Skip to main content
SpringerLink
Log in

Breaking of Beet necrotic yellow vein virus resistance in sugar beet is independent of virus and vector inoculum densities

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Beet necrotic yellow vein virus (BNYVV) is transmitted by Polymyxa betae to sugar beet, causing rhizomania disease. Resistance-breaking strains of BNYVV, overcoming single (Rz1) or double (e.g. Rz1  +  Rz2) major resistance genes in sugar beet have been observed in France and recently in the USA and Spain. To demonstrate if resistance-breaking is dependent on inoculum density, the inoculum concentration of BNYVV and P. betae in soil samples where resistance-breaking had been observed was estimated using the most probable number (MPN) method. The MPN-values obtained displayed highly significant differences with respect to the virus concentration in various soils and did not correlate with the ability to overcome resistance. Virus quantification in susceptible plants demonstrated that soils containing resistance-breaking isolates of BNYVV did not produce higher virus concentrations. The MPN assay was repeated with Rz1  +  Rz2 partially-resistant sugar beets to see if the resistance-breaking is concentration-dependent. There was no correlation between soil dilution and increased virus concentration in Rz1  +  Rz2 plants produced by BNYVV resistance-breaking strains. Determination of the absolute P. betae concentration by ELISA demonstrated that all resistance-breaking soil samples contained elevated concentrations. However, the calculation of the proportion of viruliferous P. betae did not show a positive correlation with the resistance-breaking ability. Finally resistance-breaking was studied with susceptible, Rz1 and Rz1  + Rz2 genotypes and standardised rhizomania inoculum added to sterilised soil. Results from these experiments supported the conclusion that resistance-breaking did not correlate with virus concentration or level of viruliferous P. betae in the soil.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Acosta-Leal, R., & Rush, C. M. (2007). Mutations associated with resistance-breaking isolates of Beet necrotic yellow vein virus and their allelic discrimination using TaqMan technology. Phytopathology, 97, 325–330. doi:10.1094/PHYTO-97-3-0325.

    Article  PubMed  CAS  Google Scholar 

  • Asher, M. J. C., Chwarszczynska, D. M., & Leaman, M. (2003). The evaluation of Rhizomania resistant sugar beet for the UK. Annals of Applied Biology, 141, 101–109. doi:10.1111/j.1744-7348.2002.tb00201.x.

    Article  Google Scholar 

  • Blunt, S. J., Asher, M. J. C., & Gilligan, C. A. (1991). Infection of sugar beet by Polymyxa betae in relation to soil temperature. Plant Pathology, 40, 257–267. doi:10.1111/j.1365-3059.1991.tb02375.x.

    Article  Google Scholar 

  • Chiba, S., Miyanishi, M., Andika, I. B., 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. The Journal of General Virology, 89, 1314–1323. doi:10.1099/vir.0.83624-0.

    Article  PubMed  CAS  Google Scholar 

  • Gerik, J., & Duffus, J. (1988). Differences in vectoring ability and aggressiveness of isolates of Polymyxa betae. Phytopathology, 78, 1340–1343. doi:10.1094/Phyto-78-1340.

    Article  Google Scholar 

  • Gidner, S., Lennefors, B.-L., Nilsson, N.-O., Bensefelt, J., Johansson, E., Gyllenspetz, U., et al. (2005). QTL mapping of BNYVV resistance from the WB41 source in sugar beet. Genome, 48, 279–285.

    PubMed  CAS  Google Scholar 

  • Heijbroek, W., Musters, P. M. S., & Schoone, A. H. L. (1999). Variation in pathogenicity and multiplication of Beet necrotic yellow vein virus (BNYVV) in relation to the resistance of sugar-beet cultivars. European Journal of Plant Pathology, 105, 397–405. doi:10.1023/A:1008705111232.

    Article  Google Scholar 

  • Hurley, M. A., & Roscoe, M. E. (1983). Automated statistical analysis of microbial enumeration by dilution series. Journal of Applied Bacteriology, 55, 159–164.

    Google Scholar 

  • Kaufmann, A., Koenig, R., & Lesemann, D.-E. (1992). Tissue print-immunoblotting reveals an uneven distribution of Beet necrotic yellow vein and Beet soilborne viruses. Archives of Virology, 126, 329–335. doi:10.1007/BF01309706.

    Article  PubMed  CAS  Google Scholar 

  • Keskin, B. (1964). Polymyxa betae n. sp. Ein Parasit in den Wurzeln von Beta vulgaris Tournefort, besonders während der Jugendentwicklung der Zuckerrübe. Archiv fur Mikrobiologie, 49, 348–374. doi:10.1007/BF00406857.

    Article  PubMed  CAS  Google Scholar 

  • Kingsnorth, C. S., Asher, M. J. C., Keane, G. J. P., Chwarszczynska, D. M., Luterbacher, M. C., & Mutasa-Gottgens, E. S. (2003). Development of a recombinant antibody ELISA test for the detection of Polymyxa betae and its use in resistance screening. Plant Pathology, 52, 673–680. doi:10.1111/j.1365-3059.2003.00928.x.

    Article  CAS  Google Scholar 

  • Koenig, R., & Lennefors, B.-L. (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. Archives of Virology, 145, 1561–1570. doi:10.1007/s007050070076.

    Article  PubMed  CAS  Google Scholar 

  • Koenig, R., & Stein, B. (1990). Distribution of Beet necrotic yellow vein virus in mechanically inoculated sugarbeet plantlets of cultivars with different degrees of Rhizomania resistance. In R. Koenig (Ed.), Proceedings of the First Symposium of the International Working Group on Plant Viruses with Fungal Vectors, Braunschweig. German Phytomedical Society Series (vol. Vol. 1, (pp. 83–86)). Stuttgart: Eugen Ulmer.

    Google Scholar 

  • Koenig, R., Burgermeister, W., Weich, H., Sebald, W., & Kothe, C. (1986). Uniform RNA patterns of Beet necrotic yellow vein virus in sugar beet roots, but not in leaves from several plant species. The Journal of General Virology, 67, 2043–2046. doi:10.1099/0022-1317-67-9-2043.

    Article  CAS  Google Scholar 

  • Koenig, R., Jarausch, W., Li, Y., Commandeur, U., Burgermeister, W., Gehrke, M., & Luddecke, P. (1991). Effect of recombinant Beet necrotic yellow vein virus with different RNA compositions on mechanically inoculated sugarbeets. The Journal of General Virology, 72, 2243–2246. doi:10.1099/0022-1317-72-9-2243.

    Article  PubMed  CAS  Google Scholar 

  • Koenig, R., Haeberlé, A. M., & Commandeur, U. (1997). Detection and characterization of a distinct type of Beet necrotic yellow vein virus RNA 5 in a sugar beet growing area in Europe. Archives of Virology, 142, 1499–1504. doi:10.1007/s007050050176.

    Article  PubMed  CAS  Google Scholar 

  • Kruse, M., Koenig, R., Hoffmann, A., Kaufmann, A., Commandeur, U., Solovyev, A. G., et al. (1994). RFLP analysis of RT-PCR products reveals the existence of two major strain groups of Beet necrotic yellow vein virus. The Journal of General Virology, 75, 1835–1842. doi:10.1099/0022-1317-75-8-1835.

    Article  PubMed  CAS  Google Scholar 

  • Lennefors, B.-L., Lindsten, K., & Koenig, R. (2000). First record of A and B type Beet necrotic yellow vein virus in sugar beets in Sweden. European Journal of Plant Pathology, 106, 199–201. doi:10.1023/A:1008780812215.

    Article  Google Scholar 

  • Lewellen, R. T., Skoyen, I. O., & Erichsen, A. W. (1987). Breeding sugar beet for resistance to Rhizomania: Evaluation of host—plant reactions and selection for and inheritance of resistance. (In Proceedings of the IIRB 50th Winter Congress Vol. II (pp. 139–156), Brussels).

  • Link, D., Schmidlin, L., Schirmer, A., Klein, E., Erhardt, M., Geldreich, A., et al. (2005). Functional characterization of the beet necrotic yellow vein virus RNA-5-encoded p26 protein: evidence for structural pathogenecity determinants. Journal of General Virology, 86, 2115-2125.

    Google Scholar 

  • Liu, H.-Y., & Lewellen, R. T. (2007). Distribution and molecular characterisation of resistance-breaking isolates of Beet necrotic yellow vein virus in the United States. Plant Disease, 91, 847–851. doi:10.1094/PDIS-91-7-0847.

    Article  CAS  Google Scholar 

  • Liu, H.-Y., Sears, J. L., & Lewellen, R. T. (2005). Occurrence of resistance-breaking Beet necrotic yellow vein virus of sugar beet. Plant Disease, 89, 464–468. doi:10.1094/PD-89-0464.

    Article  CAS  Google Scholar 

  • Mutasa, E. S., Chwarszczynska, D. M., Adams, M. J., Ward, E., & Asher, M. J. C. (1995). Development of PCR for the detection of Polymyxa betae in sugar-beet roots and its application in field studies. Physiological and Molecular Plant Pathology, 47, 303–313. doi:10.1006/pmpp.1995.1060.

    Article  CAS  Google Scholar 

  • Mutasa-Gottgens, E., Chwarszczynska, D., Halsey, K., & Asher, M. (2000). Specific polyclonal antibodies for the obligate plant parasite Polymyxa — a targeted recombinant DNA approach. Plant Pathology, 49, 276–287. doi:10.1046/j.1365-3059.2000.00446.x.

    Article  CAS  Google Scholar 

  • Nielsen, S. L., Nicolaisen, M., Scheel, C., & Dinesen, I. G. (2001). First record of Beet necrotic yellow vein virus in Denmark. Plant Disease, 85, 559. doi:10.1094/PDIS.2001.85.5.559C.

    Article  Google Scholar 

  • Pferdmenges, F., Korf, H., & Varrelmann, M. (2008). 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. European Journal of Plant Pathology. doi:10.2007/s10658-008-9388-9.

  • Piepho, H. P., & Ogutu, J. O. (2003). Inference for the break point in segmented regression with application to longitudinal data. Biometrical Journal. Biometrische Zeitschrift, 45, 591–601. doi:10.1002/bimj.200390035.

    Article  Google Scholar 

  • Quillet, L., Guilley, H., Jonard, G., & Richards, K. (1989). In vitro synthesis of biologically active Beet necrotic yellow vein virus RNAs. Virology, 172, 293–301. doi:10.1016/0042-6822(89)90131-1.

    Article  PubMed  CAS  Google Scholar 

  • Rush, C. M. (2003). Ecology and epidemiology of Benyviruses and plasmodiphorid vectors. Annual Review of Phytopathology, 41, 567–592. doi:10.1146/annurev.phyto.41.052002.095705.

    Article  PubMed  CAS  Google Scholar 

  • Schirmer, A., Link, D., Cognat, V., Moury, B., Beuve, M., Meunier, A., et al. (2005). Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. The Journal of General Virology, 86, 2897–2911. doi:10.1099/vir.0.81167-0.

    Article  PubMed  CAS  Google Scholar 

  • Scholten, O. E., & Lange, W. (2000). Breeding for resistance to Rhizomania in sugar beet: a review. Euphytica, 112, 219–231. doi:10.1023/A:1003988003165.

    Article  Google Scholar 

  • Scholten, O. E., Paul, H., Peters, D., Van Lent, J. W., & Goldbach, R. W. (1994). In situ localisation of Beet necrotic yellow vein virus (BNYVV) in rootlets of susceptible and resistant beet plants. Archives of Virology, 136, 349–361. doi:10.1007/BF01321063.

    Article  PubMed  CAS  Google Scholar 

  • Scholten, O. E., Jansen, R. C., Paul Keizer, L. C., De Bock, T. S. M., & Lange, W. (1996). Major genes for resistance to Beet necrotic yellow vein virus (BNYVV) in Beta vulgaris. Euphytica, 91, 331–339. doi:10.1007/BF00033095.

    Article  Google Scholar 

  • Tamada, T. (1975). Beet necrotic yellow vein virus. CMI/AAB Descriptions of Plant Viruses, No. 144.

  • Tamada, T. (1999). Benyvirus. In Granoff A. and Webster R. (Eds.), Encyclopedia of Virology 2nd ed. Vol. II (pp. 154–160). New York: Academic.

  • Tamada, T., Shirako, Y., Abe, I.-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. The Journal of General Virology, 70, 3399–3409. doi:10.1099/0022-1317-70-12-3399.

    Article  CAS  Google Scholar 

  • Tamada, T., Kusume, T., Uchino, H., Kiguchi, T., & Saito, M. (1996). Evidence that Beet necrotic yellow vein virus RNA-5 is involved in symptom development of sugar-beet roots. In J. L. Sherwood & C. M. Rush (Eds.). Proceedings of the 3rd Symposium of the International Working Group on Plant Viruses with Fungal Vectors (pp. 49–52). Dundee.

  • Tuitert, G. (1990). Assessment of the inoculum potential of Polymyxa betae and Beet necrotic yellow vein virus (BNYVV) in soil using the most probable number method. Netherlands Journal of Plant Pathology, 96, 331–341. doi:10.1007/BF01998782.

    Article  Google Scholar 

  • Ward, L., Koenig, R., Budge, G., Garrido, C., McGrath, C., Stubbley, H., et al. (2007). Occurrence of two different types of RNA-5-containing Beet necrotic yellow vein virus in the UK. Archives of Virology, 152, 59–73. doi:10.1007/s00705-006-0832-x.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Many thanks to the Department of Phytopathology (Syngenta Seeds AB, Sweden) for permission to conduct greenhouse tests in their climate chambers. Dirk Stefan, Erwin Ladewig, Elke Nitschke and Ruth Pilot are acknowledged for critical reading of the manuscript and fruitful discussions. For technical help we would like to thank Annette Walter and Helmut Korf. This research project has been carried out with the financial support of the Federal Ministry of Economics and Technology (BMWi), administered via the Arbeitsgemeinschaft industrieller Forschungsvereinigungen e.V. (AiF) and the Gemeinschaft zur Förderung der privaten deutschen Pflanzenzüchtung e.V. (GFP).

Author information

Authors and Affiliations

  1. Department of Phytopathology, Institute for Sugar Beet Research, Holtenser Landstr. 77, 37079, Göttingen, Germany

    Friederike Pferdmenges & Mark Varrelmann

Authors
  1. Friederike Pferdmenges
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark Varrelmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark Varrelmann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pferdmenges, F., Varrelmann, M. 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 (2009). https://doi.org/10.1007/s10658-008-9408-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-008-9408-9

Keywords

Search

Navigation