Skip to main content
Log in

Genetic linkage map construction and QTL mapping of cadmium accumulation in radish (Raphanus sativus L.)

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Cadmium (Cd) is a widespread soil pollutant and poses a significant threat to human health via the food chain. Large phenotypic variations in Cd concentration of radish roots and shoots have been observed. However, the genetic and molecular mechanisms of Cd accumulation in radish remain to be elucidated. In this study, a genetic linkage map was constructed using an F2 mapping population derived from a cross between a high Cd-accumulating cultivar NAU-Dysx and a low Cd-accumulating cultivar NAU-Yh. The linkage map consisted of 523 SRAP, RAPD, SSR, ISSR, RAMP, and RGA markers and had a total length of 1,678.2 cM with a mean distance of 3.4 cM between two markers. All mapped markers distributed on nine linkage groups (LGs) having sizes between 134.7 and 236.8 cM. Four quantitative trait loci (QTLs) for root Cd accumulation were mapped on LGs 1, 4, 6, and 9, which accounted for 9.86 to 48.64 % of all phenotypic variance. Two QTLs associated with shoot Cd accumulation were detected on LG1 and 3, which accounted for 17.08 and 29.53 % of phenotypic variance, respectively. A major-effect QTL, qRCd9 (QTL for root Cd accumulation on LG9), was identified on LG 9 flanked by NAUrp011_754 and EM5me6_286 markers with a high LOD value of 23.6, which accounted for 48.64 % of the total phenotypic variance in Cd accumulation of F2 lines. The results indicated that qRCd9 is a novel QTL responsible for controlling root Cd accumulation in radish, and the identification of specific molecular markers tightly linked to the major QTL could be further applied for marker-assisted selection (MAS) in low-Cd content radish breeding program.

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

  • Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745

    Article  PubMed  CAS  Google Scholar 

  • Bassam BJ, Anollés GC, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83

    Article  PubMed  CAS  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

    Article  PubMed  CAS  Google Scholar 

  • Bett KE, Lydiate DJ (2003) Genetic analysis and genome mapping in Raphanus. Genome 46:423–430

    Article  PubMed  CAS  Google Scholar 

  • Budahn H, Peterka H, Mousa MA, Ding Y, Zhang S, Li J (2009) Molecular mapping in oil radish (Raphanus sativus L.) and QTL analysis of resistance against beet cyst nematode (Heterodera schachtii). Theor Appl Genet 118:775–782

    Article  PubMed  Google Scholar 

  • Choi SR, Teakle GR, Plaha P, Kim JH, Allender CJ, Beynon E, Piao ZY, Soengas P, Han TH, King GJ, Baker GC, Hand P, Lydiate DJ, Batley J, Edwards D, Koo DH, Bang JW, Park B-S, Lim YP (2007) The reference genetic linkage map for the multinational Brassica rapa genome sequencing project. Theor Appl Genet 115:777–792

    Article  PubMed  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Clarke JM, Leisle D, Kopytko GL (1997) Inheritance of cadmium concentration in five durum wheat crosses. Crop Sci 37:1722–1725

    Article  Google Scholar 

  • Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065

    Article  PubMed  CAS  Google Scholar 

  • Deckert J (2005) Cadmium toxicity in plants: is there any analogy to its carcinogenic effect in mammalian cells? Biometals 18:475–481

    Article  PubMed  CAS  Google Scholar 

  • Deniau AX, Pieper B, Ten Bookum WM, Lindhout P, Aarts MGM, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920

    Article  PubMed  CAS  Google Scholar 

  • Fourmann M, Charlot F, Froger N, Delourme R, Brunel D (2001) Expression, mapping, and genetic variability of Brassica napus disease resistance gene analogues. Genome 44:1083–1099

    PubMed  CAS  Google Scholar 

  • Gao MQ, Li GY, Yang B, Qiu D, Farnham M, Quiros CF (2007) High-density Brassica oleracea linkage map: identification of useful new linkages. Theor Appl Genet 115:277–287

    Article  PubMed  CAS  Google Scholar 

  • Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. Can J Plant Sci 78:1–17

    Article  CAS  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa S, Ae N, Yano M (2005) Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol 168:345–350

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T, Yano M (2010) A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J Exp Bot 61:923–934

    Article  PubMed  CAS  Google Scholar 

  • Jegadeesan S, Yu KF, Poysa V, Gawalko E, Morrison MJ, Shi C, Cober E (2010) Mapping and validation of simple sequence repeat markers linked to a major gene controlling seed cadmium accumulation in soybean [Glycine max (L.) Merr]. Theor Appl Genet 121:283–294

    Article  PubMed  CAS  Google Scholar 

  • Kamei A, Tsuro M, Kubo N, Hayashi T, Wang N, Fujimura T, Hirai M (2010) QTL mapping of clubroot resistance in radish (Raphanus sativus L.). Theor Appl Genet 120:1021–1027

    Article  PubMed  Google Scholar 

  • Kashiwagi T, Shindoh K, Hirotsu N, Ishimaru K (2009) Evidence for separate pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biol 9:8. doi:10.1186/1471-2229-9-8

    Article  PubMed  Google Scholar 

  • Knox RE, Pozniak CJ, Clarke FR, Clarke JM, Houshmand S, Singh AK (2009) Chromosomal location of the cadmium uptake gene (Cdu1) in durum wheat. Genome 52:741–747

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Li GY, Quiros CF (2001) Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor Appl Genet 103:455–461

    Article  CAS  Google Scholar 

  • Li F, Hasegawa Y, Saito M, Shirasawa S, Fukushima A, Ito T, Fujii H, Kishitani S, Kitashiba H, Nishio T (2011) Extensive chromosome homoeology among Brassiceae species were revealed by comparative genetic mapping with high-density EST-based SNP markers in radish (Raphanus sativus L.). DNA Res 18:401–411

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Guo W, Zhu X, Zhang T (2003) Inheritance and fine mapping of fertility-restoration for cytoplasmic male sterility in Gossypium hirsutum L. Theor Appl Genet 106:461–469

    PubMed  CAS  Google Scholar 

  • Liu L, Zhu X, Gong Y, Song X, Wang Y, Zhao L, Wang L (2007) Genetic diversity analysis of radish germplasm with RAPD, AFLP and SRAP markers. Acta Hortic 760:125–130

    CAS  Google Scholar 

  • Liu L, Yang J, Hou X, Gong Y, Zhu X, Wang F, Zhang C, Chu R (2008) Genotypic differences of Cd uptake and distribution in radish (Raphanus sativus L.). Bioinformatics and Biomedical Engineering (ICBBE) 4696–4699. doi:10.1109/ICBBE.2008.332

  • McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214

    Article  CAS  Google Scholar 

  • Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:464–469

    Article  CAS  Google Scholar 

  • Saal B, Struss D (2005) RGA- and RAPD-derived SCAR markers for a Brassica B-genome introgression conferring resistance to blackleg in oilseed rape. Theor Appl Genet 111:281–290

    Article  PubMed  CAS  Google Scholar 

  • Shirasawa K, Oyama M, Hirakawa H, Sato S, Tabata S, Fujioka T, Kimizuka-Takagi C, Sasamoto S, Watanabe A, Kato M, Kishida Y, Kohara M, Takahashi C, Tsuruoka H, Wada T, Sakai T, Isobe S (2011) An EST-SSR linkage map of Raphanus sativus and comparative genomics of the Brassicaceae. DNA Res 18:221–232

    Article  PubMed  CAS  Google Scholar 

  • Smooker AM, Wells R, Morgan C, Beaudoin F, Cho K, Fraser F, Bancroft I (2011) The identification and mapping of candidate genes and QTL involved in the fatty acid desaturation pathway in Brassica napus. Theor Appl Genet 122:1075–1090

    Article  PubMed  CAS  Google Scholar 

  • Suwabe K, Iketani H, Nunome T, Kage T, Hirai M (2002) Isolation and characterization of microsatellites in Brassica rapa L. Theor Appl Genet 104:1092–1098

    Article  PubMed  CAS  Google Scholar 

  • 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. Genet 173:309–319

    Article  CAS  Google Scholar 

  • Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62:4843–4850

    Article  PubMed  CAS  Google Scholar 

  • Tanhuanpää P, Kalendar R, Schulman AH, Kiviharju E (2007) A major gene for grain cadmium accumulation in oat (Avena sativa L.). Genome 50:588–594

    Article  PubMed  Google Scholar 

  • Tezuka K, Miyadate H, Katou K, Kodama I, Matsumoto S, Kawamoto T, Masaki S, Satoh H, Yamagucji M, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2010) A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Kohu. Theor Appl Genet 120:1175–1182

    Article  PubMed  CAS  Google Scholar 

  • Tsuro M, Suwabe K, Kubo N, Matsumoto S, Hirai M (2005) Construction of a linkage map of radish (Raphanus sativus L.), based on AFLP and Brassica-SSR markers. Breed Sci 55:107–111

    Article  CAS  Google Scholar 

  • Tsuro M, Suwabe K, Kubo N, Matsumoto S, Hirai M (2008) Mapping of QTLs controlling for root shape and red pigmentation in radish, Raphanus sativus L. Breed Sci 58:55–61

    Article  CAS  Google Scholar 

  • Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182:644–653

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap Version 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTL. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang L, He Q (2005) China radish. Scientific and Technical Documents Publishing House, Beijing

    Google Scholar 

  • Wang N, Hu J, Ohsawa R, Ohta M, Fujimura T (2007a) Identification and characterization of microsatellite markers derived from expressed sequence tags (ESTs) of radish (Raphanus sativus L.). Mol Ecol Notes 7:503–506

    Article  CAS  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2007b) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC

  • Wiebe K, Harris NS, Faris JD, Clarke JM, Knox RE, Taylor GJ, Pozniak CJ (2010) Targeted mapping of Cdu1, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum). Theor Appl Genet 121:1047–1058

    Article  PubMed  CAS  Google Scholar 

  • Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  PubMed  CAS  Google Scholar 

  • Xue D, Chen M, Zhang G (2009) Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 165:587–596

    Article  CAS  Google Scholar 

  • Yamamoto T, Yonemaru J, Yano M (2009) Towards the understanding of complex traits in rice: Substantially or superficially? DNA Res 16:141–154

    Article  PubMed  CAS  Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was in part supported by grants from the Program for NCET, MOE (NCET-10-047), the National Key Technologies R & D Program of China (2009BADB8B03), Key Technology R & D Program of Jiangsu Province (BE2010328) and the Priority Academic Program Development of Jiangsu Higher Education Institutions(PAPD). We thank Dr. J. Hu from USDA-ARS for his critical review and helpful comments during the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liwang Liu.

Additional information

Communicated by I. Rajcan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, L., Wang, L., Gong, Y. et al. Genetic linkage map construction and QTL mapping of cadmium accumulation in radish (Raphanus sativus L.). Theor Appl Genet 125, 659–670 (2012). https://doi.org/10.1007/s00122-012-1858-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-012-1858-y

Keywords

Navigation