, Volume 67, Issue 3, pp 505–516 | Cite as

Root system morphology and primary root anatomy in natural non-metallicolous and metallicolous populations of three Arabidopsis species differing in heavy metal tolerance

  • Andrea Staňová
  • Eva Ďurišová
  • Viera Banásová
  • Erika Gurinová
  • Miriam Nadubinská
  • Lucia Kenderešová
  • Miroslav Ovečka
  • Milada ČiamporováEmail author
Full Paper Botany


Root system morphology was characterized in the seedlings of heavy-metal sensitive Arabidopsis thaliana, the non-metallicolous (NM) and metallicolous (M) populations of the tolerant A. arenosa and A. halleri, developed on the natural soils: the Zn-Pb-Cd-Cu-contaminated (C soils), the non-contaminated (NC soils), and on an identical nutrient-rich compost. Anatomy of primary roots grown on agar medium with control and elevated zinc concentrations was investigated also in the model A. thaliana ecotype Columbia.

The three Arabidopsis species differed in morphological and/or quantitative responses to the varying soil qualities. Comparing to natural NC soil, the morphology of A. thaliana root system differed only on the compost with dominating lateral root lengths while the root lengths were reduced on the C soil. In NM and M populations of A. arenosa the lateral root elongation and density were reduced on the C soil and root growth but not lateral root density were stimulated on the compost. In NM and M populations of A. halleri the root system morphology remained unaltered in all three soils. The root elongation was reduced but lateral root initiation increased on the C soil while the roots were longer and lateral root density lower on the compost. The responses of A. arenosa or A. halleri populations differed only in absolute root lengths. The similarity in morphological responses to varying soil metal contents indicated plastic responses rather than heritable traits of the root systems.

The root tissue organization three Arabidopsis species resembled the known A. thaliana ecotype Columbia. Quantitatively, the tolerant species and their M populations had thicker roots due to a greater number and size of cells in epidermis, cortex including a higher number of middle cortex cells, and endodermis. The rates of root growth and quantitative root anatomy may represent morphological traits contributing to heavy metal tolerance of the Arabidopsis species.

Key words

Arabidopsis thaliana A. arenosa A. halleri natural populations seedlings root system root tissue organization 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alfordé. R., Pilon-Smits E.A.H. & Paschke M.V. 2010. Metallophytes — a view from the rhizosphere. Plant Soil 337: 33–50.CrossRefGoogle Scholar
  2. Arduini I., Masoni A., Mariotti M. & Ercoli L. 2004. Low cadmium application increase miscanthus growth and cadmium translocation. Env. Exp. Bot. 52: 89–100.CrossRefGoogle Scholar
  3. Arrivault S., Senger T. & Kramer U. 2006. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J. 46: 861–879.PubMedCrossRefGoogle Scholar
  4. Banásová V., Ďurišová M., Gurinová E. & Čiamporová M. 2012. Natural vegetation, metal accumulation and tolerance in plants growing on heavy metal rich soils, pp. 233–250. In: Kothe E. & A. Varma A. (eds), Bio-geo Interactions in Metal-contaminated Soils, Soil Biology 31, DOI 10.1007/978-3-642-23327-2_12, Springer-Verlag Berlin Heidelberg.CrossRefGoogle Scholar
  5. Baum S.E., Dubrovsky J.G. & Rost T.L. 2002. Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots. Amer. J. Bot. 89: 908–920.CrossRefGoogle Scholar
  6. Bert V., Macnair M.R., De Laguerie P., Saumitou-Laprade P. & Petit D. 2000. Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol. 146: 225–233.CrossRefGoogle Scholar
  7. Bomblies K. & Weigel D. 2010. Arabidopsis and relatives as models for the study of genetic and genomic incompatibilities. Phil. Trans. R. Soc. B 365: 1815–1823.PubMedCrossRefGoogle Scholar
  8. Bona E., Marsano F., Cavaletto M. & Berta G. 2007. Copper stress in Cannabis sativa roots: morphological and proteomic analysis. Caryologia 60: 96–101.Google Scholar
  9. Broadley M., White P.J., Hammond J.P., Zelko I. & Lux A. 2007. Zinc in plants. New Phytol. 173: 677–702.PubMedCrossRefGoogle Scholar
  10. Chiou T.J. & Lin S.I. 2011. Signalling network in sensing phosphate availability in plants. Ann. Rev. Plant Biol. 62: 185–206.CrossRefGoogle Scholar
  11. Clauss M.J. & Koch M.A. 2006. Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11: 449–459.PubMedCrossRefGoogle Scholar
  12. Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K. & Scheres B. 1993. Cellular organisation of the Arabidopsis thaliana root. Development 119: 71–84.PubMedGoogle Scholar
  13. Fiałkiewicz B. & Rostrański A. 2006. Morphological variability of Cardaminopsis halleri (L.) Hayek from selected habitats in the Silesian Upland (Southern Poland). Biodiv. Res. Conserv. 1–2: 37–44.Google Scholar
  14. Fitter A. H. 1996. Characteristics and function of root system, pp. 1–20. In: Waisel Y., Eshel A. & Kafkafi U. (eds), Plant roots: The hidden half (2nd ed.), Marcel Dekker Inc., New York, NY, USA.Google Scholar
  15. Franiel I. & Fiałkiewicz B. 2007. Morphological variability of Cardaminopsis halleri (L.) Hayek populations from areas differing in anthropopressure level. Polish J. Environ. Stud. 16: 677–683.Google Scholar
  16. Haines B.J. 2002. Zincophilic root foraging in Thlaspi caerulescens. New Phytol. 155: 363–372.CrossRefGoogle Scholar
  17. Himmelbauer M.L., Puschenreiter M., Schnepf A., Loiskandl W. & Wenzel W. 2005. Root morphology of Thlaspi goesingense Hálácsy grown on a serpentine soil. J. Plant Nutr. Soil Sci. 161: 138–144.CrossRefGoogle Scholar
  18. Howden R. & Cobbett C.S. 1992. Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol. 99: 100–107.CrossRefGoogle Scholar
  19. Jovanovic M., Lefebvre V., Laporte P., Gonzalez-Rizzo S., Lelandais-Bri`ere C., Frugier F., Hartmann C. & Crespi M. 2007. How the environment regulates root architecture in dicots. Adv. Bot. Res. 46: 35–74.CrossRefGoogle Scholar
  20. Kasim W.A. 2006. Changes induced by copper and cadmium stress in the anatomy and grain yield of Sorghum bicolor (L.) Moench. Int. J. Agri. Biol. 8: 123–128.Google Scholar
  21. Keller C., Hammer D. Kayser A., Richner W., Brodbeck M. & Sennhauser M. 2003. Root development and heavy metal phytoextraction efficiency: comparison of different plant species in the field. Plant Soil 249: 67–81.CrossRefGoogle Scholar
  22. Kenderešovňová A., Pavlovkin J., Ďurišová M., Čiamporovčka M. 2012. Early Zn2+-induced effects on membrane potentials account for primary, unspecific demonstration of heavy metal susceptibility in tolerant and sensitive Arabidopsis species. Ann. Bot. (in press)Google Scholar
  23. Lequeux H., Hermans C., Lutts S. & Verbruggen N. 2010. Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol. Biochem. 48: 673–682.PubMedCrossRefGoogle Scholar
  24. Li W., Khan M.A., Yamaguchi S. & Kamiya Y. 2005. Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul. 46: 45–50.CrossRefGoogle Scholar
  25. Linkohr B.I., Williamson L.C., Fitter A.H. & Leyser H.M.O. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J. 29: 751–760.PubMedCrossRefGoogle Scholar
  26. López-Bucio J., Cruz-Ramírez A. & Herrera-Estrella L. 2003. The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6: 280–287.PubMedCrossRefGoogle Scholar
  27. Loudet O., Gaudon V., Trubuil A. & Daniel-Vedele F. 2005. Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family. Theor. Appl. Genet. 110: 742–753.PubMedCrossRefGoogle Scholar
  28. Lux A., Luxová M., Abe J. & Morita S. 2004. Root cortex: structural and functional variability and responses to environmental stress. Root Res. 13: 117–131.CrossRefGoogle Scholar
  29. Lux A., Martinka M., Vaculík M. & White P.J. 2011a. Root responses to cadmiumin the rhizosphere: a review. J. Exp. Bot. 62: 21–37.PubMedCrossRefGoogle Scholar
  30. Lux A., Vaculík M., Martinka M., Liškov, Stirk W.A. & Van Staden J. 2011b. Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea. Ann. Bot. 107: 285–292.PubMedCrossRefGoogle Scholar
  31. Lucas M., Swarup R., Paponov I.A., Swarup K., Casimiro I., Lake D., Peret B., Zappala S., Mairhofer S., Whitworth M., Wang J., Ljung K., Marchant A., Sandberg G., Holdsworth M.J., Palme K., Pridmore T., Mooney S. & Bennett M.J. 2011. SHORT-ROOT regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol. 155: 384–398.PubMedCrossRefGoogle Scholar
  32. Malamy J.E. 2005. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28: 67–77.PubMedCrossRefGoogle Scholar
  33. Martinka M. & Lux A. 2004. Response of roots of three populations of Silene dioica to cadmium treatment. Biologia 59: 185–189.Google Scholar
  34. Meyer C.-L., Kostecka A.A., Saumitou-Laprade P., Créach A., Castric V., Pauwels M. & Frérot H. 2010. Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytol. 185: 130–142.PubMedCrossRefGoogle Scholar
  35. Murashige T. & Skoog F. 1962. A revised medium for rapid growth and biosynthesis with tobacco tissue culture. Plant Physiol. 15: 473–497.CrossRefGoogle Scholar
  36. Nibau C., Gibbs D.J. & Coates J.C. 2008. Branching out in new directions: the control of root architecture by lateral root formation. New Phytol. 179: 595–614.PubMedCrossRefGoogle Scholar
  37. Nicola S. 1998. Transplant production and performance: understanding root systems to improve seedling quality. Hort. Technol. 8: 544–549.Google Scholar
  38. Obroucheva N.V., Bystrova E.I., Ivanov V.B., Anupova O.V. & Seregin I.V. 1998. Root growth responses to lead in young maize seedlings. Plant Soil 200: 55–61.CrossRefGoogle Scholar
  39. Paquette A.J. & Benfey P.N. 2005. Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol. 138: 636–640.PubMedCrossRefGoogle Scholar
  40. Przedpełska E. & Wierzbicka M. 2007. Arabidopsis arenosa (Brassicaceae) from a lead-zinc waste heap in southern Poland — a plant with high tolerance to heavy metals. Plant Soil 299: 43–53.CrossRefGoogle Scholar
  41. Roosens N.H.C.J., Willems G. & Saumitou-Laprade P. 2008. Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci. 13: 208–215.PubMedCrossRefGoogle Scholar
  42. Scheres B., Benfey P. & Dolan L. 2002. Root development. The Arabidopsis Book. American Society of Plant Biologists, DOI: 10.1199/tab.0101.Google Scholar
  43. Schwartz C., Morel J.L., Saumier S., Whiting S.N. & Baker A.J.M. 1999. Root development of the zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208: 103–115.CrossRefGoogle Scholar
  44. Staňová A., Banásová V. & Čiamporová M. 2010. Stratégie troch druhov rodu Arabidopsis pri nadbytku t’ažkých kovov v pôde. Bull. Slov. Bot. Spoločn. 32(Suppl. 2): 237–245Google Scholar
  45. Williamson L., Ribrioux S., Fitter A. & Leyser O. 2001. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol. 126: 1–8.CrossRefGoogle Scholar
  46. Zelko I., Lux A. & Czibula K. 2008. Difference in the root structure of hyperaccumulator Thlaspi caerulescens and nonhyperaccumulator Thlaspi arvense. Int. J. Environ. Pollut. 33: 1123–132.CrossRefGoogle Scholar
  47. Zhang H., Rong H. & Pilbeam D. 2007. Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J. Exp. Bot. 58: 2329–2338.PubMedCrossRefGoogle Scholar

Copyright information

© © Versita Warsaw and Springer-Verlag Wien 2012

Authors and Affiliations

  • Andrea Staňová
    • 1
  • Eva Ďurišová
    • 1
  • Viera Banásová
    • 1
  • Erika Gurinová
    • 1
  • Miriam Nadubinská
    • 1
  • Lucia Kenderešová
    • 1
    • 2
  • Miroslav Ovečka
    • 1
    • 2
  • Milada Čiamporová
    • 1
    Email author
  1. 1.Institute of BotanySlovak Academy of SciencesBratislavaSlovakia
  2. 2.Centre of the Region Hana for Biotechnological and Agricultural Research, Faculty of SciencePalacky UniversityOlomoucCzech Republic

Personalised recommendations