Advertisement

Plant Molecular Biology

, Volume 52, Issue 5, pp 1077–1088 | Cite as

A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization

  • Stephen H. BurleighEmail author
  • Brian K. Kristensen
  • Iben Ellegaard Bechmann
Article

Abstract

Here we present a Zn transporter cDNA named MtZIP2 from the model legume Medicago truncatula. MtZIP2 encodes a putative 37 kDa protein with 8-membrane spanning domains and has moderate amino acid identity with the Arabidopsis thaliana Zn transporter AtZIP2p. MtZIP2 complemented a Zn-uptake mutant of yeast implying that the protein encoded by this gene can transport Zn across the yeast's plasma membrane. The product of a MtZIP2-GFP fusion construct introduced into onion cells by particle bombardment likewise localized to the plasma membrane. The MtZIP2 gene was expressed in roots and stems, but not in leaves of M. truncatula and, in contrast to all other plant Zn transporters characterized thus far, MtZIP2 was up-regulated in roots by Zn fertilization. Expression was highest in roots exposed to a toxic level of Zn. MtZIP2 expression was also examined in the roots of M. truncatula when colonized by the obligate plant symbiont, arbuscular mycorrhizal (AM) fungi, since AM fungi are renowned for their ability to supply plants with mineral nutrients, including Zn. Expression was down-regulated in the roots of the mycorrhizal plants and was associated with a reduced level of Zn within the host plant tissues.

Arbuscular mycorrhizal fungi gene expression Medicago truncatula plasma membrane transporter zinc 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Assuncao, A.G.L., Costa-Martins, P.D., De Folter, S., Vooijs, R., Schat, H. and Aarts, M.G.M. 2001. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24: 217-226.Google Scholar
  2. Bradley, R., Burt, A.J. and Read, D.J. 1981. Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. Nature 292: 335-337.Google Scholar
  3. Burleigh, S.H. 2001. Relative quantitative PCR to study nutrient transport processes in arbuscular mycorrhizas. Plant Science 160: 899-904.Google Scholar
  4. Burleigh, S.H. and Bechmann, I.E. 2002. Plant nutrient transporter regulation in arbuscular mycorrhizas. Plant Soil 244: 247-251.Google Scholar
  5. Burleigh, S.H. and Harrison, M.J. 1997. A novel gene whose expression in Medicago truncatula roots is suppressed in response to colonization by vesicular-arbuscular mycorhizal (VAM) fungi and to phosphate nutrition. Plant Mol. Biol. 34: 199-208.Google Scholar
  6. Burleigh, S.H., Cavagnaro, T. and Jakobsen, I. 2002. Functional diversity in arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53: 1593-1601.Google Scholar
  7. Chiou, T.J., Liu, H. and Harrison, M.J. 2001. The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J 25: 1-15.Google Scholar
  8. Clark, R.B. and Zeto, S.K. 2000. Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23: 867-902.Google Scholar
  9. Gallaud, I. 1905. Etudes sur les mycorrhizes endotrophs. Revue Generale de Botanique 17.Google Scholar
  10. Gietz, R.D. and Woods, R.A. 1994. High Efficiency transformation in yeast. In: J.A. Johnston (Ed.), Molecular Genetics of Yeast: Practical Approaches, Oxford University Press, Oxford, pp. 121-134.Google Scholar
  11. Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M.L. and Eide, D. 1998. Identification of a family of Zn transporter genes from Arabidopsis that respond to zinc deficiency. P Natl Acad Sci USA 95: 7220-7224.Google Scholar
  12. Guerinot, M.L. 2000. The ZIP family of metal transporters. BBA 1465: 190-198.Google Scholar
  13. Guerinot, M.L. and Eide, D. 1999. Zeroing in on zinc uptake in yeast and plants. Curr Opin Plant Biol 2: 244-249.Google Scholar
  14. Jauh, G.Y., Phillips, T.E. and Rogers, J.C. 1999. Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11: 1867-1882.Google Scholar
  15. Kuepper, H., Zhao, F.J. and McGrath, S.P. 1999. Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119: 305-311.Google Scholar
  16. Li, X. and Christie, P. 2001. Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zncontaminated soil. Chemosphere 42: 201-207.Google Scholar
  17. Liu, A., Hamel, C., Hamilton, R.I., Ma, B.L. and Smith, D.L. 2000. Acquisition of Cu, Zn, Mn, and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9: 331-336.Google Scholar
  18. Liu, H., Krizek, J. and Bretscher, A. 1992. Construction of a Gal1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes leathality in yeast. Genetics 132: 665-673.Google Scholar
  19. Liu, H., Trieu, A.T., Blaylock, L.A. and Harrison, M.J. 1998. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: Regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol Plant Microbe In 11: 14-22.Google Scholar
  20. MacDiarmid, C.W., Gaither, L.A. and Eide, D. 2000. Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19: 2845-2855.Google Scholar
  21. Møberg, J.P. 1975. Mineralogical composition of a Danish soil developed on young morainic material. Kgl Vet og Landbohøjsk Årsskr 1975: 91-110.Google Scholar
  22. Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M., Garvin, D., Eide, D. and Kochian, L.V. 2000. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. P Natl Acad Sci USA 97: 4956-4960.Google Scholar
  23. Ravnskov, S. and Jakobsen, I. 1995. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129: 611-618.Google Scholar
  24. Redecker, D., Lodner, R. and Graham, L.E. 2000. Glomalean fungi from the Ordovician. Science 289: 1920-1921.Google Scholar
  25. Rosewarne, G., Barker, S., Smith, S., Smith, F. and Schachtman, D. 1999. A Lycopersicon esculentum phosphate transporter (LePT1) involved in phosphorus uptake from a vesicular-arbuscular mycorrhizal fungus. New Phytol 144: 507-516.Google Scholar
  26. Ruel, M.T. and Bouis, H.E. 1998. Plant breeding: a long-term strategy for the control of zinc deficiency in vulnerable populations. Am J Clin Nutr 68: 488-494.Google Scholar
  27. Sambrook, J., Fritisch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.Google Scholar
  28. Simon, L., Lalonde, M. and Bruns, T.D. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microb 58: 291-295.Google Scholar
  29. Smith, S.E. and Read, D.J. 1997. Mycorrhizal Symbiosis. Academic Press, San Diego, CA.Google Scholar
  30. Timmer, L.W. and Leyden, R.F. 1980. The relationship of mycorrhizal infection to phosphorus induced copper deficiency in sour orange seedlings. New Phytol. 85: 15-23.Google Scholar
  31. Vallee, B.L. and Auld, D.S. 1995. Zinc metallochemistry in biochemistry. In: P. Jolles and H. Joernvall (Eds.), Interface Between Chemistry and Biochemistry. Birkhauser Verlag, Basel, pp. 259-278.Google Scholar
  32. Verkleij, J., Koevoets, P., Blake-Kalff, M. and Chardonnens, A. 1998. Evidence for an important role of the tonoplast in the mechanism of naturally selected zinc tolerance in Silene vulgaris. J Plant Physiol 153: 188-191.Google Scholar
  33. Woolhouse, H.W. 1983. Toxicity and tolerance in the responses of plants to metals. In: O.L. Lange, P.S. Nobel, C.B. Osmond and H. Ziegler (Eds.), Encyclopedia of Plant Physiology: Responses to the Chemical and Biological Environment, New Series vol. 12, Springer Verlag, Berlin, pp. 245-300.Google Scholar
  34. Zhao, H. and Eide, D. 1996. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 271: 23203-23210.Google Scholar
  35. Zhu, Y., Christie, P. and Laidlaw, A.S. 2001. Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42: 193-199.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Stephen H. Burleigh
    • 1
    Email author
  • Brian K. Kristensen
    • 1
  • Iben Ellegaard Bechmann
    • 2
  1. 1.Plant Research DepartmentRisø National LaboratoryRoskildeDenmark
  2. 2.Department of Microbial EcologyLund University, EkologihusetLundSweden

Personalised recommendations