Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Engineering tolerance and accumulation of lead and cadmium in transgenic plants

Abstract

We have studied the utility of the yeast protein YCF1, which detoxifies cadmium by transporting it into vacuoles, for the remediation of lead and cadmium contamination. We found that the yeast YCF1-deletion mutant DTY167 was hypersensitive to Pb(II) as compared with wild-type yeast. DTY167 cells overexpressing YCF1 were more resistant to Pb(II) and Cd(II) than were wild-type cells, and accumulated more lead and cadmium. Analysis of transgenic Arabidopsis thaliana plants overexpressing YCF1 showed that YCF1 is functionally active and that the plants have enhanced tolerance of Pb(II) and Cd(II) and accumulated greater amounts of these metals. These results suggest that transgenic plants expressing YCF1 may be useful for phytoremediation of lead and cadmium.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: YCF1 confers Pb(II) and Cd(II) resistance to yeast.
Figure 2: Overexpression of YCF1 in ycf1 yeast grown on Pb(II)- or Cd(II)- containing medium elevates the lead and cadmium contents.
Figure 3: Expression of YCF1 in A. thaliana.
Figure 4: YCF1-transgenic A. thaliana plants show enhanced Pb(II) and Cd(II) resistance.
Figure 5: Lead and cadmium contents in YCF1-transgenic A. thaliana plants.

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  1. Salt, D.E., Smith, R.D. & Raskin, I. Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643–668 (1998).

    Article  CAS  Google Scholar 

  2. Lanphear, B.P. The paradox of lead poisoning prevention. Science 281, 1617–1618 (1998).

    Article  CAS  Google Scholar 

  3. Raskin, I. & Ensley, B.D. Phytoremediation of Toxic Metals (John Wiley & Sons, New York, 2000).

    Google Scholar 

  4. Vido, K.A. Proteome analysis of the cadmium response in Saccharomyces cerevisiae. J. Biol. Chem. 276, 8469–8474 (2001).

    Article  CAS  Google Scholar 

  5. Rugh, C.L. et al. Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc. Natl. Acad. Sci. USA 93, 3182–3187 (1996).

    Article  CAS  Google Scholar 

  6. Rugh, C.L. et al. Development of transgenic yellow poplar for mercury phytoremediation. Nat. Biotechnol. 16, 925–928 (1998).

    Article  CAS  Google Scholar 

  7. Zhu, Y.L. et al. Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119, 73–79 (1999).

    Article  CAS  Google Scholar 

  8. Zhu, Y.L. et al. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol. 121, 1169–1177 (1999).

    Article  CAS  Google Scholar 

  9. Salt, D.E. & Wagner, G.J. Cadmium transport across tonoplast of vesicles from oat roots. Evidence for a Cd2+/H+ antiport activity. J. Biol. Chem. 268, 12297–12302 (1993)

    CAS  PubMed  Google Scholar 

  10. Domínguez-Solís, J.R. et al. The cytosolic O-Acetylserine(thiol)lyase gene is regulated by heavy metal and can function in cadmium tolerance. J. Biol. Chem. 276, 9297–9302 (2001).

    Article  Google Scholar 

  11. Li, Z.S. et al. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc. Natl. Acad. Sci. USA 94, 42–47 (1997).

    Article  CAS  Google Scholar 

  12. Ghosh, M., Shen, J. & Rosen, B.P. Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 96, 5001–5006 (1999).

    Article  CAS  Google Scholar 

  13. Szczypka, M.S. et al. Yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem. 269, 22853–22857 (1994).

    CAS  PubMed  Google Scholar 

  14. Tommasini, R. et al. Transport of oxidized glutathione into barley vacuoles: evidence for the involvement of the glutathione-S-conjugate ATPase. Z. Naturforsch. C Biosci. 48C, 867–871 (1993).

    Article  Google Scholar 

  15. Clemens, S., Palmgren, M. & Krämer, U. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7, 309–315 (2002).

    Article  CAS  Google Scholar 

  16. Clemens, S. et al. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 18, 3325–3333 (1999).

    Article  CAS  Google Scholar 

  17. Cobbett, C.S. Phytochelatins and their roles in heavy metal detoxification. Curr. Opin. Plant Biol. 3, 211–216 (2000).

    Article  CAS  Google Scholar 

  18. Vatamaniuk, O.K. et al. AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc. Natl. Acad. Sci. USA 96, 7110–7115 (1999).

    Article  CAS  Google Scholar 

  19. Rensing, C., Sun, Y., Mitra, B. & Rosen, B.P. Pb(II)-translocating P-type ATPases. J. Biol. Chem. 273, 32614–32617 (1998).

    Article  CAS  Google Scholar 

  20. Tommasini, R. et al. The human multidrug resistance-associated protein functionally complements the yeast cadmium resistance factor. Proc. Natl. Acad. Sci. USA 93, 6743–6748 (1996).

    Article  CAS  Google Scholar 

  21. Ito, H. et al. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163–168 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Clough, S.J. & Bent, A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1988).

    Article  Google Scholar 

  23. Jin, J.B. et al. A New dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13, 1511–1526 (2001).

    Article  CAS  Google Scholar 

  24. Frangne, N. et al. Flavone glucoside uptake into barley mesophyll and Arabidopsis cell culture vacuoles. Energization occurs by H+-antiport and ATP-binding cassette-type mechanisms. Plant Physiol. 128, 726–733 (2002).

    Article  CAS  Google Scholar 

  25. Martinoia, E. et al. An ATP-dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants. Nature 364, 247–249 (1993).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dennis Thiele for the YCF1-null yeast line and its isogenic wild type, Yu-Young Kim for technical assistance, and Hyun-Soo Kim, Sandra Preveral and Pann-Ghill Suh for help with microscopy. This work was supported by grants awarded to Y.L. from POSCO and the National Research Laboratory Program of the Korean Ministry of Science and Technology, to E.M. from the Bundesamt für Bildung und Wissenschaft (BBW 00.0413; EU project Metallophytes EU Nr QLK3-CT-2000-00479) and the Körber Stiftung, and to I.H. from the Creative Research Initiative Program of the Ministry of Science and Technology of Korea (M10116000005-02F0000-00310).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Youngsook Lee.

Ethics declarations

Competing interests

The authors have applied for a Patent Cooperation Treaty patent, PCT/KR02/12934, titled “Transgenic organism expressing fungal MRP–like ABC transporters”.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, WY., Ju Sohn, E., Martinoia, E. et al. Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21, 914–919 (2003). https://doi.org/10.1038/nbt850

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt850

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing