Skip to main content
Log in

Overexpression of a yeast cadmium factor 1 (YCF1) enhances heavy metal tolerance and accumulation in Brassica juncea

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

A yeast cadmium factor 1 (YCF1) is a member of the ATP-binding cassette (ABC) transporter family associated with multi-drug resistance, and it is localized at the vacuolar membrane in Saccharomyces cerevisiae. To determine ability to increase heavy metal tolerance and accumulation, YCF1 was introduced into Brassica juncea plants by Agrobacterium-mediated genetic transformation. YCF1 gene presence in transgenic plants was demonstrated by polymerase chain reaction (PCR). Reverse transcriptase-PCR analysis confirmed YCF1 gene expression in the transgenic plants, but the degree of YCF1 expression varied among the lines. YCF1 overexpression in B. juncea conferred enhanced tolerance to cadmium (Cd[II]) and lead (Pb[II]) stress. Transgenic B. juncea seedlings showed 1.3- to 1.6-fold tolerance to Cd stress and 1.2- to 1.4-fold tolerance to Pb stress compared to wild type (WT) plants (per gram fresh weight). Most importantly, the shoot tissues of transgenic seedlings contained about 1.5- to 2-fold higher Cd(II) and Pb(II) levels than those of WT, demonstrating significantly increased accumulation of both Cd(II) and Pb(II) in transgenic plants.

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
Fig. 5

Similar content being viewed by others

Abbreviations

ABC:

ATP-binding cassette

BA:

6-Benzyladenine

HPT:

Hygromycin phosphotransferase

ICP-MS:

Inductively coupled plasma mass spectrophotometer

MS:

Murashige and Skoog medium

NAA:

α-Naphthaleneacetic acid

OD:

Optical density

RT–PCR:

Reverse transcriptase-polymerase chain reaction

YCF1:

Yeast cadmium factor 1

References

  • Bhuiyan MSU, Min SR, Choi KS, Lim YP, Liu JR (2009) Factors for high frequency plant regeneration in tissue cultures of Indian mustard (Brassica juncea L.). J Plant Biotechnol 36:137–143

    Article  Google Scholar 

  • Bowyer P (2001) DNA-mediated transformation of fungi. In: Talbot N (ed) Molecular and cellular biology of filamentous fungi. Oxford Univ Press, Oxford, pp 33–46

    Google Scholar 

  • Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  PubMed  CAS  Google Scholar 

  • Clemente R, Walker DJ, Bernal MP (2005) Uptake of heavy metals and As by Brassica juncea grown on contaminated soil in Aznalcollar (Spain): the effects of soil amendments. Environ Pollut 138:46–58

    Article  PubMed  CAS  Google Scholar 

  • Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110:715–719

    PubMed  CAS  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    Article  PubMed  CAS  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Dushenkov V, Kumar PBAN, Motto H, Raskin I (1995) Rhizofiltration: the use of plants to remove heavy metals from aqueous streams. Environ Sci Technol 29:1239–1245

    Article  CAS  Google Scholar 

  • Fassel VA (1978) Quantitative elemental analyses by plasma emission spectroscopy. Science 202:183–191

    Article  PubMed  CAS  Google Scholar 

  • Gasic K, Korban SS (2007) Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance. Plant Mol Biol 64:361–369

    Article  PubMed  CAS  Google Scholar 

  • Hirchi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–134

    Article  Google Scholar 

  • Jiang W, Liu D, Hou W (2000) Hyperaccumulation of lead by roots, hypocotyls, and shoots of Brassica juncea. Biol Plantarum 43:603–606

    Article  CAS  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–76

    CAS  Google Scholar 

  • Kim D-Y, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932

    Article  PubMed  CAS  Google Scholar 

  • Kim D-Y, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    Article  PubMed  CAS  Google Scholar 

  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    Article  PubMed  CAS  Google Scholar 

  • Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238

    Article  CAS  Google Scholar 

  • Li Z-S, Lu Y-P, Zhen R-G, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. PNAS 94:42–47

    Article  PubMed  CAS  Google Scholar 

  • Meyers DER, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localization of lead in the root system of Brassica juncea. Environ Pollut 153:323–332

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Pilon-Smits EAH (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  PubMed  CAS  Google Scholar 

  • Pilon-Smits EAH, Pilon M (2002) Phytoremediation of metals using transgenic plants. Crit Rev Plant Sci 21:439–456

    Article  CAS  Google Scholar 

  • Pilon-Smits EAH, Hwang S, Mel Lytle C, Zhu Y, Tai JC, Bravo RC, Chen YC, Leustek T, Terry N (1999) Overexpression of ATP Sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 1999:123–132

    Article  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433

    PubMed  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  PubMed  CAS  Google Scholar 

  • Song W-Y, Sohn EJ, Martinoia E, Lee YJ, Yang Y-Y, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919

    Article  PubMed  CAS  Google Scholar 

  • Tong YP, Kneer R, Zhu Y-G (2004) Vacuolar compartmentalization: a second-generation approach to engineering plants for phytoremediation. Trends Plant Sci 9:7–9

    Article  PubMed  CAS  Google Scholar 

  • Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    Article  PubMed  CAS  Google Scholar 

  • Wangeline AL, Burkhead JL, Hale KL, Lindblom SD, Terry N, Pilon M, Pilon-Smits EAH (2004) Overexpression of ATP Sulfurylase in Indian mustard: effects on tolerance and accumulation of twelve metals. J Environ Qual 33:54–60

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Chai T, Zhang Y, Lang M, Han L (2009) The cation-efflux transporter BjCET2 mediates zinc and cadmium accumulation in Brassica juncea L. leaves. Plant Cell Rep 28:1235–1242

    Article  PubMed  CAS  Google Scholar 

  • Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid digestion and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plan 18:131–146

    Article  CAS  Google Scholar 

  • Zayed AM, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil 249:139–156

    Article  CAS  Google Scholar 

  • Zhao S-J, Zhang Z-C, Gao X, Toshun G, Qiu B-S (2009) Plant regeneration of the mining ecotype Sedum alfredii and cadmium hyperaccumulation in regenerated plants. Plant Cell Tiss Org Cult 99:9–16

    Article  CAS  Google Scholar 

  • Zhigang A, Cuijie L, Yuangang Z, Yejie D, Wachter A, Gromes R, Rausch T (2006) Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. J Exp Bot 57:3575–3582

    Article  PubMed  Google Scholar 

  • Zhu YL, Pilon-Smits EAH, Jouanin L, Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–79

    Article  CAS  Google Scholar 

  • Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ- glutamylcysteine synthetase. Plant Physiol 121:1169–1177

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD) (KRF-2007-211). Special thanks to Dr. JH Lee and Dr. JW Ahn for their valuable suggestions during the experiments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jang R. Liu.

Additional information

M. S. U. Bhuiyan and S. R. Min contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhuiyan, M.S.U., Min, S.R., Jeong, W.J. et al. Overexpression of a yeast cadmium factor 1 (YCF1) enhances heavy metal tolerance and accumulation in Brassica juncea . Plant Cell Tiss Organ Cult 105, 85–91 (2011). https://doi.org/10.1007/s11240-010-9845-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-010-9845-y

Keywords

Navigation