Log in

Regulation of copper transport in Arabidopsis thaliana: a biochemical oscillator?

  • Minireview
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

Plants are among the most versatile higher eukaryotes in accommodating environmental copper availability to largely variable demands. In particular, copper deficiency in soils is a threat for plant survival since it mostly affects reproductive structures. One of the strategies that plant cells use to overcome this situation is to increase copper levels by expressing high-affinity copper transporters delivering the metal to the cytosol. In this minireview, we discuss recent advances in the structure, function, and regulation of the CTR/COPT family of copper transporters, and pay special attention to the Arabidopsis thaliana counterparts. These are constituted by transmembrane polypeptides, containing several copper-binding sequences of functional and/or regulatory value, and assembling as trimers. Copper deficiency activates the expression of some members of the COPT family via the interaction of the SPL7 transcription factor with reiterative GTAC motifs present in their promoters. Interestingly, the regulation of the synthesis of these transporters by copper itself constitutes a negative-feedback loop that could cause a sustained oscillation in the cytosolic copper levels. We analyze the theoretical conditions required for this hypothetical copper oscillation and the potential advantages of synchronization with other cycles. Diverse data in other organisms point to the relationship between copper homeostasis and circadian cycles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Halliwell B, Gutteridge JM (1984) Biochem J 219:1–14

    PubMed  CAS  Google Scholar 

  2. Lippard SJ, Berg JM (1994) Principles of bioinorganic chemistry. University Science Books, Mill Valley

    Google Scholar 

  3. Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) New Phytol 182:799–816

    Article  CAS  Google Scholar 

  4. Pilon M, Cohu CM, Ravet K, Abdel-Ghany SE, Gaymard F (2009) Curr Opin Plant Biol 12:347–357

    Article  PubMed  CAS  Google Scholar 

  5. Puig S, Penarrubia L (2009) Curr Opin Plant Biol 12:299–306

    Article  PubMed  CAS  Google Scholar 

  6. Puig S, Andres-Colas N, Garcia-Molina A, Penarrubia L (2007) Plant Cell Environ 30:271–290

    Article  PubMed  CAS  Google Scholar 

  7. Märschner H (2002) Mineral nutrition in higher plants. Academic Press, London

    Google Scholar 

  8. Bernal M, Ramiro MV, Cases R, Picorel R, Yruela I (2006) Physiol Plant 127:312–325

    Article  CAS  Google Scholar 

  9. Puig S, Thiele DJ (2002) Curr Opin Chem Biol 6:171–180

    Article  PubMed  CAS  Google Scholar 

  10. Kim BE, Nevitt T, Thiele DJ (2008) Nat Chem Biol 4:176–185

    Article  PubMed  CAS  Google Scholar 

  11. Sancenon V, Puig S, Mira H, Thiele DJ, Penarrubia L (2003) Plant Mol Biol 51:577–587

    Article  PubMed  CAS  Google Scholar 

  12. Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L (2004) J Biol Chem 279:15348–15355

    Article  PubMed  CAS  Google Scholar 

  13. Kampfenkel K, Kushnir S, Babiychuk E, Inze D, Van Montagu M (1995) J Biol Chem 270:28479–28486

    Article  PubMed  CAS  Google Scholar 

  14. Hassett R, Kosman DJ (1995) J Biol Chem 270:128–134

    Article  PubMed  CAS  Google Scholar 

  15. Lee J, Pena MM, Nose Y, Thiele DJ (2002) J Biol Chem 277:4380–4387

    Article  PubMed  CAS  Google Scholar 

  16. Mukherjee I, Campbell NH, Ash JS, Connolly EL (2006) Planta 223:1178–1190

    Article  PubMed  CAS  Google Scholar 

  17. Wu H, Li L, Du J, Yuan Y, Cheng X, Ling HQ (2005) Plant Cell Physiol 46:1505–1514

    Article  PubMed  CAS  Google Scholar 

  18. Puig S, Lee J, Lau M, Thiele DJ (2002) J Biol Chem 277:26021–26030

    Article  PubMed  CAS  Google Scholar 

  19. Eisses JF, Kaplan JH (2002) J Biol Chem 277:29162–29171

    Article  PubMed  CAS  Google Scholar 

  20. Klomp AE, Juijn JA, van der Gun LT, van den Berg IE, Berger R, Klomp LW (2003) Biochem J 370:881–889

    Article  PubMed  CAS  Google Scholar 

  21. Beaudoin J, Laliberte J, Labbe S (2006) Microbiology 152:209–222

    Article  PubMed  CAS  Google Scholar 

  22. Jiang J, Nadas IA, Kim MA, Franz KJ (2005) Inorg Chem 44:9787–9794

    Article  PubMed  CAS  Google Scholar 

  23. Page MD, Kropat J, Hamel PP, Merchant SS (2009) Plant Cell 21:928–943

    Article  PubMed  CAS  Google Scholar 

  24. Dancis A, Haile D, Yuan DS, Klausner RD (1994) J Biol Chem 269:25660–25667

    PubMed  CAS  Google Scholar 

  25. Pena MM, Puig S, Thiele DJ (2000) J Biol Chem 275:33244–33251

    Article  PubMed  CAS  Google Scholar 

  26. Aller SG, Unger VM (2006) Proc Natl Acad Sci USA 103:3627–3632

    Article  PubMed  CAS  Google Scholar 

  27. Aller SG, Eng ET, De Feo CJ, Unger VM (2004) J Biol Chem 279:53435–53441

    Article  PubMed  CAS  Google Scholar 

  28. De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM (2009) Proc Natl Acad Sci USA 106:4237–4242

    Article  PubMed  Google Scholar 

  29. Liu J, Sitaram A, Burd CG (2007) Traffic 8:1375–1384

    Article  PubMed  CAS  Google Scholar 

  30. Wu X, Sinani D, Kim H, Lee J (2009) J Biol Chem 284:4112–4122

    Article  PubMed  CAS  Google Scholar 

  31. Ooi CE, Rabinovich E, Dancis A, Bonifacino JS, Klausner RD (1996) EMBO J 15:3515–3523

    PubMed  CAS  Google Scholar 

  32. Petris MJ, Smith K, Lee J, Thiele DJ (2003) J Biol Chem 278:9639–9646

    Article  PubMed  CAS  Google Scholar 

  33. Guo Y, Smith K, Lee J, Thiele DJ, Petris MJ (2004) J Biol Chem 279:17428–17433

    Article  PubMed  CAS  Google Scholar 

  34. **ao Z, Loughlin F, George GN, Howlett GJ, Wedd AG (2004) J Am Chem Soc 126:3081–3090

    Article  PubMed  CAS  Google Scholar 

  35. **ao Z, Wedd AG (2002) Chem Commun 588–589

  36. Sinani D, Adle DJ, Kim H, Lee J (2007) J Biol Chem 282:26775–26785

    Article  PubMed  CAS  Google Scholar 

  37. Bellemare DR, Shaner L, Morano KA, Beaudoin J, Langlois R, Labbe S (2002) J Biol Chem 277:46676–46686

    Article  PubMed  CAS  Google Scholar 

  38. Rees EM, Lee J, Thiele DJ (2004) J Biol Chem 279:54221–54229

    Article  PubMed  CAS  Google Scholar 

  39. Rees EM, Thiele DJ (2007) J Biol Chem 282:21629–21638

    Article  PubMed  CAS  Google Scholar 

  40. Balamurugan AN, Chang Y, Bertera S, Sands A, Shankar V, Trucco M, Bottino R (2006) Diabetologia 49:1845–1854

    Article  PubMed  CAS  Google Scholar 

  41. Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Biochim Biophys Acta 1763:578–594

    Article  PubMed  CAS  Google Scholar 

  42. Abdel-Ghany SE, Muller-Moule P, Niyogi KK, Pilon M, Shikanai T (2005) Plant Cell 17:1233–1251

    Article  PubMed  CAS  Google Scholar 

  43. Cohu CM, Pilon M (2007) Physiol Plant 129:747–755

    Article  CAS  Google Scholar 

  44. Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant S (2005) Proc Natl Acad Sci USA 102:18730–18735

    Article  PubMed  CAS  Google Scholar 

  45. Nagae M, Nakata M, Takahashi Y (2008) Plant Physiol 146:1687–1696

    Article  PubMed  CAS  Google Scholar 

  46. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) Plant Cell 21:347–361

    Article  PubMed  CAS  Google Scholar 

  47. Klein J, Saedler H, Huijser P (1996) Mol Gen Genet 250:7–16

    PubMed  CAS  Google Scholar 

  48. Birkenbihl RP, Jach G, Saedler H, Huijser P (2005) J Mol Biol 352:585–596

    Article  PubMed  CAS  Google Scholar 

  49. Sunkar R, Kapoor A, Zhu JK (2006) Plant Cell 18:2051–2065

    Article  PubMed  CAS  Google Scholar 

  50. Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) J Biol Chem 282:16369–16378

    Article  PubMed  CAS  Google Scholar 

  51. Dugas DV, Bartel B (2008) Plant Mol Biol 67:403–417

    Article  PubMed  CAS  Google Scholar 

  52. Abdel-Ghany SE, Pilon M (2008) J Biol Chem 283:15932–15945

    Article  PubMed  CAS  Google Scholar 

  53. Novak B, Tyson JJ (2008) Nat Rev Mol Cell Biol 9:981–991

    Article  PubMed  CAS  Google Scholar 

  54. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM, Robertson FC, Jakobsen MK, Goncalves J, Sanders D, Webb AA (2007) Science 318:1789–1792

    Article  PubMed  CAS  Google Scholar 

  55. Riese M, Zobell O, Saedler H, Huijser P (2008) Planta 227:505–515

    Article  PubMed  CAS  Google Scholar 

  56. Bell-Pedersen D, Shinohara ML, Loros JJ, Dunlap JC (1996) Proc Natl Acad Sci USA 93:13096–13101

    Article  PubMed  CAS  Google Scholar 

  57. Borjigin J, Payne AS, Deng J, Li X, Wang MM, Ovodenko B, Gitlin JD, Snyder SH (1999) J Neurosci 19:1018–1026

    PubMed  CAS  Google Scholar 

  58. Tobler I, Gaus SE, Deboer T, Achermann P, Fischer M, Rulicke T, Moser M, Oesch B, McBride PA, Manson JC (1996) Nature 380:639–642

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the BIO2008-02835 grant to L.P. from the Spanish Ministry of Science and Innovation (Spain) and by FEDER funds from the European Union. S.P. is the recipient of a Ramón y Cajal contract with the University of Valencia. We apologize to colleagues whose relevant work could not be cited owing to limited space.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lola Peñarrubia.

Additional information

This article will be printed in the upcoming Journal of Biological Inorganic Chemistry special issue Cell Biology of Copper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 64 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peñarrubia, L., Andrés-Colás, N., Moreno, J. et al. Regulation of copper transport in Arabidopsis thaliana: a biochemical oscillator?. J Biol Inorg Chem 15, 29–36 (2010). https://doi.org/10.1007/s00775-009-0591-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-009-0591-8

Keywords

Navigation