Biological Trace Element Research

, Volume 115, Issue 1, pp 67–86 | Cite as

Nickel localization on tissues of hyperaccumulator species of Phyllanthus L. (euphorbiaceae) from Ultramafic Areas of Cuba

  • R. Berazaín
  • V. de la Fuente
  • D. Sánchez-Mata
  • L. Rufo
  • N. Rodríguez
  • R. Amils


Two species of perennial Phyllanthus (Euphorbiaceae) (Phyllanthus orbicularis and Phyllanthus discolor, both endemic to ultramafic areas of Cuba, and their natural hybrid, Phyllanthus xpallidus) were selected for metal localization microanalysis. Different plant tissues were analyzed by X-ray fluorescence, inductively coupled plasma—atomic emission spectroscopy, and scanning electron microscopy coupled with an energy-dispersive X-ray probe. All of the studied taxa are nickel (Ni) hyperaccumulators and significant concentrations of this element were found in different leaf and stem tissues. The highest Ni content was found in the laticifer tubes, whereas leaf epidermis Ni content resulted to be much more relevant in terms of total metal storage. Calcium and magnesium were found more evenly distributed in leaf and stem tissues.

Index Entries

Elemental mapping Euphorbiaceae nickel hyperaccumulators Phyllanthus SEM-EDX tropical genus 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    C. H. P. De Vos, R. Vooijs, H. Schat, and W. H. O. Ernst, Copper-induced damage to the permeability barrier in roots of Silene cucubalus, J. Plant Physiol. 135, 165–169 (1989).Google Scholar
  2. 2.
    Z. Krupa, G. Oquist, and N. P. A. Huner, The effect of cadmium on photosynthesis of Phaseolus vulgaris: a fluorescence analysis, Physiol. Plantarum 88, 626–630 (1993).CrossRefGoogle Scholar
  3. 3.
    R. R. Brooks, Geobotany and hyperaccumulators, in Plants That Hyperaccumulate Heavy Metals: Their Role in Phytoremediation Microbiology Archaeology, Mineral Exploration and Phytomining R. R. Brooks, ed., CAB International, Wallingford, UK, pp. 55–94, (1998).Google Scholar
  4. 4.
    W. H. O. Ernst, Physiological and biochemical aspects of metal tolerance, in Effects of Air Pollutants on Plants, T. A. Mansfeld, ed., Cambridge University Press, Cambridge, pp. 115–133 (1976).Google Scholar
  5. 5.
    R. R. Brooks, Phytochemistry and hyperaccumulators, in Plants That Hyperaccumulate Heavy Metals: Their Role in Phytoremediation, Microbiology, Archaeology, Mineral Exploration and Phytomining, R. R. Brooks, ed, CAB International, Wallingford, UK, pp. 15–53 (1998).Google Scholar
  6. 6.
    U. Krämer, J. D. Cotterhowells, J. M. Charnock, A. J. M. Baker, and J. A. C. Smith, Free histidine as a metal chelator in plants that accumulate nickel, Nature. 379, 635–638 (1996).CrossRefGoogle Scholar
  7. 7.
    U. Krämer, Cadmium for all meals: plants with an unusual appetite, New Phytol. 145, 1–5 (2000).CrossRefGoogle Scholar
  8. 8.
    S. N. Martens and R. S. Boyd, The ecological significance of Nihyperaccumulation: a plant chemical defence, Oecologia 98, 379–384 (1994).CrossRefGoogle Scholar
  9. 9.
    R. S. Boyd and S. N. Martens, The significance of metal hyperaccumulation for biotic interactions, Chemoecology 8, 1–7 (1998).CrossRefGoogle Scholar
  10. 10.
    R. S. Boyd, Hyperaccumulation as a plant defence, strategy. in Plants That Hyperaccumulate Heavy Metals: Their Role in Phytoremediation, Microbiology, Archaeology, Mineral Exploration and Phytomining, R. R. Brooks, ed., CAB International, Wallingford, UK, pp. 181–201 (1998).Google Scholar
  11. 11.
    R. S. Boyd and W. J. Moar, The defensive function of Niin plants: response of the polyphagos herbivore Spodoptera exigua (Lepidoptera: Noctuidae) to hyperaccumulator and accumulator species of Streptanthus (Brassicaceae), Oecologia 118, 218–224 (1999).CrossRefGoogle Scholar
  12. 12.
    M. A. Davis and R. S. Boyd, Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae), New Phytol. 146, 211–217 (2000).CrossRefGoogle Scholar
  13. 13.
    T. Jaffré, R. R. Brooks, J. Lee, and R. D. Reeves, Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193, 579–580 (1976).CrossRefGoogle Scholar
  14. 14.
    R. R. Brooks, J. Lee, R. D. Reeves, and T. Jaffré, Detection of Niiferous rocks by analysis of herbarium specimens of indicator plants, J. Geochem. Explor. 7, 49–57 (1977).CrossRefGoogle Scholar
  15. 15.
    A. J. M. Baker, S. P. McGrath, R. D. Reeves, and J. A. C. Smith, Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils, in Phytoremediation of Contaminated Soil and Water, N. Terry and G. Nañuelos, eds, Lewis, Boca Raton, FL, pp. 85–107 (2000).Google Scholar
  16. 16.
    R. D. Reeves and A. J. M. Baker, Metal-accumulating plants, in Phytoremediation, of Toxic Metals: Using Plants to Clean up the Environment, I. Raskin and B. D. Ensley, eds., Wiley, New York, pp. 193–229 (2000).Google Scholar
  17. 17.
    R. D. Reeves, The hyperaccumulation of Niby serpentine plants, in The Vegetation of Ultramafic (Serpentine) Soils, A. J. M. Baker, J. Proctor, and R. D. Reeves, eds., Intercept Ltd. Andover, UK pp. 253–278 (1992).Google Scholar
  18. 18.
    E. Medina, E. Cuevas, J. Figueroa, and A. E. Lugo, Mineral content of leaves from trees growing on serpentine soils under contrasting rainfall regimes in Puerto Rico, Plant Soil 158, 13–21 (1994).CrossRefGoogle Scholar
  19. 19.
    R. D. Reeves, A. J. M. Baker, A. Borhidi, and R. Berazaín, Ni-accumulating plants from the ancient serpentine soils of Cuba, New Phytol. 133, 217–224 (1996).CrossRefGoogle Scholar
  20. 20.
    R. D. Reeves, A. J. M. Baker, A. Borhidi, and R. Berazaín, Nickel hyperaccumulation in the serpentine flora of Cuba, Ann. Bot. (Lond.) 83, 29–38 (1999).CrossRefGoogle Scholar
  21. 21.
    R. R. Brooks, ed., Plants That Hyperaccumulate Heavy Metals: Their Role in Phytoremediation, Microbiology, Archaeology, Mineral Exploration and Phytomining, CAB International, Wallingford, UK (1998).Google Scholar
  22. 22.
    R. D. Reeves, Tropical hyperaccumulators of metals and their potential for phytoextraction, Plant Soil 249, 57–65 (2003).CrossRefGoogle Scholar
  23. 23.
    R. R. Brooks, S. Shaw, and A. Asensi, Some observations, on the ecology, metal uptake and Nitolerance of Alyssum serpyllifolium subspecies from the Iberian Peninsula, Vegetatio 45, 183–188 (1981).CrossRefGoogle Scholar
  24. 24.
    R. R. Brooks, S. Shaw, and A. Asensi, The chemical form and physiological function of Nickel in some Iberian Alyssum species, Physiol. Plantarum 51, 167–170 (1981).CrossRefGoogle Scholar
  25. 25.
    R. D. Reeves, R. R. Brooks, and R. M. Macfarlane, Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator, Streptanthus polygaloides Gray (Brassicaceae), Am. J. Bot. 68, 708–712 (1981).CrossRefGoogle Scholar
  26. 26.
    S. M. Heath, D. Southworth, and J. A. D'Allura, Localization of Niin epidermal subsidiary cells of leaves of Thlaspi montanum var. siskiyouense (Brassicaceae) using energydispersive X-ray microanalysis, Int. J. Plant Sci. 158(2), 184–188 (1997).CrossRefGoogle Scholar
  27. 27.
    U. Krämer, G. W. Grime, J. A. C. Smith, C. R. Hawes, and A. J. M. Baker, Micro-PIXE as a technique for studying Nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum, Nucl. Instrum. Methods B 130, 340–350 (1997).CrossRefGoogle Scholar
  28. 28.
    G. K. Psaras, T. H. Constantinidis, B. Cotsopoulos, and Y. Manetas, 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. (Lond.) 86, 73–78 (2000).CrossRefGoogle Scholar
  29. 29.
    H. Küpper, E. Lombi, F. J. Zhao, G. Wieshammer, and S. P. McGrath, Cellular compartimentation of Niin the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense, J. Exp. Bot. 52(365), 2291–2300 (2001).PubMedCrossRefGoogle Scholar
  30. 30.
    A. Asensi, N. Rodríguez, B. Díez-Garretas, R. Amils, and V. de la Fuente, Nickel hyperaccumulation of some subspecies of Alyssum serpyllifolium (Brassicaceae) from ultramafic soils of Iberian Peninsula, in Ultramfic Rocks: Their Soils, Vegetation and Fauna R. S. Boyd A. J. M. Baker, and J. Proctor eds Proceedings of the IV International Conference on Serpentine Ecology, 2003, La Habana, Cuba, Science Reviews, St. Albans, pp. 263–265 (2004).Google Scholar
  31. 31.
    B. H., Robinson, E. Lombi, F. J. Zhao, and S. P. McGrath, Uptake and distribution of Nickel and other metals in the hyperaccumulator Berkheya coddii, New Phytol. 158, 279–285 (2003).CrossRefGoogle Scholar
  32. 32.
    W. J. Przybylowicz, C. A. Pineda, V. M. Prozesky, and J. Mesiasz-Przybylowicz, Investigation of Nihyperaccumulation by true elemental imaging, Nucl. Instrum. Methods B 104, 176–181 (1995).CrossRefGoogle Scholar
  33. 33.
    j. Mesjasz-Przybylowicz, W. J. Przybylowicz, D. B. K. Rama, and C. A. Pineda, Elemental distribution in Senecio anomalochrous, a Nihyperaccumulator from South Africa, S. Afr. J. Sci. 97, 593–595 (2001).Google Scholar
  34. 34.
    N. P. Bhatia, I. Orlic, R. Siegele, N. Ashwath, A. J. M. Baker, and K. B. Walsh, Elemental mapping using PIXE shows the main pathway of Nimovement is principally symplastic within the fruit of the hyperaccumulator Stackhousia tryonii, New Phytol. 160, 479–488 (2003).CrossRefGoogle Scholar
  35. 35.
    N. Perrier, F. Colin, T. Jaffré, J. P. Ambrosi, J. Rose, and J. Y. Bottero, Nispeciation in Sebertia acuminata, a plant growing on a lateritic soil of New Caledonia, CR Geosci. 336, 567–577 (2004).CrossRefGoogle Scholar
  36. 36.
    W. J. Kersten, R. R. Brooks, R. D. Reeves, and T. Jaffré, Niuptake by New Caledonian species of Phyllanthus, Taxon 28, 529–534 (1979).CrossRefGoogle Scholar
  37. 37.
    A. J. M. Baker, J. Proctor, M. M. J. van Balgooy, and R. D. Reeves, Hyperaccumulation of Nickel by the flora of the ultramafics of Palawan, Republic of the Philippines, in The Vegetation of Ultramgfic (Serpentine) Soils, A. J. M. Baker, J. Proctor, and R. D. Reeves, eds. Intercept Ltd., Andover, UK, pp. 291–304 (1992).Google Scholar
  38. 38.
    V. Samek, Pinares de Cajálbana. Estudio sinecológico, Acad. Ciencias Cuba, Forestal 13, 1–56 (1973).Google Scholar
  39. 39.
    A. Leiva and R. Berazain, Cajalbana Tableland and Preluda mountain region, Cuba, in Centres of Plant Diversity, A Guide and Strategy for Their Conservation, Vol. 3, The Americas, eds., S. D. Davis, V. H. Heywood, O. Herrera-McBride, J. Villa-Lobos, A. C. Hamilton, IUCN Publications Unit, Cambridge, UK (1997).Google Scholar
  40. 40.
    A. Borhidi, Phytogeography and Vegetation Ecology of Cuba, Akadémiai Kiadó, Budapest (1991).Google Scholar
  41. 41.
    A. Borhidi, O. Muñiz, and E. del Risco, Clasificación fitocenológica de la vegetación de Cuba, Acta Bot. Hung. 25(3–4), 263–301 (1979).Google Scholar
  42. 42.
    C. L. Broadhurst, R. L. Chaney, J. A. Angle, E. F. Erbe, and T. K. Maugel, Nickel localization and response to increasing Nisoil levels in leaves of the Ni hyperaccumulator Alyssum murale, Plant Soil 265, 225–242 (2004).CrossRefGoogle Scholar
  43. 43.
    S. D. Bidwell, S. A. Crawford, I. E. Woodrow, J. Sommer-Knudsen, and A. T. Marshall, Sub-cellular localization of Niin the hyperaccumulator, Hybanthus floribund us (Lindley) F. Muell, Plant Cell Environ. 27, 705–716 (2004).CrossRefGoogle Scholar
  44. 44.
    W. J. Kersten, R. R. Brooks, R. D. Reeves, and T. Jaffré, Nature of Nicomplexes in Psychotria dourrei and other Nickel-accumulating plants, Phytochemistry 19, 1963–1965 (1980).CrossRefGoogle Scholar
  45. 45.
    S. Sagner, R. Kneer, G. Wanner, J. P. Cosson, B. Deus-Neumann, and M. H. Zenk, Hyperaccumulator, complexation and distribution of Niin Sebertia acuminata, Phytochemistry. 47(3), 339–347 (1998).PubMedCrossRefGoogle Scholar
  46. 46.
    A. N. Rao, Reticulate cuticle on leaf epidermis in Hevea brasiliensis Muell, Nature (Lond.) 197, 1125–1126 (1963).CrossRefGoogle Scholar
  47. 47.
    F. Gómez, A. Grau, L. Vázquez, and R. Amils, UV radiation effects over microorganisms and study of protective agents, European Space Agency 545, 21–25 (2004).Google Scholar

Copyright information

© Humana Press Inc. 2007

Authors and Affiliations

  • R. Berazaín
    • 1
  • V. de la Fuente
    • 2
  • D. Sánchez-Mata
    • 3
  • L. Rufo
    • 2
  • N. Rodríguez
    • 4
  • R. Amils
    • 4
    • 5
  1. 1.Jardín Botánico NacionalUniversidad de La HabanaCiudad HabanaCuba
  2. 2.Departmento de Biología, Facultad de CienciasUniversidad Complutense de MadridMadridSpain
  3. 3.Departmento de Biología Vegetal II, Facultad de FarmaciaUniversidad Complutense de MadridMadridSpain
  4. 4.Centro de Astrobiología, (INTA-CSIC)MadridSpain
  5. 5.Centro de Biología MolecularUniversidad Autónoma de MadridMadridSpain

Personalised recommendations