Plant Protect. Sci., 2016, 52(2):71-86 | DOI: 10.17221/87/2015-PPS

Clubroot caused by Plasmodiophora brassicae Wor.: a review of emerging serious disease of oilseed rape in the Czech RepublicReview

Veronika Řičařová, Jan Kazda, Khushwant Singh, Pavel Ryšánek
Department of Plant Protection, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic

Winter oilseed rape is the second most frequently grown crop in the Czech Republic. Clubroot, caused by Plasmodiophora brassicae (Wor.), was previously a problem in production of vegetable. The disease has been spreading on winter rape (Brassica napus L.) over the past four years. Infected stands were reported throughout the country in autumn 2011. The pathogen is probably widely spread in the whole country, its incidence depends on suitable weather conditions. Every field with clubroot is considered as contaminated for many years. The amounts of inoculum and its distribution are not sufficient yet, but this is just the initial stage of colonisation. There is a similar situation resembling experiences from other countries (Canada, Germany) where clubroot has gradually expanded in the last 15 years.

Keywords: winter oilseed rape; Brassica napus L.; clubroot disease; biology; pathopypes; resistance

Published: June 30, 2016  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Řičařová V, Kazda J, Singh K, Ryšánek P. Clubroot caused by Plasmodiophora brassicae Wor.: a review of emerging serious disease of oilseed rape in the Czech Republic. Plant Protect. Sci. 2016;52(2):71-86. doi: 10.17221/87/2015-PPS.
Download citation

References

  1. Abbasi P.A., Lazarovits G. (2006a): Reduction in the incidence and severity of clubroot caused by Plasmodiophora brassicae on bok choy and cabbage with soil applications of AG3 phosphonate. Canadian Journal of Plant Pathology, 28: 342-371.
  2. Abbasi P.A., Lazarovits G. (2006b): Effect of soil application of AG3 phosphonate on the severity of clubroot of bok choy and cabbage caused by Plasmodiophora brassicae. Plant Disease, 90: 1517-1522. Go to original source... Go to PubMed...
  3. Ahmed H.U., Hwang S. F., Strelkov S.E., Gossen B.D., Peng G., Howard R.J., Turnbull G. (2010): Assessment of bait crops to reduce inoculum of clubroot (Plasmodiophora brassicae) of canola. Canadian Journal of Plant Science, 91: 545-551. Go to original source...
  4. Ahn J.C., Kim D.W., You Y.N., Seok M.S., Park J.M., Hwang H., Kim B.G., Luan S., Park H.S., Cho H.S. (2010): Classification of rice (Oryza sativa L. japonica nipponbare) immunophilins (FKBPs, CYPs) and expression patterns under water stress. BMC Plant Biology, 10: 253-275. Go to original source... Go to PubMed...
  5. Ando S., Yamada T., Asano T., Kamachi S., Tsushima S., Hagio T., Tabei Y. (2006): Molecular cloning of PbSTKL1 gene from Plasmodiophora brassicae expressed during club root development. Journal of Phytopathology, 154: 185-189. Go to original source...
  6. Aviezer-Hagai K., Skovorodnikova J., Galigniana M. (2007): Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 doi: 10.17221/87/2015-PPS(AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Molecular Biology, 63: 237-255. Go to original source... Go to PubMed...
  7. Ayers G.W. (1944): Studies on the life history of the club root organism, Plasmodiophora brassicae. Canadian Journal of Research, 23: 143-149. Go to original source...
  8. Bhattacharya T.K., Mandal N.C. (2006): Management of clubroot (Plasmodiophora brassicae) of rapeseed and mustard by nitrogenous fertilisers. Annals of Plant Protection Sciences, 14: 260-261.
  9. Brodmann A., Schuller A., Ludwig-Muller J., Aeschbacher R.A., Wiemken A., Boller T., Wingler A. (2002): Induction of trehalase in Arabidopsis plants infected with the trehalose producing pathogen Plasmodiophora brassicae. Molecular Plant-Microbe Interaction, 15: 693-700. Go to original source... Go to PubMed...
  10. Buczacki S.T., Toxopeus H., Mattusch P., Johnston T.D., Dixon G.R., Hobolth L.A. (1975): Study of physiologic specialization in Plasmodiophora brassicae: Proposals for attempted rationalization through an international approach. Transaction of British Mycological Society, 65: 295-303. Go to original source...
  11. Bulman S., Siemens J., Ridgway H.J., Conner A.J. (2006): Identification of genes from the obligate intracellular plant pathogen, Plasmodiophora brassicae. FEMS Microbiology Letters, 264: 198-204. Go to original source... Go to PubMed...
  12. Bulman S., Ridgway H.J., Eady C., Conner A.J. (2007): Intron-rich gene structure in the intracellular plant parasite Plasmodiophora brassicae. Protist, 158: 423-433. Go to original source... Go to PubMed...
  13. Burki F., Keeling P.J. (2014): Rhizaria. Current Biology. 24: R103-R107. Go to original source... Go to PubMed...
  14. Cao T., Tewari J.P., Strelkov S.E. (2007). Molecular detection of Plasmodiophora brassicae, causal agent of clubroot of crucifers, in plant and soil. Plant Disease, 91: 80-87. Go to original source... Go to PubMed...
  15. Cavalier-Smith T., Chao E.E. (2003): Phylogeny and classification of phylum Cercozoa (Protozoa). Protist, 154: 341-358. Go to original source... Go to PubMed...
  16. Chee H.Y., Kim W.G., Cho W.D., Jee H.J., Choi Y.C. (1998): Detection of Plasmodiophora brassicae by using polymerase chain reaction. Korea Journal of Plant Pathology, 14: 589-593.
  17. Chiang M.S., Crête R. (1983): Transfer of resistance to race 2 of Plasmodiophora brassicae from Brassica napus to cabbage (B. oleracea sp. capitata). V. The inheritance of resistance. Euphytica, 32: 479-483. Go to original source...
  18. Chytilová V., Dušek K. (2007): Metodika testováni odolnosti brukvovitých plodin k nádorovitosti. Metodika pro praxi. Praha, Výzkumný ústav rostlinné výroby.
  19. Colhoun J. (1953): Observations on the incidence of club root disease of Brassicae in limed soils in relation to temperature. Annals of Applied Biology, 40: 639-644. Go to original source...
  20. Colhoun J. (1958): Club Root Disease of Crucifers Caused by Plasmodiophora brassicae Woron. A Monograph. Phytopathological Paper No 3. Surrey, Commonwealth Mycological Institute.
  21. Crute I.R., Gray A.R., Crisp P., Buczacki S.T. (1980): Variation in Plasmodiophora brassicae and resistance to clubroot disease in Brassicas and allied crops - a critical review. Plant Breeding Abstract, 50: 91-104.
  22. Deora A., Gossen B.D., McDonald M.R. (2013): Cytology of infection, development and expression of resistance to Plasmodiophora brassicae in canola. Annals of Applied Biology, 163: 56-71. Go to original source...
  23. Diederichsen E., Deppe U., Sacristán M.D. (2003): Characterization of clubroot resistance in recent winter oilseed rape material. In: Proceedings 11th International Rapeseed Congress, July 6-10, 2003, Copenhagen, Denmark: 68-70.
  24. Diederichsen E., Frauen M., Linders E.G.A., Hatakeyama K., Hirari M. (2009): Status and perspectives of clubroot resistance breeding in crucifer crops. Journal of Plant Growth Regulation, 28: 265-281. Go to original source...
  25. Diederichsen E., Frauen M., Ludwig-Müller J. (2014): Clubroot disease management challenges from a German perspective. Canadian Journal of Plant Pathology, 36: 85-98. Go to original source...
  26. Dixon G.R. (1991): Primary and secondary stages of Plasmodiophora brassicae (clubroot) as affected by metallic cations and pH. In: Beemster A.B., Bollen G.J., Gwerlagh, M., Ruissen M.A., Schippers B., Tempel A. (eds): Biotic Interactions and Soil-Borne Diseases, No. 23. Developments in Agricultural and Managed Forestry Ecology. Amsterdam, Elsevier: 381-386 Go to original source...
  27. Dixon G.R. (2009a): The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation, 28: 194-202. Go to original source...
  28. Dixon G.R. (2009b): Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation, 28: 212-228. Go to original source...
  29. Dixon G.R, Page L.V. (1998): Calcium and nitrogen eliciting alterations to growth and reproduction of Plasmodiophora brassicae (clubroot). Acta Horticulturae, 459: 343-349 Go to original source...
  30. Donald E.C., Jaudzems G., Porter I.J. (2008): Pathology of cortical invasion by Plasmodiophora brassicae in clubroot resistant and susceptible Brassicae oleracea. Plant Pathology, 57: 201-209. Go to original source...
  31. Einhorn G., Bochov H., Huber J., Krebs B. (1991): Methodological studies to detect antagonists of the clubroot pathogen Plasmodiophora brassicae Wor. Archives of Phytopathology and Plant Protection, 27: 205-208. Go to original source...
  32. Faggian R., Bulman S.R., Lawrie A.C., Porter I.J. (1999): Specific polymerase chain reaction primers for the detection of Plasmodiophora brassicae in soil and water. Phytopathology, 89: 392-397. Go to original source... Go to PubMed...
  33. Faggian R., Strelkov S.E. (2009): Detection and measurement of Plasmodiophora brassicae. Journal of Plant Growth Regulation, 28: 282-288. Go to original source...
  34. Fähling M., Graf H., Siemen J. (2003): Pathotype separation of Plasmodiophora brassicae by the host plant. Journal of Phytopathology, 151: 425-430. Go to original source...
  35. Feng J., Hwang R., Hwang S.F., Strelkov S.E., Gossen B.D., Zhou Q., Peng G. (2010): Molecular characterization of a serine protease Pro1 from Plasmodiophora brassicae that stimulates resting spore germination. Molecular Plant Pathology, 11: 503-512. Go to original source... Go to PubMed...
  36. Friberg H., Lagerlöf J., Rämert B. (2005): Germination of Plasmodiophora brassicae resting spores stimulated by a non-host plant. European Journal of Plant Pathology, 113: 275-281. Go to original source...
  37. Gossen B.D., McDonald M.R., Hwang S.F., Kalpana K.C. (2009): Manipulating seeding date to minimize clubroot (Plasmodiophora brassicae) damage in canola and vegetable Brassicas. Phytopathology, 99: S45 (Abstract).
  38. Gossen B.D., Adhikari K.K.C., McDonald M.R. (2012): Effects of temperature on infection and subsequent development of clubroot under controlled conditions. Plant Pathology, 61: 593-599. Go to original source...
  39. 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. Go to original source...
  40. Hwang S.F., Ahmed H.U., Strelkov S.E., Gossen B.D., Turnbull G.D., Peng G., Howard R.J. (2011a): Seedling age and inoculum density affect clubroot severity and seed yield in canola. Canadian Journal of Plant Science, 91: 183-190. Go to original source...
  41. Hwang S.F., Ahmed H.U., Zhou Q., Strelkov S.E., Gossen B.D., Peng G., Turnbull G.D. (2011b): Influence of cultivar resistance and inoculum concentration on root hair infection of canola (Brassica napus) by Plasmodiophora brassicae. Plant Pathology, 60: 820-829. Go to original source...
  42. Hwang S.F., Strelkov S.E., Feng J., Gossen B.D., Howard R.J. (2012): Plasmodiophora brassicae: a review of an emerging pathogen of the Canadian canola (Brassica napus) crop. Molecular Plant Pathology, 13: 105-113. Go to original source... Go to PubMed...
  43. 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 (Supl. 1): 49-65. Go to original source...
  44. Ingram D.S., Tommerup I.C. (1972): The life history of Plasmodiophora brassicaeWoron. Proceedings of the Royal Society of London, Ser. B., 180: 103-112. Go to original source...
  45. Ito S., Ichinose H., Yanagi C., Tanaka S., Kameya-Iwaki M., Kishi F. (1999): Identification of an in planta-induced mRNA of Plasmodiophora brassicae. Journal of Phytopathology, 147: 79-82. Go to original source...
  46. Jing H., Yang X., Zhang J., Liu X., Zheng H., Dong G., Nian J., Feng J., Xia B., Qian Q., Li J., Zuo J. (2015): Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling. Nature Communications, 6: Art. No. 7395. doi: 10.1038/ncomms8395 Go to original source... Go to PubMed...
  47. Jones D.R., Ingram D.S., Dixon G.R. (1982a): Characterization of isolates derived from single resting spores of Plasmodiophora brassicae and studies of their interaction. Plant Pathology, 31: 239-246. Go to original source...
  48. Jones D.R., Ingram D.S., Dixon G.R. (1982b): Factors affecting tests for differential pathogenicity in populations of Plasmodiophora brassicae. Plant Pathology, 31: 229-238. Go to original source...
  49. Karling J.S. (1968): The Plasmodiophorales. 2 nd Ed. New York, Hafner Publishing Co.
  50. Kazda J., Řičařová V., Prokinová E., Grimová L., Baranyk P. (2013): Nádorovitost kořenů brukvovitých ohrožuje ozimou řepku. Úroda, 2016 (6): 28-32.
  51. Kim C.H., Cho W.D., Kim H.M. (2000): Distribution of Plasmodiophora brassicae causing clubroot disease of Chinese cabbage in soil. Plant Disease Research 6: 27-32.
  52. Kirk P. (2014): Index Fungorum. Available at http://www.indexfungorum.org/Names/NamesRecord.asp?RecordID=214750 (accessed April 22, 2014).
  53. Kumari S., Joshi R., Singh K., Roy S., Tripathi A.K., Singh P., Singla-Pareek S.L., Pareek A. (2014): Expression of a cyclophilin OsCyp2-P isolated from a salt-tolerant landrace of rice in tobacco alleviates stress via ion homeostasis and limiting ROS accumulation. Functional and Integrative Biology, 15: 395-412. Go to original source... Go to PubMed...
  54. Lange L., Heide M., Hobolth L., Olson L.W. (1989): Serological detection of Plasmodiophora brassicae by dot immunobinding and visualization of the serological reaction by scanning electron microscopy. Phytopathology, 79: 1066-1071. Go to original source...
  55. Ludwig-Müller J., Prinsen E., Rolfe S., Scholes J. (2009): Metabolism and plant hormone action during the clubroot disease. Journal of Plant Growth Regulation, 28: 229-244. Go to original source...
  56. MacFarlane I. (1952): Factors affecting the survival of Plasmodiophora brassicae Wor. in the soil and its assessment by a host test. Annals of Applied Biology, 39: 239-256. Go to original source...
  57. MacFarlane I., Last F.T. (1957): Club root of cruciferous plants. Report of Rothamsted Experimental Station: 117-119.
  58. Manolii V.P., Strelkov S.E., Bansal V.K., Howard R.J. (2005): Liming and calcium fertiliser for clubroot control in canola (Brassica napus). Canadian Journal of Plant Pathology, 27: 472.
  59. Marivet J., Frendo P., Burkard G. (1992): Effects of abiotic stresses on cyclophilin gene expression in maize and bean and sequence analysis of cyclophilin cDNA. Plant Science, 84: 171-178. Go to original source...
  60. Meiri D., Tazat K., Cohen-Peer R. (2010): Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Molecular Biology, 72: 191-203. doi: 10.17221/87/2015-PPS Go to original source...
  61. Mellano H.M., Munnecke D.E., Endo R.M. (1970): Relationship of seedling age to development of Pythium ultimum on roots of Antirrhinum majus. Phytopathology, 60: 935-942. Go to original source...
  62. Moxham S.E., Buczacki S.T. (1983): Chemical composition of the resting spore wall of Plasmodiophora brassicae, Transaction of British Mycological Society, 80: 291-304. Go to original source...
  63. Murakami H., Tsushima S., Shishido Y. (2000): Soil suppressiveness to clubroot disease of Chinese cabbage caused by Plasmodiphora brassicae. Soil Biology and Biochemistry 32: 1637-1642. Go to original source...
  64. Naiki T., Dixon G.R. (1987): The effects of chemicals on developmental stages of Plasmodiophora brassicae (clubroot). Plant Pathology, 36: 316-327. Go to original source...
  65. Narisawa K., Shimura M., Usuki F., Fukuhara S., Hashiba T. (2005): Effects of pathogen density, soil moisture, and soil pH on biological control of clubroot in Chinese cabbage by Heteroconium chaetospira. Plant Disease, 89: 285-290. Go to original source... Go to PubMed...
  66. Neuhauser S., Kirchmair M., Gleason F.H. (2011): Ecological roles of the parasitic Phytomyxea (plasmodiophorids) in marine ecosystems - a review. Marine and Freshwater Research, 62: 365-371. Go to original source... Go to PubMed...
  67. Palm E.T. (1958): Effect of mineral nutrition on invasiveness of Plasmodiophora brassicae Wor. and the development of clubroot. Dissertation Abstracts, 19: 425-426.
  68. Palm E.T. (1963): Effect of mineral nutrition on the invasion and response of turnip tissue to P. brassicae Wor. Contributions from Thompson Institute, 22: 91-112.
  69. Page L.V. (2001): Studies of components for a potential integrated control system for Plasmodiophora brassicae. [PhD Thesis.] Glasgow, University of Strathclyde.
  70. Parlevliet J.E. (1985): Race and pathotype concepts in parasitic fungi. OEPP Bulletin, 15: 145-150. Go to original source...
  71. Peng G., Pageau., D, Strelkov S.E, Lahlali R., Hwang S.F., Hynes R.K. (2013): Assessment of crop rotation, cultivar resistance and Bacillus subtilis biofungicide for control of clubroot on canola. Acta Horticultrae, 1005: 591-598. Go to original source...
  72. Peng G., Lahlali R., Hwang S.F., Pageau D., Hynes R.K., McDonald M.R., Gossen B.D., Strelkov S.E. (2014): Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Canadian Journal of Plant Pathology, 36 (S1): 99-112. Go to original source...
  73. 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. Go to original source...
  74. Rennie D.C, Manolii V.P., Cao T., Hwang S.F., Howard R.J., Strelkov S.E. (2011): Direct evidence of surface infestation of seeds and tubers by Plasmodiophora brassicae and quantification of spore load. Plant Pathology, 60: 811-819. Go to original source...
  75. Ricarova V., Kaczmarek J., Strelkov S., Kazda J., Lueders W., Rysanek P., Manolii V., Jedryczka M. (2014): Pathotypes of Plasmodiophora brassicae damaging to oilseed rape in central Europe - the first report on the Czech and Polish situation. European Jounal of Plant Pathology (submited).
  76. Rod J. (1991): Výskyt a rozšíření patotypů nádorovitosti (Plasmodiophora brassicae Wor.) v Československu. In: Proceedings XII. Czechoslovak Plant Protection Conference, Sept 17-19, 1991, Prague, Czech Republic: 237-238.
  77. Rod J. (1994): The effect of some herbs on soil infestation with clubroot (Plasmodiophora brassicae Wor.). Ochrana rostlin, 30: 261-265.
  78. Rod J. (1996): Reports - Agent of clubroot of crucifer. Brno: ÚKZUZ, 37 (Special Issue): 1-45.
  79. Rod J., Robak J. (1994): The effect of some crops on inactivation of clubroot (Plasmodiophora brassicae Wor.) in soil. Ochrana rostlin, 30: 267-272.
  80. Sen P. (2005): Antagonistic effect of Ca, B and Mo on club-root disease of rape-mustard. Indian Agriculturist, 49(1/2): 13-16.
  81. Siemens J., Keller U., Sarx J., Kunz S., Schuller A., Nagel, W. (2006): Transcriptome analysis of Arabidopsis clubroot indicates a key role for cytokinins in disease development. Molecular Plant-Microbe Interactions Journal, 19: 480-494. Go to original source... Go to PubMed...
  82. Siemens J., Graf H., Bulman S., In O., Ludwig-Müller J. (2009): Monitoring expression of selected Plasmodiophora brassicae genes during clubroot development in Arabidopsis thaliana. Plant Pathology. 58: 130-136. Go to original source...
  83. Singh K., Zouhar M., Mazakova J., Rysanek P. (2014): Genome wide identification of the immunophilin gene family in Leptosphaeria maculans: a causal agent of blackleg disease in oilseed rape (Brassica napus). OMICS: a Journal of Integrative Biology, 18: 645-657. Go to original source... Go to PubMed...
  84. Sharma A.D., Singh P. (2003): Effect of water stress on expression of a 20 kD cyclophilin-like protein in drought susceptible and tolerant cultivars of Sorghum. Journal of Plant Biochemistry and Biotechnology. 12: 77-80. Go to original source...
  85. Sharma K., Gossen B.D., McDonald M.R. (2011): Effect of temperature on primary infection by Plasmodiophora brassicae and initiation of clubroot symptoms. Plant Pathology, 60: 830-838. Go to original source...
  86. Somé A., Manzanares M.J., Laurens F., Baron F., Thomas G., Ouxel F.R. (1996): Variation for virulence of Brassica napus L., amongst Plasmodiophora brassicae collections from France and derived single-spore isolates. Plant Pathology, 45: 432-439. Go to original source...
  87. 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. Go to original source...
  88. Strelkov S. E., Manolii V. P., Cao T., Xue S., Hwang S.F. (2007): Pathotype Classification of Plasmodiophora brassicae and its occurrence in Brassica napus in Alberta. Canada Journal of Phytopathology, 155: 706-712. Go to original source...
  89. Sundelin T., Christensen C.B., Larsen J., Møller K., Lübeck M., Bødker L., Jensen B. (2010): In planta quantification of Plasmodiophora brassicae using signature fatty acids and real time PCR. Plant Disease, 94: 432-438. Go to original source... Go to PubMed...
  90. Takahashi K., Yamaguchi T. (1988): A method for assessing the pathogenic ability of resting spores of Plasmodiophora brassicae by fluorescence microscopy. Annals of Phytopathological Society Japan, 54: 466-475. Go to original source...
  91. Takahashi K., Yamaguchi T. (1989): Assessment of pathogenicity of resting spores of Plasmodiophora brassicae in soil by fluorescence microscopy. Annals of Phytopathological Society Japan, 55: 621-628. Go to original source...
  92. Takahashi H., Takita K., Kishimoto T., Mitsui T., Hori H. (2002): Ca2+ is required by clubroot-resistant turnip cells for transient increases in PAL activity that follows inoculation with Plasmodiophora brassicae. Journal of Phytopathology, 150: 529-535. Go to original source...
  93. Takahashi H., Ishikawa T., Kaido M., Takita K., Hayakawa T., Okazaki K., Itoh K., Mitsui T., Hori H. (2006): Plasmodiophora brassicae induced cell death and medium alkalisation in clubroot-resistant cultured roots of Brassica rapa. Journal of Phytopathology, 154: 156-162. Go to original source...
  94. Tilston E.L., Pitt D., Groenhof A.C. (2002): Composted recycled organic matter suppresses soil-borne diseases of field crops. New Phytologist, 154: 731-740. Go to original source... Go to PubMed...
  95. Viaud M.C., Balhadere P.V., Talbot N.J. (2002): A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell, 14: 917-930. Go to original source... Go to PubMed...
  96. Viaud M.C., Brunet-Simon A., Brygoo Y., Pradier J.M., Levis C. (2003): Cyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporin A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea. Molecular Microbiology, 50, 1451-1465. Go to original source... Go to PubMed...
  97. Voorrips R.E. (1995): Plasmodiophora brassicae: aspects of pathogenesis and resistance in Brassica oleracea. Euphytica, 83: 139-146. Go to original source...
  98. Voorrips R.E. (1996): Production, characterization and interaction of single-spore isolates of Plasmodiophora brassicae. European Journal of Plant Pathology, 102: 377-383. Go to original source...
  99. Wakeham A.J., White J.G. (1996): Serological detection in soil of Plasmodiophora brassicae resting spores. Physiological and Molecular Plant Pathology, 48: 289-303. Go to original source...
  100. 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. Go to original source...
  101. Wallenhammar A.C. (2010): Monitoring and control of Plasmodiophpora brassicae in spring oilseed brassica crops. In: Proceedings 5th International Symposium on Brassicas and 16th Crucifer Genetics Workshop, Sept 8-12, 2008. Lillehammer, Norway: 181-190. Go to original source...
  102. Wallenhammar A.C., Arwidsson O. (2001): Detection of Plasmodiophora brassicae by PCR in naturally infested soils. European Journal of Plant Pathology, 107: 313-321. Go to original source...
  103. Wallenhammar A.C., Almquist C., Söderström, M., Jonsson A. (2012): In-field distribution of Plasmodiophora brassicae measured using quantitative real-time PCR. Plant Pathology, 61: 16-28. Go to original source...
  104. Wang P., Heitman J. (2005): The cyclophilins. Genome Biology, 6: 226. Go to original source... Go to PubMed...
  105. Webster M.A. (1986): pH and nutritional effects on infection by Plasmodiophora brassicae Wor. and on clubroot symptoms. [PhD Thesis.] Aberdeen, University of Aberdeen.
  106. Webster M.A., Dixon G.R. (1991a): Calcium, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae. Mycological Research, 95: 64-73. Go to original source...
  107. Webster M.A., Dixon G.R. (1991b): Boron, pH and inoculum concetration as factorslimiting root hair colonization by P. brassicae Wor. Mycological Research, 95: 74-79. Go to original source...
  108. Wellman F.L. (1930): Clubroot of crucifers. Technical Bulletin of the U.S. Department of Agriculture, No. 181.
  109. Williams P.H. (1966): A system for the determination of races of Plasmodiophora brassicae that infect cabbage and rutabaga. Phytopathology, 56: 624-626.
  110. Yoshikawa H. (1993): Studies on breeding of clubroot resistance in cole crops. Bulletin of National Research Institute of Vegetable, Ornamental Plants and Tea Japan, Ser. A, 7: 1-165. eagri.cz. Available http://eagri.cz/public/app/srs_pub/pp_public/rpg10a_util.download_ii?xid=2721 (accessed on April 4, 2014).

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.