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Multiscale and age-dependent leaf nickel in the Ni-hyperaccumulator Leptoplax emarginata

  • Special Feature
  • Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology
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Ecological Research

Abstract

Nickel-hyperaccumulator plants are of interest due to their potential use in agromining. We aimed to characterize leaf traits and Ni concentration variabilities occurring between individual plants, leaves of differing age or between various leaf tissues, in a single Greek population of the Ni-hyperaccumulator Leptoplax emarginata (Boiss.) O.E. Schulz. We linked these results to ecophysiological characteristics and other element concentrations at leaf and leaf tissue scales. We measured leaf gas exchanges, stomatal density, and we carried out rapid freezing and freeze-drying processes on leaf sections before microanalysis with scanning electron microscopy and energy-dispersive spectrometry. Leaf or leaf-tissue Ni concentrations were influenced by a combination of individual plant and leaf age factors. The greatest Ni concentrations were found in the highly transpiring young and thin leaves with the greatest stomatal densities. Indeed, Ni was statistically seven times more concentrated in both epidermis layers than in their bulk neighbour leaf counterparts, whatever the leaf age. In both epidermis layers, increases in the Ni–S and Mg–S correlations from the oldest leaves to the youngest ones were observed. The Mg:Ni, Ca:Ni and P:Ni mass ratios decreased from the oldest leaves to the mature leaves. We would recommend time-series characterization of leaf traits belonging to at least three plant replicates in order to take into account the allogamous character of many Ni-hyperaccumulator plants. Long-distance Ni transport via the xylem is predominant in the Ni-hyperaccumulator L. emarginata whereas a complementary redistribution via the phloem should also occur. The perspectives of this study are the validation and refinement of this process over shorter periods using relevant tracers.

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References

  • Agrawal B, Lakshmanan V, Kaushik S, Bais HP (2012) Natural variation among Arabidopsis accessions reveals malic acid as a key mediator of Nickel (Ni) tolerance. Planta 236:477–489

    Article  PubMed  CAS  Google Scholar 

  • Alves S, Nabais C, Simões Gonçalves MDL, Correia dos Santos MM (2011) Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. Lusitanicum growing on serpentine soils of northeast Portugal. J Plant Physiol 168:1715–1722

    Article  PubMed  CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Bani A, Echevarria G, Mullai A, Reeves RD, Morel JL, Sulçe S (2009) Nickel hyperaccumulation by Brassicaceae in serpentine soils of Albania and Northwest Greece. Northeast Nat 16:385–404

    Article  Google Scholar 

  • Bani A, Echevarria G, Sulçe S, Morel JL (2015) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediat 17:117–127

    Article  CAS  Google Scholar 

  • Boyd RS, Jaffré T (2009) Elemental concentrations of eleven new caledonian plant species from serpentine soils: elemental correlations and leaf-age effects. Northeast Nat 16:93–110

    Article  Google Scholar 

  • Boyd RS, Jaffré T, Odom JW (1999) Variation in nickel content in the nickel-hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia. Biotropica 31:403–410

    Article  Google Scholar 

  • Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57

    Article  CAS  Google Scholar 

  • Cecchi L, Gabbrielli R, Arnetoli M, Gonnelli C, Hasko A, Selvi F (2010) Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data. Ann Bot 106:751–767

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Centofanti T, Sayers Z, Cabello-Conejo M, Kidd P, Nishizawa N, Kakei Y, Davis A, Sicher R, Chaney R (2013) Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant Soil 373:59–75

    Article  CAS  Google Scholar 

  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tapppero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443

    Article  PubMed  CAS  Google Scholar 

  • Coinchelin D, Bartoli F, Robin C, Echevarria G (2012) Ecophysiology of nickel phytoaccumulation: a simplified biophysical approach. J Exp Bot 63:5815–5827

    Article  PubMed  CAS  Google Scholar 

  • Cosio C, DeSantis L, Frey B, Diallo S, Keller C (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775

    Article  PubMed  CAS  Google Scholar 

  • Deng THB, Tang YT, van der Ent A, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil 404:35–45

    Article  CAS  Google Scholar 

  • Echevarria G (2018) Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In: van der Ent A, Echevarria G, Baker AJM, Morel JL (eds) Agromining: farming for metals. Extracting unconventional resources using plants. Mineral Resources Series, Springer International Publishing AG, Cham, Switzerland, pp 135–156

  • Ernst WHO, Krauss GJ, Verkleij JOC, Wesenberg D (2008) Interaction of heavy metals with the sulfur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143

    PubMed  CAS  Google Scholar 

  • Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng THB, Tang YT, Morel JL (2015) Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett 423:24–25

    Article  CAS  Google Scholar 

  • Fernando DR, Mizuno T, Woodrow IE, Baker AJM, Collins RN (2010) Characterization of foliar manganese (Mn) in Mn hyperaccumulators using X-ray absorption spectroscopy. New Phytol 188:1014–1027

    Article  PubMed  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2001) Lecture notes on the major soils of the world. In: Driessen P, Deckers J, Spaargaren O, Nachtergaele F (eds) World soil resources report, no. 94. FAO, Rome

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt D (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Freeman JL, Zhang LH, Marcus MA, Fakra S, McGrath SP, Pilon-Smits AH (2006) Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol 142:124–134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  PubMed  CAS  Google Scholar 

  • Jaffré T, Schmid M (1974) Accumulation du nickel par une Rubiacée de Nouvelle-Calédonie, Psychotria douarrei (G. Beauvisage) Däniker. CR Acad Sci D Nat 278:1727–1730

    Google Scholar 

  • Kachenko AG, Siegele R, Bhatia NP, Singh B, Ionescu M (2008a) Evaluation of specimen preparation techniques for micro-PIXE localisation of elements in hyperaccumulating plants. Nucl Inst Methods Phys Res B 266:1598–1604

    Article  CAS  Google Scholar 

  • Kachenko AG, Singh B, Bhatia NP, Siegele R (2008b) Quantitative elemental localisation in leaves and stems of nickel hyperaccumulating shrub Hybanthus floribundus subsp. floribundus using micro-PIXE spectroscopy. Nucl Inst Methods Phys Res B 266:667–676

    Article  CAS  Google Scholar 

  • Koopmans GF, Römkens PFAM, Song J, Temminghoff EJM, Japenga J (2007) Predicting the phytoextration duration to remediate heavy metals contaminated soils. Wat Air Soil Poll 181:355–371

    Article  CAS  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Ann Rev Plant Biol 61:517–534

    Article  CAS  Google Scholar 

  • Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353

    Article  PubMed  PubMed Central  Google Scholar 

  • Küpper H, Lombi E, Zhao F-J, Wieshammer G, McGrath SP (2001) Cellular compartimentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300

    Article  PubMed  Google Scholar 

  • Küpper H, Mijovilovich A, Meyer-Klaucke W, Kroneck MH (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-Ray absorption spectrometry. Plant Physiol 134:748–757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lange B, van der Ent A, Baker AJM, Mahy G, Malaisse F, Meerts P, Echevarria G, Pourré O, Verbruggen N, Faucon MP (2017a) Copper and cobalt accumulation in plants: a critical assessment of the current status of knowledge. New Phytol 213:537–551

    Article  PubMed  CAS  Google Scholar 

  • Lange B, Faucon MP, Delhaye G, Hamiti N, Meerts P (2017b) Functional traits of a facultative metallophyte from tropical Africa: population variation and plasticity in response to cobalt. Environ Exp Bot 136:1–8

    Article  CAS  Google Scholar 

  • Le Thiec D, Rose C, Garrec JP, Laffray D, Louguet P, Galaup S, Loosveldt P (1994) Alteration of element subjected to ozone fumigation and (or) water stress: X-ray microanalysis study. Can J Bot 72:86–92

    Article  Google Scholar 

  • Leustek T (2002) Sulfate metabolism. The Arabidopsis book 1. https://doi.org/10.1199/tab.0017

  • Leustek T, Martin MN, Bick J-A, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Ann Rev Plant Phys Plant Mol Biol 51:141–165

    Article  CAS  Google Scholar 

  • Li Y-M, Chaney RL, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids and radionuclides. Adv Agron 75:1–56

    Article  CAS  Google Scholar 

  • McNear DH, Chaney RL, Sparks DL (2010) The hyperaccumulator Allyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochemistry 71:188–200

    Article  PubMed  CAS  Google Scholar 

  • Mesjasz-Przybylowicz J, Przybylowicz WJ (2011) PIXE and metal hyperaccumulation: from soil to plants and insects. X-Ray Spectrom 40:181–185

    Article  CAS  Google Scholar 

  • Mesjasz-Przybylowicz J, Przybylowicz WJ, Pineda CA (2001) Nuclear microprobe studies of elemental distribution in apical leaves of the Ni hyperaccumulator Berkheya coddii. S Afr J Sci 97:591–593

    CAS  Google Scholar 

  • Mijovilovich A, Leitenmaier B, Meyer-Klaucke W, Kroneck MH, Götz B, Küpper H (2009) Complexation and toxicity of copper in higher plants. II. Different mechanisms for copper versus cadmium detoxification in the copper-sensitive cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype). Plant Physiol 151:715–731

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Montargès-Pelletier E, Chardot V, Echevarria G, Michot LJ, Bauer A, Morel JL (2008) Identification of nickel chelators in three hyperaccumulating plants: an X-ray spectroscopic study. Phytochemistry 69:1695–1709

    Article  PubMed  CAS  Google Scholar 

  • Nick LJ, Chambers MF (1995) Farming for metals? Mining Environ Manag 3:15–18

    Google Scholar 

  • Peer WA, Mahmoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulation plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Perronnet K, Schwartz C, Morel JL (2003) Distribution of cadmium and zinc in the hyperaccumulator Thlaspi caerulescens grown on multicontaminated soil. Plant Soil 249:19–25

    Article  CAS  Google Scholar 

  • Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxonomy 29:629–633

    Article  Google Scholar 

  • Richau KH, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant Soil 314:253–262

    Article  CAS  Google Scholar 

  • Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PLM, Smith JAC, Ivanov VB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116

    Article  PubMed  CAS  Google Scholar 

  • Robinson BH, Fernández JE, Madejón P, Marañón T, Murillo JM, Green S, Clothier B (2003a) Phytoextraction: an assessment of biogeochemical and economic viability. Plant Soil 249:117–125

    Article  CAS  Google Scholar 

  • Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003b) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158:279–285

    Article  CAS  Google Scholar 

  • Tang YT, Deng THB, Wu QH, Qiu RL, Wei ZB, Guo XF, Wu QT, Lei M, Chen TB, Echevarria G, Sterckeman T, Simonnot MO, Morel JL (2012) Designing cropping systems adapted to metal contaminated sites: a review. Pedosphere 22:470–488

    Article  CAS  Google Scholar 

  • Tian SK, Lu LL, Yang XE, Labavitch JM, Huang YY, Brown P (2009) Stem and leaf sequestration of zinc at the cellular level in the hyperaccumulator Sedum alfredii. New Phytol 182:116–126

    Article  PubMed  CAS  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780

    Article  PubMed  CAS  Google Scholar 

  • van der Ent A, Callahan DL, Noller BN, Mesjasz-Przybylowicz J, Przybylowicz WJ, Barnabas A, Harris HH (2017) Nickel biopathways in tropical nickel hyperaccumulating trees from Sabah (Malaysia). Sci Rep 7:41861

    Article  PubMed  PubMed Central  CAS  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 

  • Vogel-Mikuš K, Regvar M, Mesjasz-Przybyłowicz J, Przybyłowicz W, Simčič J, Pelicon P, Budnar M (2008) Spatial distribution of cadmium in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE. New Phytol 179:712–721

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Shi J, Chen Y, Chen X, Wang H, Perera A (2006) Distribution and mobility of manganese in the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceaae). Plant Soil 285:323–331

    Article  CAS  Google Scholar 

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Acknowledgements

Trust and financial support from the Université de Lorraine, ADEME and Lorraine Regional Council given to Dr. David Coinchelin for his PhD Grant were greatly appreciated. We thank Helen Selliez for improving the English. The authors deeply acknowledge their co-author, the late Dr. François Bartoli, for the many years shared in developing creative research together and for his valuable friendship.

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  1. Deceased: François Bartoli.

    • François Bartoli
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Correspondence to Guillaume Echevarria.

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Bartoli, F., Royer, M., Coinchelin, D. et al. Multiscale and age-dependent leaf nickel in the Ni-hyperaccumulator Leptoplax emarginata. Ecol Res 33, 723–736 (2018). https://doi.org/10.1007/s11284-018-1594-0

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  • DOI: https://doi.org/10.1007/s11284-018-1594-0

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