Article | 12. 2014 Vol. 32, Issue. 6
Development of Molecular Markers and Application for Breeding in Chinese Cabbage

Korea Institute of Science and Technology Information1
Theragen Bio Institute, Theragen Etex2
College of Agriculture and Life Sciences, Chungnam National University3

2014.12. 745:752


Chinese cabbage (Brassica rapa L. ssp. pekinensis) is an economically important vegetable crop as a source of the traditional food Kimchi in Korea. Although many varieties exhibiting desirable traits have been developed by the conventional selective breeding approach, breeding related to abiotic or biotic stresses, such as a particular pests or diseases, or tolerance to climatic conditions, is likely to be slow. This could be helped by an efficient method for selection from various, rapidly-evolved genetic resources on the basis of molecular markers. In particular, the Brassica genome sequencing project enables genome-wide discovery of genes or genetic variants associated with agricultural traits. We here discuss the recent progress in the field of Chinese cabbage breeding with regard to the application of molecular markers.

1. Ahn, S.D. and S.S. Lee. 2013. NHERI report for 2013; 2013 Trend of domestic Kimchi industry, Investigation of consumer Gimjang plan. NongHyup Economic Res. Inst. Rpt. 230:1-2  

2. Abe, H., T. Shimoda, J. Ohnishi, S. Kugimiya, M. Narusaka, S. Seo, Y. Narusaka, S. Tsuda, and M. Kobayashi. 2009. Jasmonate- dependent plant defense restricts thrips performance and preference. BMC Plant Biol. 9:97.  

3. Ajisaka, H., Y. Kuginuki, S. Yui, S. Enomoto, and M. Hirai. 2001. Identification and mapping of a quantitative trait locus controlling extreme late bolting in Chinese cabbage (Brassica rapa L. ssp. pekinensis syn. campestris L.) using bulked segregant analysis. Euphytica 118:75-81.  

4. Cardi, T. and E.D. Earle. 1997. Production of new CMS Brassica oleracea by transfer of ‘Anand’ cytoplasm from B. rapa through protoplast fusion. Theor. Appl. Genet. 94:204-212.  

5. Chase, C.D. 2007. Cytoplasmic male sterility: A window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23:81-90.  

6. Chia, J.M. and D. Ware. 2011. Sequencing for the cream of the crop. Nat. Biotechnol. 29:138-139.  

7. Chung, H., Y.M. Jeong, J.H. Mun, S.S. Lee, W.H. Chung, and H.J. Yu. 2014. Construction of a genetic map based on high- throughput SNP genotyping and genetic mapping of a TuMV resistance locus in Brassica rapa. Mol. Genet. Genomics 289:149-160.  

8. Dong, X., W.K. Kim, Y.P. Lim, Y.K. Kim, and Y. Hur. 2013. Ogura-CMS in Chinese cabbage (Brassica rapa ssp. pekinensis) causes delayed expression of many nuclear genes. Plant Sci. 199-200:7-17.  

9. Farinhó, M., P. Coelho, J. Carlier, D. Svetleva, A. Monteiro, and J. Leitão. 2004. Mapping of a locus for adult plant resistance to downy mildew in broccoli (Brassica oleracea convar. italica). Theor. Appl. Genet. 109:1392-1398.  

10. Feng, H., P. Wei, C.Y. Li, S.R. Choi, Y.P. Lim, and Z.Y. Piao 2009a. Identification of SSR markers linked to a genic multiple-allele male sterile gene. Acta Hortic. Sinica 36: 103-108.  

11. Feng, H., P. Wei, Z.Y. Piao, Z.Y. Liu, C.Y. Li, Y.G. Wang, R.Q. Ji, S.J. Ji, T. Zou, S.R. Choi, and Y.P. Lim. 2009b. SSR and SCAR mapping of a multiple-allele male-sterile gene in Chinese cabbage (Brassica rapa L.). Theor. Appl. Genet. 119:333-339.  

12. Geddy, R., L. Mahe, and G.G. Brown. 2005. Cell-specific regulation of a Brassica napus CMS-associated gene by a nuclear restorer with related effects on a floral homeotic gene promoter. Plant J. 41:333-345.  

13. Guo, Y., S. Chen, Z. Li, and W.A. Cowling. 2014. Center of origin and centers of diversity in an ancient crop, Brassica rapa (turnip rape). J. Heredity 105:555-565.  

14. Gruber, M.Y., S. Wang, S. Ethier, J. Holowachuk, P.C. Bonham- Smith, J. Soroka, and A. Lloyd. 2006. “HAIRY CANOLA”- Arabidopsis GL3 induces a dense covering of trichomes on Brassica napus seedlings. Plant Mol. Biol. 60:679-698.  

15. Hatakeyama, K., K. Suwabe, R.N. Tomita, T. Kato, T. Nunome, H. Fukuoka, and S. Matsumoto. 2013. Identification and Characterization of Crr1a, a Gene for Resistance to Clubroot Disease (Plasmodiophora brassicae Woronin) in Brassica rapa L. PLOS ONE. 8(Special section P1).  

16. Hayashida, N., Y. Takabatake, N. Nakazawa, D. Arugal, H. Nakanishi, G. Taguchi, K. Sakamoto, and E. Matsumoto. 2008. Construction of a practical SCAR marker linked to clubroot resistance in Chinese cabbage, with intensive analysis of HC352b genes. J. Jpn. Soc. Hort. Sci. 77:150-154.  

17. He, Y., J. Tu, T. Fu, D. Li, and B. Chen. 2002. Genetic diversity of germplasm resources of Brassica campestris L. in China by RAPD markers. Zuo Wu Xue Bao 28:607-703.  

18. Hirai, M., T. Harada, N. Kubo, M. Tsukada, K. Suwabe, and S. Matsumoto. 2004. A novel locus for clubroot resistance in and its linkage markers. Theor. Appl. Genet. 108:639-643.  

19. Hirani, A.H., C.D. Zelmer, P.B.E. McVetty, F. Daayf, and G. Li. 2013. Homoeologous GSL-ELONG gene replacement for manipulation of aliphatic glucosinolates in Brassica rapa L. by marker assisted selection. Frontiers Plant Sci. 4(55):1-12.  

20. Hirata, Y., T. Motegi, Y. Takeda, and K. Morikawa. 2001. Induction of cytoplasmic male sterility in the seed progeny derived from artificially-synthesized interspecific chimera in Brassica. Euphytica 117:143-149.  

21. Hiscock, S.J. and S.M. McInnis. 2003. Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. Trends Plant Sci. 8:606-613.  

22. Huang, X., T. Lu, and B. Han. 2012. Resequencing rice genomes: An emerging new era of rice genomics. Trends Genet. 29: 225-232.  

23. Huang, X., X. Wei, T. Sang, Q. Zhao, Q. Feng, Y. Zhao, C. Li, C. Zhu, T. Lu, Z. Zhang, M. Li, D. Fan, Y. Guo, A. Wang, L. Wang, L. Deng, W. Li, Y. Lu, Q. Weng, K. Liu, T. Huang, T. Zhou, Y. Jing, W. Li, Z. Lin, E.S. Buckler, Q. Qian, Q.F. Zhang, J. Li, and B. Han. 2010. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42:961-967.  

24. Jin, M., S.S. Lee, L. Ke, J.S. Kim, M.S. Seo, S.H. Sohn, B.S. Park, and G. Bonnema. 2014. Identification and mapping of a novel dominant resistance gene, TuRB07 to Turnip mosaic virus in Brassica rapa. Theor. Appl. Genet. 127:509-519.  

25. Kakizaki, T., T. Kato, N. Fukino, M. Ishida, K. Hatakeyama, and S. Matsumoto. 2011. Identification of quantitative trait loci controlling late bolting in Chinese cabbage (Brassica rapa L.) parental line Nou 6 gou. Breeding Sci. 61:151-159.  

26. Kato, T., K. Hatakeyama, N. Fukino, and S. Matsumoto. 2012. Identificaiton of a clubroot resistance locus conferring resistance to a Plasmodiophora brassicae classified into pathotype group 3 in Chinese cabbage (Brassica rapa L.). Breeding Sci. 62: 282-287.  

27. Kato, T., K. Hatakeyama, N. Fukino, and S. Matsumoto. 2013. Fine mapping of the clubroot resistance gene CRb and development of a useful selectable marker in Brassica rapa. Breeding Sci. 63:116-124.  

28. Kim, C.H., W.D. Cho, and S.B. Lee. 2003. Review of researches on clubroot disease of Chinese cabbage in Korea and future tasks for its management. Res. Plant. Dis. 9:57-63.  

29. Kim, J.H., W.H. Kang, H.B. Yang, S.H. Park, C.S. Jang, H.J. Yu, and B.C. Kang. 2013. Identification of a broad-spectrum recessive gene in Brassica rapa and molecular analysis of the eIF4E gene family to develop molecular markers. Mol. Breeding 32:385-398.  

30. Kim, S.G., Y.H. Song, J.Y. Lee, S.R. Choi, V. Dhandapani, C.S. Jang, Y.P. Lim, and T.H. Han. 2011. Identification of the BrRHP1 locus that confers resistance to downy mildew in Chinese cabbage (Brassica rapa ssp. pekinensis) and development of linked molecular markers. Theor. Appl. Genet. 123:1183-1192.  

31. Krishnasamy, S. and C.A. Makaroff. 1993. Characterization of the radish mitochondrial orfB locus: Possible relationship with male sterility in Ogura radish. Curr. Genet. 24:156-163.  

32. Kuginuki, Y., H. Yoshikawa, and M. Hirai. 1999. Variation in virulence of Plasmodiophora brassicae in Japan tested with clubroot resistant cultivars of Chinese cabbage (Brassica rapa L. ssp. pekinensis). Eur. J. Plant Pathol. 105:327-332.  

33. Lee, K.A., H.J. Lee, Y.S. Park, W.K. Choi, N.H. Hur, J.H. Lee, S.G. Yang, C.H. Harn, and S.H. Nahm. 2006. Molecular markers linked to downy mildew resistance locus in Chinese cabbage. J. Plant Biotechnol. 33(1s):24-24.  

34. Lee, S.H., S.C. Lee, D.H. Byun, D.Y. Lee, J.Y. Park, J.H. Lee, H.O. Lee, S.H. Sung, and T.J. Yang. 2014. Association of molecular markers derived from the BrCRISTO1 gene with prolycopene-enriched orange-colored leaves in Brassica rapa. Theor. Appl. Genet. 127:179-191.  

35. Li, H., S.C. Yu, F.L. Zhang, Y.J. Yu, X.Y. Zhao, D.S. Zhang, and X. Zhao. 2011. Development of molecular markers linked to the resistant QTL for downy mildew in Brassica rapa L. ssp. pekinensis. Yi Chuan 33:1271-1278.  

36. Li, X., N. Ramchiary, S.R. Choi, V.D. Nguyen, M.J. Hossain, H.K. Yang, and Y.P. Lim. 2010. Development of a high density integrated reference genetic linkage map for the multinational Brassica rapa Genome Sequencing Project. Genome 53:939-947.  

37. Li, X., N. Ramchiary, V. Dhandapani, S.R. Choi, Y.K. Hur, I.S. Nou, M.K. Yoon, and Y.P. Lim. 2013. Quantitative trait loci mapping in Brassica rapa revealed the structural and functional conservation of genetic loci governing morphological and yield component traits in the A, B, and C subgenomes of Brassica species. DNA Res. 20:1-16.  

38. Lou, P., J.J. Zhao, H.J. He, C. Hanhart, D.P.D. Carpio, R. Verkerk, J. Custers, M. Koornneef, and G. Bonnema. 2008. Quantitative trait loci for glucosinolate accumulation in Brassica rapa leaves. New Phytologist 179:1017-1032.  

39. Makaroff, C.A. and J.D. Palmer. 1988. Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol. Cell. Biol. 8:1474-1480.  

40. Matsumoto, E., H. Ueno, D. Aruga, K. Sakamoto, and N. Hayashida. 2012. Accumulation of three clubroot resistance genes through marker-assisted selection in Chinese cabbage (Brassica rapa ssp. pekinensis). J. Jpn. Soc. Hort. Sci. 81:184-190.  

41. Matsumoto, E., N. Hayashida, L. Sakamoto, and M. Ohi. 2005. Behavior of DNA markers linked to a clubroot resistance gene in segregating populations of Chinese cabbage (Brassica rapa ssp. pekinensis). J. Jpn. Soc. Hort. Sci. 74:367-373.  

42. Matsumoto, E., C. Yasui, M. Ohi, and M. Tsukada. 1998. Linkage analysis of RFLP markers for clubroot resistance and pigmentation in Chinese cabbage (Brassica rapa ssp. pekinensis). Euphytica 104:79-86.  

43. Muangprom, A. and T.C. Osborn. 2004. Characterization of a dwarf gene in Brassica rapa, including the identification of a candidate gene. Theor. Appl. Genet. 108:1378-1384.  

44. Ofori, A., H.C. Becker, and F.J. Kopisch-Obuch. 2008. Effect of crop improvement on genetic diversity in oilseed Brassica rapa (turnip-rape) cultivars, detected by SSR markers. J. Appl. Genet. 49:207-212.  

45. Piao, Z.Y., Y.Q. Deng, Y.J. Park, Y.S. Choi, and Y.P. Lim. 2004. SCAR and CAPS mapping of a resistance gene, CRb, that confers resistance to Plasmodiophora brassicae in Chinese cabbage (Brassica rapa ssp. pekinensis). Theor. Appl. Genet. 108:1458-1465.  

46. Ramchiary, N., V.D. Nguyen, X. Li, C.P. Hong, V. Dhandapani, S.R. Choi, G. Yu, Z.Y. Piao, and Y.P. Lim. 2011. Genic micro-satellite markers in Brassica rapa: Development, characterization, mapping, and their utility in other cultivated and wild Brassica relatives. DNA Res. 18:305-320.  

47. Ramchiary, N., K.L. Padmaja, S. Sharma, V. Gupta, Y.S. Sodhi, A. Mukhopadhyay, N. Arumugam, D. Pental, and A.K. Pradhan. 2007. Mapping of yield influencing QTL in Brassica juncea: Implications for breeding of a major oilseed crop of dryland areas. Theor. Appl. Genet. 115:807-817.  

48. Rusholme, R.L., E.E. Higgins, J.A. Walsh, and D.J. Lydiate. 2007. Genetic control of broad-spectrum resistance to turnip mosaic virus in Brassica rapa (Chinese cabbage). J. Gen. Virol. 88:3177-3186.  

49. Saito, M., N. Kubo, S. Matsumoto, K. Suwabe, M. Tsukada, and M. Hirai. 2006. Fine mapping of the clubroot resistance gene, Crr3, in Brassica rapa. Theor. Appl. Genet. 114:81-91.  

50. Sakamoto, K., A. Saito, N. Hayashida, G. Taguchi, and E. Matsumoto. 2008. Mapping of isolate-specific QTLs for clubroot resistance in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Theor. Appl. Genet. 117:759-767.  

51. Song, K.M., T.C. Osborn, and P.H. Wilfiams. 1988a. Brassica taxonomy based on nuclear restriction fragment length poly-morphisms (RFLPs). Theor. Appl. Genet. 76:593-600.  

52. Song, K.M., J.Y. Suzuki, M.K. Slocum, P.H. Williams, and T.C. Osborn. 1988b. A linkage map of Brassica rapa (syn. campestris) based on restriction fragment length polymorphism loci. Theor. Appl. Genet. 82:296-304.  

53. Statistics Korea. 2013. Crop production statistics for 2012. Statistics Korea, Social Statistics Bureau, Agriculture and Fisheries Statistics Division, Daejeon, Korea. p. 22-23.  

54. Suwabe, K., H. Tsukazaki, H. Iketani, K. Hatakeyama, M. Fujimura, T. Nunome, H. Fukuoka, S. Matsumoto, and M. Hirai. 2003. Identification of two loci for resistance to clubroot (Plasmodiophora brassicae Woronin) in Brassica rapa L. Theor. Appl. Genet. 107:997-1002.  

55. Suwabe, K., H. Tsukazaki, H. Iketani, K. Hatakeyama, M. Kondo, M. Fujimura, T. Nunome, H. Fukuoka, M. Hirai, and S. Matsumoto. 2006. Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: The genetic origin of clubroot resistance. Genetics 173:309-319.  

56. Tanhuanpää, P.K., J.P. Vilkki, and H.J. Vilkki. 1995. Identification of a RAPD marker for palmitic-acid concentration in the seed oil of spring turnip rape (Brassica rapa ssp. oleifera). Theor. Appl. Genet. 91:477-480.  

57. The Brassica rapa Genome Sequencing Project Consortium. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43:1035-1039.  

58. Ueno, H., E. Matsumoto, D. Aruga, S. Kitagawa, H. Matsumura, and N. Hayashida. 2012. Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol. Biol. 80:621-629.  

59. Verma, J.K., Y.S. Sodhi, A. Mukhopadhyay, N. Arumugam, V. Gupta, D. Pental, and A.K. Pradhan. 2000. Identification of stable maintainer and fertility restorer lines for ‘Polima’ CMS in Brassica campestris. Plant Breeding 119:90-92.  

60. Voorrips, R.E. 1995. Plasmodiophora brassicae: Aspects of pathogenesis and resistance in Brassica oleracea. Euphytica 83:139-146.  

61. Wang, J., D.J. Lydiate, I.A. Parkin, C. Falentin, R. Delourme, P.W. Carion, and G.J. King. 2011. Integration of linkage maps for the Amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Genomics 12:101.  

62. Wang, X., H. Chen, Y. Zhu, and R. Hou. 2009. An AFLP marker linked to turnip mosaic virus resistance gene in pak-choi. African J. Biotechnol. 8:2508-2512.  

63. Yang, J., X. Liu, X. Yang, and M. Zhang. 2007. Mitochondrially- targeted expression of a cytoplasmic male sterility-associated orf220 gene causes male sterility in Brassica juncea. BMC Plant Biol. 10:231-241.  

64. Yang, Y.W., P.Y. Tai, Y. Chen, and W.H. Li. 2002. A study of the phylogeny of Brassica rapa, B. nigra, Raphanus sativus, and their related genera using noncoding regions of chloroplast DNA. Mol. Phylogenet. Evol. 23:268-275.  

65. Ying, M., F. Dreyer, D. Cai, and C. Jung. 2003. Molecular markers for genic male sterility in Chinese cabbage. Euphytica 132:227-234.  

66. Yu, H.F., X.M. Zhong, B.Y. Li, and H.H. Gu. 2010. A Molecular marker linked to downy mildew resistant gene in heading Chinese cabbage (Brassica rapa L. ssp. Pekinensis (Lour) Olsson). Chinese Agricultural Sci. Bul. 26(15):66-70.  

67. Yu, S., F. Zhang, R. Yu, Y. Zou, J. Qi, X. Zhao, Y. Yu, D. Zhang, and L. Li. 2009. Genetic mapping and localization of a major QTL for seedling resistance to downy mildew in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol. Breeding 23:573-590.   

68. Yu, S., F. Zhang, X. Zhao, Y. Yu, and D. Zhang. 2011. Sequence-characterized amplified region and simple sequence repeat markers for identifying the major quantitative trait locus responsible for seedling resistance to downy mildew in Chinese cabbage (Brassica rapa ssp. pekinensis). Plant Breeding 130: 580-583.  

69. Yuan, Y.X., R.F. Sun, X.W. Zhang, J. Wu, D.H. Xu, H. Zhang, J.M. He, Y.G. Zhang, Y.G. Hang, and X.W. Wang. 2008. A CAPS marker linked to bolting related gene BrFLC1 in Brassica rapa. Acta Hort. Sinica 35:1635-1640.  

70. Zhao, J., V. Kulkarni, N. Liu, D.P.D. Carpio, J. Bucher, and G. Bonnema. 2010. BrFLC2 (FLOWERING LOCUS C) as a candidate gene for a vernalization response QTL in Brassica rapa. J. Expt. Bot. 61:1817-1825.  

71. Zhang, J., Y. Lu, Y. Yuan, X. Zhang, J. Geng, Y. Chen, S. Cloutier, P.B.E. McVetty, and G. Li. 2009. Map-based cloning and characterization of a gene controlling hairiness and seed coat color traits in Brassica rapa. Plant Mol. Biol. 69:553-563.  

72. Zhao, J., X. Wang, B. Deng, P. Lou, J. Wu, R. Sun, Z. Xu, J. Vromans, M. Koornneef, and G. Bonnema. 2005. Genetic relationships within Brassica rapa as inferred from AFLP fingerprints. Theor. Appl. Genet. 110:1301-1314.