Skip to main content
Log in

Construction of a genetic map based on high-throughput SNP genotyping and genetic mapping of a TuMV resistance locus in Brassica rapa

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Brassica rapa is a member of the Brassicaceae family and includes vegetables and oil crops that are cultivated worldwide. The introduction of durable resistance against turnip mosaic virus (TuMV) into agronomically important cultivars has been a significant challenge for genetic and horticultural breeding studies of B. rapa. Based on our previous genome-wide analysis of DNA polymorphisms between the TuMV-resistant doubled haploid (DH) line VC40 and the TuMV-susceptible DH line SR5, we constructed a core genetic map of the VCS-13M DH population, which is composed of 83 individuals derived from microspore cultures of a F1 cross between VC40 and SR5, by analyzing the segregation of 314 sequence-characterized genetic markers. The genetic markers correspond to 221 SNPs and 31 InDels of genes as well as 62 SSRs, covering 1,115.9 cM with an average distance of 3.6 cM between the adjacent marker loci. The alignment and orientation of the constructed map showed good agreement with the draft genome sequence of Chiifu, thus providing an efficient strategy to map genic sequences. Using the genetic map, a novel dominant TuMV resistance locus (TuMV-R) in the VCS-13M DH population was identified as a 0.34 Mb region in the short arm of chromosome A6 in which four CC–NBS–LRR resistance genes and two pathogenesis-related-1 genes reside. The genetic map developed in this study can play an important role in the genetic study of TuMV resistance and the molecular breeding of B. rapa.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119:507–517

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chen H, He H, Zou Y, Chen W, Yu R, Liu X, Yang Y, Gao YM, Xu JL, Fan LM, Li Y, Li ZK, Deng XW (2011) Development and application of a set of breeder-friendly SNP markers for genetic analyses and molecular breeding of rice (Oryza sativa L.). Theor Appl Genet 123:869–879

    Article  PubMed  Google Scholar 

  • Cole AB, Király L, Lane LC, Wiggins BE, Ross K, Schoelz JE (2004) Temporal expression of PR-1 and enhanced mature plant resistance to virus infection is controlled by a single dominant gene in a new Nicotiana hybrid. Mol Plant Microbe Interact 17:976–985

    Article  PubMed  CAS  Google Scholar 

  • Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32:927–934

    Article  PubMed  CAS  Google Scholar 

  • Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, Gibbs RA, Belmont JW, Boudreau A, Hardenbol P, Leal SM, Pasternak S, Wheeler DA, Willis TD, Yu F, Yang H, Zeng C, Gao Y, Hu H, Hu W, Li C, Lin W, Liu S, Pan H, Tang X, Wang J, Wang W, Yu J, Zhang B, Zhang Q, Zhao H, Zhou J, Gabriel SB, Barry R, Blumenstiel B, Camargo A, Defelice M, Faggart M, Goyette M, Gupta S, Moore J, Nguyen H, Onofrio RC, Parkin M, Roy J, Stahl E, Winchester E, Ziaugra L, Altshuler D, Shen Y, Yao Z, Huang W, Chu X, He Y, Jin L, Liu Y, Sun W, Wang H, Wang Y, Xiong X, Xu L, Waye MM, Tsui SK, Xue H, Wong JT, Galver LM, Fan JB, Gunderson K, Murray SS, Oliphant AR, Chee MS, Montpetit A, Chagnon F, Ferretti V, Leboeuf M, Olivier JF, Phillips MS, Roumy S, Sallee C, Verner A, Hudson TJ, Kwok PY, Cai D, Koboldt DC, Miller RD, Pawlikowska L, Taillon-Miller P, Xiao M, Tsui LC, Mak W, Song YQ, Tam PK, Nakamura Y, Kawaguchi T, Kitamoto T, Morizono T, Nagashima A, Ohnishi Y, Sekine A, Tanaka T, Tsunoda T, Deloukas P, Bird CP, Delgado M, Dermitzakis ET, Gwilliam R, Hunt S, Morrison J, Powell D, Stranger BE, Whittaker P, Bentley DR, Daly MJ, de Bakker PI, Barrett J, Chretien YR, Maller J, McCarroll S, Patterson N, Pe’er I, Price A, Purcell S, Richter DJ, Sabeti P, Saxena R, Schaffner SF, Sham PC, Varilly P, Stein LD, Krishnan L, Smith AV, Tello-Ruiz MK, Thorisson GA, Chakravarti A, Chen PE, Cutler DJ, Kashuk CS, Lin S, Abecasis GR, Guan W, Li Y, Munro HM, Qin ZS, Thomas DJ, McVean G, Auton A, Bottolo L, Cardin N, Eyheramendy S, Freeman C, Marchini J, Myers S, Spencer C, Stephens M, Donnelly P, Cardon LR, Clarke G, Evans DM, Morris AP, Weir BS, Mullikin JC, Sherry ST, Feolo M, Skol A, Zhang H, Matsuda I, Fukushima Y, Macer DR, Suda E, Rotimi CN, Adebamowo CA, Ajayi I, Aniagwu T, Marshall PA, Nkwodimmah C, Royal CD, Leppert MF, Dixon M, Peiffer A, Qiu R, Kent A, Kato K, Niikawa N, Adewole IF, Knoppers BM, Foster MW, Clayton EW, Watkin J, Muzny D, Nazareth L, Sodergren E, Weinstock GM, Yakub I, Birren BW, Wilson RK, Fulton LL, Rogers J, Burton J, Carter NP, Clee CM, Griffiths M, Jones MC, McLay K, Plumb RW, Ross MT, Sims SK, Willey DL, Chen Z, Han H, Kang L, Godbout M, Wallenburg JC, L’Archeveque P, Bellemare G, Saeki K, An D, Fu H, Li Q, Wang Z, Wang R, Holden AL, Brooks LD, McEwen JE, Guyer MS, Wang VO, Peterson JL, Shi M, Spiegel J, Sung LM, Zacharia LF, Collins FS, Kennedy K, Jamieson R, Stewart J (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449:851–861

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara A, Inukai T, Kim BM, Masuta C (2011) Combinations of a host resistance gene and the CI gene of turnip mosaic virus differentially regulate symptom expression in Brassica rapa cultivars. Arch Virol 156:1575–1581

    Article  PubMed  CAS  Google Scholar 

  • Gallois JL, Charron C, Sanchez F, Pagny G, Houvenaghel MC, Moretti A, Ponz F, Revers F, Caranta C, German-Retana S (2010) Single amino acid changes in the turnip mosaic virus viral genome-linked protein (VPg) confer virulence towards Arabidopsis thaliana mutants knocked out for eukaryotic initiation factors eIF(iso)4E and eIF(iso)4G. J Gen Virol 91:288–293

    Article  PubMed  CAS  Google Scholar 

  • Green SK, Deng TC (1985) Turnip mosaic virus strains in cruciferous hosts in Taiwan. Plant Dis 69:28–31

    Article  Google Scholar 

  • He XF, Fang YY, Feng L, Guo HS (2008) Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR–NBS–LRR class R gene-derived novel miRNA in Brassica. FEBS Lett 582:2445–2452

    Article  PubMed  CAS  Google Scholar 

  • Hughes SL, Hunter PJ, Sharpe AG, Kearsey MJ, Lydiate DJ, Walsh JA (2003) Genetic mapping of the novel Turnip mosaic virus resistance gene TuRB03 in Brassica napus. Theor Appl Genet 107:1169–1173

    Article  PubMed  CAS  Google Scholar 

  • Hyten DL, Song Q, Choi IY, Yoon MS, Specht JE, Matukumalli LK, Nelson RL, Shoemaker RC, Young ND, Cregan PB (2008) High-throughput genotyping with the GoldenGate assay in the complex genome of soybean. Theor Appl Genet 116:945–952

    Article  PubMed  CAS  Google Scholar 

  • Jenner CE, Walsh JA (1996) Pathotypic variation in turnip mosaic virus with special reference to European isolates. Plant Pathol 45:848–856

    Article  Google Scholar 

  • Jenner CE, Wang X, Ponz F, Walsh JA (2002) A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Res 86:1–6

    Article  PubMed  CAS  Google Scholar 

  • Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, Drabek J, Lopez R, Price HJ (2005) Evolution of genome size in Brassicaceae. Ann Bot 95:229–235

    Article  PubMed  CAS  Google Scholar 

  • Kaneko YH, Inukai T, Suehiro N, Natsuaki T, Masuta C (2004) Fine genetic mapping of the TuNI locus causing systemic veinal necrosis by turnip mosaic virus infection in Arabidopsis thaliana. Theor Appl Genet 110:33–40

    Article  PubMed  CAS  Google Scholar 

  • Kang BC, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Chung TY, King GJ, Jin M, Yang TJ, Jin YM, Kim HI, Park BS (2006) A sequence-tagged linkage map of Brassica rapa. Genetics 174:29–39

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim H, Choi SR, Bae J, Hong CP, Lee SY, Hossain MJ, Van Nguyen D, Jin M, Park BS, Bang JW, Bancroft I, Lim YP (2009) Sequenced BAC anchored reference genetic map that reconciles the ten individual chromosomes of Brassica rapa. BMC Genomics 10:432

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim J, Kang W-H, Yang H-B, Park S, YuH J, Jang C-S, Kang B-C (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

    Article  CAS  Google Scholar 

  • Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12:1046–1051

    Article  PubMed  CAS  Google Scholar 

  • Liu XP, Lu WC, Liu BX, Li SY, Li JL, Zhao ZY, Wang HJ, Wang CH (1990a) A study on TuMV strain differentiation on cruciferous vegetables from ten regions of China: identification results with Green’s methods. Virologica Sinica 1:82–87

    Google Scholar 

  • Liu XP, Lu WC, Liu YK, Li JL (1990b) A study on TuMV strain differentiation of cruciferous vegetables from ten provinces in China: new host differentiator screening and strain classification. Chin Sci Bull 35:1734–1739

    Google Scholar 

  • Liu B, Wang Y, Zhai W, Deng J, Wang H, Cui Y, Cheng F, Wang X, Wu J (2013) Development of InDel markers for Brassica rapa based on whole-genome re-sequencing. Theor Appl Genet 126:231–239

    Article  PubMed  CAS  Google Scholar 

  • Mun J-H, Yu H-J, Park S, Park BS (2009) Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Mol Genet Genomics 282:617–631

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Park S, Yu H-J, Mun J-H, Lee SC (2010) Genome-wide discovery of DNA polymorphism in Brassica rapa. Mol Genet Genomics 283:135–145

    Article  PubMed  CAS  Google Scholar 

  • Provvidenti R (1980) Evaluation of Chinese cabbage cultivars from Japan and the People’s Republic of China for resistance to turnip mosaic virus and cauliflower mosaic virus. J Amer Soc Hort Sci 105:571–573

    Google Scholar 

  • Qian W, Zhang S, Li F, Zhang H, Wu J, Wang X, Walsh JA, Sun R (2013) Mapping and candidate-gene screening of the novel Turnip mosaic virus resistance gene retr02 in Chinese cabbage (Brassica rapa L.). Theor Appl Genet 126:179–188

    Google Scholar 

  • Ramchiary N, Lim YP (2011) Genetics of Brassica rapa L. In: Schmidt R, Bancroft I (eds) Genetics and genomics of the Brassicaceae. Springer, New York

    Google Scholar 

  • Ramchiary N, Nguyen VD, Li X, Hong CP, Dhandapani V, Choi SR, Yu G, Piao ZY, Lim YP (2011) Genic microsatellite markers in Brassica rapa: development, characterization, mapping, and their utility in other cultivated and wild Brassica relatives. DNA Res 18:305–320

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR, Roose ML, Svensson JT, Stein N, Varshney RK, Marshall DF, Graner A, Close TJ, Waugh R (2006) Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc Natl Acad Sci USA 103:18656–18661

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Misener S, Krawetz S (eds) Bioinformatics methods and protocols. Humana Press, p 365–386

  • Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32:1067–1075

    Article  PubMed  CAS  Google Scholar 

  • Rusholme RL, Higgins EE, Walsh JA, Lydiate DJ (2007) Genetic control of broad-spectrum resistance to turnip mosaic virus in Brassica rapa (Chinese cabbage). J Gen Virol 88:3177–3186

    Article  PubMed  CAS  Google Scholar 

  • Seo MS, Jin M, Lee SS, Kwon SJ, Mun J-H, Park BS, Visser RG, Bonnema G, Sohn SH (2013) Mapping quantitative trait loci for tissue culture response in VCS3M-DH population of Brassica rapa. Plant Cell Rep 32:1251–1261

    Article  PubMed  CAS  Google Scholar 

  • Suh SK, Green SK, Park HG (1995) Genetics of resistance to five strains of turnip mosaic virus in Chinese cabbage. Euphytica 81:71–77

    Article  Google Scholar 

  • The Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

  • U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389–452

    Google Scholar 

  • van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands

  • Walsh JA, Sharpe AG, Jenner CE, Lydiate DJ (1999) Characterisation of resistance to turnip mosaic virus in oilseed rape (Brassica napus) and genetic mapping of TuRB01. Theor Appl Genet 99:1149–1154

    Google Scholar 

  • Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4:e8451

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yoshii M, Nishikiori M, Tomita K, Yoshioka N, Kozuka R, Naito S, Ishikawa M (2004) The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J Virol 78:6102–6111

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang FL, Wang M, Liu XC, Zhao XY, Yang JP (2008) Quantitative trait loci analysis for resistance against turnip mosaic virus based on a doubled-haploid population in Chinese cabbage. Plant Breeding 127:82–86

    Google Scholar 

  • Zhang X, Cal AJ, Borevitz JO (2011) Genetic architecture of regulatory variation in Arabidopsis thaliana. Genome Res 21:725–733

    Article  PubMed Central  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants to HJY from The Catholic University of Korea (M-2010-B0002-00157), the Next-Generation Biogreen21 program (PJ008019), and the National Research Foundation of Korea (2011–0013214).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hee-Ju Yu.

Additional information

Communicated by S. Hohmann.

H. Chung, Y.-M. Jeong, and J.-H. Mun contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chung, H., Jeong, YM., Mun, JH. et al. 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 (2014). https://doi.org/10.1007/s00438-013-0798-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-013-0798-9

Keywords

Navigation