Skip to main content
SpringerLink
Log in

Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Noccaea caerulescens is a model plant for the understanding of trace metal accumulation and a source of cultivars for phytoextraction. The aim of this study was to investigate natural variation for trace metal accumulation, major nutrient uptake and growth parameters in 22 populations. The correlations among these traits were particularly examined to better understand the eco-physiology and the phytoextraction potential of the species.

Methods

Populations from three edaphic groups, i.e. calamine (CAL), serpentine (SERP) and non metalliferous (NMET) sites were grown in hydroponics for seven weeks at moderate trace metal exposure. Growth indicators, element contents and correlations between these variables were compared.

Results

All the phenotypic characteristics showed a wide variability among groups and populations. The SERP populations showed a smaller plant size, higher cation contents and strong correlations between all element concentrations. NMET populations did not differ in plant size from the CAL ones, but had higher Zn and Ni contents. The CAL populations showed higher Cd and Mn accumulations and lower Ca contents. The trade-off between biomass production and Cd, Ni and Zn accumulation was high in SERP populations and low in the CAL and NMET ones.

Conclusions

N. caerulescens is a genetically diverse species, showing specific features depending on the group and the population. These features may reflect the wide adaptive capacities of the species, and also reveal promising potential for phytoextraction of Cd, Ni and Zn.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamidis GC, Kazakou E, Fyllas NM, Dimitrakopoulos PG (2014) Species adaptive strategies and leaf economic relationships across serpentine and Non-serpentine habitats on Lesbos, eastern Mediterranean. PLoS One 9:e96034. doi:10.1371/journal.pone.0096034

    Article  PubMed  PubMed Central  Google Scholar 

  • Assunção AGL, Bookum WM, Nelissen HJ et al (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Article  Google Scholar 

  • Assuncão AGL, Bleeker P, Wilma M et al (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant Soil 303:289–299

    Article  Google Scholar 

  • Basic N, Keller C, Fontanillas P et al (2006) Cadmium hyperaccumulation and reproductive traits in natural Thlaspi caerulescens populations. Plant Biol Stuttg 8:64–72

    Article  PubMed  CAS  Google Scholar 

  • Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266

    Article  Google Scholar 

  • Chardot V, Echevarria G, Gury M et al (2007) Nickel bioavailability in an ultramafic toposequence in the Vosges mountains (France). Plant Soil 293:7–21

    Article  CAS  Google Scholar 

  • Cheng S-H, Willmann MR, Chen H-C, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485. doi:10.1104/pp. 005645

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cheng N-H, Pittman JK, Shigaki T et al (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  PubMed  CAS  Google Scholar 

  • 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 273:327–335

    Article  CAS  Google Scholar 

  • Escarré J, Lefèbvre C, Gruber W et al (2000) Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. New Phytol 145:429–437

    Article  Google Scholar 

  • Escarré J, Lefèbvre C, Raboyeau S et al (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 216:485–504. doi:10.1007/s11270-010-0547-1

    Article  Google Scholar 

  • Escarré J, Lefèbvre C, Frérot H, et al. (2013) Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media. Plant Soil 1–25. doi: 10.1007/s11104-013-1618-z

  • 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 interecotype crosses of Thlaspi caerulescens. New Phytol 165:111–119

  • Halimaa P, Lin Y-F, Ahonen VH et al (2014) Gene expression differences between Noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353. doi:10.1021/es4042995

    Article  PubMed  CAS  Google Scholar 

  • Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:252–259

    Article  PubMed  CAS  Google Scholar 

  • Kazakou E, Dimitrakopoulos PG, Baker AJM et al (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508

    PubMed  CAS  Google Scholar 

  • Kazakou E, Adamidis GC, Baker AJM et al (2010) Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332:369–385. doi:10.1007/s11104-010-0302-9

    Article  CAS  Google Scholar 

  • Keller C, Diallo S, Cosio C et al (2006) Cadmium tolerance and hyperaccumulation by Thlaspi caerulescens populations grown in hydroponics are related to plant uptake characteristics in the field. Funct Plant Biol 33:673–684

    Article  CAS  Google Scholar 

  • Koopmans GF, Römkens P, Fokkema MJ et al (2008) Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils. Environ Pollut 156:905–914

    Article  PubMed  CAS  Google Scholar 

  • Kruckeberg AR (1954) The ecology of serpentine soils. III. Plant species in relation to serpentine soils. Ecology 267–274.

  • Küpper H, Parameswaran A, Leitenmaier B et al (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674

    Article  PubMed  Google Scholar 

  • Lee J, Brooks RR, Reeves RD et al (1977) Plant-soil relationships in a new Caledonian serpentine flora. Plant Soil 46:675–680

    Article  CAS  Google Scholar 

  • Maxted AP, Black CR, West HM et al (2007) Phytoextraction of cadmium and zinc from arable soils amended with sewage sludge using Thlaspi caerulescens: development of a predictive model. Environ Pollut 150:363–372. doi:10.1016/j.envpol.2007.01.021

    Article  PubMed  CAS  Google Scholar 

  • McDowell SC, Akmakjian G, Sladek C, Mendoza-Cozatl D, Morrissey JB, Saini N, Mittler R, Baxter I, Salt DE, Ward JM, Schroeder JI, Guerinot ML, Harper JF (2013) Elemental concentrations in the seed of mutants and natural variants of Arabidopsis thaliana grown under varying soil conditions. Plos One 8. doi:10.1371/journal.pone.0063014

  • Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–231

    Article  Google Scholar 

  • Milner MJ, Mitani-Ueno N, Yamaji N, et al. (2014) Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation. Plant J n/a–n/a. doi: 10.1111/tpj.12480

  • 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 165:503–512

    Article  PubMed  Google Scholar 

  • Peer WA, Mahmoudian M, Freeman JL, Lahner B, Richards EL, Reeves RD, Murphy AS, Salt DE (2006) Assessment of plants from the Brassicaceae family as genetic models for the study of nickel and zinc hyperaccumulation. New Phytol 172:248–260

  • Proctor J (1971) The plant ecology of serpentine: II. Plant response to serpentine soils. The Journal of Ecology 59:397. doi:10.2307/2258320

    Article  Google Scholar 

  • Redjala T, Sterckeman T, Morel JL (2009) Cadmium uptake by roots: contribution of apoplast and of high-and low-affinity membrane transport systems. Environ Exp Bot 67:235–242

    Article  CAS  Google Scholar 

  • Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172

    Article  CAS  Google Scholar 

  • Roosens N, Verbruggen N, Meerts P et al (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672

    Article  CAS  Google Scholar 

  • Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35. doi:10.1023/A:1022584220411

    Article  CAS  Google Scholar 

  • Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press

  • Van de Mortel JE, Almar Villanueva L, Schat H et al (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal Hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147. doi:10.1104/pp. 106.082073

    Article  PubMed  PubMed Central  Google Scholar 

  • Van de Mortel JE, Schat H, Moerland PD et al (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324. doi:10.1111/j.1365-3040.2007.01764.x

    Article  PubMed  Google Scholar 

  • Van der Ent A, Baker AJ, Reeves RD et al (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 1–16:319–334

    Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    Article  PubMed  CAS  Google Scholar 

  • Visioli G, Vincenzi S, Marmiroli M, Marmiroli N (2011) Correlation between phenotype and proteome in the Ni hyperaccumulator Noccaea caerulescens subsp. caerulescens. Environ. Exp. Bot.

  • Walker RB (1954) The ecology of serpentine soils. II. Factors affecting plant growth on serpentine soils. Ecology 259–266.

  • Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors are grateful to Fabrice Roux (Laboratoire de Génétique et Evolution des Populations Végétales) and Nausicaa Noret (Laboratory of Plant Ecology and Biogeochemistry) for providing seeds and Romain Goudon of the Laboratoire Sols et Environnement for its precious help. They also thank Maxime Pauwels for carefully revising the manuscript.

Author information

Authors and Affiliations

  1. Université de Lorraine, LSE, UMR1120, Vandœuvre-lès-Nancy cedex, F-54518, France

    Cédric Gonneau, Nicolas Genevois, Catherine Sirguey & Thibault Sterckeman

  2. INRA, LSE, UMR1120, Vandœuvre-lès-Nancy cedex, F-54518, France

    Cédric Gonneau, Nicolas Genevois, Catherine Sirguey & Thibault Sterckeman

  3. Laboratoire Génétique et Evolution des Populations Végétales, CNRS UMR 8198, Université Lille1, F-59655, Villeneuve d’Ascq cedex, France

    Hélène Frérot

Authors
  1. Cédric Gonneau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicolas Genevois
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hélène Frérot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Catherine Sirguey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thibault Sterckeman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catherine Sirguey.

Additional information

Responsible Editor: Henk Schat.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 164 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gonneau, C., Genevois, N., Frérot, H. et al. Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens . Plant Soil 384, 271–287 (2014). https://doi.org/10.1007/s11104-014-2208-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2208-4

Keywords

Search

Navigation