Skip to main content

Advertisement

Log in

Metal Availability and Chemical Properties in the Rhizosphere of Lupinus albus L. Growing in a High-Metal Calcareous Soil

  • Published:
Water, Air, and Soil Pollution Aims and scope Submit manuscript

Abstract

Chemical processes in the rhizosphere play a major role in the availability of metals to plants. The objective of this study was to assess the potential of white lupin (Lupinus albus L.) for the phytoimmobilisation of heavy metals in a calcareous soil with high levels of Zn and Pb (2,058 and 2,947 μg g−1, respectively) by evaluating the chemical changes in the rhizosphere, relative to bulk soil, which modify the solubility of heavy metals. Plants were cultivated for 74 days in specially designed pots (rhizopots) in which rhizosphere was sampled easily under controlled conditions. White lupin accumulated high concentrations of Mn in the shoots (average of 4,960 μg g−1), well above the normal concentration in plants (300 μg g−1). But the metal concentrations found in shoots were not at toxic levels. Rhizosphere soil showed a significantly greater redox potential (245 mV) and water-soluble organic carbon content (34.6 μg C g−1) than bulk soil (227 mV; 27.6 μg C g−1). Root activity decreased EDTA-extractable Pb, Zn and Fe and promoted their precipitation as insoluble compounds in the residual fraction (acid digestion), hardly available to plants. These results indicate the suitability of this annual N2-fixing species for the initial phytoimmobilisation of heavy metals in contaminated soils.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Abrisqueta, C., & Romero, M. (1969). Digestión húmeda rápida de suelos y materiales orgánicos. Anales de Edafología y Agrobiología, 27, 855–867.

    Google Scholar 

  • Baker, A. J. M. (1981). Accumulators and excluders—Strategies in the response of plants to heavy metals. Journal of Plant Nutrition, 3, 643–654.

    Article  CAS  Google Scholar 

  • Beckett, P. H. T. (1989). The use of extractants in studies on trace metals in soil, sewage sludges, and sludge-treated soils. Advances in Soil Science, 9, 143–176.

    Google Scholar 

  • Castro, I. V., & Ferreira, E. M. (2006). Contaminación y fertilización: metales pesados y lodos de depuradoras. In E. J. Bedmar Gomez, J. Gonzáles-López, C. Lluch Plá, M. B. Rodelas Gonzáles (Ed.), Fijación de Nitrógeno: Fundamentos y Aplicaciones (pp. 291–303). Granada, Spain: Sociedad Española de Fijación de Nitrógeno.

    Google Scholar 

  • Canellas, L. P., Teixeira Junior, L. R. L., Dobbss, L. B., Silva, C. A., Medici, L. O., Zandonadi, D. B., et al. (2008). Humic acids crossinteractions with root and organic acids. The Annals of Applied Biology, 153, 157–166.

    CAS  Google Scholar 

  • Castaldi, P., Santona, L., & Melis, P. (2005). Heavy metal immobilization by chemical amendments in a polluted soil and influence on white lupin growth. Chemosphere, 60, 365–371. doi:10.1016/j.chemosphere.2004.11.098.

    Article  CAS  Google Scholar 

  • Chaney, R. L., Coloumbe, B. A., Bell, P. F., & Angle, S. J. (1992). Detailed method to screen dicot cultivars for resistance to Fe-chlorosis using FeDTPA and bicarbonate nutrient solutions. Journal of Plant Nutrition, 15, 2045–2062.

    Article  CAS  Google Scholar 

  • Clemente, R., Paredes, C., & Bernal, M. P. (2007). A field experiment investigating the effects of olive husk and cow manure on heavy metal availability in a contaminated calcareous soil from Murcia (Spain). Agriculture Ecosystems & Environment, 118, 319–326. doi:10.1016/j.agee.2006.06.002.

    Article  CAS  Google Scholar 

  • Council of the European Communities, (1986). Council directive of 12 of June on the protection of the environment, and in particular of the soil when sewage sludge is used in agriculture. Official Journal of the European Communities, No. L 181/6-12, 4 July 1986.

  • De la Fuente, C., Clemente, R., & Bernal, M. P. (2008). Changes in metal speciation and pH in olive processing waste and sulphur-treated contaminated soil. Ecotoxicology and Environmental Safety, 70, 207–215. doi:10.1016/j.ecoenv.2007.05.021.

    Article  CAS  Google Scholar 

  • Dinkelaker, B., Römheld, V., & Marschner, H. (1989). Citric acid excretion and precipitation of calcium in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell & Environment, 12, 285–292. doi:10.1111/j.1365-3040.1989.tb01942.x.

    Article  CAS  Google Scholar 

  • Haynes, R. J. (1990). Active ion uptake and maintenance of cation–anion balance: A critical examination of their role in regulating rhizosphere pH. Plant and Soil, 126, 247–264. doi:10.1007/BF00012828.

    Article  CAS  Google Scholar 

  • Hernández, A. J., Adarve, M. J., Pastor, J., & Gil, A. (1999). Soil salination from landfill leachates: Effects on the macronutrient content and plant growth of four grassland species. Chemosphere, 38, 1693–1711. doi:10.1016/S0045-6535(98)00367-1.

    Article  Google Scholar 

  • Hinsinger, P., Plassard, C., Tang, C., & Jaillard, B. (2003). Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant and Soil, 248, 43–59. doi:10.1023/A:1022371130939.

    Article  CAS  Google Scholar 

  • Huyghe, C. (1997). White lupin (Lupinus albus L.). Field Crops Research, 53, 147–160. doi:10.1016/S0378-4290(97)00028-2.

    Article  Google Scholar 

  • Joergensen, R. G., & Brookes, P. C. (1990). Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 m K2SO4 soil extracts. Soil Biology & Biochemistry, 22, 1023–1027. doi:10.1016/0038-0717(90)90027-W.

    Article  CAS  Google Scholar 

  • Johnson, J. F., Vance, C. P., & Allan, D. L. (1996). Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolopyruvate carboxylase. Plant Physiology, 112, 31–41. doi:10.1104/pp.112.1.31.

    Article  CAS  Google Scholar 

  • Jones, D. L. (1998). Organic acids in the rhizosphere—A critical review. Plant and Soil, 205, 25–44. doi:10.1023/A:1004356007312.

    Article  CAS  Google Scholar 

  • Jones, D. L., & Darrah, P. R. (1994). Role of root derived organic-acids in the mobilization of nutrients from the rhizosphere. Plant and Soil, 166, 247–257. doi:10.1007/BF00008338.

    Article  CAS  Google Scholar 

  • Jung, C., Maeder, V., Funk, F., Frey, B., Sticher, H., & Frossard, E. (2003). Release of phenols from Lupinus albus L. roots exposed to Cu and their possible role in Cu detoxification. Plant and Soil, 252, 301–312. doi:10.1023/A:1024775803759.

    Article  CAS  Google Scholar 

  • Kabata-Pendias, A. (2001). Trace elements in soils and plants (3rd ed.). Boca Raton, Florida: CRC.

    Google Scholar 

  • Kerley, S. J. (2000). Changes in root morphology of white lupin (Lupinus albus L.) and its adaptation to soils with heterogeneous alkaline/acid profiles. Plant and Soil, 218, 197–205. doi:10.1023/A:1014967720952.

    Article  CAS  Google Scholar 

  • Knox, A. S., Gamerdinger, A. P., Adriano, D. C., Kolka, R. K., & Kaplan, D. I. (1999). Sources and practices contributing to soil contamination. In D. C. Adriano, J. M. Bollag, W. T. Frankenberger, & R. C. Sims (Eds.), Bioremediation of contaminated soils (pp. 53–87). Madison: ASA Monog. no. 37.

    Google Scholar 

  • Loosemore, N., Straczek, A., Hinsinger, P., & Jaillard, B. (2004). Zinc mobilisation from a contaminated soil by three genotypes of tobacco as affected by soil and rhizosphere pH. Plant and Soil, 260, 19–32. doi:10.1023/B:PLSO.0000030173.71500.e1.

    Article  CAS  Google Scholar 

  • Lutts, S., Lefèvre, I., Delpèrèe, C., Kivits, S., Deschamps, C., Robledo, A., et al. (2004). Heavy metal accumulation by the halophyte species Mediterranean saltbush. Journal of Environmental Quality, 33, 1271–1279.

    CAS  Google Scholar 

  • Macnicol, R. D., & Beckett, P. H. T. (1985). Critical tissue concentrations of potentially toxic elements. Plant and Soil, 85, 107–129. doi:10.1007/BF02197805.

    Article  CAS  Google Scholar 

  • Marschner, H. (1983). Nutrient mobility, root growth and root-induced changes in the rhizosphere as factors of nutrient availability in soils of semi-arid and arid areas. In International Potash Institute, Nutrient balances and the need for fertilisers in semi-arid and arid regions (pp. 107–128). Bern: International Potash Institute.

  • Marschner, H. (1995). Mineral nutrition of higher plants (2nd ed.). London: Academic.

    Google Scholar 

  • Marschner, H., Römheld, V., & Cakmak, I. (1987). Root-induced changes of nutrient availability in the rhizosphere. Journal of Plant Nutrition, 10, 1175–1184.

    Article  CAS  Google Scholar 

  • Marschner, H., Treeby, M., & Römheld, V. (1989). Role of root-induced changes in the rhizosphere for iron acquisition in higher plants. Zeitschrift fur Pflanzenernahrung und Bodenkunde, 152, 197–204. doi:10.1002/jpln.19891520210.

    Article  CAS  Google Scholar 

  • McBride, M. B. (1987). Adsorption and oxidation of phenolic compounds by iron and manganese oxides. Soil Science Society of America, 51, 1466–1472.

    Article  CAS  Google Scholar 

  • McGrath, S. P., & Cegarra, J. (1992). Chemical extractability of heavy metals during and after long-term applications of sewage sludge to soil. Journal of Soil Science, 43, 313–321. doi:10.1111/j.1365-2389.1992.tb00139.x.

    Article  CAS  Google Scholar 

  • Mench, M., & Martin, E. (1990). Mobilization of cadmium and another metals from two soils by root exudates of Zea mays L., Nicotiana tabacum L. and Nicotiana rustica L. Plant and Soil, 132, 187–196.

    Google Scholar 

  • Mengel, K., & Kirkby, E. A. (2001). Principles of plant nutrition (5th ed.). Dordrecht, The Netherlands: Kluwer.

    Google Scholar 

  • Neumann, G., Massonneau, A., Martinoia, E., & Römheld, V. (1999). Physiological adaptations to phosphorous deficiency during proteoid root development in white lupin. Planta, 208, 373–382. doi:10.1007/s004250050572.

    Article  CAS  Google Scholar 

  • Neumann, G., Massonneau, A., Langlade, N., Dinkelaker, B., Hengeler, C., Römheld, V., et al. (2000). Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Annals of Botany, 85, 909–919. doi:10.1006/anbo.2000.1135.

    Article  CAS  Google Scholar 

  • Page, V., Le Bayon, R. C., & Feller, U. (2006). Partitioning of zinc, cadmium, manganese and cobalt in wheat (Triticum aestivum) and lupin (Lupinus albus) and further release into the soil. Environmental and Experimental Botany, 58, 269–278. doi:10.1016/j.envexpbot.2005.09.005.

    Article  CAS  Google Scholar 

  • Pastor, J., Hernández, A. J., Prieto, N., & Fernández-Pascual, M. (2003). Accumulating behaviour of Lupinus albus L. growing in a normal and a decalcified calcic luvisol polluted with Zn. Journal of Plant Physiology, 160, 1457–1465. doi:10.1078/0176-1617-01007.

    Article  CAS  Google Scholar 

  • Piccolo, A. (2001). The supramolecular structure of humic acids. Soil Science, 166, 810–832. doi:10.1097/00010694-200111000-00007.

    Article  CAS  Google Scholar 

  • Poschenrieder, C., & Barceló, J. (1981). Efectos tóxicos del manganeso sobre el crecimiento y el metabolismo de Phaseolus vulgaris. II. Interacciones Fe/Mn. Anales de Edafología y Agrobiología, 40, 927–934.

    CAS  Google Scholar 

  • Przymusiński, R., Banaszak, A., & Gwóźdź, E. A. (2001). Organospecific responses of lupin seedlings to lead I. Localization of lead ions and stress proteins. Acta Physiologiae Plantarum, 23, 109–116.

    Article  Google Scholar 

  • Puschenreiter, M., Schnepf, A., Millán, I. M., Fitz, W. J., Horak, O., Klepp, J., et al. (2005). Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant and Soil, 271, 205–218.

    Article  CAS  Google Scholar 

  • Ross, S. M. (1994). Retention, transformation and mobility of toxic metals in soils. In S. M. Ross (Ed.), Toxic metals in soil–plant systems (pp. 63–152). Chichester, UK: Wiley.

    Google Scholar 

  • Salt, D. E., Smith, R. D., & Raskin, I. (1998). Phytoremediation. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 643–668.

    Article  CAS  Google Scholar 

  • Sas, L., Rengel, Z., & Tang, C. (2001). Excess cation uptake and extrusion of protons and organic acids anions by Lupinus albus under phosphorus deficiency. Plant Science, 160, 1191–1198.

    Article  CAS  Google Scholar 

  • Shane, M. W., Lambers, H., & Cawthray, G. R. (2008). Impact of phosphorous mineral source (Al–P or Fe–P) and pH on cluster-root formation and carboxylate exudation in Lupinus albus L. Plant and Soil, 304, 169–178.

    Article  CAS  Google Scholar 

  • Shu, L., Shen, J., Rengel, Z., Tang, C., & Zhang, F. (2005). Growth medium and phosphorous supply affect cluster root formation and citrate exudation by Lupinus albus grown in a sand/solution split–root system. Plant and Soil, 276, 85–94.

    Article  CAS  Google Scholar 

  • Tang, C., McLay, C. D. A., & Barton, L. (1997). A comparison of proton excretion of twelve pasture legumes grown in nutrient solution. Australian Journal of Experimental Agriculture, 37, 563–570.

    Article  Google Scholar 

  • Tao, S., Chen, Y. J., Xu, F. L., Cao, J., & Li, B. G. (2003). Changes of copper speciation in maize rhizosphere soil. Environmental Pollution, 122, 447–454.

    Article  CAS  Google Scholar 

  • Tyler, G., & Olsson, T. (2001). Plant uptake of major and minor mineral elements as influenced by soil acidity and liming. Plant and Soil, 230, 307–321.

    Article  CAS  Google Scholar 

  • Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry, 19, 689–696.

    Article  Google Scholar 

  • Vázquez, S., Agha, R., Granado, A., Sarro, M. J., Esteban, E., Peñalosa, J. M., et al. (2006). Use of white lupin plant for phytostabilization of Cd and As polluted acid soil. Water, Air, and Soil Pollution, 177, 349–365.

    Article  CAS  Google Scholar 

  • Walker, D. J., Clemente, R., Roig, A., & Bernal, M. P. (2003). The effects of soil amendments on heavy metal bioavailability in two contaminated Mediterranean soils. Environmental Pollution, 122, 303–312.

    Article  CAS  Google Scholar 

  • Walker, D. J., Bernal, M. P., & Correal, E. (2007). The influence of heavy metals and mineral nutrient supply on Bituminaria bituminosa. Water, Air, and Soil Pollution, 184, 335–345.

    Article  CAS  Google Scholar 

  • Weisskopf, L., Tomasi, N., Santelia, D., Martinoia, E., Langlade, N. B., Tabacchi, R., et al. (2006). Isoflavonoid exudation from white lupin roots is influenced by phosphate supply, root type and cluster-root stage. New Phytologist, 171, 657–668.

    CAS  Google Scholar 

  • Wenzel, W. W., Adriano, D. C., Salt, D., & Smith, R. (1999). Phytoremediation: a plant–microbe-based remediation system. In D. C. Adriano, J. M. Bollag, W. T. Frankenberger, & R. C. Sims (Eds.), Bioremediation of contaminated soils (pp. 457–508). Madison: ASA Monog. no. 37.

    Google Scholar 

  • Wenzel, W. W., Wieshammer, G., Fitz, W. J., & Puschenreiter, M. (2001). Novel rhizobox design to assess rhizosphere characteristics at high spatial resolution. Plant and Soil, 237, 37–45.

    Article  CAS  Google Scholar 

  • Ximénez-Embún, P., Rodríguez-Sanz, B., Madrid-Albarrán, Y., & Cámara, C. (2002). Uptake of heavy metals by lupin plants in artificially contaminated sand: Preliminary results. International Journal of Environmental Analytical Chemistry, 82, 805–814.

    Article  CAS  Google Scholar 

  • Zornoza, P., Vázquez, S., Esteban, E., Fernández-Pascual, M., & Carpena, R. O. (2002). Cadmium-stress in nodulated white lupin: Strategies to avoid toxicity. Plant Physiology Biochemistry, 40, 1003–1009.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financed by the Ministry of Education and Science (ref.: CTM2004-06715-C02-02) and the Fundación Séneca (ref.: 00571/PI/04). The authors thank the Ministry of Education and Science for the FPI grant awarded to Isabel Martínez Alcalá.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Pilar Bernal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martínez-Alcalá, I., Clemente, R. & Bernal, M.P. Metal Availability and Chemical Properties in the Rhizosphere of Lupinus albus L. Growing in a High-Metal Calcareous Soil. Water Air Soil Pollut 201, 283–293 (2009). https://doi.org/10.1007/s11270-008-9944-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-008-9944-0

Keywords