Skip to main content
Log in

Emergence of new virulence phenotypes of Plasmodiophora brassicae on canola (Brassica napus) in Alberta, Canada

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

Abstract

Clubroot, caused by Plasmodiophora brassicae, is an important soilborne disease of canola (Brassica napus) in Alberta, Canada. Genetic resistance is the most effective clubroot management tool, and resistant cultivars are grown extensively in affected regions. In 2013, relatively severe symptoms of clubroot were observed in some fields of resistant canola. In greenhouse tests, four populations of P. brassicae from two of these fields caused significantly increased levels of clubroot on the cultivars from which they had been first recovered; these included three populations (L-G1, L-G2 and L-G3) recovered from the cultivar ‘L135C’, and one population (D-G3) recovered from ‘D3152’. Further testing showed that L-G1, L-G2 and L-G3 were highly virulent on a suite of six resistant canola cultivars (‘45H29’, ‘D3152’, ‘74–47CR’, ‘1960’, ‘L135C’ and ‘6056CR’) representing a cross-section of products available in Canada, while a seventh cultivar (‘9558c’) was moderately resistant to moderately susceptible. Bioassays of field soil with a dozen clubroot-resistant host genotypes confirmed that in most cases, resistance was no longer effective. Host responses to the population D-G3 were more variable, with most cultivars developing intermediate levels of disease. All four P. brassicae populations were classified as pathotypes 5, P3 and 16/6/8 on the differentials of Williams, Somé et al., and the European Clubroot Differential set. The pathotype classifications, however, do not reflect the increased virulence of these populations on clubroot-resistant canola. The identification of new virulence phenotypes of P. brassicae capable of overcoming genetic resistance underscores the need for increased stewardship of resistance sources.

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.

Similar content being viewed by others

References

  • Buczacki, S. T., Toxopeus, H., Johnston, T. D., Dixon, G. R., & Holboth, L. A. (1975). Study of physiologic specialization in Plasmodiophora brassicae: proposals for attempted rationalization through an international approach. Transactions of the British Mycological Society, 65, 295–303.

    Article  Google Scholar 

  • Cao, T., Manolii, V. P., Hwang, S. F., Howard, R. J., & Strelkov, S. E. (2009). Virulence and spread of Plasmodiophora brassicae [clubroot] in Alberta, Canada. Canadian Journal of Plant Pathology, 31, 321–329.

    Article  Google Scholar 

  • Chittem, K., Mansouripour, S. M., & del Río Mendoza, L. E. (2014). First report of clubroot on canola caused by Plasmodiophora brassicae in North Dakota. Plant Disease, 98, 1438.

    Article  Google Scholar 

  • Diederichsen, E., Frauen, M., Linders, E. G. A., Hatakeyama, K., & Hirai, M. (2009). Status and perspectives of clubroot resistance breeding in crucifer crops. Journal of Plant Growth Regulation, 28, 265–281.

    Article  CAS  Google Scholar 

  • Diederichsen, E., Frauen, M., & Ludwig-Müller (2014). Clubroot disease management challenges from a German perspective. Canadian Journal of Plant Pathology, 36(S1), 85–98.

    Article  Google Scholar 

  • Dixon, G. R. (2006). The biology of Plasmodiophora brassicae Wor. – A review of recent advances. Acta Horticulturae, 706, 271–282.

    Article  Google Scholar 

  • Dixon, G. R. (2009). The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation, 28, 194–202.

    Article  CAS  Google Scholar 

  • Dokken-Bouchard, F. L., Anderson, K., Bassendowski, K. A., Bouchard, A., Brown, B., et al. (2012). Survey of canola diseases in Saskatchewan, 2011. Canadian Plant Disease Survey, 92, 125–129.

    Google Scholar 

  • Donald, E. C. & Porter, I. J. (2014). Clubroot in Australia: the history and impact of Plasmodiophora brassicae in Brassica crops and research efforts directed towards its control. Canadian Journal of Plant Pathology, 36(S1), 66–84.

    Article  Google Scholar 

  • Gossen, B. D., Adhikari, K. K. C., & McDonald, M. R. (2012). Effect of seeding date on development of clubroot in vegetable Brassica crops. Canadian Journal of Plant Pathology, 34, 516–523.

    Article  Google Scholar 

  • Gowers, S. (1982). The transfer of characters from Brassica campestris L. to Brassica napus L.: production of clubroot-resistant oilseed rape (B. napus ssp. oleifera). Euphytica, 31, 971–976.

    Article  Google Scholar 

  • Gulden, R. H., Shirtliffe, S. J., & Thomas, A. G. (2003). Secondary seed dormancy prolongs persistence of volunteer canola in western Canada. Weed Science, 51, 904–913.

    Article  CAS  Google Scholar 

  • Hatakeyama, K., Fujimura, M., Ishida, M., Suzuki, T., & Sato, T. (2006). Classification of pathogenicity of Plasmodiophora brassicae field isolates in Japan based on resistance of F1 cultivars of Chinese cabbage (Brassica rapa L.) to clubroot. Acta Horticulturae, 706, 323–328.

    Article  Google Scholar 

  • Hirai, M. (2006). Genetic analysis of clubroot resistance in Brassica crops. Breeding Science, 56, 223–229.

    Article  Google Scholar 

  • Horiuchi, S. & Hori, M. (1980). A simple greenhouse technique for obtaining high levels of clubroot incidence. Bulletin of the Chugoku National Agricultural Experiment Station: Series E, 17, 33–55.

    Google Scholar 

  • Howard, R. J., Strelkov, S. E., & Harding, M. W. (2010). Clubroot of cruciferous crops – new perspectives on an old disease. Canadian Journal of Plant Pathology, 32, 43–57.

    Article  Google Scholar 

  • Hwang, S. F., Ahmed, H. U., Zhou, Q., Rashi, A., Strelkov, S. E., et al. (2013). Effect of susceptible and resistant canola plants on Plasmodiophora brassicae resting spore populations in the soil. Plant Pathology, 62, 404–412.

    Article  Google Scholar 

  • Hwang, S. F., Howard, R. J., Strelkov, S. E., Gossen, B. D., & Peng, G. (2014). Management of clubroot (Plasmodiophora brassicae) on canola (Brassica napus) in western Canada. Canadian Journal of Plant Pathology, 36(S1), 49–65.

    Article  Google Scholar 

  • Kuginuki, Y., Hiroaki, Y., & Hirai, M. (1999). Variation in virulence of Plasmodiophora brassicae in Japan tested with clubroot-resistant cultivars of Chinese cabbage (Brassica rapa L. spp. pekinensis). European Journal of Plant Pathology, 105, 327–332.

    Article  Google Scholar 

  • LeBoldus, J. M., Manolii, V. P., Turkington, T. K., & Strelkov, S. E. (2012). Adaptation to Brassica host genotypes by a single-spore isolate and population of Plasmodiophora brassicae [clubroot]. Plant Disease, 96, 833–838.

    Article  Google Scholar 

  • Murakami, H., Tshushima, S., Kuroyagani, Y., & Shishido, Y. (2002). Reduction in resting spore density of Plasmodiophora brassicae and clubroot severity by liming. Soil Science & Plant Nutrition, 48, 685–691.

    Article  CAS  Google Scholar 

  • Osaki, K., Tanaka, S., & Ito, S. (2004). A case of breakdown in clubroot-resistant cultivars of Chinese cabbage. Japanese Journal of Phytopathology, 70, 66.

    Google Scholar 

  • Oxley, S. (2007). Clubroot disease of oilseed rape and other brassica crops. Technical Note 602. Edinburgh: Scottish Agricultural College.

    Google Scholar 

  • Peng, G., Lahlali, R., Hwang, S. F., Pageau, D., Hynes, R. K., et al. (2014). Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Canadian Journal of Plant Pathology, 36(S1), 99–112.

    Article  Google Scholar 

  • Rahman, H., Peng, G., Yu, F., Falk, K. C., Kulkarni, M., & Selvaraj, G. (2014). Genetics and breeding for clubroot resistance in Canadian spring canola (Brassica napus L.). Canadian Journal of Plant Pathology, 36(S1), 122–134.

    Article  Google Scholar 

  • Rempel, C. B., Hutton, S. N., & Jurke, C. J. (2014). Clubroot and the importance of canola in Canada. Canadian Journal of Plant Pathology, 36(S1), 19–26.

    Article  Google Scholar 

  • Rennie, D. C., Holtz, M. D., Turkington, T. K., Leboldus, J. M., et al. (2015). Movement of Plasmodiophora brassicae resting spores in windblown dust. Canadian Journal of Plant Pathology, 37, 188–196.

    Article  Google Scholar 

  • Seaman, W. L., Walker, J. C., & Larson, R. (1963). A new race of Plasmodiophora brassicae affecting Badger shipper cabbage. Phytopathology, 53, 1426–1429.

    Google Scholar 

  • Somé, A., Manzanares, M. J., Laurens, F., Baron, F., Thomas, G., & Rouxel, F. (1996). Variation for virulence on Brassica napus L. amongst Plasmodiophora brassicae collections from France and derived single-spore isolates. Plant Pathology, 45, 432–439.

    Article  Google Scholar 

  • Strelkov, S. E. & Hwang, S. F. (2014). Clubroot in the Canadian canola crop: 10 years into the outbreak. Canadian Journal of Plant Pathology, 36(S1), 27–36.

    Article  Google Scholar 

  • Strelkov, S. E., Tewari, J. P., & Smith-Degenhardt, E. (2006). Characterization of Plasmodiophora brassicae populations from Alberta, Canada. Canadian Journal of Plant Pathology, 28, 467–474.

    Article  Google Scholar 

  • Strelkov, S. E., Hwang, S. F., Howard, R. J., Hartman, M., & Turkington, T. K. (2011). Progress towards the sustainable management of clubroot [Plasmodiophora brassicae] of canola on the Canadian prairies. Prairie Soils and Crops, 4, 114–121.

    Google Scholar 

  • Strelkov, S. E., Manolii, V. P., Harding, M. W., Hwang, S. F., Poscente, N., et al. (2014). The occurrence of clubroot on canola in Alberta in 2013. Canadian Plant Disease Survey, 94, 158–161.

    Google Scholar 

  • Strelkov, S. E., Manolii, V. P., Harding, M. W., Hwang, S. F., Fei, W., et al. (2015). The spread of clubroot on canola in Alberta in 2014. Canadian Plant Disease Survey, 95, 155–158.

    Google Scholar 

  • Tanaka, S. & Ito, S. (2013). Pathogenic and genetic diversity in Plasmodiophora brassicae (clubroot) from Japan. Journal of General Plant Pathology, 79, 297–306.

    Article  Google Scholar 

  • Tewari, J. P., Strelkov, S. E., Orchard, D., Hartman, M., Lange, R. M., & Turkington, T. K. (2005). Identification of clubroot disease of crucifers on canola (Brassica napus) in Alberta. Canadian Journal of Plant Pathology, 27, 143–144.

    Article  Google Scholar 

  • Wallenhammar, A. C. (1996). Prevalence of Plasmodiophora brassicae in a spring oilseed rape growing area in central Sweden and factors influencing soil infestation levels. Plant Pathology, 45, 710–719.

    Article  Google Scholar 

  • Webster, M. A. & Dixon, G. R. (1991). Calcium, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae. Mycological Research, 95, 64–73.

    Article  CAS  Google Scholar 

  • Williams, P. H. (1966). A system for the determination of races of Plasmodiophora brassicae that infect cabbage and rutabaga. Phytopathology, 56, 624–626.

    Google Scholar 

  • Xue, S., Cao, T., Howard, R. J., Hwang, S. F., & Strelkov, S. E. (2008). Isolation and variation in virulence of single spore isolates of Plasmodiophora brassicae from Canada. Plant Disease, 92, 456–462.

    Article  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the financial support provided by the Alberta Crop Industry Development Fund Ltd., the Canola Agronomic Research Program, the Growing Forward 2 Program (Agriculture and Agri-Food Canada/Canola Council of Canada), and the provincial canola grower groups including the Alberta Canola Producers Commission, SaskCanola, and the Manitoba Canola Growers Association. The assistance of Canola Council of Canada agronomists and cooperating farmers also is gratefully acknowledged, as is the technical assistance of G. Turnbull, Q. Zhou (Alberta Agriculture and Forestry), and several summer students.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen E. Strelkov.

Additional information

Submitted for Inclusion in the Special Issue on Clubroot Disease of Crucifers

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Strelkov, S.E., Hwang, SF., Manolii, V.P. et al. Emergence of new virulence phenotypes of Plasmodiophora brassicae on canola (Brassica napus) in Alberta, Canada. Eur J Plant Pathol 145, 517–529 (2016). https://doi.org/10.1007/s10658-016-0888-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-016-0888-8

Keywords

Navigation