Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels

Plant Journal

Volumn 39, Issue 3, 2004, Pages 425-439

  Dräger, Dörthe B ^a   Desbrosses Fonrouge, Anne Garlonn ^a   Krach, Christian ^a,c   Chardonnens, Agnes N ^a,d   Meyer, Rhonda C ^a   Saumitou Laprade, Pierre ^b   Krämer, Ute ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIV LILLE   (France)

^c UNIVERSITY OF POTSDAM   (Germany)

^d Metanomics GmbH   (Germany)

Author keywords

Cation diffusion facilitator; Hyperaccumulator; Tonoplast; ZAT; Zn

Indexed keywords

CELL MEMBRANES; CONCENTRATION (PROCESS); PLANTS (BOTANY); PROTEINS; TOXICITY; ZINC;

GENE ENCODING; GREEN FLUORESCENT PROTEIN (GFP);

GENES;

ARABIDOPSIS PROTEIN; CATION TRANSPORT PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MESSENGER RNA; MICROSATELLITE DNA; PHOTOPROTEIN; PLANT DNA; PLANT RNA; ZINC;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL VACUOLE; CROSS BREEDING; GENE; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CLONING, MOLECULAR; CROSSES, GENETIC; DNA, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; RNA, PLANT; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; VACUOLES; ZINC;

CONCENTRATION; GENES; PLANTS; PROTEINS; TOXICITY; ZINC;

ARABIDOPSIS; ARABIDOPSIS HALLERI; ARABIDOPSIS LYRATA; ARABIDOPSIS THALIANA; EMBRYOPHYTA; EUKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 3843079529     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02143.x     Document Type: Article

References (63)

1. Adams, A., Gottschling, D.E., Kaiser, C.A. and Stearns, T. (1997) Methods in Yeast Genetics - A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. Anton, A., Grosse, C., Reissmann, J., Pribyl, T. and Nies, D.H. (1999) CzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp. strain CH34. J. Bacteriol. 181, 6876-6881.
3. Assuncao, A.G.L., Da Costa Martins, P., 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.
4. Baker, A.J.M. and Brooks, R.R. (1989) Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery, 1, 81-126.
5. Baker, A.J.M., Reeves, R.D. and Hajar, A.S.M. (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brasicaceae). New Phytologist, 127, 61-68.
6. Becher, M., Talke, I.N., Krall, L. and Krämer, U. (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37, 251-268.
7. Bert, V., Macnair, M.R., de Laguerie, P., Saumitou-Laprade, P. and Petit, D. (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytologist, 146, 225-233.
8. Bert, V., Bonnin, I., Saumitou-Laprade, P., de Laguerie, P. and Petit, D. (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytologist, 155, 47-57.
9. Bert, V., Meerts, P., Saumitou-Laprade, P., Salis, P., Gruber, W. and Verbruggen, N. (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil, 249, 9-18.
10. Blaudez, D., Kohler, A., Martin, F., Sanders, D. and Chalot, M. (2003) Poplar metal tolerance protein 1 (MTP1) confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell, 15, 2911-2928.
11. Bloss, T., Clemens, S. and Nies, D.H. (2002) Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta, 214, 783-791.
12. Borrelly, G.P., Harrison, M.D., Robinson, A.K., Cox, S.G., Robinson, N.J. and Whitehall, S.K. (2002) Surplus zinc is handled by Zym1 metallothionein and Zhf endoplasmic reticulum transporter in Schizosaccharomyces pombe. J. Biol. Chem. 277, 30394-30400.
13. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P. and Boeke, J.D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C:a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast, 14, 115-132.
14. Chaney, R.L., Malik, M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S. and Baker, A.J.M. (1997) Phytoremediation of soil metals. Curr. Opin. Biotechnol. 8, 279-284.
15. Cho, M., Chardonnens, A.N. and Dietz, K.-J. (2003) Differential heavy metal tolerance of Arabidopsis halleri and Arabidopsis thaliana: a leaf slice test. New Phytologist, 158, 287-293.
16. Clemens, S., Bloss, T., Vess, C., Neumann, D., Nies, D.H. and Zur Nieden, U. (2002a) A transporter in the endoplasmic reticulum of Schizosaccharomyces pombe cells mediates zinc storage and differentially affects transition metal tolerance. J. Biol. Chem. 277, 18215-18221.
17. Clemens, S., Palmgren, M.G. and Kraemer, U. (2002b) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7, 309-315.
18. Conklin, D.S., McMaster, J.A., Culbertson, M.R. and Kung, C. (1992) COT1, a gene involved in cobalt accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 3678-3688.
19. Dahmani-Muller, H., van Oort, F., Gelie, B. and Balabane, M. (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ. Pollut. 109, 231-238.
20. Davis, S.J. and Vierstra, R.D. (1998) Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol. Biol. 36, 521-528.
21. Delhaize, E., Kataoka, T., Hebb, D.M., White, R.G. and Ryan, P.R. (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell, 15, 1131-1142.
22. Dellaporta, S.L. (1983) A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1, 19.
23. Dohmen, R.J., Strasser, A.W., Honer, C.B. and Hollenberg, C.P. (1991) An efficient transformation procedure enabling long-term storage of competent cells of various yeast genera. Yeast, 7, 691-692.
24. Elble, R. (1992) A simple and efficient procedure for the transformation of yeast. Biotechniques, 13, 18-20.
25. Ernst, W.H.O. (1974) Schwermetallvegetationen der Erde. Stuttgart, Germany: Gustav Fischer Verlag.
26. Ernst, K., Kumar, A., Kriseleit, D., Kloos, D.U., Phillips, M.S. and Ganal, M.W. (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J. 31, 127-136.
27. Gaedeke, N., Klein, M., Kolukisaoglu, U. et al. (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J. 20, 1875-1887.
28. Gaither, L.A. and Eide, D.J. (2001) Eukaryotic zinc transporters and their regulation. Biometals, 14, 251-270.
29. Goldstein, A.L. and McCusker, J.H. (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast, 15, 1541-1553.
30. +. Mol. Microbiol. 45, 145-153.
31. Haseloff, J., Siemering, K.R., Prasher, D.C. and Hodge, S. (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl Acad. Sci. USA, 94, 2122-2127.
32. Hirschi, K.D., Korenkov, V.D., Wilganowski, N.L. and Wagner, G.J. (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol. 124, 125-133.
33. Hofmann, K. and Stoffel, W. (1993) TMbase - a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler, 374, 166.
34. Jones, D.A., Thomas, C.M., Hammond-Kosack, K.E., Balint-Kurti, P.J. and Jones, J.D. (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266, 789-793.
35. Koch, M.A., Haubold, B. and Mitchell-Olds, T. (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17, 1483-1498.
36. Krämer, U., Cotter-Howells Janet, D., Charnock John, M., Baker Alan, J.M. and Smith, J.A.C. (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature, 379, 635-638.
37. Küpper, H., Lombi, E., Zhao, F.J. and McGrath, S.P. (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta, 212, 75-84.
38. Lämmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
39. Lee, J., Bae, H., Jeong, J., Lee, J.Y., Yang, Y.Y., Hwang, I., Martinoia, E. and Lee, Y. (2003) Functional expression of a bacterial heavy metal transporter in Arabidopsis enhances resistance to and decreases uptake of heavy metals. Plant Physiol. 133, 589-596.
40. Longtine, M.S., McKenzie, A.I., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J.R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast, 14, 953-961.
41. MacDiarmid, C.W., Gaither, A.L. and Eide, D. (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J. 19, 2845-2855.
42. MacDiarmid, C.W., Milanick, M.A. and Eide, D.J. (2002) Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae. J. Biol. Chem. 277, 39187-39194.
43. Macnair, M.R. (1993) Tansley review no. 49: the genetics of metal tolerance in vascular plants. New Phytologist, 124, 541-559.
44. Macnair, M.R., Bert, V., Huitson, S.B., Saumitou-Laprade, P. and Petit, D. (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc. R. Soc. Lond. B, 266, 2175-2179.
45. Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd edn. London: Academic Press Ltd.
46. Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D. and Tanksley, S.D. (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science, 262, 1432-1436.
47. Minet, M., Dufour, M.E. and Lacroute, F. (1992) Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2, 417-422.
48. Palmiter, R.D. and Huang, L. (2004) Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch. 447, 744-751.
49. Paulsen, I.T. and Saier, M.H. Jr. (1997) A novel family of ubiquitous heavy metal ion transport proteins. J. Membr. Biol. 156, 99-103.
50. Persans, M.W., Nieman, K. and Salt, D.E. (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc. Natl Acad. Sci. USA, 98, 9995-10000.
51. Ross, C.A. (2002) Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron, 35, 819-822.
52. Salt, D.E., Smith, R.D. and Raskin, I. (1998) Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643-668.
53. Sambrook, J. and Russel, D.W. (2001) Molecular Cloning - A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
54. Sarret, G., Saumitou-Laprade, P., Bert, V., Proux, O., Hazemann, J.L., Traverse, A., Marcus, M.A. and Manceau, A. (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol. 130, 1815-1826.
55. Saumitou-Laprade, P., Piquot, Y., Raspé, O., Bernard, J. and Vrieling, K. (1999) Plant DNA fingerprinting and profiling. In DNA Profiling and DNA Fingerprinting (Epplen, J.T. and Lubjuhn, T., eds). Basel: Birkhäuser, pp. 17-38.
56. Sherman, F., Fink, G.R. and Hicks, J.B. (1986) Methods in Yeast Genetics. Cold Spring Harbor, NY, USA: Cold Spring Harbor Press.
57. Song, W.Y., Sohn, E.J., Martinoia, E., Lee, Y.J., Yang, Y.Y., Jasinski, M., Forestier, C., Hwang, I. and Lee, Y. (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat. Biotechnol. 21, 914-919.
58. von Stein, O.D., Thies, W.-G. and Hofmann, M. (1997) A high throughput screening for rarely transcribed differentially expressed genes. Nucl. Acids Res. 25, 2598-2602.
59. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 46, 4350-4354.
60. Van der Zaal, B.J., Neuteboom, L.W., Pinas, J.E., Chardonnens, A.N., Schat, H., Verkleij, J.A.C. and Hooykaas, P.J.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.
61. Van Hoof, N.A., Hassinen, V.H., Hakvoort, H.W., Ballintijn, K.F., Schat, H., Verkleij, J.A., Ernst, W.H.O., Karenlampi, S.O. and Tervahauta, A.I. (2001) Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiol. 126, 1519-1526.
62. Weber, M., Harada, E., Vess, C., von Roepenack-Lahaye, E. and Clemens, S. (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37, 269-281.
63. Zhao, F.J., Lombi, E., Breedon, T. and McGrath, S.P. (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ. 23, 507-514.