Skip to main content
Log in

p25 pathogenicity factor deletion mutants of beet necrotic yellow vein virus occurring in sugar beet fields in Turkey

  • Original Article
  • Published:
Journal of Plant Diseases and Protection Aims and scope Submit manuscript

Abstract

Beet necrotic yellow vein virus (BNYVV) causes rhizomania which is one of the most devastating diseases in sugar beet fields worldwide. BNYVV symptoms were observed in Rz1-resistant sugar beet plants in a number of fields in Aksaray and Konya Provinces during surveys in 2011. Seven soil samples, taken from problematic areas in these provinces and known to be infested with populations of Polymyxa betae Keskin carrying BNYVV, were used in bait plant and molecular studies. Initially, the presence of other soil-borne viruses was investigated by using ELISA and RT-PCR. It was determined that BNYVV was in co-infections with pomoviruses, namely beet soil-borne virus and/or beet virus Q. The partial RNA-3 segment of BNYVV was amplified by RT-PCR, and the nucleotide sequences involving the p25 coding region were obtained. The deduced amino acid (aa) sequences of the p25 protein indicated that four BNYVV populations had ‘ACHG’ or ‘VHHG’ residues at positions 67–70. In addition, three populations containing three nucleotide deletions, not shifting the reading frame but affecting the aa at position 67 (-DHG) or 68 (D-HG), were identified. A deleted form of the p25 was identified in both the A- and J-type BNYVV populations. The pathogenicities of these BNYVV populations in the sugar beet genotypes rz1 and Rz1 were investigated under controlled conditions. All seven BNYVV isolates were capable of overcoming Rz1 resistance. These results seem to indicate that mutants of BNYVV with a deletion are aggressive, as are the isolates without deletion. Resistant beet cultivars will most likely be more productive in the future if these isolates become widespread in Turkey.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abe H, Tamada T (1986) Association of beet necrotic yellow vein virus with isolates of Polymyxa betae Keskin. Ann Phytopathol Soc Jpn 52:235–247

    Article  Google Scholar 

  • Acosta-Leal R, Fawley MW, Rush CM (2008) Changes in the intra isolate genetic structure of beet necrotic yellow vein virus populations associated with plant resistance breakdown. Virology 376:60–68

    Article  CAS  PubMed  Google Scholar 

  • Acosta-Leal R, Bryan BK, Smith JT, Rush CM (2010) 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 100:127–133

    Article  CAS  PubMed  Google Scholar 

  • Adams MJ, Antoniw JF, Mullins JGL (2001) Plant virus transmission by plasmodiophorid fungi is associated with distinctive transmembrane regions of virus-encoded proteins. Adv Virol 146:1139–1153

    CAS  Google Scholar 

  • Asher MJC (1993) Rhizomania. In: Cooke DA, Scottieds RK (eds) The sugar beet crop: science into practice. Chapman & Hall, London, pp 311–346

    Chapter  Google Scholar 

  • Biancardi E, Lewellen RT, De Biaggi M, Erichsen AW, Stevanato P (2002) The origin of rhizomania resistance in sugar beet. Euphytica 127:383–397

    Article  CAS  Google Scholar 

  • Bornemann K, Varrelmann M (2013) Effect of sugar beet genotype on the beet necrotic yellow vein virus p25 pathogenicity factor and evidence for a fitness penalty in resistance-breaking strains. Mol Plant Pathol 14(4):356–364

    Article  CAS  PubMed  Google Scholar 

  • Bornemann K, Hanse B, Varrelmann M, Stevens M (2015) 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 64:25–34

    Article  CAS  Google Scholar 

  • Borodynko N, Rymelska N, Hasiow-Jaroszewska B, Pospieszny H (2009) Molecular characterization of three soil-borne sugar beet-infecting viruses based on the coat protein gene. J Plant Pathol 91(1):191–193

    CAS  Google Scholar 

  • Bouzoubaa S, Guilley H, Jonard G, Richards K, Putz C (1985) Nucleotide sequence analysis of RNA-3 and RNA-4 of beet necrotic yellow vein virus, isolates F2 and G1. J Gen Virol 66:1553–1564

    Article  CAS  Google Scholar 

  • Bouzoubaa S, Niesbach-Klösgen U, Jupin I, Guilley H, Richards K, Jonard G (1991) Shortened forms of beet necrotic yellow vein virus RNA-3 and -4: internal deletions and a subgenomic RNA. J Gen Virol 72:259–266

    Article  CAS  PubMed  Google Scholar 

  • Chiba S, Miyanishi M, Andika IB, Kondo H, Tamada T (2008) Identification of amino acids of the beet necrotic yellow vein virus p25 protein required for induction of the resistance response in leaves of Beta vulgaris plants. J Gen Virol 89:1314–1323

    Article  CAS  PubMed  Google Scholar 

  • Chiba S, Kondo H, Miyanishi M, Andika IB, Han C, Tamada T (2011) 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 24(2):207–218

    Article  CAS  PubMed  Google Scholar 

  • Dijkstra J, De Jager CP (1998) Practical plant virology. Protocols and exercises. Department of Virology, Wageningen Agricultural University, Wageningen

    Book  Google Scholar 

  • Erkan E, Kutluk Yilmaz ND (2016) Distribution and molecular characterization of beet virus Q in sugar beet production areas of Turkey. In: Turkey 6th plant protection congress with international participation, 5–8 Sept 2016, Konya, p 680

  • Gerik JS, Duffus JE (1998) Differences in vectoring ability and aggressiveness of isolates of Polymyxa betae. Phytopathology 78:1340–1343

    Article  Google Scholar 

  • Gilmer D, Ratti C, ICTV Report Consortium (2017) ICTV virus taxonomy profile: Benyviridae. J Gen Virol. https://doi.org/10.1099/jgv.0.000864

    Google Scholar 

  • Goffart J-P, Maraite H (1992) Influence de la temperature sur Polymyxa betae Keskin et le beet necrotic yellow vein virus (BNYVV). Med Fac Landbouww Univ Gent 57(2a):287–293

    Google Scholar 

  • Gonzalez Vazquez M, Ayala J, Garcia Arenal F, Fraile A (2009) Occurrence of beet black scorch virus infecting sugarbeet in Europe. Plant Dis 93:21–24

    Article  Google Scholar 

  • Gumus M, Erbay E, Erkan S, Paylan IC (2014) Occurrence of viruses infecting spinach in Western Anatolia of Turkey: the first field survey report. J Food Agric Environ 12:272–275

    Google Scholar 

  • Hanse B, Raaijmaker E (2016) Rhizomania: spread of and research on resistance breaking BNYVV tetrad types in the Netherlands. In: 75th IIRB congress, 16–17 Feb 2016, Brussels. https://doi.org/10.13140/rg.2.1.1927.4004

  • Heijbroek W, Musters PMS, Schoone AHL (1999) Variation in pathogenicity and multiplication of beet necrotic yellow vein virus (BNYVV) in relation to resistance of sugar-beet cultivars. Eur J Plant Pathol 105:397–405

    Article  Google Scholar 

  • Jiang J-X, Zhang J-F, Che S-C, Yang D-J, Yu J-L, Cai Z-N, Liu Y (1999) Transmission of beet black scorch virus by Olpidium brassicae. J Jiangxi Agric Univ 21:525–528

    Google Scholar 

  • Klein E, Link D, Schirmer A, Erhardt M, Gilmer D (2007) Sequence variation within beet necrotic yellow vein virus p25 protein influences its oligomerization and isolate pathogenicity on Tetragonia expansa. Virus Res 126:53–61

    Article  CAS  PubMed  Google Scholar 

  • Koenig R, Lennefors BL (2000) 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. Adv Virol 145:1561–1570

    CAS  Google Scholar 

  • Koenig R, Valizadeh J (2008) Molecular and serological characterization of an Iranian isolate of beet black scorch virus. Adv Virol 153:1397–1400

    CAS  Google Scholar 

  • Koenig R, Commandeur U, Loss S, Beir C, Kaufmann A, Lesemann DE (1997) Beet soil-borne virus RNA2: similarities and dissimilarities to the coat protein gene-carrying RNAs of other furoviruses. J Gen Virol 78:469–477

    Article  CAS  PubMed  Google Scholar 

  • Koenig R, Pleij CWA, Commandeur U (1998) Genome properties of beet virus Q, a new furo-like virus from sugar beet determined from unpurified virus. J Gen Virol 79:2027–2036

    Article  CAS  PubMed  Google Scholar 

  • Koenig R, Kastirr U, Holtschulte B, Deml G, Varrelmann M (2008) Distribution of various types and p25 subtypes of beet necrotic yellow vein virus in Germany and other European countries. Adv Virol 153:2139–2144

    CAS  Google Scholar 

  • Koenig R, Loss S, Specht SJ, Varrelmann M, Lüddecke P, Deml G (2009) 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 90:759–763

    Article  CAS  PubMed  Google Scholar 

  • Kruse M, Koenig R, Hoffman A, Kaufmann A, Commandeur U, Solevyev AG, Savenkov I, Burgermeister W (1994) 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 75:1835–1842

    Article  CAS  PubMed  Google Scholar 

  • Kutluk Yilmaz ND, Meunier A, Schmit JF, Stas A, Bragard C (2007) Partial nucleotide sequence analysis of Turkish isolates of beet necrotic yellow vein virus (BNYVV) RNA-3. Plant Patholol 56:311–316

    Article  Google Scholar 

  • Kutluk Yilmaz ND, Arli Sokmen M, Kaya R, Sevik MA, Tunali B, Demirtas S (2016a) The widespread occurrences of beet soil-borne virus and RNA-5 containing beet necrotic yellow vein virus isolates in sugar beet production areas in Turkey. Eur J Plant Pathol 144:443–455

    Article  Google Scholar 

  • Kutluk Yilmaz ND, Kaya Altop E, Phillippo CJ, Mennan H (2016b) New natural weed host Raphanus raphanistrum L. (Brassicaceae) for beet necrotic yellow vein virus and its vector Polymyxa betae Keskin. Turk J Agric For 40:120–126

    Article  Google Scholar 

  • Lennefors BL, van Roggen PM, Yndgaard F, Savenkov EI, Valkonen JPT (2008) Efficient dsRNA-mediated transgenic resistance beet necrotic yellow vein virus in sugar beets is not affected by other soilborne and aphid transmitted viruses. Transgenic Res 17(2):219–228

    Article  CAS  PubMed  Google Scholar 

  • Lennofors BL (2006) Molecular breeding for resistance torhizomania in sugar beets. Ph.D. thesis, Swedish University of Agricultural Sciences, Uppsala

  • Li M, Liu T, Wang B, Han CG, Li DW, Yu JL (2008) Phylogenetic analysis of beet necrotic yellow vein virus isolates from China. Virus Genes 36:429–432

    Article  CAS  PubMed  Google Scholar 

  • Liu HY, Lewellen RT (2007) Distribution and molecular characterization of resistance-breaking isolates of beet necrotic yellow vein virus in the United States. Plant Dis 91:847–851

    Article  CAS  Google Scholar 

  • Liu J, Xian H (1995) Preliminary report on beet black scorch virus. China Sugar Beet 3:30–31

    Google Scholar 

  • Liu H-Y, Sears JL, Lewellen RT (2005) Occurrences of resistance-breaking beet necrotic yellow vein virus of sugar beet. Plant Dis 89:464–468

    Article  CAS  Google Scholar 

  • Mehrvar M, Valizadeh J, Koenig R, Bragard CG (2009) 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. Adv Virol 154:501–506

    CAS  Google Scholar 

  • Meunier A, Schmit JF, Stas A, Kutluk N, Bragard C (2003) Multiplex reverse transcription for simultaneous detection of beet necrotic yellow vein virus, beet soilborne virus, and beet virus Q and their vector Polymyxa betae KESKIN on sugar beet. Appl Environ Microbiol 69:2356–2360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyanishi M, Kusume T, Saito M, Tamada T (1999) Evidence for three groups of sequence variants of beet necrotic yellow vein virus RNA 5. Adv Virol 144:879–892

    CAS  Google Scholar 

  • Mouhanna AM, Nasrallah A, Langen G, Schlösser E (2002) Surveys for beet necrotic yellow vein virus (the cause of rhizomania), other viruses, and soil-borne fungi infecting sugar beet in Syria. J Phytopathol 150:657–662

    Article  Google Scholar 

  • Pavli O, Prins M, Skaracis GN (2010) Detection of beet soil-borne virus and beet virus Q in sugar beet in Greece. J Plant Pathol 92(3):793–796

    CAS  Google Scholar 

  • Pavli O, Prins M, Goldbach R, Skaracis GN (2011) Efficiency of Rz1-based rhizomania resistance and molecular studies on BNYVV isolates from sugar beet cultivation in Greece. Eur J Plant Pathol 130:133–142

    Article  CAS  Google Scholar 

  • Pferdmenges F (2007) Occurrence, spread and pathogenicity of different beet necrotic yellow vein virus (BNYVV) isolates, 23rd edn. Cuvillier Verlag, Göttingen

    Google Scholar 

  • Pferdmenges F, Varrelmann M (2009) Breaking of beet necrotic yellow vein virus resistance in sugar beet is independent of virus and vector inoculum densities. Eur J Plant Pathol 124:231–245

    Article  Google Scholar 

  • Prillwitz H, Schlösser E (1992) Beet soil-borne virus: occurrence, symptoms and effect on plant development. Med Fac Landbouw Univ Gent 57(2a):295–302

    Google Scholar 

  • Prillwitz H, Schlösser E (1993) Interaction between beet soil-borne virus (BSBV-2) and beet necrotic yellow vein virus (BNYVV). In: Proceedings of the 2nd symposium of the international working group on plant viruses with fungal vectors, Denver, pp 71–74

  • Rahim MD, Andika IB, Han C, Kondo H, Tamada T (2007) RNA-4 encoded p31 of beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. J Gen Virol 88:1611–1619

    Article  CAS  PubMed  Google Scholar 

  • Ratti C, Clover GRG, Autonell CR, Harju VA, Henry CM (2005) A multiplex RT-PCR assay capable of distinguishing beet necrotic yellow vein virus types A and B. J Virol Methods 124:41–47

    Article  CAS  PubMed  Google Scholar 

  • Reavy B, Arif M, Cowan GH, Torrance L (1998) Association of sequences in the coat protein/readthrough protein domain of potato mop-top virus with transmission by Spongospora subterranea. J Gen Virol 79:2343–2347

    Article  CAS  PubMed  Google Scholar 

  • Richards K, Jonard G, Guilley H, Ziegler V, Putz C (1985) In vitro translation of beet necrotic yellow vein virus RNA and studies of sequence homology among the RNA species using cloned cDNA probes. J Gen Virol 66:345–350

    Article  CAS  Google Scholar 

  • Rush CM, Heidel GB (1995) Furovirus diseases of sugar beets in the United States. Plant Dis 79(9):868–875

    Article  Google Scholar 

  • Rush CM, Liu HY, Lewellen R, Acosta-Leal R (2006) The continuing saga of rhizomania of sugar beets in the United States. Plant Dis 90:4–15

    Article  Google Scholar 

  • Schirmer A, Link D, Cognat V, Moury B, Beuve M, Meunier A, Bragard C, Gilmer D, Lemaire O (2005) Phylogenetic analysis of isolates of beet necrotic yellow vein virus collected worldwide. J Gen Virol 86:2897–2911

    Article  CAS  PubMed  Google Scholar 

  • Smith HG (1991) Beet mild yellowing luteo virus. In: Brunt AH, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L (eds) Viruses of plants. University Press, Cambridge, pp 209–211

    Google Scholar 

  • Sohi HH, Maleki M (2004) Evidence for presence of types A and B of beet necrotic yellow vein virus (BNYVV) in Iran. Virus Genes 29(3):353–358

    Article  CAS  PubMed  Google Scholar 

  • Tamada T (1999) Benyviruses. In: Webster RG, Granoff A (eds) Encyclopedia of virology, 2nd edn. Academic, London, pp 154–160

    Chapter  Google Scholar 

  • Tamada T, Kusume T (1991) Evidence that the 75 K readthrough protein of beet necrotic yellow vein virus RNA-2 is essential for transmission by the fungus Polymyxa betae. J Gen Virol 72:1496–1504

    Article  Google Scholar 

  • Tamada T, Abe H, Saito M, Kiguchi T, Harada T (1989) Production and pathogenicity of isolates of beet necrotic yellow vein virus with different numbers of RNA components. J Gen Virol 70:3399–3409

    Article  CAS  Google Scholar 

  • Tamada T, Uchino H, Kusume T, Saito M (1999) RNA 3 deletion mutants of beet necrotic yellow vein virus do not cause rhizomania disease in sugar beets. Phytopathology 89:1000–1006

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward L, Koenig R, Budge G, Garrido C, McGrath C, Stubbey H, Boonham N (2007) Occurrence of two different types of RNA-5 containing beet necrotic yellow vein virus in the UK. Adv Virol 152:59–73

    CAS  Google Scholar 

  • Webb KM, Wintermantel WM, Kaur N, Prenni JE, Broccardo CJ, Wolfe LM, Hladky LL (2015) Differential abundance of proteins in response to beet necrotic yellow vein virus during compatible and incompatible interactions in sugar beet containing Rz1 or Rz2. Physiol Mol Plant Pathol 91:96–105

    Article  CAS  Google Scholar 

  • Weiland JJ, Van Winkle D, Edwards MC, Larson RL, Shelver WL, Freeman TP, Liu H-Y (2007) Characterization of a U.S. isolate of beet black scorch virus. Phytopathology 97:1245–1254

    Article  CAS  PubMed  Google Scholar 

  • Wisler GC, Lewellen RT, Sears JL, Wasson JW, Liu H-Y, Wintermantel WM (2003) Interactions between beet necrotic yellow vein virus and beet soilborne mosaic virus in sugar beet. Plant Dis 87:1170–1175

    Article  Google Scholar 

  • Zhuo N, Jiang N, Zhang C, Zhang Z-Y, Zhang G-Z, Han C-G, Wang Y (2015) Genetic diversity and population structure of beet necrotic yellow vein virus in China. Virus Res 205:54–62

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Gregory T. Sullivan of the University of Queensland for editing the English in an earlier version of this manuscript.

Funding

The work presented, which was funded by The Scientific and Technological Research Council of Turkey (TUBITAK) (Grant No.: TOVAG110O188), did not include any human or animal participants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nazli Dide Kutluk Yilmaz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kutluk Yilmaz, N.D., 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 125, 89–98 (2018). https://doi.org/10.1007/s41348-017-0142-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41348-017-0142-4

Keywords

Navigation