Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula

Plant Molecular Biology

Volumn 54, Issue 4, 2004, Pages 583-596

  López Millán, Ana Flor ^a   Ellis, Danielle R ^a   Grusak, Michael A ^a  

^a CHILDREN S NUTRITION RESEARCH CENTER   (United States)

Author keywords

gene expression; Medicago truncatula; metals; plasma membrane; transporters; ZIP genes

Indexed keywords

METAL TRANSPORT; TRANSMEMBRANE;

BIOLOGICAL MEMBRANES; DNA; PROTEINS;

PLANTS (BOTANY);

CATION TRANSPORT PROTEIN; COMPLEMENTARY DNA; IRON; ISOPROTEIN; MANGANESE; VEGETABLE PROTEIN; ZINC;

AMINO ACID SEQUENCE; ARTICLE; CELL DIVISION; CHEMISTRY; DNA SEQUENCE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; MEDICAGO; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CATION TRANSPORT PROTEINS; CELL DIVISION; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; IRON; MANGANESE; MEDICAGO; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PLANT PROTEINS; PROTEIN ISOFORMS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

MEMBRANES; NUCLEIC ACIDS; PLANTS; PROTEINS;

MEDICAGO; MEDICAGO TRUNCATULA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 4444312941     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PLAN.0000038271.96019.aa     Document Type: Article

References (64)

1. Altschul, S.F. and Lipman, D.J. 1990. Protein database searches for multiple alignments. Proc. Natl. Acad. Sci. USA 87: 5509-5513.
2. Assuncao, A., Da Costa Martins, P., De Folter, S., Vooijs, R. and Aarts, G.M. 2001. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlapsi caerulescens. Plant Cell Environ. 24: 217-226.
3. Brune, A. and Dietz, K. 1995. Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation; a comparison of Cd-, Mo-, Ni- and Zn-stress. New Phytol. 125: 403-409.
4. Burleigh, S.H., Kristensen, B. and Bechmann, I.E. 2003. A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol. Biol. 52: 1077-1088.
5. Claros, M.G. and Vincens, P. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241: 779-786.
6. Claros, M.G. and von Heijne, G. 1994. TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10: 685-686.
7. Cohen, C.K., Fox, T.C., Garvin, D.F. and Kochian, L.V. 1998. The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol. 116: 1063-1072.
8. Connolly, E.L., Fett, J.P. and Guerinot, M.L. 2002. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14: 1347-1357.
9. Curie, C., Alonso, J.M., Le Jean, M., Ecker, J.R. and Briat, J.F. 2000. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem. J. 347 Pt 3: 749-755.
10. Eckhardt, U., Mas Marques, A. and Buckhout, T.J. 2001. Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol. Biol. 45: 437-448.
11. Eide, D., Broderius, M., Fett, J. and Guerinot, M.L. 1996. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA 93: 5624-5628.
12. Ellis, D.R., López-Millán, A.-F. and Grusak, M.A. 2003. Metal physiology and accumulation in a Medicago truncatula mutant exhibiting an elevated requirement for zinc. New Phytol. 158: 207-218.
13. Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300: 1005-1016.
14. Eng, B.H., Guerinot, M.L., Eide, D. and Saier, M.H. Jr. 1998. Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J. Membr. Biol. 166: 1-7.
15. Fox, T. and Guerinot, M. 1998. Molecular biology of cation transport in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49: 669-696.
16. Gaither, L.A. and Eide, D.J. 2001. Eukaryotic zinc transporters and their regulation. Biometals 14: 251-270.
17. Gietz, R.D. and Schiestl, R.H. 1991. Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier. Yeast 7: 253-263.
18. Gonzales, A. and Lynch, J. 1999. Subcellular and tissue Mn compartmentation in bean leaves under Mn toxicity stress. Aust. Plant Physiol. 26: 203-209.
19. Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M.L. and Eide, D. 1998. Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc. Natl. Acad. Sci. USA 95: 7220-7224.
20. Grusak, M.A., DellaPenna, D. and Welch, R.M. 1999. Physiologic processes affecting the content and distribution of phytonutrients in plants. Nutr. Rev. 57: S27-S33.
21. Guerinot, M.L. 2000a. To improve nutrition for the world's population. Science 288: 1966-1967.
22. Guerinot, M.L. 2000b. The ZIP family of metal transporters. Biochim. Biophys. Acta 1465: 190-198.
23. Guerinot, M.L. and Eide, D. 1999. Zeroing in on zinc uptake in yeast and plants. Curr. Opin. Plant Biol. 2: 244-249.
24. Gupta, R., Jung, E., Gooley, A.A., Williams, K.L., Brunak, S. and Hansen, J. 1999. Scanning the available Dictyostelium discoideum proteome for O-linked GlcNAc glycosylation sites using neural networks. Glycobiology 9: 1009-1022.
25. Henriques, R., Jasik, J., Klein, M., Martinoia, E., Feller, U., Schell, J., Pais, M.S. and Koncz, C. 2002. Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol. Biol. 50: 587-597.
26. 2+ transport: who's directing the traffic? Trends Plant Sci. 6: 100-104.
27. Hofmann, K. and Stoffel, W. 1993. TMbase - a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374: 166.
28. + channels do it all? Plant Cell 5: 720-721.
29. Korshunova, Y.O., Eide, D., Clark, W.G., Guerinot, M.L. and Pakrasi, H.B. 1999. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40: 37-44.
30. Kriedmann, P., Graham, R. and Wiskich, J. 1985. Photosynthetic disfunction and in vivo changes in chlorophyll a fluorescence from manganese deficient wheat leaves. Aust. J. Agric. Res. 36: 157-169.
31. Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E.L. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305: 567-580.
32. Kulikova, O., Gualtieri, G., Geurts, R., Kim, D.J., Cook, D., Huguet, T., de Jong, J.H., Fransz, P.F. and Bisseling, T. 2001. Integration of the FISH pachytene and genetic maps of Medicago truncatula. Plant J. 27: 49-58.
33. Kyte, J. and Doolittle, R.F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157: 105-132.
34. Lasat, M.M., Pence, N.S., Garvin, D.F., Ebbs, S.D. and Kochian, L.V. 2000. Molecular physiology of zinc transport in the Zn hyperaccumulator and nonhyperaccumulator species of Thlaspi. J. Exp. Bot. 51: 71-79.
35. Marschner, H. 1985. Mineral Nutrition of Higher Plants. Academic Press, San Diego, CA.
36. Maser, P., Thomine, S., Schroeder, J.I., Ward, J.M., Hirschi, K., Sze, H., Talke, I.N., Amtmann, A., Maathuis, F.J., Sanders, D., Harper, J.F., Tchieu, J., Gribskov, M., Persans, M.W., Salt, D.E., Kim, S.A. and Guerinot, M.L. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126: 1646-1667.
37. Minet, M., Dufour, M.E. and Lacroute, F. 1992. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2: 417-422.
38. Moreau, S., Thomson, R.M., Kaiser, B.N., Trevaskis, B., Guerinot, M.L., Udvardi, M.K., Puppo, A. and Day, D.A. 2002. GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J. Biol. Chem. 277: 4738-4746.
39. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10: 1-6.
40. Page, R.D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358.
41. Pahlsson, A. 1989. Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Literature Review. Water, Air Soil Pollu. 47: 287-319.
42. Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M.M., Garvin, D.F., Eide, D. and Kochian, L.V. 2000. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 97: 4956-4960.
43. Portnoy, M.E., Liu, X.F. and Culotta, V.C. 2000. Saccharomyces cerevisiae expresses three functionally distinct homologues of the nramp family of metal transporters. Mol. Cell Biol. 20: 7893-7902.
44. Price, A. and Hendry, G. 1991. Iron-catalysed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ. 14: 477-484.
45. Ramesh, S.A., Shin, R., Eide, D.J. and Schachtman, P. 2003. Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Phys. 133: 126-134.
46. Rengel, Z. 2000. Manganese uptake and transport in plants. Metal Ions Biol. Systems 37: 57-87.
47. Robinson, N.J., Procter, C.M., Connolly, E.L. and Guerinot, M.L. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397: 694-697.
48. 2+ in sycamore (Acer pseudoplatanus) cells and excised maize root tips. A comparative 31P n.m.r. study in vivo. Biochem. J. 252: 401-408.
49. Rogers, E.E., Eide, D.J. and Guerinot, M.L. 2000. Altered selectivity in an Arabidopsis metal transporter. Proc. Natl. Acad. Sci. USA 97: 12356-12360.
50. Rogers, E.E. and Guerinot, M.L. 2002. FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell. 14: 1787-1799.
51. Terry, N. and Abadia, J. 1986. Leaf chlorophyll content and its relation to the intracellular location of iron. J. Plant Nutr. 9: 609-546.
52. Thomine, S., Wang, R., Ward, J.M., Crawford, N.M. and Schroeder, J.I. 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. USA 97: 4991-4996.
53. Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
54. Thoquet, P., Gherardi, M., Journet, E.P., Kereszt, A., Ane, J.M., Prosperi, J.M. and Huguet, T. 2002. The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biol. 2: 1-13.
55. Van Assche, F. and Clijsters, H. 1986a. Inhibition of photosynthesis in Phaseolus vulgaris by treatment with toxic concentration of zinc: effect on ribulose-1,5-biphosphate carboxylase/oxygenase. J. Plant Physiol. 125: 355-360.
56. Van Assche, F. and Clijsters, H. 1986b. Inhibition of photosynthesis in Phaseolus vulgaris by treatment with toxic concentration of zinc: effects on electron transport and photophosphorylation. Physiol. Plant 66: 717-721.
57. van der Zaal, B.J., Neuteboom, L.W., Pinas, J.E., Chardonnens, A.N., Schat, H., Verkleij, J. A. and Hooykaas, P.J. 1999. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 119: 1047-1055.
58. Varotto, C., Maiwald, D., Pesaresi, P., Jahns, P., Salamini, F. and Leister, D. 2002. The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J. 31: 589-599.
59. Vert, G., Briat, J.F. and Curie, C. 2001. Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J. 26: 181-189.
60. Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F. and Curie, C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14: 1223-1233.
61. von Heijne, G. 1992. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 225: 487-494.
62. White, M.C., Baker, F.D., Chaney, R.L. and Decker, A.M. 1981. Metal complexation in xylem fluid: II. Theoretical equilibrium model and computational computer program. Plant Physiol. 67: 301-310.
63. Zhao, H. and Eide, D. 1996a. The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc. Natl. Acad. Sci. USA 93: 2454-2458.
64. Zhao, H. and Eide, D. 1996b. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271: 23203-23210.