, Volume 211, Issue 2, pp 201–213 | Cite as

Mapping of the clubroot disease resistance in spring Brassica napus canola introgressed from European winter canola cv. ‘Mendel’

  • Rudolph Fredua-Agyeman
  • Habibur Rahman


Clubroot disease caused by the soil-borne pathogen Plasmodiophora brassicae Woronin is a major threat to the production of Brassica crops worldwide. The European winter canola cv. ‘Mendel’ shows resistance to many P. brassicae isolates including pathotypes 3, 5, 6 and 8 that are prevalent in Canada. To introgress clubroot resistance (CR) into Canadian spring Brassica napus canola, crosses between Canadian spring and European winter B. napus canola cv. ‘Mendel’ were made and several resistant lines were developed through pedigree breeding. Two of the resistant lines were further crossed with the clubroot susceptible spring canola line A07-26NR to produce two doubled haploid (DH) populations from nine F1 plants. Segregation for resistance followed a 1:1 ratio for resistant and susceptible phenotypes suggesting that a single Mendelian gene is involved in the control of resistance to P. brassicae single spore isolate SACAN-ss1 (pathotype 3) in the DH population where the ‘favourable allele’ for resistance is derived from the cv. ‘Mendel’. Genetic and physical mapping study positioned five previously described CR loci (CRk, Crr3, CRb, CRa and CRb Kato ) on the B. rapa chromosome A3, and identified twelve markers (1.5–2.0 % recombination) from the genomic region that houses the CRa and CRb Kato loci to be associated with the resistance derived from ‘Mendel’. The identified markers can be used in breeding as well as pyramiding of multiple clubroot resistance genes.


Plasmodiophora brassicae Single spore isolate SACAN-ss1 Pathotype 3 Clubroot resistance Spring canola Winter canola Mapping Molecular marker 



We thank Dr. Stephen Strelkov and Dr. Victor Manolii, University of Alberta for providing galls for all inoculation experiments. We also thank Drs. Zahidur Rahman, Abdus Shakir, Berisso Kebede, Neil Hobson and Mrs. An Vo for technical support. We are grateful to Drs. Selvaraj Gopalan and Kulkarni Manoj for discussion in this project. Our greatest appreciation goes to Alberta Crop Industry Development Fund (ACIDF) and Alberta Canola Producers Commission (ACPC) for financial support to this project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10681_2016_1730_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 kb)


  1. Bhattacharya I, Dutta S, Mondal S, Mondal B (2014) Clubroot disease on Brassica crops in India. Can J Plant Pathol 36:154–160. doi: 10.1080/07060661.2013.875064 CrossRefGoogle Scholar
  2. Bradshaw JE, Gemmell DJ, Wilson RN (1997) Transfer of resistance to clubroot (Plasmodiophora brassicae) to swedes (Brassica napus L. var. napobrassica Peterm) from B. rapa. Ann Appl Biol 130:337–348. doi: 10.1111/j.1744-7348.1997.tb06837.x CrossRefGoogle Scholar
  3. Buczacki ST, Ockendon JG, White JG (1974) General studies. Report of the national vegetable research station for 1974, p 113Google Scholar
  4. Chai AL, Xie XW, Shi YX, Li BJ (2014) Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Can J Plant Pathol 36:142–153. doi: 10.1080/07060661.2013.868829 CrossRefGoogle Scholar
  5. Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier M-C, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee T-H, Ha Dinh Thi V, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury J-M, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953Google Scholar
  6. Colhoun J (1953) A study of the epidemiology of club-root disease of Brassicae. Ann Appl Biol 40:262–283CrossRefGoogle Scholar
  7. Crête R (1981) Worldwide importance of clubroot. Clubroot Newsl 11:6–7Google Scholar
  8. Crisp P, Crute IR, Sutherland RA, Angell SM, Bloor K, Burges H, Gordon PL (1989) The exploitation of genetic resources of Brassica oleracea in breeding for resistance to clubroot (Plasmodiophora brassicae). Euphytica 42:215–226Google Scholar
  9. Derksen H, Kubinec AM, McLaren DL (2013) Detection of Plasmodiophora brassicae in Manitoba, 2011. Can Plant Dis Surv 92:159Google Scholar
  10. Diederichsen E, Sacristán MD (1996) Disease response of resynthesized Brassica napus L. lines carrying different combinations of resistance to Plasmodiophora brassicae Wor. Plant Breeding 115:5–10. doi: 10.1111/j.1439-0523.1996.tb00862.x CrossRefGoogle Scholar
  11. Diederichsen E, Beckmann J, Schondelmeier J, Dreyer F (2006) Genetics of clubroot resistance in Brassica napus ‘Mendel’. Acta Hortic 706:307–312CrossRefGoogle Scholar
  12. Diederichsen E, Frauen M, Linders EGA, Hatakeyama K, Hirai M (2009) Status and perspectives of clubroot resistance breeding in crucifer crops. J Plant Growth Regul 28:265–281. doi: 10.1007/s00344-009-9100-0 CrossRefGoogle Scholar
  13. Diederichsen E, Frauen M, Ludwig-Müller J (2014) Clubroot disease management challenges from a German perspective. Can J Plant Pathol 36:85–98. doi: 10.1080/07060661.2013.861871 CrossRefGoogle Scholar
  14. Dixon GR (2006) The biology of Plasmodiophora brassicae Wor.—a review of recent advances. Acta Hortic 706:271–282CrossRefGoogle Scholar
  15. Dixon GR (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J Plant Growth Regul 28:194–202. doi: 10.1007/s00344-009-9090-y CrossRefGoogle Scholar
  16. Dobson RL, Gabrielson RL, Baker AS, Bennett L (1983) Effects of lime particle size and distribution and fertilizer formulation on clubroot disease caused by plasmodiophora brassicae. Plant Dis 67:50–52CrossRefGoogle Scholar
  17. Dokken-Bouchard FL, Bouchard AJ, Ippolito J, Peng G, Strelkov SE, Kirkham L, Kutcher HR (2010) Detection of Plasmodiophora brassicae in Saskatchewan. Can Plant Dis Surv 90:126Google Scholar
  18. Donald C, Porter I (2009) Integrated control of clubroot. J Plant Growth Regul 28:289–303. doi: 10.1007/s00344-009-9094-7 CrossRefGoogle Scholar
  19. Donald EC, Porter IJ (2014) Clubroot in Australia: the history and impact of Plasmodiophora brassicae in Brassica crops and research efforts directed towards its control. Can J Plant Pathol 36:66–84. doi: 10.1080/07060661.2013.873482 CrossRefGoogle Scholar
  20. Faggian R, Strelkov SE (2009) Detection and measurement of Plasmodiophora brassicae. J Plant Growth Regul 28:282–288CrossRefGoogle Scholar
  21. Frauen M (1999) A new clubroot resistant variety in winter oilseed rape. In: Proceedings of the 10th International Rapeseed Congress, Canberra, AustraliaGoogle Scholar
  22. Fredua-Agyeman R, Coriton O, Huteau V, Parkin IAP, Chevre AM, Rahman H (2014) Molecular cytogenetic identification of B genome chromosomes linked to blackleg disease resistance in Brassica napus × B. carinata interspecific hybrids. Theor Appl Genet 127:1305–1318CrossRefPubMedGoogle Scholar
  23. 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 31:971–976CrossRefGoogle Scholar
  24. Hasan MJ, Strelkov SE, Howard RJ, Rahman H (2012) Screening of Brassica germplasm for resistance to Plasmodiophora brassicae pathotypes prevalent in Canada for broadening diversity in clubroot resistance. Can J Plant Sci 92:501–515. doi: 10.4141/CJPS2010-006 CrossRefGoogle Scholar
  25. Hayashida N, Takabatake Y, Nakazawa N, Aruga D, Nakanishi H, Taguchi G, Sakamoto K, Matsumoto E (2008) Construction of a practical SCAR marker linked to clubroot resistance in Chinese cabbage, with intensive analysis of HC352b genes. J Jpn Soc Hortic Sci 77:150–154CrossRefGoogle Scholar
  26. Hirai M, Harada T, Kubo N, Tsukada M, Suwabe K, Matsumoto S (2004) A novel locus for clubroot resistance in Brassica rapa and its linkage markers. Theor Appl Genet 108:639–643CrossRefPubMedGoogle Scholar
  27. Howard RJ, Strelkov SE, Harding MW (2010) Clubroot of cruciferous crops—new perspectives on an old disease. Can J Plant Pathol 32:43–57. doi: 10.1080/07060661003621761 CrossRefGoogle Scholar
  28. Jiang C, Ramchiary N, Ma Y, Jin M, Feng J, Li R, Wang H, Long Y, Choi SR, Zhang C, Cowling WA, Park BS, Lim YP, Meng J (2011) Structural and functional comparative mapping between the Brassica A genomes in allotetraploid Brassica napus and diploid Brassica rapa. Theor Appl Genet 123:927–941CrossRefPubMedGoogle Scholar
  29. Kato T, Hatakeyama K, Fukino N, Matsumoto S (2012) Identification of a clubroot resistance locus conferring resistance to a Plasmodiophora brassicae classified into pathotype group 3 in Chinese cabbage (Brassica rapa L.). Breed Sci 62:282–287CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kato T, Hatakeyama K, Fukino N, Matsumoto S (2013) Fine mapping of the clubroot resistance gene CRb and development of a useful selectable marker in Brassica rapa. Breed Sci 63:116–124. doi: 10.1270/jsbbs.63.116 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kebede B, Thiagarajah MR, Zimmer C, Rahman MH (2010) Improvement of open-pollinated spring rapeseed (Brassica napus L.) through introgression of genetic diversity from winter rapeseed. Crop Sci 50:1236–1243CrossRefGoogle Scholar
  32. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  33. Kowata-Dresch LS, May-De Mio LL (2012) Clubroot management of highly infested soils. Crop Prot 35:47–52CrossRefGoogle Scholar
  34. Kubinec AM, Derksen H, Desjardins ML, McLaren DL (2014) Monitoring and occurrence of clubroot in Manitoba in 2013. Can Plant Dis Surv 94:184–185Google Scholar
  35. 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 var. pekinensis). Eur J Plant Pathol 105:327–332CrossRefGoogle Scholar
  36. Larson RH, Walker JC (1934) Soil treatment in relation to clubroot of cabbage. J Agric Res 48:749–759Google Scholar
  37. Lincoln S, Daly M, Lander (1992) Constructing genetic maps with MAPMAKER/EXP 3.0, 3rd ed. Whitehead Institute Technical reportGoogle Scholar
  38. Matsumoto E, Yasui C, Ohi M, Tsukada M (1998) Linkage analysis of RFLP markers for clubroot resistance and pigmentation in Chinese cabbage (Brassica rapa ssp. pekinensis). Euphytica 104:79–86CrossRefGoogle Scholar
  39. Matsumoto E, Ueno H, Aruga D (2012) Accumulation of three clubroot resistance genes through marker-assisted selection in Chinese cabbage (Brassica rapa ssp Pekinensis). Jpn Soc Hortic Sci 81:184–190CrossRefGoogle Scholar
  40. McLaren DL, Platford RG, Kutcher HR, Bisht V, Kubinec A, Kristjanson I, Hammond D, Henderson TL, Hausermann D, Kaskiw L, Williamson K, Jersak S, Johnson H, Souquel J, Heshka J, Farooq A (2011) Survey of canola diseases in Manitoba in 2010. Can Plant Dis Surv 91:124–126Google Scholar
  41. McLaren DL, Platford RG, Kubinec A, Derksen H, Kutcher HR, Bargen E (2013) Survey of canola diseases in Manitoba in 2012. Can Plant Dis Surv 93:155–158Google Scholar
  42. McLaren DL, Platford RG, Kubinec A, Derksen H, Bargen E, Brackenreed A, Brown-Livingston K, Buss T, Chomokovski D, Farooq A, Hausermann D, Heshka J, Henderson T, Jersak S, Kaskiw E, Kaskiw L, Kristjanson I, Lange D, McCracken M, Nernberg E, Picard R, Stoyanowski D (2014) Survey of canola diseases in Manitoba in 2013. Can Plant Dis Surv 94:180–183Google Scholar
  43. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832CrossRefPubMedPubMedCentralGoogle Scholar
  44. Miller SG, Anderson K, Bassendowski KA, Britz L, Buitenhuis N, Campbell E, Chant S, Christopher J, Cowell LE, Cranston R, Dokken-Bouchard FL, Friesen S, Gugel RK, Hicks L, Ippolito J, Jurke C, Kennedy V, Kirkham CL, Martinka T, Moore M, Oster K, Peng G, Phelps SM, Platford RG, Senko S, Stonehouse K, Vakulabharanam V (2013) Survey of canola diseases in Saskatchewan, 2012. Can Plant Dis Surv 93:149–153Google Scholar
  45. Monteith J (1924) Relation of soil temperature and soil moisture to infection, by Plasmodiophora brassicae. J Agric Res 28:549–561Google Scholar
  46. Nieuwhof M, Wiering D (1961) Testing cabbage plants for clubroot resistance. Euphytica 10:191–200Google Scholar
  47. Piao ZY, Deng YQ, Choi SR, Park YJ, Lim YP (2004) SCAR and CAPS mapping of CRb, a gene conferring resistance to Plasmodiophora brassicae in Chinese cabbage (Brassica rapa ssp. pekinensis). Theor Appl Genet 108:1458–1465CrossRefPubMedGoogle Scholar
  48. Piao Z, Ramchiary N, Lim YP (2009) Genetics of clubroot resistance in Brassica species. J Plant Growth Regul 28:252–264CrossRefGoogle Scholar
  49. Rahman H, Shakir A, Hassan MJ (2011) Breeding for clubroot resistant spring canola (Brassica napus L.) for the Canadian prairies: can the European winter canola cv. ‘Mendel’ be used as a source of resistance? Can J Plant Sci 91:447–458. doi: 10.4141/CJPS10073 CrossRefGoogle Scholar
  50. Rahman H, Peng G, Yu F, Falk KC, Kulkarni M, Selvaraj G (2014) Genetics and breeding for clubroot resistance in Canadian spring canola (Brassica napus L.). Can J Plant Pathol 36:122–134. doi: 10.1080/07060661.2013.862571 CrossRefGoogle Scholar
  51. Saito M, Kubo N, Matsumoto S, Suwabe K, Tsukada M, Hirai M (2006) Fine mapping of the clubroot resistance gene, Crr3, in Brassica rapa. Theor Appl Genet 114:81–91CrossRefPubMedGoogle Scholar
  52. Sakamoto K, Saito A, Hayashida N, Taguchi G, Matsumoto E (2008) Mapping of isolate-specific QTLs for clubroot resistance in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Theor Appl Genet 117:759–767CrossRefPubMedGoogle Scholar
  53. Saude C, McKeown A, Gossen BD, McDonald MR (2012) Effect of host resistance and fungicide application on clubroot Pathotype 6 in Green cabbage and Napa cabbage. Hort Technol 22:311–319Google Scholar
  54. Strelkov SE, Hwang SF (2014) Clubroot in the Canadian canola crop: 10 years into the outbreak. Can J Plant Pathol 36:27–36. doi: 10.1080/07060661.2013.863807 CrossRefGoogle Scholar
  55. Strelkov SE, Tewari JP, Hartman M, Orchard D (2005) Clubroot on canola in Alberta in 2003 and 2004. Can Plant Dis Surv 85:72–73Google Scholar
  56. Strelkov SE, Manolii VP, Harding MW, Hwang SF, Poscente N, Lisowski SLI, Pugh CA, Burke DA (2014) The occurrence of clubroot on canola in Alberta in 2013. Can Plant Dis Surv 94:158–161Google Scholar
  57. Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Fujimura M, Nunome T, Fukuoka H, Matsumoto S, Hirai M (2003) Identification of two loci for resistance to clubroot (Plasmodiophora brassicae Woronin) in Brassica rapa L. Theor Appl Genet 107:997–1002CrossRefPubMedGoogle Scholar
  58. Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Kondo M, Fujimura M, Nunome T, Fukuoka H, Hirai M, Matsumoto S (2006) Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 173:309–319CrossRefPubMedPubMedCentralGoogle Scholar
  59. Suwabe K, Morgan C, Bancroft I (2008) Integration of Brassica A genome genetic linkage map between Brassica napus and B. rapa. Genome 51:169–176CrossRefPubMedGoogle Scholar
  60. Tewari JP, Strelkov SE, Orchard D, Hartman M, Lange RM, Turkington TK (2005) Identification of clubroot of crucifers on canola (Brassica napus) in Alberta. Can J Plant Pathol 27:143–144CrossRefGoogle Scholar
  61. Tomerrup IC, Ingram DS (1971) The life-cycle of Plasmodiophora brassicae Woron. in Brassica tissue cultures and intact roots. New Phytol 70:327–332CrossRefGoogle Scholar
  62. Ueno H, Matsumoto E, Aruga D, Kitagawa S, Matsumura H, Hayashida N (2012) Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol Biol 80:621–629. doi: 10.1007/s11103-012-9971-5 CrossRefPubMedGoogle Scholar
  63. Voorrips RE (1995) Plasmodiophora brassicae: aspects of pathogenesis and resistance in Brassica oleracea. Euphytica 83:139–146CrossRefGoogle Scholar
  64. Voorrips RE, Visser DL (1993) Examination of resistance to clubroot in accessions of Brassica oleracea using a glasshouse seedling test. Neth J Plant Pathol 99:269–276CrossRefGoogle Scholar
  65. Wallenhammar AC (1996) Prevalence of Plasmiodophora brassicae in a spring oilseed rape growing area in central Sweden and factors influencing soil infection levels. Plant Pathol 45:710–719CrossRefGoogle Scholar
  66. Wallenhammar AC, Almquist C, Schwelm A, Roos J, Marzec-Schmidt K, Jonsson A, Dixelius C (2014) Clubroot, a persistent threat to Swedish oilseed rape production. Can J Plant Pathol 36:135–141. doi: 10.1080/07060661.2013.870606 CrossRefGoogle Scholar
  67. Werner S, Diederichsen E, Frauen M, Schondelmaier J, Jung C (2008) Genetic mapping of clubroot resistance genes in oilseed rape. Theor Appl Genet 116:363–372CrossRefPubMedGoogle Scholar
  68. Yoshikawa H (1981) Breeding for clubroot resistance in Chinese cabbage. In: Taleker NS, Griggs TD (eds) Chinese cabbage. AVRDC, Shanhua, Tainan, pp 405–413Google Scholar
  69. Zhang T, Zhao Z, Zhang C, Pang W, Choi SR, Lim YP, Piao Z (2014) Fine genetic and physical mapping of the CRb gene conferring resistance to clubroot disease in Brassica rapa. Mol Breed 34:1173–1183. doi: 10.1007/s11032-014-0108-1 CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Agricultural, Food and Nutritional ScienceUniversity of AlbertaEdmontonCanada

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