Plant and Soil

, Volume 423, Issue 1–2, pp 157–174 | Cite as

Habitat heterogeneity in the pseudometallophyte Arabidopsis halleri and its structuring effect on natural variation of zinc and cadmium hyperaccumulation

  • Hélène Frérot
  • Nina-Coralie Hautekèete
  • Isabelle Decombeix
  • Marie-Hélène Bouchet
  • Anne Créach
  • Pierre Saumitou-Laprade
  • Yves Piquot
  • Maxime Pauwels
Regular Article


Background and aims

Arabidopsis halleri is a pseudometallophyte plant model hyperaccumulating zinc and cadmium. This study investigates which abiotic parameters may cause phenotypic divergence among accessions for hyperaccumulation traits.


We studied 23 sites from a mining and industrial area in Italian Alps. Sites were characterized for altitude, topographic data, absolute humidity, and accompanying flora. Plant-soil couples were also sampled to measure shoot metal concentrations and soil elemental concentrations, particles size distribution, and pH. Using PLSR analyses, we investigated whether the natural variation in hyperaccumulation abilities could be explained by variation of abiotic parameters.


Habitats heterogeneity was high, distinguishing metalliferous and non-metalliferous sites. However, heterogeneity was also observed for soil metal concentrations, particles size distribution and altitude, particularly among metalliferous habitats. This result was supported by floristic data. Soil zinc and cadmium concentrations showed the most contrasting effects on phenotypic divergence between metalliferous and non-metalliferous habitats. However, except for cadmium-related traits in non-metalliferous habitats, other abiotic parameters may affect the variation of zinc or cadmium hyperaccumulation within each habitat type.


The classical dichotomous distinction between metalliferous and non-metalliferous habitats may hide the ecological diversity existing within each category for abiotic parameters. This study reveals abiotic parameters that may shape the natural variation of hyperaccumulation abilities.


Abiotic parameters Ecological niche evolution Habitat heterogeneity Local adaptation Metal hyperaccumulation Phenotypic divergence 



The authors are grateful to Angélique Bourceaux and Cédric Glorieux for their technical help. They thank Philippe Ghysels (Laboratory of Plant Ecology and Biogeochemistry, University of Brussels) for plant and soil analyses. They thank Pr. Daniel Petit for its contribution to plant identification. They thank Enzo Bona, from Department of Life Sciences, University of Trieste, for localization of sampling sites in Italy. They also thank Dr. Palmyre Boucherie for its help as a young student at the time of this study. Many thanks to Thibault Sterckeman for carefully revising the manuscript, and to two anonymous reviewers for their constructive comments. This work is a contribution to the CPER research project CLIMIBIO. The authors thank the French Ministry of Higher Education and Research, the Hauts de France Region and the European Funds for Regional Economical Development for their financial support to this project. Isabelle Decombeix was funded by the French Ministry of Higher Education and Research.

Supplementary material

11104_2017_3509_MOESM1_ESM.xlsx (37 kb)
Table S1 (XLSX 37 kb)
11104_2017_3509_MOESM2_ESM.xlsx (34 kb)
Table S2 (XLSX 33 kb)


  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 et al (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419CrossRefGoogle Scholar
  3. Ben Hamed K, Ellouzi H, Zribi Talbi O et al (2013) Physiological response of halophytes to multiple stresses. Funct Plant Biol 40:883–896Google Scholar
  4. Bert V, Macnair MR, De Laguérie P, Saumitou-Laprade P, Petit D (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol 146:225–233CrossRefGoogle Scholar
  5. Bert V, Bonnin I, Saumitou-Laprade P, de Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetalicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57CrossRefGoogle Scholar
  6. Berton A (1946) Présentation des plantes: Arabidopsis halleri, Armeria maritima, Oenanthe fluviatilis, Galinsoga parviflora dicoidea. Bulletin de la Société Botanique Du Nord de la France 93:139–145CrossRefGoogle Scholar
  7. Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176CrossRefGoogle Scholar
  8. Boyd RS, Martens SN (1992) The raison d'être for metal hyperaccumulation by plants. In: AJM B, Proctor J, Reeves RD (eds) The Ecology of Ultramafic (Serpentine) Soils. Intercept, Andover, pp 279–289Google Scholar
  9. Boyd RS, Martens SN (1994) Nickel hyperaccumulation by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore. Oikos 70:21–25CrossRefGoogle Scholar
  10. Boyd RS, Martens SN (1998) Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait. Am J Bot 85:259–265CrossRefPubMedGoogle Scholar
  11. Brachi B, Villoutreix R, Faure N et al (2013) Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana. Mol Ecol 22:4222–4240CrossRefPubMedGoogle Scholar
  12. Dechamps C, Noret N, Mozek R et al (2008) Cost of adaptation to a metalliferous environment for Thlaspi caerulescens: a field reciprocal transplantation approach. New Phytol 177:167–177PubMedGoogle Scholar
  13. Dechamps C, Elvinger N, Meerts P et al (2011) Life history traits of the pseudometallophyte Thlaspi caerulescens in natural populations from Northern Europe. Plant Biol 13:125–135CrossRefPubMedGoogle Scholar
  14. Degryse F, Smolders E, Parker DR (2009) Partitioning of metals (Cd, Co, Cu, Ni, Pb, Zn) in soils: concepts, methodologies, prediction and applications - a review. Eur J Soil Sci 60:590–612CrossRefGoogle Scholar
  15. Delhaye G, Violle C, Séleck M et al (2016) Community variation in plant traits along copper and cobalt gradients. J Veg Sci 27:854–864CrossRefGoogle Scholar
  16. Enquist BJ, Norberg J, Bonser SP et al (2015) Scaling from traits to ecosystems: developing a general trait driver theory via integrating trait-based and metabolic scaling theory. Adv Ecol Res 52:249–318CrossRefGoogle Scholar
  17. Escarré J, Lefèbvre C, Frérot H, Mahieu S, Noret N (2013) Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media. Plant Soil 370:197–221CrossRefGoogle Scholar
  18. Gargominy O, Tercerie S, Régnier C et al (2016) TAXREF v10.0, référentiel taxonomique pour la France: méthodologie, mise en œuvre et diffusion. Rapport SPN-MNHN 2016–101. Muséum National d’Histoire Naturelle, ParisGoogle Scholar
  19. Holt R (2003) On the evolutionary ecology of species' ranges. Evol Ecol Res 5:159–178Google Scholar
  20. Hörger AC, Fones HN, Preston GM (2013) The current status of the elemental defense hypothesis in relation to pathogens. Front Plant Sci 4:395Google Scholar
  21. Janišová M, Hegedüšová K, Kráľ P, Škodová I (2012) Ecology and distribution of Tephroseris longifolia subsp. moravica in relation to environmental variation at a micro-scale. Biologia 67(1):97–109Google Scholar
  22. Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms, and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508PubMedGoogle Scholar
  23. Kazemi-Dinan A, Thomaschky S, Stein RJ, Krämer U, Müller C (2014) Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol 202:628–639CrossRefPubMedGoogle Scholar
  24. Lange B, Faucon M-P, Delhaye G, Hamiti N, Meerts P (2017) Functional traits of a facultative metallophyte from tropical Africa: population variation and plasticity in response to cobalt. Environ Exp Bot 136:1–8CrossRefGoogle Scholar
  25. Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  26. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277CrossRefGoogle Scholar
  27. Lovy L, Latt D, Sterckeman T (2013) Cadmium uptake and partitioning in the hyperaccumulator Noccaea caerulescens exposed to constant cd concentrations throughout complete growth cycles. Plant Soil 362:345–354CrossRefGoogle Scholar
  28. Macnair MR (1987) Heavy metal tolerance in plants: a model evolutionary system. Trends Evol Ecol 2:354–358CrossRefGoogle Scholar
  29. Macnair MR (1997) The evolution of plants in metal-contaminated environments. In: Bijlsma R, Loeschcke V (eds) Environmental stress, adaptation and evolution. Birkhäuser-Verlag, Basel, pp 3–24CrossRefGoogle Scholar
  30. Macnair MR (2002) Within and between population genetic variation for zinc accumulation in Arabidopsis halleri. New Phytol 155:59–66CrossRefGoogle Scholar
  31. 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 150:363–372CrossRefPubMedGoogle Scholar
  32. Merilä J, Sheldon BC, Kruuk LEB (2001) Explaining stasis: microevolutionary studies in natural populations. Genetica 112-113:199–222CrossRefPubMedGoogle Scholar
  33. Meyer C-L, Kostecka AA, Saumitou-Laprade P et al (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte Arabidopsis halleri and possible role of directional selection. New Phytol 185:130–142CrossRefPubMedGoogle Scholar
  34. Meyer C-L, Juraniec M, Sp H et al (2015) Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:3215–3227CrossRefPubMedPubMedCentralGoogle Scholar
  35. Meyer C-L, Pauwels M, Briset L et al (2016) Potential preadaptation to anthropogenic pollution: evidence from a common quantitative trait locus for zinc and cadmium tolerance in metallicolous and nonmetallicolous accessions of Arabidopsis halleri. New Phytol 212:934–943CrossRefPubMedGoogle Scholar
  36. 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 165:503–512CrossRefPubMedGoogle Scholar
  37. 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 152:92–100CrossRefPubMedGoogle Scholar
  38. Pauwels M, Frérot H, Bonnin I, Saumitou-Laprade P (2006) A broad-scale study of population differentiation for Zn-tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). J Evol Biol 19:1838–1850CrossRefPubMedGoogle Scholar
  39. Pauwels M, Vekemans X, Godé C et al (2012) Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytol 193:916–928CrossRefPubMedGoogle Scholar
  40. Pironon S, Papuga G, Villellas J et al (2017) Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biol Rev 92:1877–1909CrossRefPubMedGoogle Scholar
  41. Plaza S, Weber J, Pajonk S et al (2015) Wounding of Arabidopsis halleri leaves enhances cadmium accumulation that acts as a defense against herbivory. Biometals 28:521–528CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217-218:8–17CrossRefPubMedGoogle Scholar
  43. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefPubMedGoogle Scholar
  44. Roosens N, Verbruggen N, Meerts P, Ximénez-Embun P, Smith JA (2003) Natural variation in cadmium tolerance and its relationship to metal accumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1673CrossRefGoogle Scholar
  45. SAS Institute Inc. (2011) SAS user’s guide: statistics, Version 9.3. SAS Campus Drive, CaryGoogle Scholar
  46. Šrámková G, Záveská E, Kolář F et al (2017) Range-wide genetic structure of Arabidopsis halleri (Brassicaceae): glacial persistence in multiple refugia and origin of the Northern Hemisphere disjunction. Bot J Linn Soc 185:321–342CrossRefGoogle Scholar
  47. Stein RJ, Höreth S, de Melo JRF et al (2016) Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286Google Scholar
  48. Stein RJ, Höreth S, de Melo JRF et al (2017) Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286CrossRefPubMedGoogle Scholar
  49. Tenenhaus M (1998) La Régression PLS: Théorie et Pratique. Technip, ParisGoogle Scholar
  50. Vaissie P, Monge A, Husson F (2015) Factoshiny: perform factorial analysis from FactoMineR with a shiny application. R package version 1Google Scholar
  51. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  52. Van Rossum F, Bonnin I, Fénart S et al (2004) Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible and heavy-metal-tolerant species. Mol Ecol 13:2959–2967CrossRefPubMedGoogle Scholar
  53. Wagmann K, Hautekeète N-C, Piquot Y et al (2012) Seed dormancy distribution: explanatory ecological factors. Ann Bot 110:1205–1219CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Hélène Frérot
    • 1
  • Nina-Coralie Hautekèete
    • 1
  • Isabelle Decombeix
    • 1
  • Marie-Hélène Bouchet
    • 1
  • Anne Créach
    • 2
  • Pierre Saumitou-Laprade
    • 1
  • Yves Piquot
    • 1
  • Maxime Pauwels
    • 1
  1. 1.University of Lille, CNRS, UMR 8198 - Unité Evolution-Ecologie-PaléontologieLilleFrance
  2. 2.University of Lille, CNRS, UMR 8576 - Unité de Glycobiologie Structurale et FonctionnelleLilleFrance

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