Journal of Plant Pathology

, Volume 101, Issue 1, pp 173–177 | Cite as

Detection and prevalence of viruses associated with sugarbeet in the Tadla region of Morocco

  • Fatima Nouayti
  • Abdessalem TahiriEmail author
  • Ilham Madani
  • Abdelali Blenzar
  • Rachid LahlaliEmail author
Short Communication


Fifty-five soil samples were collected from sugarbeet fields with rhizomania occurrence in the region of Tadla. BNYVV was ascertained by RT-PCR in 40 out of 55 fields surveyed and the positive samples were subsequently examined for the presence of the different pathotype of BNYVV. Using the same technique, a survey was simultaneously undertaken to identify the occurrence of other soil-borne viruses, which might frequently associate with BNYVV such as beet soilborne virus (BSBV), beet soilborne mosaic virus (BSBMV) and beet virus Q (BVQ). Results indicated that most samples were infected with A-type BNYVV, but only 9% of the samples were positive for B-type BNYVV. BNYVV (72.7%) was the most frequently detected, followed respectively by BSBV (36.36%) and BVQ (30.9%). However, P-type BNYVV was not detected at all. Our results also indicated the likely absence of BSBMV in the Tadla region. Surprisingly, among the 40 BNYVV-infected samples, 17 were also infected with BVQ and 20 with BSBV. In conclusion, BSBV occurred in triple infections with BNYVV and BVQ. In addition, there was only one sample revealed positive for both viruses BNYVV-B and BVQ and four samples for BSBV infection. Therefore, this study is the first investigation of BSBV and BVQ in fields-grown sugarbeet of Morocco.


Beet soil-borne virus Beet virus Q Rhizomania Sugarbeet 



The authors are grateful to the Phytopathology Unit of the Ecole Nationale d’Agriculture de Meknès for supporting this work and express their gratitude to the laboratory staffs and students for their involvement in collecting samples.


  1. Abe H, Tamada T (1986) Association of Beet necrotic yellow vein virus with isolates of Polymyxa betae Keskin. Ann Phytopathol Soc Jpn 52:235–247CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  3. Borodynko N, Rymelska N, Hasiow-Jaroszewska B, Pospieszny H (2009a) Molecular characterization of three soil-borne sugar beet-infecting viruses based on the coat protein gene. J Plant Pathol 91:191–193Google Scholar
  4. Borodynko N, Hasiow-Jaroszewska B, Pospieszny H (2009b) Evidence for the presence of Beet necrotic yellow virus type A and B in Poland. J Plant Dis Protect 116:106–108CrossRefGoogle Scholar
  5. European and Mediterranean Plant Protection Organization (OEPP/EPPO) (2005) First record of Beet necrotic yellow benyvirus in Morocco. EPPO Reporting Service 7:2005/102Google Scholar
  6. Farzadfar SH, Pourrahim R, Golnaraghi AR, Shahraeen N (2002) First report of Beet soil-borne virus on sugar beet in Iran. Plant Dis 86:187CrossRefGoogle Scholar
  7. Fujisawa I, Sugimoto T (1977) Transmission of Beet necrotic yellow vein virus by Polymyxa betae. Ann Phytopathol Soc Jpn 43:583–586CrossRefGoogle Scholar
  8. Harju VA, Mumford RA, Blockley A, Boonham N, Clover GRG, Weekes R, Henry CM (2002) Occurrence in the United Kingdom of Beet necrotic yellow vein virus isolate which contain RNA-5. Plant Pathol 51:811CrossRefGoogle Scholar
  9. Heidel GB, Rush CM (1997) Characteristics of Beet soil-borne mosaic virus, a furo-like virus infecting sugarbeet. Plant Dis 81:1070–1076CrossRefGoogle Scholar
  10. Heijbroek W, Musters PMS, Schoon AHL (1999) 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 105:397–405CrossRefGoogle Scholar
  11. Henry C (1996) Rhizomania-its effect on sugar-beet yield in the UK. British Sugar Beet Review 64:24–26Google Scholar
  12. Henry CM, Jones RAC (1986) Occurrence of a soil-borne virus of sugar beet in England. Plant Pathol 35:585–591CrossRefGoogle Scholar
  13. Hughes DW, Galau G (1988) Preparation of RNA from cotton leaves and pollen. Plant Mol Biol Report 6:253–257CrossRefGoogle Scholar
  14. Hutchinson PJ, Henry CM, Coutts RHA (1992) A comparison, using dsRNA analysis, between Beet soil-borne virus and some other tubular viruses isolated from sugarbeet. J Gen Virol 73:1317–1320CrossRefGoogle Scholar
  15. Ivanović M, Macfarlane I (1982) A tubular virus associated with infection of sugar beet by Polymyxa betae. Report of Rothamsted Experimental Station for 1981, pp 190–191Google Scholar
  16. Koenig R, Lennefors 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. Arch Virol 145:1561–1570CrossRefGoogle Scholar
  17. Koenig R, Lüddecke P, Haeberle AM (1995) Detection of Beet necrotic yellow vein virus strains, variants and mixed infections by examining single-strand conformation polymorphisms of immunocapture RT-PCR products. J Gen Virol 76:2051–2055CrossRefGoogle Scholar
  18. Koenig R, Pleij CWA, Beier C, Commandeur U (1998) Genome properties of Beet virus Q, a new furo-like virus from sugarbeet, determined from unpurified virus. J Gen Virol 79:2027–2036CrossRefGoogle Scholar
  19. Koenig R, Haeberle AM, Commandeur U (1999) Detection and characterization of a distinct type of Beet necrotic yellow vein virus RNA-5 in a sugar growing area in Europe. Arch Virol 142:1499–1504CrossRefGoogle Scholar
  20. Koenig R, Pleij CWA, Büttner G (2000) Structure and variability of the 3’end of RNA 3 of Beet soil-borne pomovirus, a virus with uncertain pathogenic effects. Arch Virol 145:1173–1181CrossRefGoogle Scholar
  21. KutlukYilmaz ND, Yanar Y, Günal H, Erkan S (2004) Effects of soil properties on disease occurrence of Beet necrotic yellow vein virus and Beet soil-borne virus on sugar beet in Tokat, Turkey. Plant Pathol J 3:56–60CrossRefGoogle Scholar
  22. Lee L, Tedford EB, Batten JS, Scholthof KBG, Rush CM (2001) Complete nucleotide sequence and genome organization of Beet soil-borne mosaic virus. Arch Virol 146:2443–2453CrossRefGoogle Scholar
  23. Lennefors BL, Lindsten K, Koenig R (2000) First report of A and B type Beet necrotic yellow vein virus in sugar beets in Sweden. Eur J Plant Pathol 106:199–201CrossRefGoogle Scholar
  24. Mahmood T, Rush CM (1999) Evidence of cross-protection between Beet soil-borne mosaic virus and Beet necrotic yellow vein virus in sugar beet. Plant Dis 83:521–526CrossRefGoogle Scholar
  25. Meunier A, Schmit JFO, Stas A, Kutluk N, Bragard C (2003) Multiplex reverse transcription-PCR 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 69:2356–2360CrossRefGoogle Scholar
  26. Miyanishi M, Kusume T, Saito M, Tamada T (1999) Evidence for three groups of sequence variants of Beet necrotic yellow vein virus RNA 5. Arch Virol 144:879–892CrossRefGoogle Scholar
  27. 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(11–12):657–662CrossRefGoogle Scholar
  28. Pavli OI, Prins M, Skaracis GN (2010) Detection of Beet soilborne virus and Beet virus Q in sugarbeet in Greece. J Plant Pathol 92:793–796Google Scholar
  29. Prillwitz H, Schlösser E (1992) Beet soil-borne virus: occurrence, symptoms and effect on plant development. Mededelingenvan de Faculteit Landbouwwetenschapen, Rijksuniversiteit Gent 57:295–302Google Scholar
  30. Prillwitz H, Schlösser E (1993) Interactions between Beet soil-borne virus (BSBV-2) and Beet necrotic yellow vein virus (BNYVV). Proceedings of the 2nd symposium of the international working group on plant viruses with fungal vectors, Denver 1993, pp 71–74Google Scholar
  31. Ratti C, Clover GR, 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 124:41–47CrossRefGoogle Scholar
  32. Rush CM (2003) Ecology and epidemiology of benyviruses and plasmodiophorid vectors. Annu Rev Phytopathol 41:567–592CrossRefGoogle Scholar
  33. Rush CM, Heidel GB (1995) Furovirus diseases of sugar beets in the United States. Plant Dis 79:868–875CrossRefGoogle Scholar
  34. Saito M, Kiguchi T, Kusume T, Tamada T (1996) Complete nucleotide sequence of the Japanese isolate S of Beet necrotic yellow vein virus RNA and comparison with European isolates. Arch Virol 141:2163–2175CrossRefGoogle Scholar
  35. Sohi H, Maleki M (2004) Evidence for presence of types A and B of Beet necrotic yellow vein virus (BNYVV) in Iran. Virus Genes 29:353–358CrossRefGoogle Scholar
  36. Stas A, Meunier A, Schmit JF, Bragard C (2001) First report of Beet virus Q in Belgium. Plant Dis 85:1288–1288CrossRefGoogle Scholar
  37. Tahiri A, Akallouf K, Chofqui M (2010) Cartographie de la rhizomanie sur betterave sucrière dans le périmètre du Tadla pendant les deux campagnes agricoles 07–08 et 08–09. Proceedings du Septième Congrès de l’Association Marocaine de Protection des Plantes, Mai 2010, Rabat, Maroc 21–26Google Scholar
  38. Tamada T (1975) Beet necrotic yellow vein virus. CMI/AAB Descriptions of plant viruses, 144Google Scholar
  39. Tamada T (1999) Benyviruses. In: Webster RG, Granoff A (eds) Encyclopedia of virology, 2nd edn. Academic Press, London, UK, pp 154–160CrossRefGoogle Scholar
  40. Tamada T, Shirako Y, Abe H, Saito M, Kigushi T, Harada T (1989) Production and pathogenicity of isolates of Beetnecrotic yellow vein virus with different numbers of RNA components. J Gen Virol 70:3399–3409CrossRefGoogle Scholar
  41. 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 Acids Res 22(22):4673–4680CrossRefGoogle Scholar
  42. Turina M, Resca R, Rubies-Autonell C (1996) Surveys of soilborne virus diseases of sugar beet in Italy. Proceedings of the 3rd symposium of the international working group on plant viruses with fungal Vectors, Dundee 1996, pp 121–124Google Scholar
  43. Wauters A (2004) IRBAB: Explosion de la rhizomanie en 2004: plus de 50% des champs contaminés? Le Betteravier:7-9Google Scholar
  44. Weiland JJ, Van Winkle D, Edwards MC, Larson RL, Shelver WL, Freeman TP, Liu HY (2007) Characterization of a U.S. isolate of Beet black scorch virus. Phytopathology 97:1245–1254CrossRefGoogle Scholar
  45. Whitney ED, Duffus IE (1995) Rhizomania (Beet Necrotic Yellow Vein Virus). Compendium of beet diseases and insects. The American Phytopathological Society, St. Paul, pp 29–30Google Scholar
  46. Wisler GC, Liu HY, Duffus JE (1994) Beet necrotic yellow vein virus and its relationship to eight sugar beet furo-like viruses from the United States. Plant Dis 78:995–1001CrossRefGoogle Scholar
  47. Wisler GC, Lewellen RT, Sears JL, Wasson JW, Liu H-Y, Wintermantel WM (2003) Interactions between Beet necrotic yellow vein virus and Beet soil-borne mosaic virus in sugar beet. Plant Dis 87:1170–1175CrossRefGoogle Scholar

Copyright information

© Società Italiana di Patologia Vegetale (S.I.Pa.V.) 2018

Authors and Affiliations

  1. 1.Phytopathology Unit, Department of Plant ProtectionEcole Nationale d’Agriculture de MeknèsMeknèsMorocco
  2. 2.Faculty of Sciences, Department of BiologyMoulay Ismail UniversityMeknesMorocco

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