European Journal of Plant Pathology

, Volume 142, Issue 2, pp 319–330 | Cite as

Stemphylium sp., the cause of yellow leaf spot disease in sugar beet (Beta vulgaris L.) in the Netherlands

  • B. Hanse
  • E. E. M. Raaijmakers
  • A. H. L. Schoone
  • P. M. S. van Oorschot


During the summer of 2007, a distinctive type of yellow leaf spot was observed for the first time in sugar beet (Beta vulgaris L.) in the Netherlands. In the following years a rapid spread over all regions of the Netherlands was reported. The infestation appears in June-August on the leaves of sugar beet and starts with small, irregular, yellow spots. Subsequently the yellow spots become necrotic from the centre of the lesion outward, with the tissue becoming brown (or brownish). The spots spread over the leaves and infest all the leaves of the plant. Due to the loss of leaves the size of the canopy declines and yield loss occurs. Research was conducted to identify the causal agent. Climate room trials with isolates obtained from infested sugar beet leaves showed that Stemphylium sp. was able to infest leaves of healthy growing sugar beet plants with brown spots, similar to the necrotic spots seen in the field. From the leaf spots in the climate room trials, Stemphylium sp. was re-isolated, according to Koch’s postulates. Thus, it was confirmed that this Stemphylium sp. is a primary pathogen for sugar beet. In field trials of fungicide efficacy a sugar yield loss of up to 42 % (a financial yield loss of 51 %) was found. Field trials show that it is hard to control this Stemphylium sp. with the fungicides registered for sugar beet in the Netherlands and efficacy of control of Stemphylium sp. differs between fungicides with active ingredients belonging to the same chemical class. In addition to sugar beet, potato (Solanum tuberosum L.), white mustard (Sinapsis alba L.), red beet (Beta vulgaris L.), spinach (Spinacia oleracea L.) and fat hen (Chenopodium album L.) were identified as hosts in an assay of plants grown and inoculated in climate rooms.


Stemphylium Sugar beet Yield loss Fungicide efficacy Emerging pathogens 


  1. Aly, A. H., Debbab, A., Edrada-Ebel, R. A., Müller, W. E. G., Kubbutat, M. H. G., Wray, V., et al. (2010). Protein kinase inhibitors and other cytotoxic metabolites from the fungal endophyte Stemphylium botryosum isolated from Chenopodium album. Mycosphere, 1(2), 153–162.Google Scholar
  2. Aly, A. H., Debbab, A., & Proksch, P. (2011). Fungal endophytes: unique plant inhabitants with great promises. Applied Microbiology and Biotechnology, 90(6), 1829–1845. doi: 10.1007/s00253-011-3270-y.CrossRefPubMedGoogle Scholar
  3. Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R., & Daszk, P. (2004). Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution, 19(10), 535–544.CrossRefGoogle Scholar
  4. Barbetti, M. J. (1985). Survey of fungi associated with subterranean clover leaves and petioles in Western Australia. Plant Pathology, 34(1), 49–53. doi: 10.1111/j.1365-3059.1985.tb02759.x.CrossRefGoogle Scholar
  5. Bolton, M. D., Rivera-Varas, V., del Río Mendoza, L. E., Khan, M. F. R., & Secor, G. A. (2012). Efficacy of variable tetraconazole rates against Cercospora beticola isolates with differing in vitro sensitivities to DMI fungicides. Plant Disease, 96(12), 1749–1756. doi: 10.1094/pdis-03-12-0255-re.CrossRefGoogle Scholar
  6. Bolton, M. D., Rivera, V., & Secor, G. (2013). Identification of the G143A mutation associated with QoI resistance in Cercospora beticola field isolates from Michigan, United States. Pest Management Science, 69(1), 35–39. doi: 10.1002/ps.3358.CrossRefPubMedGoogle Scholar
  7. Bornemann, K., Hanse, B., Varrelmann, M., & Stevens, M. (2014). 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 Pathology. doi: 10.1111/ppa.12249.Google Scholar
  8. Bugbee, W. (1995). Cercospora beticola tolerant to triphenyltin hydroxide. Journal of Sugar Beet Research, 32(4), 167–174.CrossRefGoogle Scholar
  9. Bugbee, W. (1996). Cercospora beticola strains from sugar beet tolerant to triphenyltin hydroxide and resistant to thiophanate methyl. Plant Disease, 80(1), 103.CrossRefGoogle Scholar
  10. Câmara, M. P. S., O’Neill, N. R., & van Berkum, P. (2002). Phylogeny of Stemphylium spp. based on ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia, 94(4), 660–672.CrossRefPubMedGoogle Scholar
  11. Clark, M. F., & Adams, A. N. (1977). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475–483.CrossRefPubMedGoogle Scholar
  12. Debbab, A., Aly, A. H., Edrada-Ebel, R., Wray, V., Müller, W. E. G., Totzke, F., et al. (2009). Bioactive metabolites from the endophytic fungus Stemphylium globuliferum isolated from Mentha pulegium. Journal of Natural Products, 72(4), 626–631. doi: 10.1021/np8004997.CrossRefPubMedGoogle Scholar
  13. Devonshire, A. L., Field, L. M., Foster, S. P., Moores, G. D., Williamson, M. S., & Blackman, R. (1998). The evolution of insecticide resistance in the peach–potato aphid, Myzus persicae. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 353(1376), 1677–1684.CrossRefPubMedCentralGoogle Scholar
  14. Directive 2009/128/EC. (2009). Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Official Journal of the European Union, 309, 71–86.Google Scholar
  15. Everts, K. L., & Armentrout, D. K. (2001). Report of leaf spot of spinach caused by Stemphylium botryosum in Maryland and Delaware. Plant Disease, 85(11), 1209–1209. doi: 10.1094/pdis.2001.85.11.1209b.CrossRefGoogle Scholar
  16. Farr, D. F., Bills, G. F., Chamuris, G. P., & Rossman, A. Y. (1989). Fungi on plant and plant products in the United States. St. Paul Minnesota USA: APS Press.Google Scholar
  17. FRAC (2014). FRAC Code List 2014: Fungicides sorted by mode of action (including FRAC Code numbering), Fungicide Resistance Action Committee, Accessed 9-10-2014 2014.
  18. Gado, E. A. M. (2007). Management of Cercospora leaf spot disease of sugar beet plants by some fungicides and plant extracts. Egyptian Journal of Phytopathology, 35(2), 1–10.Google Scholar
  19. Georgopoulos, S., & Dovas, C. (1973). A serious outbreak of strains of Cercospora beticola resistant to benzimidazole fungicides in Northern Greece. Plant Disease Report, 57(4), 321–324.Google Scholar
  20. Giannopolitis, C. (1978). Occurrence of strains of Cercospora beticola resistant to triphenyltin fungicides in Greece. Plant Disease Report, 62(3), 205–208.Google Scholar
  21. Hanse, B., Schneider, J. H. M., Termorshuizen, A. J., & Varrelmann, M. (2011). Pests and diseases contribute to sugar beet yield difference between top and averagely managed farms. Crop Protection, 30(6), 671–678. doi: 10.1016/j.cropro.2011.02.018.CrossRefGoogle Scholar
  22. Horsfield, A., Wicks, T., Davies, K., Wilson, D., & Paton, S. (2010). Effect of fungicide use strategies on the control of early blight (Alternaria solani) and potato yield. Australasian Plant Pathology, 39(4), 368–375. doi: 10.1071/ap09090.CrossRefGoogle Scholar
  23. Inderbitzin, P., Mehta, Y. R., & Berbee, M. L. (2009). Pleospora species with Stemphylium anamorphs: a four locus phylogeny resolves new lineages yet does not distinguish among species in the Pleospora herbarum clade. Mycologia, 101(3), 329–339.CrossRefPubMedGoogle Scholar
  24. International Commission for Uniform Methods of Sugar Analysis. (2007). Methods book 2007. Berlin, Germany: Verlag Dr. Albert Bartens KG.Google Scholar
  25. Karaoglanidis, G. S., & Bardas, G. (2006). Control of benzimidazole- and DMI-resistant strains of Cercospora beticola with strobilurin fungicides. Plant Disease, 90, 419–424.CrossRefGoogle Scholar
  26. Karaoglanidis, G. S., & Thanassoulopoulos, C. C. (2003). Cross-resistance patterns among sterol biosynthesis inhibiting fungicides (SBIs) in Cercospora beticola. European Journal of Plant Pathology, 109(9), 929–934. doi: 10.1023/B:EJPP.0000003672.36076.8a.CrossRefGoogle Scholar
  27. Koenig, R., Loss, S., Specht, J., 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. Journal of General Virology, 90(3), 759–763. doi: 10.1099/vir. 0.007112-0.CrossRefPubMedGoogle Scholar
  28. Köhl, J., Groenenboom-de Haas, B., Goossen-van de Geijn, H., Speksnijder, A., Kastelein, P., Hoog, S., et al. (2009). Pathogenicity of Stemphylium vesicarium from different hosts causing brown spot in pear. European Journal of Plant Pathology, 124(1), 151–162. doi: 10.1007/s10658-008-9402-2.CrossRefGoogle Scholar
  29. Koike, S. T., Henderson, D. M., & Butler, E. E. (2001). Leaf spot disease of spinach in California caused by Stemphylium botryosum. Plant Disease, 85(2), 126–130. doi: 10.1094/pdis.2001.85.2.126.CrossRefGoogle Scholar
  30. Larran, S., Mónaco, C., & Alippi, H. E. (2000). Endophytic fungi in beet (Beta vulgaris var. esculenta L.) leaves. Advances in Horticultural Science, 14(4), 193–196. doi: 10.1400/14064.Google Scholar
  31. 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(5), 464–468. doi: 10.1094/PD-89-0464.CrossRefGoogle Scholar
  32. Oerke, E. C., & Dehne, H. W. (2004). Safeguarding production—losses in major crops and the role of crop protection. Crop Protection, 23(4), 275–285. doi: 10.1016/j.cropro.2003.10.001.CrossRefGoogle Scholar
  33. Pasche, J. S., Wharam, C. M., & Gudmestad, N. C. (2004). Shift in sensitivity of Alternaria solani in response to QoI fungicides. Plant Disease, 88(2), 181–187. doi: 10.1094/pdis.2004.88.2.181.CrossRefGoogle Scholar
  34. Pautasso, M., Döring, T. F., Garbelotto, M., Pellis, L., & Jeger, M. J. (2012). Impacts of climate change on plant diseases—opinions and trends. European Journal of Plant Pathology, 133(1), 295–313. doi: 10.1007/s10658-012-9936-1.CrossRefGoogle Scholar
  35. Payne, R., Murray, D., Harding, S., Baird, D., & Soutar, D. (2013). Introduction to GenStat for windows (16th ed.). Hemel Hempstead, UK: VSN International Ltd.Google Scholar
  36. Pferdmenges, F., Korf, H., & Varrelmann, M. (2009). 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, 124(1), 31–43. doi: 10.1007/s10658-008-9388-9.CrossRefGoogle Scholar
  37. Ruppel E., Scott P. (1974). Strains of Cercospora beticola resistant to benomyl in the USA. Plant Disease Reporter. Google Scholar
  38. Samac, D. A., Halfman, B., Jensen, B., Brietenbach, F., Behnken, L., Willbur, J., et al. (2013). Evaluating headline fungicide on alfalfa production and sensitivity of pathogens to pyraclostrobin. Plant Health Progress. doi: 10.1094/PHP-2013-0917-01-RS.Google Scholar
  39. Samac, D. A., Willbur, J., Behnken, L., Brietenbach, F., Blonde, G., Halfman, B., et al. (2014). First report of Stemphylium globuliferum causing Stemphylium leaf spot on alfalfa (Medicago sativa) in the United States. Plant Disease, 98(7), 993–993. doi: 10.1094/pdis-08-13-0828-pdn.CrossRefGoogle Scholar
  40. Sawicki, R. M., Devonshire, A. L., Rice, A. D., Moores, G. D., Petzing, S. M., & Cameron, A. (1978). The detection and distribution of organophosphorus and carbamate insecticide-resistant Myzus persicae (Sulz.) in Britain in 1976. Pesticide Science, 9(3), 189–201.CrossRefGoogle Scholar
  41. Secor, G. A., Rivera, V. V., Khan, M. F. R., & Gudmestad, N. C. (2010). Monitoring fungicide sensitivity of Cercospora beticola of sugar beet for disease management decisions. Plant Disease, 94(11), 1272–1282. doi: 10.1094/pdis-07-09-0471.CrossRefGoogle Scholar
  42. Uchino, H. H., Kanzawa, K. K., & Ui, T. T. (1986). Stemphylium leaf spot of sugar beet. Annals of the Phytopathological Society of Japan, 52(1), 31–38.CrossRefGoogle Scholar
  43. Van Welsenes, C. H. R. (1973). Farming problems and farming principles in the Dutch fen-colonies. Tijdschrift voor Economische en Sociale Geografie, 64(4), 218–225. doi: 10.1111/j.1467-9663.1973.tb00086.x.CrossRefGoogle Scholar
  44. Vereijssen, J., Schneider, J. H. M., & Jeger, M. J. (2007). Supervised control of Cercospora leaf spot in sugar beet. Crop Protection, 26(1), 19–28. doi: 10.1016/j.cropro.2006.03.012.CrossRefGoogle Scholar
  45. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. Innis, D. H. Gelfand, J. J. Snisky, & T. J. White (Eds.), PCR protocols: a guide to methods andapplications (pp. 315–322). New York: Academic.CrossRefGoogle Scholar
  46. Woudenberg, J. H. C., Meijer, M. (2014). Identification Stemphylium sp. Personal communication to B. Hanse on 19 September 2014.Google Scholar
  47. Zheng, L., Lv, R., Hsiang, T., & Huang, J. (2009). Host range and phytotoxicity of Stemphylium solani, causing leaf blight of garlic (Allium sativum) in China. European Journal of Plant Pathology, 124(1), 21–30. doi: 10.1007/s10658-008-9387-x.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2015

Authors and Affiliations

  • B. Hanse
    • 1
  • E. E. M. Raaijmakers
    • 1
  • A. H. L. Schoone
    • 1
  • P. M. S. van Oorschot
    • 1
  1. 1.IRSBergen op ZoomThe Netherlands

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