Advertisement

Cell and Tissue Biology

, Volume 5, Issue 6, pp 603–611 | Cite as

Heterogeneity of epidermal cells in relation to nickel accumulation in hyperaccumulator plants belonging to the genus Alyssum L.

  • I. A. Baklanov
Article

Abstract

Epidermal cells of some plants are able to accumulate high levels of heavy metals (Zn, Ni, Cd). We studied this ability in plants in the genus Alyssum L. distinguished by tolerance to nickel (Ni). It was established that the predominant Ni accumulation occurred in epidermis, whereas in other tissues lower concentrations of the metal were revealed. It was also found that epidermal cells were characterized by heterogeneity in relation to Ni accumulation. The highest metal amount was accumulated in ordinary epidermal cells and in trichomes. Species-specific features of Ni distribution in leaf tissues in Alyssum spp. were shown. The reasons for the heterogeneity of epidermal cells in relation to Ni accumulation were discussed. We have attempted to resolve the contradictions encountered in the literature concerning the distribution and accumulation of Ni in the leaf tissues of plants belonging to the genus Alyssum L.

Keywords

epidermis trichomes heterogeneity of cells compartmentalization nickel hyperaccumulator Alyssum 

Abbreviations

LE

lower epidermis

M

mesophyll

P

phloem

PM

palisade mesophyll

SM

spongy mesophyll

TBC

trichome basal compartment

TP

trichome pedicle

TR

trichome ray(s)

UE

upper epidermis

VB

vascular bundle

X

xylem

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Asemaneh, T., Ghaderian, S.M., Crawford, S.A., Marshall, A.T., and Baker, A.J., Cellular and Subcellular Compartmentation of Ni in the Eurasian Serpentine Plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae), Planta, 2006, vol. 225, pp. 193–202.PubMedCrossRefGoogle Scholar
  2. Baker, A.J.M., Accumulators and Excluders-Strategies in the Response of Plants to Heavy Metals, J. Plant. Nutr., 1981, vol. 3, pp. 643–654.CrossRefGoogle Scholar
  3. Baklanov, I.A., Seregin, I.V., and Ivanov, V.B., Histochemical Analysis of Nickel Distribution in the Hyperaccumulator and Excluder in the Genus Alyssum L., Dokl. Biol. Sci., 2009, vol. 429, pp. 548–550.PubMedCrossRefGoogle Scholar
  4. Boyd, R.S., Shaw, J.J., and Martens, S.N., Nickel Hyperaccumulation Defends Streptanthus polygaloides (Brassicaceae) against Pathogens, Amer. J. Bot., 1994, vol. 81, pp. 294–300.CrossRefGoogle Scholar
  5. Broadhurst, C.L., Chaney, R.L., Angle, J.S., Erbe, E.F., and Maugel, T.K., Nickel Localization and Response to Increasing Ni Soil Levels in Leaves of the Ni Hyperaccumulator Alyssum murale, Plant Soil, 2004a, vol. 265, pp. 225–242.CrossRefGoogle Scholar
  6. Broadhurst, C.L., Chaney, R.L., Angle, J.S., Maugel, T.K., Erbe, E.F., and Murphy, C.A., Simultaneous Hyperaccumulation of Nickel, Manganese, and Calcium in Alyssum Leaf Trichomes, Environ. Sci. Technol., 2004b, vol. 38, pp. 5797–5802.PubMedCrossRefGoogle Scholar
  7. Broadhurst, C.L., Tappero, R.V., Maugel, T.K., Erbe, E.F., Sparks, D.L., and Chaney, R.L., Interaction of Nickel and Manganese in Accumulation and Localization in Leaves of the Ni Hyperaccumulators Alyssum murale and Alyssum corsicum, Plant Soil, 2009, vol. 314, pp. 35–48.CrossRefGoogle Scholar
  8. Brooks, R.R., Lee, J., Reeves, R.D., and Jaffré, T., Detection of Nickeliferous Rocks by Analysis of Herbarium Specimens of Indicator Plants, J. Geochem. Explor., 1977, vol. 7, pp. 49–57.CrossRefGoogle Scholar
  9. Cataldo, D.A., Garland, T.R., and Wildung, R.E., Nickel in Plants, II. Distribution and Chemical Form in Soybean Plants, Plant Phys., 1978, vol. 62, pp. 566–570.CrossRefGoogle Scholar
  10. Chen, C., Huang, D., and Liu, J., Functions and Toxicity of Nickel in Plants: Recent Advances and Future Prospects, Clean-Soil Air Water, 2009, vol. 37, pp. 304–313.CrossRefGoogle Scholar
  11. Dixon, N.E., Gazola, C., Blakeley, R.L., and Zerner, B., Jack bean Urease (EC 3.5.1.5), a Metalloenzyme. A Simple Biological Role for Nickel?, J. Am. Chem. Soc., 1975, vol. 97, pp. 4131–4133.PubMedCrossRefGoogle Scholar
  12. Esau, K., The Epidermis, Plant Anatomy, New York: Wiley; London: Chapman and Hall, 1953.Google Scholar
  13. Gerendás, J., Polacco, J.C., Freyermuth, S.K., and Sattelmacher, B., Significance of Nickel for Plant Growth and Metabolism, J. Soil Sci. Plant Nutr., 1999, vol. 162, pp. ê241–256.CrossRefGoogle Scholar
  14. Ghasemi, R., and Ghaderian, S.M., Responses of Two Populations of an Iranian Nickel-Hyperaccumulating Serpentine Plant, Alyssum inflatum Nyar., to Substrate Ca/Mg Quotient and Nickel, Environ. Exp. Bot., 2009a, vol. 67, pp. 260–268.CrossRefGoogle Scholar
  15. Ghasemi, R., Ghaderian, S.M., and Krämer, U., Accumulation of Nickel in Trichomes of a Nickel Hyperaccumulator Plant, Alyssum inflatum, Northeast. Nat., 2009b, vol. 16, pp. 81–92.CrossRefGoogle Scholar
  16. Glover, B.J., Differentiation in Plant Epidermal Cells, J. Exp. Bot., 2000, vol. 51, pp. 497–505.PubMedCrossRefGoogle Scholar
  17. Guimil, S., and Dunand, C., Patterning of Arabidopsis Epidermal Cells: Epigenetic Factors Regulate the Complex Epidermal Cell Fate Pathway, Trends Plant Sci., 2006, vol. 11, pp. 601–609.PubMedCrossRefGoogle Scholar
  18. Heath, S.M., Southworth, D., and D’Allura, J.A., Localization of Nickel in Epidermal Subsidiary Cells of Leaves of Thlaspi montanum var. siskiyouense (Brassicaceae) using Energy-Dispersive X-Ray Microanalysis, Int. J. Plant Sci., 1997, vol. 158, pp. 184–188.CrossRefGoogle Scholar
  19. Javelle, M., Vernoud, V., Rogowsky, P.M., and Ingram, G.C., Epidermis: the Formation and Functions of a Fundamental Plant Tissue, New Phytol., 2011, vol. 189, pp. 17–39.PubMedCrossRefGoogle Scholar
  20. Küpper, H., Lombi, E., Zhao, F.-J., Wieshammer, G., and McGrath, S.P., Cellular Compartmentation of Nickel in the Hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense, J. Exp. Bot., 2001, vol. 52, pp. 2291–2300.PubMedCrossRefGoogle Scholar
  21. Krämer, U., Pickering, J.J., Prince, R.C., Raskin, J., Salt, D.E., Subcellular Localization and Speciation of Nickel in Hyperaccumulator and Non-accumulator Thlaspi Species, Plant Physiol., 2000, vol. 122, pp. 1343–1354.PubMedCrossRefGoogle Scholar
  22. Larkin, J.C., Brown, M.L., and Schiefelbein, J., How Do Cells Know What They Want to Be When They Grow up? Lessons from Epidermal Patterning in Arabidopsis, Annu. Rev. Plant Biol., 2003, vol. 54, pp. 403–430.PubMedCrossRefGoogle Scholar
  23. Linsbauer, K., Die Epidermis, Handbuch der Pflanzenanatomie, Berlin: Borntraeger, Bd. 4. Lief., 1930.Google Scholar
  24. Marmiroli, M., Maestri, E., Antonioli, G., Gonnelli, C., Gabbrielli, R., and Marmiroli, N., Microanalysis and Microfluorescence Application for Elemental Mapping in Alyssum: Techniques Results and Comparisons, in FOR-MATEX Microscopy Book Series (N°2): Current Issues on Multidisciplinary Microscopy Research and Education, 2004, pp. 165–172.Google Scholar
  25. McNear, D.H.Jr., Peltier, E., Everhart, J., Chaney, R.L., Sutton, S., Newville, M., Rivers, M., and Sparks, D.L., Application of Quantitative Fluorescence and Absorptionedge Computed Microtomography to Image Metal Compartmentalization in Alyssum murale, Environ. Sci. Technol., 2005, vol. 39, pp. 2210–2218.PubMedCrossRefGoogle Scholar
  26. Mishra, D., and Kar, M., Nickel in Plant Growth and Metabolism, Bot. Rev., 1974, vol. 40, pp. 395–452.CrossRefGoogle Scholar
  27. Psaras, G.K., Constantinidis, T., Cotsopoulos, B., and Manetas, Y., 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., 2000, vol. 86, pp. 73–78.CrossRefGoogle Scholar
  28. Richau, K.H., Kozhevnikova, A.D., Seregin, I.V., Vooijs, R., Koevoets, P.L., Smith, J.A., Ivanov, V.B., and Schat, H., Chelation by Histidine Inhibits the Vacuolar Sequestration of Nickel in Roots of the Hyperaccumulator Thlaspi caerulescens, New Phytol., 2009, vol. 183, pp. 106–116.PubMedCrossRefGoogle Scholar
  29. Seregin, I.V. and Kozhevnikova, A.D., Roles of Root and Shoot Tissues in Transport and Accumulation of Cadmium, Lead, Nickel, and Strontium, Russ. J. Plant Physiol., 2008, vol. 55, no. 1, pp. 1–22.CrossRefGoogle Scholar
  30. Seregin, I.V., Kozhevnikova, A.D., Kazyumina, E.M., and Ivanov, V.B., Nickel Toxicity and Distribution in Maize Roots, Russ. J. Plant Physiol., 2003, vol. 50, no. 5, pp. 711–718.CrossRefGoogle Scholar
  31. Shaumlöffel, E., ber die Colorimetrische Bestimmung der Mikronärschtoffe Kupfer, Zink, Kobalt, Mangan, Eisen und Molibdän aus Einer Aschenlösung Durch Fraktionierte Extraktion, Landwirtschaftliche Forshung, Sonderheft, 1960, vol. 13, pp. 278–286.Google Scholar
  32. Smart, K.E., Kilburn, M.R., Salter, C.J., Smith, J.A.C., and Grovenor, C.R.M., NanoSIMS and EPMA Analysis of Nickel Localisation in Leaves of the Hyperaccumulator Plant Alyssum lesbiacum, Int. J. Mass. Spectrom., 2007, vol. 260, pp. 107–114.CrossRefGoogle Scholar
  33. Tappero, R., Peltier, E., Gräfe, M., Heidel, K., Ginder-Vogel, M., Livi, K.J.T., Rivers, M.L., Marcus, M.A., Chaney, R.L., and Sparks, D.L., Hyperaccumulator Alyssum murale Relies on a Different Metal Storage Mechanism for Cobalt than for Nickel, New Phytol., 2007, vol. 175, pp. 641–654.PubMedCrossRefGoogle Scholar
  34. Welch, R.M., Micronutrient Nutrition of Plants, Crit. Rev. Plant Sci., 1995, vol. 14, pp. 49–82.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations