Plant and Soil

, Volume 370, Issue 1–2, pp 197–221 | Cite as

Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media

  • J. Escarré
  • C. Lefèbvre
  • H. Frérot
  • S. Mahieu
  • N. Noret
Regular Article



Evaluate the genetic and environmental variability of metal concentration and metal mass of Noccaea caerulescens, from metalliferous (MET), non metalliferous (NMET) and serpentine (SERP) soils.


18 populations were cultivated in 18 different growth conditions, such as a soil mine tailing, soils amended with zinc (Zn), cadmium (Cd) and nickel (Ni) salts (in mixtures or in monometallic salts) and a hydroponic solution with two Zn concentrations.


MET populations had Zn concentrations lower than NMET and SERP in the different soils but higher Cd mass (the product of aerial biomass and foliar metal concentration). SERP had the highest Ni concentration and Ni mass values. The addition of Cd or Ni to a Zn-contaminated soil significantly decreases Zn concentration. In hydroponics, MET and NMET had equivalent Zn concentrations but these were three times higher than those obtained in soil experiments. Zn mass of NMET was significantly lower than MET with the latter having Zn mass values largely above those obtained in mine soil.


Results showed a large heterogeneity of responses among populations depending on the substrate used, and it was not possible to correctly assign a single population to its accurate origin with only one experiment. Finally, data on metal concentration obtained in culture soils are closer to those in field soils than those from hydroponics so that they could give a more accurate information on the accumulating capacity of Noccaea caerulescens and its use in phytoextraction of metals in field conditions.


Thlaspi caerulescens Mine soil Plant populations Phytoremediation Zn/Cd/Ni hyperaccumulation Metal tolerance 


  1. Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85CrossRefGoogle Scholar
  2. Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003a) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419CrossRefGoogle Scholar
  3. Assunção AGL, Schat H, Aarts MGM (2003b) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360CrossRefGoogle Scholar
  4. Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003c) A co-segregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390CrossRefGoogle Scholar
  5. Assunção AGL, Bleeker P, ten Bookum WM, Vooijs R, Schat H (2008) Intra-specific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant Soil 303:289–299CrossRefGoogle Scholar
  6. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  7. Baker AJM, Walker PL (1990) Ecophysiology of metal mass by tolerant plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 155–177Google Scholar
  8. Banásová V, Horak O, Nadubinská M, Čiamporová M, Lichtscheidl I (2008) Heavy metal content in Thlaspi caerulescens J. et C. Presl growing on metalliferous and non-metalliferous soils in Central Slovakia. Int J Environ Pollut 33:133–145CrossRefGoogle Scholar
  9. Basic N, Keller C, Fontanillas P, Vittoz P, Besnard G, Galland N (2006) Cadmium hyperaccumulation and reproductive traits in natural Thlaspi caerulescens populations. Plant Biology 8:64–72PubMedCrossRefGoogle Scholar
  10. Berglund ABN, Dahlgren S, Westerbergh A (2004) Evidence for parallel evolution and site-specific selection of serpentine tolerance in Cerastium alpinum during the colonization of Scandinavia. New Phytol 161:199–209CrossRefGoogle Scholar
  11. Brown SL, Chaney RL, Angle JS, Baker AJM (1995) Zinc and cadmium mass by hyperaccumulator Thlaspi caerulescens grown in nutrient solution. Soil Sci Soc Am Proc 59:125–133CrossRefGoogle Scholar
  12. Cataldo DA, Garland TR, Wildung RE (1978) Nickel in Plants. I. Uptake kinetics using intact soybean seedlings. Plant Physiol 62:563–565PubMedCrossRefGoogle Scholar
  13. Chardot V, Echevarria G, Gury M, Massoura S, Morel JL (2007) Nickel bioavailability in an ultramafic toposequence in the Vosges Mountains (France). Plant Soil 293:7–21CrossRefGoogle Scholar
  14. Cottenie A, Verloo M, Kiekens L, Velghe G, Camerlynck R (1982) Chemical analysis of plants and soils. State University Ghent, Belgium, Laboratory of Analytical and Agrochemistry, 63pGoogle Scholar
  15. Dechamps C, Roosens NH, Hotte C, Meerts P (2005) Growth and mineral element composition in two ecotypes of Thlaspi caerulescens on Cd contaminated soil. Plant Soil 273:327–335CrossRefGoogle Scholar
  16. Dechamps C, Lefèbvre C, Noret N, Meerts P (2007) Reaction norms of life history traits in response to zinc in Thlaspi caerulescens from metalliferous and nonmetalliferous sites. New Phytol 173:191–198PubMedCrossRefGoogle Scholar
  17. Dechamps C, Noret N, Mozek R, Draye X, Meerts P (2008a) Root allocation in metal-rich patch by Thlaspi caerulescens from normal and metalliferous soil - new insights into the rhizobox approach. Plant Soil 310:211–224CrossRefGoogle Scholar
  18. Dechamps C, Noret N, Mozek R, Escarré J, Lefèbvre C, Gruber W, Meerts P (2008b) Cost of adaptation to a metalliferous environment for Thlaspi caerulescens: a field reciprocal transplantation approach. New Phytol 177:167–177PubMedGoogle Scholar
  19. Escarré J, Lefèbvre C, Gruber W, Leblanc M, Lepart J, Rivière Y, Delay B (2000) Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. New Phytol 145:429–437CrossRefGoogle Scholar
  20. Escarré J, Lefèbvre C, Raboyeau S, Dossantos A, Gruber W, Cleyet-Marel JC, Frérot H, Noret N, Mahieu S, Collin C, van Oort F (2011) Heavy metal concentration survey in soils and plants of the Les Malines mining district (Southern France): Implications for soil restoration. Water Air Soil Pollut 216:485–504CrossRefGoogle Scholar
  21. Fangueiro D, Bermond A, Santos E, Carapuça H, Duarte A (2005) Kinetic approach to heavy metal mobilization assessment in sediments: choose of kinetic equations and models to achieve maximum information. Talanta 66:844–857PubMedCrossRefGoogle Scholar
  22. Faucon MP (2004) Adaptation des plantes aux sites métallifères. I. Réponse à l'hétérogénéité du substrat (calcaire et schisteux) chez Thlaspi caerulescens. II. Propriétés allélopathiques chez Armeria maritima. Mémoire de Licence. Université Libre de Bruxelles, Brussels (Belgium)Google Scholar
  23. Frérot H, Lefèbvre C, Petit C, Collin C, Dos Santos A, Escarré J (2005) Zinc tolerance and hyperaccumulation in F1 and F2 offspring from intra- and inter-ecotype crosses of Thlaspi caerulescens. New Phytol 165:111–119PubMedCrossRefGoogle Scholar
  24. Frérot H, Lefèbvre C, Gruber W, Collin C, Dos Santos A, Escarré J (2006) Specific interactions between local metallicolous plants improve the phytostabilization of mine soils. Plant Soil 282:53–65CrossRefGoogle Scholar
  25. Garnier E (1992) Growth analysis of congeneric annual and perennial grass species. J Ecol 80:665–675CrossRefGoogle Scholar
  26. Gregor JW, Watson PJ (1961) Ecotypic differentiation: Observations and reflections. Evolution 15:166–173CrossRefGoogle Scholar
  27. Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci SA 95:7220–7224CrossRefGoogle Scholar
  28. Hart J, Welch R, Norvell W, Clarke J, Kochian L (2005) Zinc effects on cadmium accumulation and partitioning in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol 167:391–401PubMedCrossRefGoogle Scholar
  29. Koch GW, Winner WE, Nardone A, Mooney HA (1987) A system for controlling the root and shoot environment for plant growth studies. Environ Exp Bot 27:365–377CrossRefGoogle Scholar
  30. Labanowski J, Monna F, Bermond A, Cambier P, Fernandez C, Lamy I, van Oort F (2008) Kinetic extractions to assess mobilization of Zn, Pb, Cu, and Cd in a metal-contaminated soil: EDTA vs. citrate. Environ Pollut 153:693–701CrossRefGoogle Scholar
  31. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2001a) Phytoremediation of heavy metal-contaminated soils: Natural hyperaccumulation versus chemically enhanced phytoextraction. J Environ Qual 30:1919–1926PubMedCrossRefGoogle Scholar
  32. Lombi E, Zhao FJ, McGrath SP, Young SD, Sacchi GA (2001b) Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol 149:53–60CrossRefGoogle Scholar
  33. Macnair MR, Smirnoff N (1999) Use of zincon to study mass and accumulation of zinc by zinc tolerant and hyperaccumulating plants. Commun Soil Sci Plant Anal 30:1127–1136CrossRefGoogle Scholar
  34. Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecology 133:221–231CrossRefGoogle Scholar
  35. Meerts P, Duchêne P, Gruber W, Lefèbvre C (2003) Metal accumulation and competitive ability in metallicolous and non-metallicolous Thlaspi caerulescens fed with different Zn salts. Plant Soil 249:1–8CrossRefGoogle Scholar
  36. Meyer FK (2006) Kritische Revision der “Thlaspi”-Arten Europas, Afrikas und Vorderasiens. Spezieller Teil. IX. Noccaea Moench. Thüringische Botanische Gesellschaft, Haussknechtia Suppl.12. 343p.Google Scholar
  37. Molitor M, Dechamps C, Gruber W, Meerts P (2005) Thlaspi caerulescens on nonmetalliferous soil in Luxembourg: ecological niche and genetic variation in mineral element composition. New Phytol 165:503–512PubMedCrossRefGoogle Scholar
  38. Noret N, Meerts P, Tolrà R, Poschenrieder C, Barceló J, Escarré J (2005) Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates. New Phytol 165:763–772PubMedCrossRefGoogle Scholar
  39. Noret N, Meerts P, Vanhaelen M, Dos Santos A, Escarré J (2007) Do metal-rich plants deter herbivores? A field test of the defence hypothesis. Oecologia 152:92–100PubMedCrossRefGoogle Scholar
  40. Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430CrossRefGoogle Scholar
  41. Reeves RD, Baker AJM (1984) Studies on metal mass by plants from serpentine and non-serpentine populations of Thlaspi goesingense Hálácsy (Cruciferae). New Phytol 98:191–204CrossRefGoogle Scholar
  42. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behaviour of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172CrossRefGoogle Scholar
  43. Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56CrossRefGoogle Scholar
  44. Roosens N, Verbruggen N, Meerts P, Ximénez-Embún P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672CrossRefGoogle Scholar
  45. Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60:696–710PubMedGoogle Scholar
  46. SAS (2004) SAS-STAT® 9.1 User’s guide. In: SAS Institute Inc, Cary, NC, USAGoogle Scholar
  47. Shen ZG, Li XD, Chen HM (2000) Comparison of elemental composition and solubility in the zinc hyperaccumulator Thlaspi caerulescens with the non-hyperaccumulator Thlaspi ochroleucum. Bull Environ Contam Toxicol 65:343–350PubMedCrossRefGoogle Scholar
  48. STATISTIX (2003) STATISTIX 8. User’s manual. Analytical Software. Tallahassee, FL. USAGoogle Scholar
  49. Taylor SI, Macnair MR (2006) Within and between population variation for zinc and nickel accumulation in two species of Thlaspi (Brassicaceae). New Phytol 169:505–513PubMedCrossRefGoogle Scholar
  50. Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (1964–1993) Flora Europaea. Cambridge University Press, Cambridge, UKGoogle Scholar
  51. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2012) Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  52. Wright JW, Stanton ML, Scherson R (2006) Local adaptation to serpentine and non-serpentine soils in Collinsia sparsiflora. Evol Ecol Res 8:1–21Google Scholar
  53. Zhao FJ, Shen ZG, McGrath SP (1998) Solubility of zinc and interactions between zinc and phosphorus in the hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 21:108–114CrossRefGoogle Scholar
  54. Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium mass in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543PubMedCrossRefGoogle Scholar
  55. Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • J. Escarré
    • 1
  • C. Lefèbvre
    • 2
  • H. Frérot
    • 3
  • S. Mahieu
    • 1
  • N. Noret
    • 2
  1. 1.Centre d’Ecologie Fonctionnelle et Evolutive (CNRS) – UMR 5175Montpellier Cedex 05France
  2. 2.Laboratoire d’Ecologie végétale et BiogéochimieUniversité Libre de BruxellesBruxellesBelgium
  3. 3.Laboratoire de Génétique et Evolution des Populations Végétales, UMR CNRS 8198Université Lille 1Villeneuve d’Ascq CedexFrance

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