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Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species

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Abstract

Aims

An improved understanding of the Ni root-to-shoot translocation mechanism in hyperaccumulators is necessary to increase Ni uptake efficiency for phytoextraction technologies. It has been presumed that an important aspect of Ni translocation and storage involves chelation with organic ligands. It has been reported that exposing several Ni hyperaccumulator species of Alyssum to Ni elicited a large increase in the histidine level of the xylem sap. In later studies it was shown that as time progressed the histidine:Ni ratio dropped considerably. Moreover, previous studies analyzed the relationship between Ni and ligands in plants that were exposed to Ni only for a few hours and therefore obtained results that are unlikely to represent field soils where plants are at steady-state Ni uptake. The aim of this study was to understand the quantitative relationship between Ni and organic ligands in the xylem sap of various Alyssum genotypes or species that reached steady-state Ni uptake after being exposed to Ni in either nutrient solution or serpentine soil for up to 6 weeks.

Methods

Total Ni concentration, 17 amino acids, 9 organic acids, and nicotianamine were measured in xylem sap of 100-day old plants of Alyssum.

Results

Results showed that the concentration of Ni in xylem sap of various Alyssum genotypes was 10–100 fold higher than the concentration of histidine, malate, citrate, and nicotianamine, which were the predominant Ni ligands measured in the sap.

Conclusion

When the physiology of the whole plant is taken into account, our results indicate that the concentration of organic chelators is too low to account for the complexation of all the Ni present in the xylem sap of Alyssum at steady-state Ni hyperaccumulation, and suggest that most of the Ni in xylem sap of this species is present as the hydrated cation.

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References

  • 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 (1987) Metal tolerance. New Phytol 106:93–111

    Article  CAS  Google Scholar 

  • Broadhurst CL, Chaney RL, Angle JS, Erbe EF, Maugel TK (2004) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265:225–242

    Article  CAS  Google Scholar 

  • Brooks RR (ed) (1987) Serpentine and its vegetation. A multidisciplinary approach. Dioscorides Press, Portland

    Google Scholar 

  • Brooks RR, Shaw S, Marfil AA (1981) The chemical form and physiological functions of nickel in some Iberian Alyssum species. Physiol Plant 51:167–170

    Article  CAS  Google Scholar 

  • Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362

    Article  Google Scholar 

  • Cabello-Conejo MI, Centofanti T, Kidd PS, Prieto-Fernández Á, Chaney RL (2012) Evaluation of plant growth regulators to increase nickel phytoextraction by Alyssum species. Int J Phytoremediation 15:365–375

    Article  Google Scholar 

  • Callahan DL, Roessner U, Kolev SD, O’Hair RAJ, Salt DE, Baker AJM (2007) Relationships of nicotianamine and other amino acids with nickel, zinc and iron in Thlaspi hyperaccumulators. New Phytol 176:836–848

    Article  PubMed  CAS  Google Scholar 

  • Callahan DL, Roessner U, Dumontet V, Perrier N, Wedd AG, O’Hair RAJ, Baker AJM, Kolev SD (2008) LC-MS and GC-MS metabolite profiling of nickel(II) complexes in the latex of the nickel-hyperaccumulating tree Sebertia acuminata and identification of methylated aldaric acid as a new nickel(II) ligand. Phytochem 69:240–251

    Article  CAS  Google Scholar 

  • Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284

    Article  PubMed  CAS  Google Scholar 

  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1433

    Article  PubMed  CAS  Google Scholar 

  • Chaney R, Centofanti T, Broadhurst CL (2010) Phytoremediation of soil trace elements. In: Hooda PS (ed) Trace elements in soils. John Wiley & Sons Ltd, Chichester, pp 311–352

    Chapter  Google Scholar 

  • Frausto da Silva JJR, Williams RJP (1991) The biological chemistry of the elements: the inorganic chemistry of life. Clarendon Press, Oxford

    Google Scholar 

  • Homer FA, Morrison RS, Brooks RR, Clemens J, Reeves RD (1991) Comparative studies of nickel, cobalt, and copper uptake by some nickel hyperaccumulators of the genus Alyssum. Plant Soil 138:195–205

    Article  CAS  Google Scholar 

  • Kakei Y, Yamaguchi I, Kobayashi T, Takahashi M, Nakanishi H, Yamakawa T, Nishizawa NK (2009) A highly sensitive, quick and simple quantification method for nicotianamine and 2′-deoxymugineic acid from minimum samples using LC/ESI-TOF-MS achieves functional analysis of these components in plants. Plant Cell Physiol 50:1988–1993

    Article  PubMed  CAS  Google Scholar 

  • Kerkeb L, Krämer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724

    Article  PubMed  CAS  Google Scholar 

  • Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638

    Article  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  Google Scholar 

  • Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33:2090–2102

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Reeves RD, Brooks RR, Jaffre T (1978) The relation between nickel and citric acid in some nickel-accumulating plants. Phytochemistry 17:1033–1035

    Article  CAS  Google Scholar 

  • Li Y-M, Chaney R, 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 

  • Liang J, Zhang J (1997) Collection of xylem sap at flow rate similar to in vivo transpiration flux. Plant Cell Physiol 38:1375–1381

    Article  CAS  Google Scholar 

  • Mari S, Gendre D, Pianelli K, Ouerdane L, Lobinski R, Briat JF, Lebrun M, Czernic P (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57:4111–4122

    Article  PubMed  CAS  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ouerdane L, Mari S, Czernic P, Lebrun M, Lobinski R (2006) Speciation of non-covalent nickel species in plant tissue extracts by electrospray Q-TOFMS/MS after their isolation by 2D size exclusion-hydrophilic interaction LC (SEC-HILIC) monitored by ICP-MS. J Anal Atom Spectrom 21:676–683

    Article  CAS  Google Scholar 

  • Pancaro L, Pelosi P, Vergnano O, Galoppini C (1978) Further contribution on the relationship between nickel and malic and malonic acids in Alyssum. G Bot Ital 112:282–283

    Article  Google Scholar 

  • Parker DR, Chaney RL, Norvell WA (1995) Chemical equilibrium models: applications to plant nutrition research. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. Soil Sci. Soc. Am, Madison, pp 163–200

    Google Scholar 

  • Persans MW, Yan X, Patnoe JMML, Krämer U, Salt DE (1999) Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Halacsy). Plant Physiol 121:1117–1126

    Article  PubMed  CAS  Google Scholar 

  • Pianelli K, Mari S, Marquès L, Lebrun M, Czernic P (2005) Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res 14:739–748

    Article  PubMed  CAS  Google Scholar 

  • Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    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 

  • Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L (2000) Simultaneous analysis of metabolites in potato tuber by gas chromatography–mass spectrometry. Plant J 23:131–142

    Article  PubMed  CAS  Google Scholar 

  • Smith JAC, Harper FA, Leighton RS, Thompson IP, Vaughan DJ and Baker AJM (1999) Comparative analysis of metal uptake, transport and sequestration in hyperaccumulator plants. In Proceedings of the 5th Inter. Conf. on the biogeochemistry of trace elements. In: Wenzel WW, Adriano DC, Alloway B, Doner HE, Keller C, Lepp NW, Mench M, Naidu R and Pierzynski GM (eds) Vienna, pp 22–23

  • Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. BioMetals 9:84–90

    Article  CAS  Google Scholar 

  • Tiffin LO (1971) Translocation of nickel in xylem exudate of plants. Plant Physiol 48:273–277, 48, 273–277

    Article  PubMed  CAS  Google Scholar 

  • Turner NC (1988) Measurement of plant water status by the pressure chamber technique. Irrig Sci 9:289–308

    Article  Google Scholar 

  • White MC, Decker AM, Chaney RL (1981) Metal complexation in xylem fluid: I. Chemical composition of tomato and soybean stem exudate. Plant Physiol 67:292–300

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Dimitrakopoulos for providing the seeds of A. lesbiacum; Dr. Alan J.M. Baker, Dr. Roger D. Reeves and staff of the seed collection team which worked with Viridian LLC and USDA-ARS to conduct Ni phytomining research; and Dr. Carrie E. Green for carrying out the ICP analyses.

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Authors and Affiliations

  1. Department of Civil and Environmental Engineering, University of Maryland, College Park, MD, USA

    Tiziana Centofanti & Allen P. Davis

  2. Faculty of Engineering and Natural Sciences, Sabanci University, Tuzla, Istanbul, Turkey

    Zehra Sayers

  3. USDA-ARS, Environmental Management and Byproduct Utilization Laboratory, Beltsville, MD, USA

    Tiziana Centofanti & Rufus L. Chaney

  4. Consejo Superior de Investigaciones Científicas (CSIC), Instituto de Investigaciones Agrobiologicas de Galicia (IIAG), Santiago de Compostela, 15706, Spain

    Maria Isabel Cabello-Conejo & Petra Kidd

  5. Department of Global Agricultural Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Naoko K. Nishizawa & Yusuke Kakei

  6. USDA-ARS, Plant Sciences Institute, Crop Systems and Global Change Laboratory, Beltsville, MD, USA

    Richard C. Sicher

  7. Water Management Research USDA-ARS, 9611 S. Riverbend Avenue, Parlier, CA, 93648, USA

    Tiziana Centofanti

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  1. Tiziana Centofanti
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  2. Zehra Sayers
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  3. Maria Isabel Cabello-Conejo
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  7. Allen P. Davis
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  9. Rufus L. Chaney
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Correspondence to Tiziana Centofanti.

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Responsible Editor: Jian Feng Ma.

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Centofanti, T., Sayers, Z., Cabello-Conejo, M.I. et al. Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant Soil 373, 59–75 (2013). https://doi.org/10.1007/s11104-013-1782-1

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