Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator Thlaspi praecox as revealed by micro-PIXE

Plant, Cell and Environment

Volumn 31, Issue 10, 2008, Pages 1484-1496

  Vogel Mikuš, Katarina ^a   Simčič, Jure ^b   Pelicon, Primož ^b   Budnar, Miloš ^b   Kump, Peter ^b   Nečemer, Marijan ^b   Mesjasz Przybyłowicz, Jolanta ^c   Przybyłowicz, Wojciech J ^c,d   Regvar, Marjana ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

^c MATERIALS RESEARCH GROUP   (South Africa)

^d AGH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Poland)

Author keywords

Hyperaccumulation; Nuclear microprobe; Pb; Phytoremediation; STIM; X ray microanalysis

Indexed keywords

CADMIUM; LEAD; ZINC;

ANGIOSPERM; CADMIUM; CONCENTRATION (COMPOSITION); DETOXIFICATION; HYPERACCUMULATION; LEAD; LEAF; PHYTOREMEDIATION; X-RAY SPECTROSCOPY; ZINC;

ARTICLE; BIOREMEDIATION; CELL COMPARTMENTALIZATION; CHEMISTRY; HISTOLOGY; METHODOLOGY; PLANT LEAF; SOIL POLLUTANT; SPECTROMETRY; THLASPI;

BIODEGRADATION, ENVIRONMENTAL; CADMIUM; CELL COMPARTMENTATION; LEAD; PLANT LEAVES; SOIL POLLUTANTS; SPECTROMETRY, X-RAY EMISSION; THLASPI; ZINC;

BRASSICACEAE; THLASPI; THLASPI PRAECOX;

EID: 51249088139     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2008.01858.x     Document Type: Article

References (67)

1. Ager F.J., Ynsa M.D., Dominguez-Solis J.R., Gotor C., Respaldiza M.A. Romero L.C. (2002) Cadmium localization and quantification in the plant Arabidopsis thaliana using micro-PIXE. Nuclear Instruments and Methods in Physics Research B 189, 494 498.
2. Antosiewicz D.M. Hennig J. (2004) Overexpression of LCT1 in tobacco enhances the protective action of calcium against cadmium toxicity. Environmental Pollution 129, 237 245.
3. Assunção A.G.L., Schat H. Aarts M.G. (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytologist 159, 351 360.
4. Baker A.J.M. (1981) Accumulators and excluders - strategies in the response of plants to heavy metals. Journal of Plant Nutrition 3, 643 654.
5. Baker A.J.M. Whiting S.N. (2002) In search of the Holy Grail - a further step in understanding metal hyperaccumulation? New Phytologist 155, 1 4.
6. Baker A.J.M., Reeves R.D. Hajar A.S.M. (1994) Heavy metal accumulation and tolerance in British population of metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytologist 127, 61 68.
7. Basic N., Salamin N., Keller C., Galland N. Besnard G. (2006) Cadmium hyperaccumulation and genetic differentiation of Thlaspi caerulescens populations. Biochemical Systematics and Ecology 34, 667 677.
8. Bhatia N.P., Orlic I., Siegele R., Ashwath N., Baker A.J.M. Walsh K.B. (2004) Quantitative cellular localisation of nickel in leaves and stem of the hyperaccumulator plant Stackhousia tryonii Bailey using nuclear-microprobe (Micro-PIXE) and energy dispersive X-ray microanalysis (EDXMA) techniques. Functional Plant Biology 31, 1 14.
9. Brooks R.R. (1998) Geobotany in hyperaccumulators. In Plants that Hyperaccumulate Heavy Metals (ed. R.R. Brooks pp. 55 94. CAB International, Cambridge, UK.
10. Callahan D.L., Baker A.J.M., Kolev S.D. Wedd A.G. (2006) Metal ion ligands in hyperaccumulating plants. Journal of Biological Inorganic Chemistry 11, 2 12.
11. Campbell J.L., Hopman T.L., Maxwell J.A. Nejedly Z. (2000) The Guelph PIXE software package III: alternative proton database. Nuclear Instruments and Methods in Physics Research B 170, 193 204.
12. Clemens S., Palmgren M.G. Krämer U. (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends in Plant Science 7, 309 315.
13. Cosio C., DeSantis L., Frey B., Diallo S. Keller C. (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. Journal of Experimental Botany 56, 765 775.
14. De Silva D.L.R., Hetherington A.M. Mansfield T.A. (1985) Synergism between calcium ions and abscisic acid in preventing stomatal opening. New Phytologist 100, 473 482.
15. Ebbs S., Lau I., Ahner B. Kochian I. (2002) Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214, 635 640.
16. Ernst W.H.O. (2005) Phytoextraction of mine wastes - options and impossibilities. Chemie der Erde 65 (Suppl. 1 29 42.
17. 2+ site. Biochimica et Biophysica Acta 1706, 158 164.
18. Fernando D.R., Bakkaus E.J., Perrier N., Baker A.J.M., Woodrow I.E., Batianoff G.N. Collins R.N. (2006) Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytologist 171, 751 758.
19. Frey B., Keller C., Zierold K. Schulin R. (2000) Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 23, 675 687.
20. Haydon M.J. Cobbett C.S. (2007) Transporters of ligands for essential metal ions in plants. New Phytologist 174, 499 506.
21. Hernandez-Allica J., Garbisu C., Becerril J.M., Barrutia O., Garcia-Plazola J.I., Zhao F.J. McGrath S.P. (2006) Synthesis of low molecular weight thiols in response to Cd exposure in Thlaspi caerulescens. Plant, Cell & Environment 29, 1422 1429.
22. Hokura A., Onuma R., Kitajima N., Nakai I., Terada Y., Abe T., Saito H. Yoshida S. (2005) Cadmium distribution in a cadmium hyperaccumulator plant as determined by Micro-XRF imaging. Proc. 8th Int. Conf. X-ray Microscopy, 323 325.
23. Isaure M.P., Fayard B., Saret G., Pairis S. Bourguignon J. (2006) Localization and chemical speciation of cadmium in plant samples by combining analytical electron microscopy and X-ray spectromicroscopy. Spectrochimica Acta Part B 61, 1242 1252.
24. Kachenko A.G., Bhatia N.P., Singh B. Siegele R. (2007) Arsenic hyperaccumulation and localization in the pinnule and stipe tissues of the gold-dust fern (Pityrogramma calomelanos (L.) Link var. austroamericana (Domin) Farw.) using quantitative micro-PIXE spectroscopy. Plant and Soil 300, 207 219.
25. Kachenko A.G., Singh B., Bhatia N.P. Siegele R. (2008) Quantitative elemental localisation in leaves and stems of nickel hyperaccumulating shrub Hybanthus floribundus subsp. floribundus using micro-PIXE spectroscopy. Nuclear Instruments and Methods in Physics Research B 266, 667 676.
26. Küpper H., Zhao F.J. McGrath S.P. (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiology 119, 305 311.
27. Küpper H., Lombi E., Zhao F.J. McGrath S.P. (2000) Cellular compartmentation of cadmium and zinc in the relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212, 75 84.
28. Küpper H., Lombi E., Zhao F.J., Wieshammer G. McGrath S.P. (2001) Cellular compartmentation of nickel in the hyperaccumulators Alysum lesbiacum, Alysum bertolonii and Thlaspi goesingense. Journal of Experimental Botany 52, 2291 2300.
29. Küpper H., Mijovilovich A., Meyer-Klaucke W. Kroneck P.H.M. (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiology 134, 748 757.
30. Küpper H., Parameswaran A., Leitenmaier B., Trtílek M. Šetlík I. (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytologist 175, 655 674.
31. 2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiology 112, 1715 1722.
32. 2+ absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiology 118, 875 883.
33. Lasat M., Kochian L., Toaspern M., Smolenski K.W., Finkelstein K., Fontes E. Bilderback D. (1999) Amazing plants uptake large quantities of toxic metals. News at CHESS. Available at: http://news.chess.cornell.edu/archive/highlights/ plnts99.htm (accessed 6 November 2007).
34. Legge G.J.F. Cholewa M. (1994) The principles of proton probe microanalysis in biology. Scanning Microscopy Supplement 8, 295 315.
35. Lombi E., Zhao F.J., Dunham S.J. McGrath S.P. (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytologist 145, 11 20.
36. Ma J.F., Ueno D., Zhao F.J. McGrath S.P. (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220, 731 736.
37. McGrath S.P. (1998) Phytoextraction for soil remediation. In Plants that Hyperaccumulate Heavy Metals (ed. R.R. Brooks pp. 261 287. CAB International, Cambridge, UK.
38. Mesjasz-Przybyłowicz J. Przybyłowicz W.J. (2002) Micro-PIXE in plant sciences: present status and perspectives. Nuclear Instruments and Methods in Physics Research B 189, 470 481.
39. Mesjasz-Przybyłowicz J., Przybyłowicz W.J., Prozesky V.M. Pineda C.A. (1997) Quantitative micro-PIXE comparison of elemental distribution in Ni-hyperaccumulating and non-accumulating genotypes of Senecio coronatus. Nuclear Instruments and Methods in Physics Research B 130, 368 373.
40. Milner M.J. Kochian L.V. (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Annals of Botany 102, 3 12.
41. Pelicon P., Simčič J., Jakšič M., Medunic Z., Naab F. McDaniel F.D. (2005) Spherical chamber-effective solution for multipurpose nuclear microprobe. Nuclear Instruments and Methods in Physics Research B 231, 53 59.
42. Perronet K., Schwartz C. Morel J.L. (2003) Distribution of cadmium and zinc in the hyperaccumulator Thlaspi caerulescens grown on multicontaminated soil. Plant and Soil 249, 19 25.
43. Pollard A.J. Baker A.J.M. (1995) Quantitative genetics of zinc hyperaccumulation in Thlaspi caerulescens. New Phytologist 132, 113 118.
44. Pongrac P., Vogel-Mikuš K., Kump P., Nečemer M., Tolrà R., Poschenrieder C., Barceló J. Regvar M. (2007) Changes in elemental uptake and arbuscular mycorrhizal during the life cycle of Thlaspi praecox Wulfen colonisation. Chemosphere 69, 1602 1609.
45. Przybyłowicz W.J., Mesjasz-Przybyłowicz J., Prozesky V.M. Pineda C.A. (1997) Botanical applications in nuclear microscopy. Nuclear Instruments and Methods in Physics Research B 130, 335 345.
46. Przybyłowicz W.J., Mesjasz-Przybyłowicz J., Migula P., Turnau K., Nakonieczny M., Augustyniak M. Glowacka E. (2004) Elemental microanalysis in ecophysiology using ion microbeam. Nuclear Instruments and Methods in Physics Research B 219-220, 57 66.
47. 2+ inhibition in photosystem II. FEBS Letters 271, 181 184.
48. Reeves R.D. Baker A.J.M. (2000) Metal-accumulating plants. In Phytoremediation of Toxic Metals. Using Plants to Clean Up the Environment (eds I. Raskin B.D. Ensley pp. 193 229. John Whiley & Sons, Inc., New York, NY, USA.
49. Reeves R.D. Brooks R.R. (1983) Hyperaccumulation of lead and zinc by two metallophytes from mining areas of central Europe. Environmental Pollution Series A, Ecological and Biological 31, 277 285.
50. Regvar M., Vogel-Mikuš K., Kugonič N., Turk B. Batič F. (2006) Vegetational and mycorrhizal successions at a metal polluted site - indications for the direction of phytostabilisation? Environmental Pollution 144, 976 984.
51. Salt D.E. Krämer U. (2000) Mechanisms of metal hyperaccumulation in plants. In Phytoremediation of Toxic Metals. Using Plants to Clean Up the Environment (eds I. Raskin B.D. Ensley pp. 231 246. John Whiley & Sons, Inc., New York, NY, USA.
52. Salt D.E., Prince R.C., Pickering I.J. Raskin I. (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiology 109, 1427 1433.
53. Schat H., Llugany M., Voojis R., Hartley-Whitaker J. Bleeker P.M. (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. Journal of Experimental Botany 53, 2382 2392.
54. Schneider T., Scheloske S. Povh B. (2002) A method for cryosectioning of plant roots for proton microprobe analysis. International Journal of PIXE 12, 101 107.
55. Seregin I.V. Ivanov V.B. (2001) Physiological aspects of cadmium and lead toxic effects on higher plants. Russian Journal of Plant Physiology 48, 523 544.
56. Simčič J., Pelicon P., Budnar M. Šmit Ž. (2002) The performance of the Ljubljana ion microprobe. Nuclear Instruments and Methods in Physics Research B 190, 283 286.
57. Storey R. Leigh R.A. (2004) Processes modulating calcium distribution in citrus leaves. An investigation using X-ray microanalysis with strontium as a tracer. Plant Physiology 136, 3838 3848.
58. Van Belleghem F., Cuypers A., Semane B., Smeets K., Vangronsveld J., d'Haen J. Valcke R. (2007) Subcellular localization of cadmium in rots and leaves of Arabidopsis thaliana. New Phytologist 173, 495 508.
59. Vázquez M.D., Barceló J., Poschenreider C., Mádico J., Hatton P., Baker A.J.M. Cope G.H. (1992) Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metallophyte that can hyperaccumulate both metals. Journal of Plant Physiology 140, 350 355.
60. Vázquez M.D., Poschenreider C., Barceló J., Baker A.J.M., Hatton P. Cope G.H. (1994) Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens J & C Presl. Botanica Acta 107, 243 250.
61. Vogel-Mikuš K., Drobne D. Regvar M. (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environmental Pollution 133, 233 242.
62. Vogel-Mikuš K., Pongrac P., Kump P., Nečemer M. Regvar M. (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environmental Pollution 139, 362 371.
63. Vogel-Mikuš K., Pongrac P., Kump P., Nečemer M., Simčič J., Pelicon J., Budnar M., Povh B. Regvar M. (2007) Localisation and quantification of elements within seeds of Cd/Zn hyperaccumulator Thlaspi praecox by micro-PIXE. Environmental Pollution 147, 50 59.
64. Vogel-Mikuš K., Regvar M., Mesjasz-Przybyłowicz J., Przybyłowicz W., Simčič J., Pelicon J. Budnar M. (2008) Spatial distribution of Cd in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE. New Phytologist 179, 712 721.
65. Vollenweider P., Cosio C., Günthard-Goerg S. Keller C. (2006) Localization and effects of cadmium in leaves of cadmium-tolerant willow (Salix viminalis L.). Part II - Microlocalization and cellular effects of cadmium. Environmental and Experimental Botany 58, 25 40.
66. Wójcik M., Vangronsveld J., d'Haen J. Tukiendorf A. (2005) Cadmium tolerance in Thlaspi caerulescens II. Localization of cadmium in Thlaspi caerulescens. Environmental and Experimental Botany 53, 163 171.
67. Zhao F.J., Lombi E. McGrath S.P. (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant and Soil 249, 37 43.