
  21. Weiland JJ, Bornemann K, Neubauer JD, Khan MFR, Bolton MD. Prevalence and distribution of beet necrotic yellow vein virus strains in north dakota and minnesota. Plant Dis 2019; 103:2083–2089 [View Article] [PubMed]
    [Google Scholar]
  22. Galein Y, Legrève A, Bragard C. Long term management of rhizomania disease-insight into the changes of the Beet necrotic yellow vein virus RNA-3 Observed under resistant and non-resistant sugar beet fields. Front Plant Sci 2018; 9:795 [View Article] [PubMed]
    [Google Scholar]
  23. Pferdmenges F, Korf H, Varrelmann M. Identification of rhizomania-infected soil in Europe able to overcome Rz1 resistance in sugar beet and comparison with other resistance-breaking soils from different geographic origins. Eur J Plant Pathol 2008; 124:31–43 [View Article]
    [Google Scholar]
  24. Kutluk Yilmaz ND, Arli-Sokmen M, Kaya R. p25 pathogenicity factor deletion mutants of beet necrotic yellow vein virus occurring in sugar beet fields in Turkey. J Plant Dis Prot 2017; 125:89–98 [View Article]
    [Google Scholar]
  25. Liu H-Y, Lewellen RT. Distribution and molecular characterization of resistance-breaking isolates of Beet necrotic yellow vein virus in the United States. Plant Dis 2007; 91:847–851 [View Article] [PubMed]
    [Google Scholar]
  26. Chiba S, Kondo H, Miyanishi M, Andika IB, Han C et al. The evolutionary history of Beet necrotic yellow vein virus deduced from genetic variation, geographical origin and spread, and the breaking of host resistance. Mol Plant Microbe Interact 2011; 24:207–218 [View Article] [PubMed]
    [Google Scholar]
  27. Schirmer A, Link D, Cognat V, Moury B, Beuve M et al. Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. J Gen Virol 2005; 86:2897–2911 [View Article] [PubMed]
    [Google Scholar]
  28. Acosta-Leal R, Bryan BK, Smith JT, Rush CM. Breakdown of host resistance by independent evolutionary lineages of Beet necrotic yellow vein virus involves a parallel c/u mutation in its p25 gene. Phytopathology 2010; 100:127–133 [View Article] [PubMed]
    [Google Scholar]
  29. Koenig R, Loss S, Specht J, Varrelmann M, Lüddecke P et al. A single U/C nucleotide substitution changing alanine to valine in the beet necrotic yellow vein virus P25 protein promotes increased virus accumulation in roots of mechanically inoculated, partially resistant sugar beet seedlings. J Gen Virol 2009; 90:759–763 [View Article] [PubMed]
    [Google Scholar]
  30. Liebe S, Wibberg D, Maiss E, Varrelmann M. Application of a reverse genetic system for Beet Necrotic Yellow Vein Virus to study Rz1 resistance response in Sugar beet. Front Plant Sci 2019; 10:1703 [View Article]
    [Google Scholar]
  31. Kruse M, Koenig R, Hoffmann A, Kaufmann A, Commandeur U et al. Restriction fragment length polymorphism analysis of reverse transcription-PCR products reveals the existence of two major strain groups of beet necrotic yellow vein virus. J Gen Virol 1994; 75:1835–1842 [View Article] [PubMed]
    [Google Scholar]
  32. Miyanishi M, Kusume T, Saito M, Tamada T. Evidence for three groups of sequence variants of beet necrotic yellow vein virus RNA 5. Arch Virol 1999; 144:879–892 [View Article] [PubMed]
    [Google Scholar]
  33. Mehrvar M, Valizadeh J, Koenig R, Bragard CG. Iranian beet necrotic yellow vein virus (BNYVV): pronounced diversity of the p25 coding region in A-type BNYVV and identification of P-type BNYVV lacking A fifth RNA species. Arch Virol 2009; 154:501–506 [View Article] [PubMed]
    [Google Scholar]
  34. Ward L, Koenig R, Budge G, Garrido C, McGrath C et al. Occurrence of two different types of RNA-5-containing beet necrotic yellow vein virus in the UK. Arch Virol 2007; 152:59–73 [View Article] [PubMed]
    [Google Scholar]
  35. Koenig R, Lennefors BL. Molecular analyses of European A, B and P type sources of Beet necrotic yellow vein virus and detection of the rare P type in Kazakhstan. Arch Virol 2000; 145:1561–1570 [View Article] [PubMed]
    [Google Scholar]
  36. Tamada T, Uchino H, Kusume T, Iketani‐Saito M, Chiba S et al. 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. Plant Pathol 2020; 70:219–232 [View Article]
    [Google Scholar]
  37. Koenig R, Holtschulte B, Deml G, Lüddecke P, Schuhmann S et al. Beet necrotic yellow vein virus genome reassortments in a resistant sugar beet variety showing–in a small area in France–strong rhizomania symptoms. J Plant Dis Prot 2016; 116:7–9 [View Article]
    [Google Scholar]
  38. Bornemann K, Varrelmann M. Analysis of the resistance-breaking ability of different beet necrotic yellow vein virus isolates loaded into a single Polymyxa betae population in soil. Phytopathology 2011; 101:718–724 [View Article] [PubMed]
    [Google Scholar]
  39. Heijbroek W, Musters PMS, Schoone AHL. Variation in pathogenicity and multiplication of beet necrotic yellow vein virus (BNYVV) in relation to the resistance of sugar-beet cultivars. Eur J Plant Pathol 1999; 105:397–405 [View Article]
    [Google Scholar]
  40. Wetzel V, Willlems G, Darracq A, Galein Y, Liebe S et al. The Beta vulgaris-derived resistance gene Rz2 confers broad-spectrum resistance against soilborne sugar beet-infecting viruses from different families by recognizing triple gene block protein 1. Mol Plant Pathol 2021; 22:829–842 [View Article] [PubMed]
    [Google Scholar]
  41. Laufer M, Mohammad H, Maiss E, Richert-Pöggeler K, Dall’Ara M et al. Biological properties of Beet soil-borne mosaic virus and Beet necrotic yellow vein virus cDNA clones produced by isothermal in vitro recombination: Insights for reassortant appearance. Virology 2018; 518:25–33 [View Article] [PubMed]
    [Google Scholar]
  42. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 2009; 6:343–345 [View Article] [PubMed]
    [Google Scholar]
  43. Voinnet O, Vain P, Angell S, Baulcombe DC. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 1998; 95:177–187 [View Article]
    [Google Scholar]
  44. Laufer M, Mohammad H, Christ DS, Riedel D, Maiss E et al. Fluorescent labelling of Beet necrotic yellow vein virus and Beet soil-borne mosaic virus for co- and superinfection experiments in Nicotiana benthamiana. J Gen Virol 2018 [View Article] [PubMed]
    [Google Scholar]
  45. Tamada T, Uchino H, Kusume T, Saito M. RNA 3 deletion mutants of beet necrotic yellow vein virus do not cause rhizomania disease in sugar beets. Phytopathology 1999; 89:1000–1006 [View Article]
    [Google Scholar]
  46. Ratti C, Hleibieh K, Bianchi L, Schirmer A, Autonell CR et al. Beet soil-borne mosaic virus RNA-3 is replicated and encapsidated in the presence of BNYVV RNA-1 and -2 and allows long distance movement in Beta macrocarpa. Virology 2009; 385:392–399 [View Article] [PubMed]
    [Google Scholar]
  47. Meulemans M, Janssens L, Horemans S. Interactions between major genes and infl uence of the genetic background in the expression of rhizomania resistance. Proc IIRB-ASSBT 2003; 2003:161–173
    [Google Scholar]
  48. Biancardi E, Lewellen RT, De Biaggi M, Erichsen AW, Stevanato P. The origin of rhizomania resistance in sugar beet. Euphytica 2002; 127:383–397 [View Article]
    [Google Scholar]
  49. Nakagami R, Chiba S, Yoshida N, Senoo Y, Iketani‐Saito M et al. Epidemic progress of beet necrotic yellow vein virus: Evidence from an investigation in Japan spanning half a century. Plant Pathol 2021; 71:715–728 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001777
Loading
/content/journal/jgv/10.1099/jgv.0.001777
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error