Evidence for nickel/proton antiport activity at the tonoplast of the hyperaccumulator plant Alyssum lesbiacum

Plant Biology

Volumn 10, Issue 6, 2008, Pages 746-753

  Ingle, R A ^a   Fricker, M D ^b   Smith, J A C ^b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b Department of Plant Sciences ^*  (United Kingdom)

Author keywords

Alyssum; Antiport; Hyperaccumulator; Nickel; Tonoplast; Vacuole

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIPORTER; BAFILOMYCIN A1; FLUORESCENT DYE; MACROLIDE; NICKEL; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

BIOLOGICAL UPTAKE; DYE; HERB; HYPERACCUMULATION; IMAGING METHOD; NICKEL;

ARTICLE; BRASSICACEAE; CELL VACUOLE; DRUG EFFECT; FLUORESCENCE MICROSCOPY; METABOLISM; PH;

ADENOSINE TRIPHOSPHATE; ANTIPORTERS; BRASSICACEAE; FLUORESCENT DYES; HYDROGEN-ION CONCENTRATION; MACROLIDES; MICROSCOPY, FLUORESCENCE; NICKEL; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES;

ALYSSUM; ALYSSUM LESBIACUM;

EID: 53549093590     PISSN: 14358603     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2008.00080.x     Document Type: Article

References (38)

1. Asemaneh T., Ghaderian S.M., Crawford S.A., Marshall A.T., Baker A.J.M. (2006) Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae). Planta, 225, 193 202.
2. Assunção A.G., DaCosta Martins P., De Folter S., Vooijs R., Schat H., Aarts M.G. (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant, Cell and Environment, 24, 217 226.
3. Baker A.J.M., Brooks R.R. (1989) Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery, 1, 81 126.
4. Baker A.J.M., McGrath S.P., Reeves R.D., Smith J.A.C. (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N., Bañuelos G. (Eds Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, FL: pp. 85 107.
5. +-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiology, 109, 549 556.
6. Bidwell S.D., Crawford S.A., Woodrow I.E., Sommer-Knudsen J., Marshall A.T. (2004) Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant, Cell and Environment, 27, 705 716.
7. Bowman E.J., Siebers A., Altendorf K. (1988) Bafilomycins: A class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proceedings of the National Academy of Sciences USA, 85, 7972 7976.
8. Chardonnens A.N., Koevoets P.L.M., van Zanten A., Schat H., Verkleij J.A.C. (1999) Properties of enhanced tonoplast zinc transport in naturally selected zinc-tolerant Silene vulgaris. Plant Physiology, 120, 779 785.
9. Dineley K.E., Malaiyandi L.M., Reynolds I.J. (2002) A re-evaluation of neuronal zinc measurements: artifacts associated with high intracellular dye concentration. Molecular Pharmacology, 62, 618 627.
10. Dräger D.B., Desbrosses-Fonrouge A., Krach C., Chardonnens A.N., Meyer R.C., Saumitou-Laprade P., Krämer U. (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. The Plant Journal, 39, 425 439.
11. de la Fuente V., Rodriguez N., Diez-Garretas B., Rufo L., Asensi A., Amils R. (2007) Nickel distribution in the hyperaccumulator Alyssum serpyllifolium Desf. spp. from the Iberian Peninsula. Plant Biosystems, 141, 170 180.
12. Gendre D., Czernic P., Conéjéro G., Pianelli K., Briat J.-F., Lebrun M., Mari S. (2007) TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. The Plant Journal, 49, 1 15.
13. Gonzalez A., Koren'kov V., Wagner G.J. (1999) A comparison of Zn, Mn, Cd, and Ca transport mechanisms in oat root transport vesicles. Physiologia Plantarum, 106, 203 209.
14. Gries G.E., Wagner G.J. (1998) Association of nickel versus transport of cadmium and calcium in tonoplast vesicles of oat roots. Planta, 204, 390 396.
15. Haugland R.P. (2002) Handbook of Fluorescent Probes and Research Products, 9th edn. Molecular Probes, Inc., Eugene, OR.
16. Ingle R.A., Mugford S.T., Rees J.D., Campbell M.M., Smith J.A.C. (2005a) Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants. Plant Cell, 17, 2089 2106.
17. Ingle R.A., Smith J.A.C., Sweetlove L.J. (2005b) Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. BioMetals, 18, 627 641.
18. Joho M., Ishikawa Y., Kunikane M., Inouhe M., Tohoyama H., Murayama T. (1992) The subcellular-distribution of nickel in Ni-sensitive and Ni-resistant strains of Saccharomyces cerevisiae. Microbios, 71, 149 159.
19. Kerkeb L., Krämer U. (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiology, 131, 716 724.
20. Krämer U., Cotter-Howells J.D., Charnock J.M., Baker A.J.M., Smith J.A.C. (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature, 379, 635 638.
21. Krämer U., Pickering I.J., Prince R.C., Raskin I., Salt D.E. (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiology, 122, 1343 1353.
22. Küpper H., Lombi E., Zhao F.J., Wieshammer G., McGrath S.P. (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. Journal of Experimental Botany, 52, 2291 2300.
23. Li L., Tutone A.F., Drummond R.S.M., Gardner R.C., Luan S. (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell, 13, 2761 2775.
24. Marquès L., Cossegal M., Bodin S., Czernic P., Lebrun M. (2004) Heavy metal specificity of cellular tolerance in two hyperaccumulating plants, Arabidopsis halleri and Thlaspi caerulescens. New Phytologist, 164, 289 295.
25. Martinoia E., Maeshima M., Neuhaus H.E. (2007) Vacuolar transporters and their essential role in plant metabolism. Journal of Experimental Botany, 58, 83 102.
26. Mesjasz-Przybyłowicz J., Balkwill K., Przybyłowicz W.J., Annegarn H.J. (1994) Proton microprobe and X-ray fluorescence investigations of nickel distribution in serpentine flora from South Africa. Nuclear Instruments and Methods in Physics Research B, 89, 208 212.
27. Nishimura K., Igarashi K., Kakinuma Y. (1998) Proton gradient-driven nickel uptake by vacuolar membrane vesicles of Saccharomyces cerevisiae. Journal of Bacteriology, 180, 1962 1964.
28. Pence N.S., Larsen P.B., Ebbs S.D., Letham D.L., Lasat M.M., Garvin D.F., Eide D., Kochian L.V. (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences USA, 97, 4956 4960.
29. Persans M.W., Nieman K., Salt D.E. (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proceedings of the National Academy of Sciences USA, 98, 9995 10000.
30. Reeves R.D., Baker A.J.M. (2000) Metal-accumulating plants. In: Raskin I., Ensley B.D. (Eds Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. Wiley and sons, New York: pp. 193 229.
31. Saito A., Higuchi K., Hirai M., Nakane R., Yoshiba M., Tadano T. (2005) Selection and characterization of a nickel-tolerant cell line from tobacco (Nicotiana tabacum cv. bright yellow-2) suspension culture. Physiologia Plantarum, 125, 441 453.
32. Schaaf G., Honsbein A., Meda A.R., Kirchner S., Wipf D., von Wirén N. (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. Journal of Biological Chemistry, 281, 25532 25540.
33. + exchangers in plants. Plant Biology, 8, 419 429.
34. Smart K.E., Kilburn M.R., Salter C.J., Smith J.A.C., Grovenor C.R.M. (2007) NanoSIMS and EPMA analysis of nickel localisation in leaves of the hyperaccumulator plant Alyssum lesbiacum. International Journal of Mass Spectrometry, 260, 107 114.
35. 2+ pore. Journal of Biological Chemistry, 273, 28663 28669.
36. Vacchina V., Mari S., Czernic P., Marquès L., Pianelli K., Schaumlöffel D., Lebrun M., Łobiński R. (2003) Speciation of nickel in a hyperaccumulating plant by high-performance liquid chromatography-inductively coupled plasma mass spectrometry and electrospray MS/MS assisted by cloning using yeast complementation. Analytical Chemistry, 75, 2740 2745.
37. + transport in reconstituted liposomes. Journal of Biological Chemistry, 277, 2413 2418.
38. Weber H., Harada E., Vess C., Roepenack-Lahaye E., 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. The Plant Journal, 37, 269 281.