Plant and Soil

, Volume 251, Issue 1, pp 55–63 | Cite as

Different mechanisms account for enhanced copper resistance in Silene armeria ecotypes from mine spoil and serpentine sites

  • Mercè Llugany
  • Alessandra Lombini
  • Charlotte Poschenrieder
  • Enrico Dinelli
  • Juan Barceló


The resistance to excess Cu was evaluated in solution culture in three ecotypes of Silene armeria from different origin, a garden soil (Cadriano), a serpentine site (Prinzera) and a Cu mine spoil (Vigonzano). Root elongation and viability staining of root tip cells were used as indicators for Cu resistance. The Cu resistance increased in the order Cadriano <Prinzera<Vigonzano. Renewal of the root cap in Prinzera and enhanced border cell production in Vigonzano in response to excess Cu provided a more efficient protection of the root tip meristem than in Cu sensitive Cadriano. The enhanced Cu resistance in Prinzeracould not be attributed to high soil Cu acting as a natural selection factor at the serpentine site. In PrinzeraCu exclusion from roots and shoots probably was a consequence of root impermeabilization causing reduced radial water and ion flux in roots. In contrast, the high Cu resistance in the mine spoil ecotype, Vigonzano, was due to both reduced Cu uptake and higher tissue tolerance of Cu.

Cell viability copper toxicity copper resistance serpentine Silene armeria xylem sap 


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  1. Baker A J M, Brooks R R, Pease A J and Malaisse F 1983 Studies on copper and cobalt tolerance in three closely related taxa within the genus Silene L. (Caryophyllaceae) from Zaire. Plant Soil 73, 377–385.Google Scholar
  2. Barceló J and Poschenrieder C 2002 Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ. Exp. Botany 48, 75–92.Google Scholar
  3. Barrowclough D E, Peterson C A and Steudle E 2000 Radial hydraulic conductivity along developing onion roots. J. Exp. Bot. 51, 547–557.Google Scholar
  4. Clarkson D T 1969 Metabolic aspects of aluminium toxicity and some possible mechanisms of resistance. In Ecological Aspects of the Mineral Nutrition of Plants. Ed. I H Rorison. pp. 381–397. Blackwell Scientific Publications, Oxford.Google Scholar
  5. Cox R M and Hutchinson T C 1981 Multiple and co-tolerance to metals in the grass Deschampsia caespitosa: adaptation, preadaptation and 'cost'. J. Plant Nutr. 3, 731–741.Google Scholar
  6. Delisle G, Champoux M and Houde M 2001 Characterization of oxalate oxidase and cell death in Al-sensitive and tolerant wheat roots. Plant Cell Physiol. 42, 324–333.Google Scholar
  7. De Vos C H R, Vooijs R, Schat H and Ernst W H O 1989 Copperinduced damage to the permeability barrier in roots of Silene cucubalus. J. Plant Physiol. 135, 165–169.Google Scholar
  8. De Vos C H R 1991 Copper-Induced Oxidative Stress and Free Radical Damage in Roots of Copper Tolerant and Sensitive Silene cucubalus. Ph. D. Thesis Vrije Universiteit Amsterdam.Google Scholar
  9. De Vos C H R, Schat H, De Waal M A M, Vooijs R and Ernst W H O 1991 Increased resistance to copper-induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiol. Plant. 82, 523–528.Google Scholar
  10. De Vos C H, Vonk M J, Vooijs R and Schat H 1992 Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol. 98, 853–858.Google Scholar
  11. De Vos C H R, Ten Bookum WM, Vooijs R, Schat H and De Kok L J 1993 Effect of copper on fatty acid composition and peroxidation of lipids in the roots of copper tolerant and sensitive Silene cucubalus. Plant Physiol. Biochem. 31, 151–158.Google Scholar
  12. Dinelli E and Lombini A 1996 Metal distribution in plants growing on copper mine spoils in Northern Apennines (Italy): the evaluation of seasonal variations. Applied Geochem. 11, 375–385.Google Scholar
  13. Dinelli E, Lombini A, Ferrari C and Simoni A 1997 Heavy metals in the serpentinite soils of selected outcrops of Piacenza and Parma provinces (Northern Apennines, Italy). Miner. Petrog. Acta 40, 241–255.Google Scholar
  14. Ernst W H O 1978 Schwermetallvegetation der Erde. Fischer-Verlag, Stuttgart.Google Scholar
  15. Ernst W H O, Verkleij J A C and Schat V 1992 Metal tolerance in plants. Acta Bot. Neerl. 41, 229–248.Google Scholar
  16. Frenckell-Insam von B A K and Hutchinson T C 1993 Occurrence of heavy metal tolerance and co-tolerance in Deschampsia cespitosa (L) Beauv. From European and Canadian populations. New Phytol. 125, 555–564.Google Scholar
  17. Gonnelli C, Galardi F and Gabbrielli R 2001 Nickel and copper tolerance and toxicity in three Tuscan populations of Silene paradoxa. Physiol Plant 113, 507–514.Google Scholar
  18. Jones K H and Senet J A 1985 An improved method to determine cell viability by simultaneous staining with fluorescein diacetatepropidium iodide. J. Histochem, Cytochem. 33, 77–79.Google Scholar
  19. Kochian L V 1995 Cellular mechanisms of aluminum toxicity and resistance in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 46, 237–260.Google Scholar
  20. Koyama H, Today T, Dawair Z and Hara T 1995 Effects of aluminium and pH on root growth and cell viability in Arabidopsis thaliana strain Landsberg in hydroponic culture Plant Cell Physiol. 36, 201–205.Google Scholar
  21. Lolkema P C and Vooijs R 1986 Copper tolerance in Silene cucubalus. Subcellular distribution of copper and its effects on chloroplasts and plastocyanin synthesis. Planta 167, 30–36Google Scholar
  22. Lombini A, Dinelli E, Ferrari C and Simoni A 1998 Plant-soil relationships in the serpentinite screes of Mt Prinzera (Northern Apennines). J. Geochem Explor. 64, 19–33.Google Scholar
  23. Macnair MR 1993 The genetics of metal tolerance in vascular plants. New Phytol 124, 541–559.Google Scholar
  24. Macnair M R, Tilstone G H and Smith S E 2000 The genetics of metal tolerance and accumulation in higher plants. In Phytoremediation of Contaminated Soil and Water. Eds. N Terry and G Bañuelos. pp. 235–250. Lewis Publisher, Boca Raton.Google Scholar
  25. Mengoni A, Barabesi C, Gonnelli C, Galardi F, Gabbrielli R and Bazzicalupo M 2001 Genetic diversity of heavy metal-tolerant populations in Silene paradoxa L. (Caryophyllaceae): a chloroplast microsatellite analysis. Mol. Ecol. 10, 1909–1916.Google Scholar
  26. Miyasaka S C and Hawes C 2000 Possible role of root border cells in detection and avoidance of aluminium toxicity. Plant Physiol. 125, 1978–1987.Google Scholar
  27. Murphy A and Taiz L 1997 Correlation between long term K+ leakage and copper tolerance in ten Arabidopsis ecosystems. New Phytol. 136, 211–222.Google Scholar
  28. Murphy A, Eisinger W, Shaff J, Kochian L V, Taiz L 1999. Early copper induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate effluse. Plant Physiol. 121, 1375–1382.Google Scholar
  29. Poschenrieder C and Barceló J 1999 Water relations in heavy metal stressed plants. In Heavy Metal Stress in Plants. From Molecules to Ecosystems. Eds. M N V Prasad and J Hagemeyer. pp. 207–229. Springer Verlag, Berlin.Google Scholar
  30. Quiroga M, Guerrero C, Botella M, Barceló A, Amaya I, Medina M I, Alonso F J, Milrad de Forchetii S, Tigier H and Valpuesta V 2000 A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol. 122, 1119–1127.Google Scholar
  31. Schat H and Ten Bookum W M 1992a Metal specificity of metal tolerance syndromes in higher plants. In The Vegetation of Ultramafic (Serpentine) Soils. Eds. A J M Baker, R D Reeves and J Proctor. pp. 337–352. Intercept Ltd., Andover, UK.Google Scholar
  32. Schat H and Ten Bookum W M 1992b Genetic control of copper tolerance in Silene vulgaris. Heredity 68, 219–229.Google Scholar
  33. Schat H and Vooijs R 1997 Multiple tolerance and co-tolerance to heavy metals in Silene vulgaris: a co-segregation analysis. New Phytol. 136, 489–496.Google Scholar
  34. Schat H, Llugany M and Bernhard R 2000 Metal-specific patterns of tolerance, uptake, and transport of heavy metals in hyperaccumulating and nonaccumulating metallophytes. In Phytoremediation of Contaminated Soil and Water. Eds. B Terry and G Bañuelos. pp. 171–188. Lewis Publisher, Boca Raton.Google Scholar
  35. Symeonidis L, McNeilly T and Bradshaw A D 1985 Differential tolerance of three cultivars of Agrostis capillaris L. to cadmium, copper, lead, nickel and zinc. New Phytol. 101, 309–315.Google Scholar
  36. Strange J and Macnair M R 1991 Evidence for a role for the cell membrane in copper tolerance of Mimulus guttatus Fisher ex D.C. New Phytol. 119, 383–388.Google Scholar
  37. Van Hoof N A L M, Koevoets P L M, Hakvoort H W J, Ten Bookum W M, Schat H, Verkleij J A C and Ernst W H O 2001a Enhanced ATP-dependent copper efflux across the root cell plasma membrane in copper-tolerant Silene vulgaris. Physiol. Plant. 113, 225–232.Google Scholar
  38. Van Hoof N A L M, Hassinen V H, Hakvoort H W J, Ballintijn K F, Schat H, Verkleij J A C, Ernst W H O, Karenlampi S O and Tervahoneta A I 2001b Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of 2b-type metallothioneine gene. Plant Physiol. 126, 1519–1526.Google Scholar
  39. Wainwright S J and Woolhouse H W 1977 Some physiological aspects of copper and zinc tolerance in Agrostis tenuis Sibth.: cell elongation and membrane damage. J. Exp. Bot. 28, 1029–1036.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Mercè Llugany
    • 1
  • Alessandra Lombini
    • 1
  • Charlotte Poschenrieder
    • 1
  • Enrico Dinelli
    • 2
  • Juan Barceló
    • 1
  1. 1.Laboratorio Fisiología Vegetal, Facultad de CienciasUniversidad Autónoma de BarcelonaBellaterraSpain
  2. 2.Dipartamento de Scienze della Terra e Geologico-AmbientaliUniversità di BolognaBolognaItaly

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