Plant and Soil

, Volume 290, Issue 1–2, pp 51–60 | Cite as

Synchrotron X-ray absorption-edge computed microtomography imaging of thallium compartmentalization in Iberis intermedia

  • Kirk G. ScheckelEmail author
  • Rebecca Hamon
  • Laurence Jassogne
  • Mark Rivers
  • Enzo Lombi
Original Paper


Thallium is an extremely toxic metal which, due to its similarities to K, is readily taken up by plants grown in Tl-contaminated soils. Thallium is also a precious metal nearly as economically valuable as gold. Thallium is efficiently hyperaccumulated in Iberis intermedia as aqueous Tl(I) with highest concentrations within the vascular network of leaves. In this study we examine the utility of synchrotron X-ray differential absorption-edge computed microtomography (CMT) in determining the distribution and compartmentalization of thallium (Tl) in Iberis intermedia. We found Tl to be distributed in solution throughout the vascular system of I. intermedia. Current laboratory experiments are examining the characteristics and potential recovery of Tl by I. intermedia with the objectives to remediate its toxic risks and to facilitate its reclamation for reuse. However, the recovery and reuse of Tl from I. intermedia by way of phytomining requires knowledge on the speciation, distribution and compartmentalization of thallium. CMT shows great promise for application in a wide variety of metal-related structural issues due to its high 3D resolution and being a non-destructive analysis tool.


computed microtomography (CMT) Iberis intermedia thallium hyperaccumulation synchrotron spectroscopy metal compartmentalization 



The US EPA has not subjected this manuscript to internal policy review. Therefore, the research results presented herein do not, necessarily, reflect Agency policy. Mention of trade names of commercial products and companies does not constitute endorsement or recommendation for use. This work was performed at GeoSoilEnviroCARS (Sector 13), Advanced Photon Source (APS), Argonne National Laboratory. GeoSoilEnviroCARS is supported by the National Science Foundation—Earth Sciences (EAR−0217473), Department of Energy—Geosciences (DE-FG02-94ER14466) and the State of Illinois. Use of the APS was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. W-31-109-ENG-38.

Supplementary material

11104_2006_9102_MOESM1_ESM.mpg (6.5 mb)
Movie 1 ESM1 (MPG 6605 KB)
11104_2006_9102_MOESM2_ESM.mpg (4 mb)
Movie 2 ESM2 (MPG 4054 KB)


  1. Altman SJ, Peplinski WJ, Rivers ML (2005a) Evaluation of synchrotron X-ray computerized microtomography for the visualization of transport processes in low-porosity materials. J Contam Hydrol 78:167–183CrossRefGoogle Scholar
  2. Altman SJ, Rivers ML, Reno MD, Cygan RT, McLain AA (2005b) Characterization of adsorption sites on aggregate soil samples using synchrotron X-ray computerized microtomography. Environ Sci Technol 39:2679–2685CrossRefGoogle Scholar
  3. Anderson CWN, Brooks RR, Chiarucci A, LaCoste CJ, Leblanc M, Robinson BH, Simcock R, Stewart RB (1999) Phytomining for nickel, thallium and gold. J Geochem Explor 67:407–415CrossRefGoogle Scholar
  4. Angle JS, Chaney RL, Baker AJM, Li Y, Reeves R, Volk V, Roseberg R, Brewer E, Burke S, Nelkin J (2001) Developing commercial phytoextraction technologies: practical considerations. S Afr J Sci 97:619–623Google Scholar
  5. Appenroth D, Gambaryan S, Winnefeld K, Leiterer M, Fleck C, Braunlich H (1995) Functional and morphological aspects of thallium-induced nephrotoxicity in rats. Toxicology 96:203–215PubMedCrossRefGoogle Scholar
  6. Baker A J M, McGrath S P, Sidoli C M D, Reeves R D (1995) The potential for heavy metal decontamination. Mining Environmental Management September, 12–14Google Scholar
  7. Bamford SA, Wegrzynek D, Chinea-Cano E, Markowicz A (2004) Application of X-ray fluorescence techniques for the determination of hazardous and essential trace elements in environmental and biological materials. Nukleonika 49:87–95Google Scholar
  8. Borgmann U, Cheam V, Norwood WP, Lechner J (1998) Toxicity and bioaccumulation of thallium in Hyalella azteca, with comparison to other metals and prediction of environmental impact. Environ Pollut 99:105–114PubMedCrossRefGoogle Scholar
  9. Broadhurst CL, Chaney RL, Angle JS, Erbe EF, Maugel TK (2004) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265:225–242CrossRefGoogle Scholar
  10. Chaney R, Brown S, Li YM, Angle JS, Homer F, Green C (1995) Potential use of metal hyperaccumulators. Mining Environmental Management September, 9–11Google Scholar
  11. Chaney RL, Angle JS, McLntosh MS, Reeves RD, Li YM, Brewer EP, Chen KY, Roseberg RJ, Perner H, Synkowski EC, Broadhurst CL, Wang S, Baker AJM (2005) Using hyperaccumulator plants to phytoextract soil Ni and Cd. Z Naturforsch, C-A J Biosci 60:190–198Google Scholar
  12. Cotter-Howells JD, Champness PE, Charnock JM (1999) Mineralogy of Pb-P grains in the roots of Agrostis capillaris l-by ATEM and EXAFS. Mineral Mag 63:777–789CrossRefGoogle Scholar
  13. Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110:715–719PubMedGoogle Scholar
  14. Drobne D, Milani M, Zrimec A, Zrimec MB, Tatti F, Draslar K (2005) Focused ion beam/scanning electron microscopy studies of Porcellio scaber (Isopoda, Crustacea) digestive gland epithelium cells. Scanning 27:30–34PubMedCrossRefGoogle Scholar
  15. 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 Environ 23:675–687CrossRefGoogle Scholar
  16. Fukumoto M, Kurohara A, Yoshimura N, Yoshida D, Akagi N, Yoshida S (1998) Relationship between ATP synthesis and Tl-201 uptake in transformed and non-transformed cell lines. Nucl Med Commun 19:1169–1175PubMedCrossRefGoogle Scholar
  17. Galván-Arzate S, Santamaria A (1998) Thallium toxicity. Toxicol Lett 99:1–13PubMedCrossRefGoogle Scholar
  18. Gardea-Torresdey JL, Peralta-Videa JR, de la Rosa G, Parsons JG (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249:1797–1810CrossRefGoogle Scholar
  19. Gregory PJ, Hinsinger P (1999) New approaches to studying chemical and physical changes in the rhizosphere: an overview. Plant Soil 211:1–9CrossRefGoogle Scholar
  20. Hansel CM, La Force MJ, Fendorf S, Sutton SR (2002) Spatial and temporal association of As and Fe species on aquatic plant roots. Envion Sci Technol 36:1988–1994CrossRefGoogle Scholar
  21. Howe JA, Loeppert RH, DeRose VJ, Hunter DB, Bertsch PM (2003) Localization and speciation of chromium in subterranean clover using XRF, XANES, and EPR spectroscopy. Environ Sci Technol 37:4091–4097PubMedCrossRefGoogle Scholar
  22. Johnson SN, Read DB, Gregory PJ (2004) Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecol Entomol 29:117–122CrossRefGoogle Scholar
  23. Kaczmarek D (2001) Backscattered electrons topographic mode problems in the scanning electron microscope. Optica Appl 31:649–658Google Scholar
  24. Kaiser J, Reale L, Ritucci A, Tomassetti G, Poma A, Spano L, Tucci A, Flora F, Lai A, Faenov A, Pikuz T, Mancini L, Tromba G, Zanini F (2005) Mapping of the metal intake in plants by large-field X-ray microradiography and preliminary feasibility studies in microtomography. Eur Phys J D 32:113–118CrossRefGoogle Scholar
  25. Kazantzis G (2000) Thallium in the environment and health effects. Environ Geochem Health 22:275–280CrossRefGoogle Scholar
  26. Keith LH, Telliard WA (1979) ES&T special report: priority pollutants: I-a perspective view. Envion Sci Technol 13:416–423CrossRefGoogle Scholar
  27. Kim HK, Lee SC, Cho MH, Lee SY, Cho G (2005) Use of a flat-panel detector for microtomography: a feasibility study for small-animal imaging. IEEE Trans Nucl Sci 52:193–198CrossRefGoogle Scholar
  28. Küpper H, Lombi E, Wieshammer G, Zhao FJ, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300PubMedCrossRefGoogle Scholar
  29. Kupper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311CrossRefGoogle Scholar
  30. Li YM, Chaney RL, Angle JS, Baker AJM (2000) Phytoremediation of heavy metal contaminated soils. In: Bioremediation of contaminated soils. pp 837–857Google Scholar
  31. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2001) Phytoremediation of heavy metal-contaminated soils: natural hyperaccumulation versus chemically enhanced phytoextraction. J Environ Qual 30:1919–1926PubMedCrossRefGoogle Scholar
  32. McCarthy JJ, McMillan DJ (1998) Application of x-ray optics to energy-dispersive spectroscopy. Microsc Microanal 4:632–639PubMedGoogle Scholar
  33. McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids, and radio nuclides. Adv Agron 75:1–56Google Scholar
  34. McNear DH, Peltier E, Everhart J, Chaney RL, Sutton S, Newville M, Rivers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. Environ Sci Technol 39:2210–2218PubMedCrossRefGoogle Scholar
  35. Muscariello L, Rosso F, Marino G, Giordano A, Barbarisi M, Cafiero G, Barbarisi A (2005) A critical overview of ESEM applications in the biological field. J Cell Physiol 205:328–334PubMedCrossRefGoogle Scholar
  36. Nolan A, Schaumlöffel D, Lombi E, Ouerdane L, Lobinski R, McLaughlin M (2004) Determination of Tl(I) and Tl(III) by IC-ICP-MS and application to Tl speciation analysis in the Tl hyperaccumulator plant Iberis intermedia. J Anal Atom Spect 19:757–761CrossRefGoogle Scholar
  37. Nriagu JO (1998) History, production, and uses of thallium. In: Nriagu JO (ed), Thallium in the environment. John Wiley & Sons Inc, New York, pp 1–14Google Scholar
  38. Plouraboue F, Cloetens P, Fonta C, Steyer A, Lauwers F, Marc-Vergnes JP (2004) X-ray high-resolution vascular network imaging. J Microsc Oxford 215:139–148CrossRefGoogle Scholar
  39. Postnov AA, Meurrens K, Weiler H, Van Dyck D, Hu X, Terpstra P, De Clerck NM (2005) In vivo assessment of emphysema in mice by high resolution X-ray microtomography. J Microsc Oxford 220:70–75CrossRefGoogle Scholar
  40. Prymak O, Tiemann H, Sotje I, Marxen JC, Klocke A, Kahl-Nieke B, Beckmann F, Donath T, Epple M (2005) Application of synchrotron-radiation-based computer microtomography (SRmCT) to selected biominerals: embryonic snails, statoliths of medusae, and human teeth. J Biol Inorg Chem 10:688–695PubMedCrossRefGoogle Scholar
  41. Psaras GK, Constantinidis T, Cotsopoulos B, Manetas Y (2000) Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: evidence that the metal is excluded from both guard cells and trichomes. Ann Bot 86:73–78CrossRefGoogle Scholar
  42. Punshon T, Jackson BP, Lanzirotti A, Hopkins WA, Bertsch PM, Burger J (2005) Application of synchrotron X-ray microbeam spectroscopy to the determination of metal distribution and speciation in biological tissues. Spectr Lett 38:343–363Google Scholar
  43. Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158:279–285CrossRefGoogle Scholar
  44. Sato T, Indo H, Kawabata Y, Kobayashi T, Suenaga S, Iwashita Y, Nitta T, Sugihara K, Majima HJ (2005) Thallium-201 chloride (Tl-201) accumulation and Na+/K+-ATPase expression in tumours of the head and neck. Dentomaxillofac Radiol 34:212–217PubMedCrossRefGoogle Scholar
  45. Scheckel KG, Lombi E, Rock SA, McLaughlin NJ (2004) In vivo synchrotron study of thallium speciation and compartmentation in lberis intermedia. Environ Sci Technol 38:5095–5100PubMedCrossRefGoogle Scholar
  46. Skulsky IA (1991) Isomorphism of Ti+ and K+ in membrane-transport processes. Tsitologiya 33:118–129Google Scholar
  47. Skulsky IA, Lapin AV (1983) Effect of Tl+-ions on transport of Na+ and K+ in the frog-skin. Tsitologiya 25:1284–1288Google Scholar
  48. Tremel A, Mench M (1997) Thallium in plants. Agronomie 17:261–269Google Scholar
  49. Vazquez MD, Barcelo J, Poschenrieder C, Madico J, Hatton P, Baker AJM, Cope GH (1992) Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metallophyte that can hyperaccumulate both metals. J Plant Physiol 140:350–355Google Scholar
  50. Vyskocil F, Edwards C, Teisinger J (1983) Correlation between resting membrane-potential, electrogenic sodium-pump and Na+/K+ ATPase in mouse diaphragm fibers during replacement of K+ by Tl+, Rb+ and NH4+. Physiol Bohemoslov 32:572–572Google Scholar
  51. Wildenschild D, Hopmans JW, Rivers ML, Kent AJR (2005) Quantitative analysis of flow processes in a sand using synchrotron-based X-ray microtomography. Vadose Zone J 4:112–126CrossRefGoogle Scholar
  52. Wildenschild D, Hopmans JW, Vaz CMP, Rivers ML, Rikard D, Christensen BSB (2002) Using X-ray computed tomography in hydrology: systems, resolutions, and limitations. J Hydrol 267:285–297CrossRefGoogle Scholar
  53. Xiao T, Guha J, Boyle D, Liu C, Zheng B, Wilson GC, Rouleau A, Chen J (2004) Naturally occurring thallium: a hidden geoenvironmental health hazzard? Environ Int 30:501–507PubMedCrossRefGoogle Scholar
  54. Yoon SJ, Jones KW, Lanzirotti A, Feng HE, Um W, Serne RJ, Karthikeyan KG, Bleam WF (2003) X-ray microtomography study of metal distribution in sediments related to pore structure modification by mineral dissolution and neophase formation under extremely alkaline conditions. Abstr Pap Am Chem Soc 225:U256–U256Google Scholar
  55. Zhang WH, Cai Y, Downum KR, Ma LQ (2004) Arsenic complexes in the arsenic hyperaccumulator Pteris vittata (Chinese brake fern). J Chromatogr A 1043:249–254PubMedCrossRefGoogle Scholar
  56. Zhao FJ, Wang JR, Barker JHA, Schat H, Bleeker PM, McGrath SP (2003) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol 159:403–410CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Kirk G. Scheckel
    • 1
    Email author
  • Rebecca Hamon
    • 2
  • Laurence Jassogne
    • 3
  • Mark Rivers
    • 4
  • Enzo Lombi
    • 2
  2. 2.CSIRO Land and Water Adelaide LaboratoryGlen OsmondAustralia
  3. 3.School of Plant BiologyUniversity of Western AustraliaGlen OsmondAustralia
  4. 4.GSECARSUniversity of ChicagoChicagoUSA

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